植物防卫反应过程中核黄素信号调节的遗传与转录组分析
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摘要
核黄素可通过生物合成、代谢与功能途径的多个环节,尤其是黄素介导的氧化还原作用,影响植物防卫和生长发育。核黄素是一种新的植物抗病激发子,外源施用核黄素能够诱导植物对多种病害的抗性,启动不同于其它已知的抗病信号通路,其机制仍不清楚。转中华鳖核黄素受体蛋白基因拟南芥体內含有高于野生型水平的核黄素,而且转基因植物也表现增强的抗病反应,但其机制尚不清楚。因此,本博士学位论文着重解析体外喷施核黄素诱导的抗病机制、转核黄素受体基因植物的抗病机制以及内源核黄素含量调控所影响的生理过程和代谢途径,为阐明核黄素参与调控植物生长和防卫反应的机制及与其他激素或非激素信号传导途径的交叉对话提供研究基础。
1外源核黄素诱导的引发抗病防卫反应依赖过氧化氢和NPR1基因
致坏死型病原菌接种后,植物具备了增强的防卫反应激活能力以应对生物和非生物胁迫,这一过程称为引发(priming)。引发状态(primed state)也可以被有益微生物根部定殖和许多天然或合成物质处理植物后诱导产生。近几年的研究表明,引发可能是植物诱导抗性的重要机制。核黄素处理拟南芥诱导PR-1和PR-2基因的表达,而PAL1诱导表达不显著。核黄素预先处理,再接种丁香假单胞番茄致病变种DC3000后,激发植物体內更强的细胞防卫反应并诱导防卫反应基因更强更快的表达,同时诱发过氧化氢的积累、胼胝质沉积和过敏性细胞死亡。用过氧化氢清除剂完全消弱了植物细胞和分子水平的防卫反应及其对病原菌的抗性。核黄素处理并接种病原菌诱发的细胞防卫反应在水杨酸、乙烯、茉莉酸和脱落酸信号通路的突变体上可以产生,但在npr1突变体中消失。研究结果表明,外施核黄素使植物进入引发状态,接种病原菌时,植物体內积累高浓度的过氧化氢,并激发细胞防卫反应和相关基因的快速且高强度表达以及对病原菌的抗性,这一过程依赖于过氧化氢和NPR1基因,但不依赖于水杨酸、乙烯、茉莉酸和脱落酸信号通路。
2转中华鳖核黄素受体基因植物表达谱分析
本实验室把中华鳖的核黄素受体基因转入拟南芥,借以调节核黄素含量及对防卫反应和有关生长发育过程的影响。转基因植物体内核黄素含量高于野生型水平,沉默核黄素受体基因后,沉默植物内的核黄素恢复到野生型水平。我们利用拟南芥基因组芯片(ATH1 Affymetrix chip)分析转基因植物表达谱的变化。预杂交实验和质量控制检验显示,表达谱芯片及样品CRNA产物质量较好,表达谱芯片实验成功,数据可靠。应用GCOS(GeneChip(?)Operating Software)软件进行数据分析获得的原始数据,再用RMA(robust multiarray analysis)进行数据预处理后,根据随机方差模型的单因素方差分析对实验组与对照进行比较,以筛选两两分组之间的差异基因。对于差异基因的筛选方法基于FDR(fdlse discovery rate)＜0.1,p＜0.05,Permutation P＜0.05.根据基因在两个分组中的几何平均数的比值倍数决定差异基因的变化方向,我们选取比值≥2的基因为显著上调基因,比值≤0.5的为显著下调基因。结果表明,共有320个基因显著上调,630个基因显著下调。我们随机选取部分基因对芯片结果进行RT-PCR和Real-time PCR验证,结果显示表达结果与芯片数据相吻合。随后,对表达差异显著的基因在拟南芥信息中心进行基因本体(Gene Ontology,GO)分析,按照GO数据库的主子集生物学过程以获取它们确切的GO分类信息。接着,我们又利用代谢途径分析程序MapMan,分析差异表达基因所属的代谢途径,以期了解转基因植物中代谢过程的变化。我们着重列举了次级代谢、物质运输、转录因子、线粒体电子传递、氧化还原调控等代谢过程的变化。同时我们选取了植物防卫反应相关基因、激素信号途径相关基因和蛋白激酶基因这三类基因及其他个别基因进行了简要的分析。结果表明,转基因植物中差异表达的基因涉及很多生理过程、代谢途径、激素及非激素信号途径。尤其令人感兴趣的是,线粒体电子传递链的部分组成基因下调表达以及氧化还原调控过程中一些清除活性氧(reacfive oxygen species,ROS)的酶基因上调表达,这暗示着转基因植株具有较高氧化态。差异表达的基因对我们进一步研究核黄素调控的代谢过程和防卫反应机制提供了线索。
3转核黄素受体基因植物抗病机制解析
基因表达谱的数据表明,转基因植株线粒体电子传递链的部分基因下调表达,而参与抗氧化体系中的有些基因上调表达,这暗示转基因植物可能具有较高氧化态。通过活性氧原位组织染色和叶片过氧化氢含量测定,发现转基因植株中的活性氧水平比野生型和沉默植株均高;喷施ROS供体百草枯(Paraquat)后,发现转基因植物对百草枯表现较敏感,表明转基因植物体内的氧化还原平衡被打破(具有较高的氧化态)。为了解析转基因植物抗病性与氧化还原平衡改变的关系,以及氧化平衡改变是否受体内核黄素含量升高的影响,我们通过注射过氧化氢清除剂Catalase及核黄素,并结合DC3000接种,检测不同处理中植物的氧爆发、胼胝质积累和细胞坏死这三种细胞防卫反应的产生情况,并对植物抗病性和菌落生长数量进行观测。结果表明,转基因植物体内的氧化还原改变对引发植物抗病防卫反应是必需的,而且植物体内核黄素含量的变化是引起植物体内氧化还原状态改变的原因。我们又利用本实验室产生的转基因植物与基本防卫信号通路突变体npr1-1、etr1-1、jar1-1和abi1-1杂交或转基因获得的双突变体,解析内源核黄素介导的抗病性所依赖的信号通路。结果发现,双突变体均具有较高的氧化态,但接种后,npr1-1中没有显著的活性氧积累,也没有出现胼胝质积累和细胞坏死,而其他双突变体均产生增强的细胞防卫反应,这表明內源核黄素引发抗病防卫反应需要NPR1,但不依赖于乙烯、茉莉酸和脱落酸信号通路。本章的研究结果表明,转基因植物内高水平的核黄素引起植物体内ROS积累及较高的氧化态,使得植物进入引发状态,当接种病原物时,转基因植物能够表现快速增强的细胞和分子防卫反应,从而引发对病原菌的增强抗性,而且引发防卫反应过程需要NPR1的参与。
4核黄素引发抗病防卫信号传导机制研究
转核黄素受体基因拟南芥RIRA11中氧化还原平衡状态的改变和ROS的积累在植物抗病性中是必需的。为了证明外施核黄素是否导致体內氧化还原态的改变并且这一改变在引发抗病防卫反应中的作用,我们检测了核黄素处理拟南芥5天内的氧化还原动态变化。结果发现,在0小时至5天內,外源核黄素处理植物激发体内的ROS积累且在2小时的达到高峰值,5天后恢复到原来水平;我们通过DAB染色、过氧化氢含量测定、百草枯(PQ)敏感性测定,发现核黄素处理拟南芥后导致氧化还原态的改变,致使体内的氧化态升高。核黄素喷施植物后再注射Catalase,体內的氧化态降低;而且5天后接种DC3000后,植物体内没有出现细胞防卫反应,其抗病性与喷施核黄素植株相比显著降低,这表明,核黄素处理拟南芥导致还原状态的改变对核黄素诱导的抗病性是必需的。根据转基因植物表达谱信息,我们选取线粒体电子传递链复合Ⅰ上的两个基因,利用Real-time PCR技术检测核黄素处理过程中的这两个基因的表达动态变化,发现两个基因的表达明显受抑制且在6小时表达量最低,这表明核黄素可能通过抑制线粒体电子传递链而导致ROS积累并打破胞内正常的氧化还原平衡,但也不能排除是线粒体行使ROS动态平衡初始变化的第一个转播站并且将信号放大的结果。核黄素处理导致体內氧化还原平衡的改变,使植物对外来刺激更加敏感并进入引发状态,当病原菌侵染时,植物能够表现快速增强的细胞防卫反应,这可能是核黄素引发防卫反应的细胞机制。
5防卫反应引发激发子引发植物抗病的生产应用
研究表明,水稻细菌性条斑病菌(Xanthomonas oryzae pv.oryzicola)的HpaG_(xooc)功能片段HpaG_(10-42)在引发水稻防卫反应中的活性最强。通过浓度/植物处理时期组合试验发现,在水稻苗期喷施一次和大田移栽后喷施三次浓度为6μg/ml的HpaG_(10-42)后,同对照处理相比,处理的籼稻和粳稻上水稻白叶枯病(X.oryzae pv.oryzae)和穗颈瘟(Magnaporthe grisea)的病情指数均显著降低;而且,该浓度的蛋白在水稻苗期,返青期、分蘖后期、始穗期单独处理一次,均可高效引发水稻在该时期的抗病性;与常规农事操作相比,水稻生长的四个时期施用6μg/ml的蛋白处理后,两种病害的病情指数显著降低,在9个测试水稻品种上的诱导抗病效果也很显著。结果表明,该激发子可以高效引发大田植物的抗病性,为其在田间作物上的大规模应用提供了基础。
6总结
本研究利用外源喷施核黄素及內源核黄素调控两种手段,对核黄素引发植物防卫反应的信号传导机制进行了初步解析,同时利用基因表达谱技术,分析了內源核黄素含量调控所影响的生理过程和代谢途径,还对防卫反应激发子HpaG_(10-42)引发田间水稻抗病性进行了研究.研究发现:第一,引发是核黄素诱导抗病防卫反应的细胞机制,引发病原菌刺激时产生的细胞和分子防卫反应依赖于NPR1,但不依赖于SA.第二,核黄素通过引起植物体內氧化还原平衡改变而使植物进入引发状态,但氧化还原状态的改变不依赖于NPR1。第三,内源核黄素影响了次级代谢、物质运输、转录调控等多种生理代谢过程以及激素、非激素信号传导信号通路,这为解析核黄素调控植物生长和防卫的机制及与激素、非激素信号通路的交叉对话提供了有益的线索。第四,核黄素可能通过作用于线粒体电子传递链而激发活性氧积累,并因此改变了植物体内的氧化还原平衡。第五,HpaG_(10-42)可以高效引发田间水稻的抗病性。
Riboflavin (vitamin B_2) biosynthetic and functional pathways affect plant growth, development, and defensive responses by multiple mechanisms. Riboflavin is involved in anti-oxidation and peroxidation. Both processes affect the production of reactive oxygen species (ROS) in oxidative burst. Our previous studies suggest that riboflavin is a novel elicitor of systemic acquired resistance (SAR) in plants and activates a distinct defense signaling pathway from several known ones, but the underlying molecular mechanism remains unclear. Endogenous-modulated riboflavin also triggers plant disease resistance in Arabidopsis expressing the riboflavin receptor protein encoding gene of soft-shelled turtle (Trionyx sinensis japonicus). However, the mechanism of disease resistance in transgenetic plants is still unknown. Studies in this Ph.D thesis aim at determination of signaling pathways and components in plant responses to exogenous and endogenous riboflavin, as well as the physiological processes and metabolic pathways, which are affected by endogenous riboflavin with higher levels. The results here will provide basic clues to explore the riboflavin mediated plant defense and growth pathways and crosstalk with hormonal and non-hormonal signaling pathways.
1. Riboflavin-induced priming for pathogen responses in Arabidopsis requires hydrogen peroxide and NPR1
Besides having a pivotal biological function as a component of coenzymes, riboflavin appears as an elicitor of systemic acquired resistance (SAR) in plants, but the underlying molecular mechanism remains unclear. SAR is associated with the ability to induce cellular defense responses more rapidly and to a greater degree than in non-induced plants, a process called "priming." Here we report that the application of riboflavin to Arabidopsis thaliana induces priming of defense responses toward infection with virulent Psedumonas syringae pv. tomato DC3000 (Pst). Induced plant resistance to the bacterial pathogen was mechanistically connected with the expression of defense response genes and cellular defensive events, including H_2O_2 burst, HCD, and callose deposition. Riboflavin treatment and inoculation of plants with Pst were neither active but both synergized to induce priming events. The defense-priming process needed NPR1 (essential regulator of systemic acquired resistance) and maintenance of H_2O_2 burst but was independent of salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA). Our results suggest that the role of riboflavin in priming defenses is subject to signaling process distinct from the known pathways of hormone signal transduction.
2. Genome-wide transcriptional profiling and metabolism analysis of transgenetic Arabidopsis plants expressing an oviparal riboflavin receptor gene
We have cloned the riboflavin receptor protein encoding gene RIR from soft-shelled turtle and transferred it into Arabidopsis and got several homozygous lines. We also constructed RIR-silencing vector, which was able to silence RIR in RIRA11 and got SiRB11, for further study on the roles of riboflavin in plant growth and defense regulation network. We used the Arabidopsis ATH1 Affymetrix chip to analyze the global transcriptional profiling. Based on the pre-hybridization and quality control results, our microarray experiments were successful and data we got was credible. Then we used the GCOS software to analyze the original data and pre-treated with robust multiarray analysis (RMA), and we got the differentially regulated genes between Col-0 and RIRA11 plants. Our choosing criterion was based on the FDR < 0.1, p < 0.05, Permutation P<0.05. Further data analysis was carried out by selecting for the genes exhibiting >2-fold differences. There were 320 genes found to be significantly up-regulated and 630 down-regulated. We then performed RT-PCR and Real-time PCR on a select group of genes and compared the results with those obtained from the array. Although the ratios from the PCR data are not the same as those in the chip, the correlation between the two groups of data are very good. Subsequently, Gene ontology analysis was carried out on the Arabidopsis Biological Research Center. To analyze the metabolism processes changed in RIRA11, we used the MapMan software to visualize the metabolic pathway assigned from the significantly regulated genes. The results suggested that there are some genes involved in secondary metabolism, transport, transcription and mitochondrial electron transport, redox homeostasis. Meanwhile, some genes involved in plant defense response, hormonal signaling pathway and protein kinase were analyzed in the text. To our great interesting, some genes in the mitochondrial electron transport chain were depressed but some ROS detoxification genes were up-regulated, suggesting that there is escalated oxidative state in RIRA11.These results provide us the insights into the effect of riboflavin on plants and explore a list of candidate genes that may act to regulate plant defense and development, hormonal and non-hormonal signaling pathways.
3. Modulated riboflavin may activate the mitochondrial pathway of ROS signaling and primes pathogen defense response in transgenetic Arabidopsis plants
Compared with Col-0 and SiRB11 plants, RIRA11 contains higher endogenous riboflavin than that in Col-0 and SiRB11. Moreover, RIRA11 exhibits alleviative symptoms and reduced bacterial propagation after DC3000 infection, but the underlying mechanisms are unclear. Based on the microarray data, we deduced that the inhibition of the mitochondrial electron transport chain may result in the escalated oxidative state in RIRA11.Then we detected the ROS levels by DAB and DCFH-DA staining and H_2O_2 content measuring, as well as the sensitivity of the plants to the extra oxidative stresses, generated by Paraquat (PQ), the results suggested that there was escalated oxidative state in RIRA11. Combined with catalase, riboflavin, and DC3000 inoculation, we analyzed the cellular and molecular defense responses. Thus, our results suggested that riboflavin may inactive the mitochondrial electron transport chain resulting in the escalated oxidative state and shifted the plants to the primed state, which plays a pivotal role in augmented defense response in RIRA11 when infected by DC3000. Endogenous riboflavin-induced priming is the mechanism of disease resistance in RIRA11. Then we analyzed the signaling pathways required in endogenous riboflavin-induced priming using the mutants npr1-1、etr1-1、jar1-、and abi1-1, each of which has the RIR gene by the methods of gene transferring and crossing with RIRA11. The results show that endogenous riboflavin-induced priming requires NPR1, but is independent of ET, JA and ABA signaling pathways.
4. Priming of pathogen defense signal transduction by riboflavin in Arabidopsis
Our previously studies suggest that the disturbed redox homeostasis plays a pivotal role in endogenous riboflavin-mediated priming. To explore whether it also functions in the exogenous riboflavin-induced priming, we detected the ROS accumulation in plants from the beginning of riboflavin sprayed till 5 dpt. The results showed that riboflavin trigger ROS accumulation in plants during the period tested and the levels of ROS reach the highest at 2 hpt, but restore to the original level at 5dpt. Meanwhile, the riboflavin-treated plants are more sensitive to the extra oxidative stresses, generated by Paraquat, suggesting that the plants have escalated oxidative state. Combined with catalase and DC3000 inoculation, we analyzed the cellular and molecular defense responses. Catalse, which infiltrated at 30min after riboflavin treatment, nullifies the escalated oxidative state and the augmented ROS accumulation when infected by Pst. Moreover, the disease resistance is also abolished in riboflavin pretreated but catalase treated plants, which suggest that the disrupted redox homeostasis is required in riboflavin-induced priming. However, the disrupted redox homeostasis is independent of NPR1. Based on the microarray data, we then analyzed the two genes involved in mitochondrial electron transport with Real-time PCR technology. Both of the genes were depressed during the course of riboflavin treatment. Therefore, the results here suggest that disrupted redox homeostasis plays a pivotal role in riboflavin-induced priming and may connect with functional inhabitation of mitochondria.
5. Practical use of defense priming by harpin in rice
HpaG_(10-42), which generated from truncating the Xanthomonas oryzae pv. oryzicola HpaG_(Xooc) protein, is active in priming defense responses in rice. When 6μg/ml HpaG_(10-42) was applied once to seedling nursery and three times to transplanting fields of indica and japonica rice varieties, bacterial blight caused by X. oryzae pv. oryzae and panicle blast caused by Magnaporthe grisea were both less severe, relative to controls. Meanwhile, when HpaG_(10-42) applied once at the four stages of rice growth, the effects on decreasing disease severities were also significant. HpaG_(10-42) treatment was similar to local agronomic measures, including use of chemicals, in decreasing disease severities of 9 rice varieties. Hence, results here provide an example for effective use of beneficial pathogen defense priming agents to control diseases in the staple food crop.
Conclusive remarks
Results described above have provided us with further understanding on the mechanisms of riboflavin-mediated pathogen defense in plants. Firstly, priming is an important cellular mechanism in SAR by riboflavin and requires hydrogen peroxide and intact NPR1. Secondly, disrupted redox homeostasis induced by riboflavin, which is independent of NPR1, plays a pivotal role in shifting the plants to primed state. Thirdly, Endogenous riboflavin dose affect many physiological processes, such as secondary metabolism, transport, transcription, redox metabolism, as well as hormonal and non-hormonal signaling pathways, which provide us the cues to explore the mechanisms of riboflavin mediated plant defense and development, the crosstalk between riboflavin signaling with hormonal and non-hormonal signaling pathways. Fourthly, riboflavin may inactivate mitochondrial electron transport, resulting in ROS accumulation and disrupted redox homeostasis in plants. Fifthly, HpaG_(10-42), a selected fragment of HpaG_(Xooc), could prime disease resistance of rice effectively in fields.
1外源核黄素诱导的引发抗病防卫反应依赖过氧化氢和NPR1基因
致坏死型病原菌接种后,植物具备了增强的防卫反应激活能力以应对生物和非生物胁迫,这一过程称为引发(priming)。引发状态(primed state)也可以被有益微生物根部定殖和许多天然或合成物质处理植物后诱导产生。近几年的研究表明,引发可能是植物诱导抗性的重要机制。核黄素处理拟南芥诱导PR-1和PR-2基因的表达,而PAL1诱导表达不显著。核黄素预先处理,再接种丁香假单胞番茄致病变种DC3000后,激发植物体內更强的细胞防卫反应并诱导防卫反应基因更强更快的表达,同时诱发过氧化氢的积累、胼胝质沉积和过敏性细胞死亡。用过氧化氢清除剂完全消弱了植物细胞和分子水平的防卫反应及其对病原菌的抗性。核黄素处理并接种病原菌诱发的细胞防卫反应在水杨酸、乙烯、茉莉酸和脱落酸信号通路的突变体上可以产生,但在npr1突变体中消失。研究结果表明,外施核黄素使植物进入引发状态,接种病原菌时,植物体內积累高浓度的过氧化氢,并激发细胞防卫反应和相关基因的快速且高强度表达以及对病原菌的抗性,这一过程依赖于过氧化氢和NPR1基因,但不依赖于水杨酸、乙烯、茉莉酸和脱落酸信号通路。
2转中华鳖核黄素受体基因植物表达谱分析
本实验室把中华鳖的核黄素受体基因转入拟南芥,借以调节核黄素含量及对防卫反应和有关生长发育过程的影响。转基因植物体内核黄素含量高于野生型水平,沉默核黄素受体基因后,沉默植物内的核黄素恢复到野生型水平。我们利用拟南芥基因组芯片(ATH1 Affymetrix chip)分析转基因植物表达谱的变化。预杂交实验和质量控制检验显示,表达谱芯片及样品CRNA产物质量较好,表达谱芯片实验成功,数据可靠。应用GCOS(GeneChip(?)Operating Software)软件进行数据分析获得的原始数据,再用RMA(robust multiarray analysis)进行数据预处理后,根据随机方差模型的单因素方差分析对实验组与对照进行比较,以筛选两两分组之间的差异基因。对于差异基因的筛选方法基于FDR(fdlse discovery rate)＜0.1,p＜0.05,Permutation P＜0.05.根据基因在两个分组中的几何平均数的比值倍数决定差异基因的变化方向,我们选取比值≥2的基因为显著上调基因,比值≤0.5的为显著下调基因。结果表明,共有320个基因显著上调,630个基因显著下调。我们随机选取部分基因对芯片结果进行RT-PCR和Real-time PCR验证,结果显示表达结果与芯片数据相吻合。随后,对表达差异显著的基因在拟南芥信息中心进行基因本体(Gene Ontology,GO)分析,按照GO数据库的主子集生物学过程以获取它们确切的GO分类信息。接着,我们又利用代谢途径分析程序MapMan,分析差异表达基因所属的代谢途径,以期了解转基因植物中代谢过程的变化。我们着重列举了次级代谢、物质运输、转录因子、线粒体电子传递、氧化还原调控等代谢过程的变化。同时我们选取了植物防卫反应相关基因、激素信号途径相关基因和蛋白激酶基因这三类基因及其他个别基因进行了简要的分析。结果表明,转基因植物中差异表达的基因涉及很多生理过程、代谢途径、激素及非激素信号途径。尤其令人感兴趣的是,线粒体电子传递链的部分组成基因下调表达以及氧化还原调控过程中一些清除活性氧(reacfive oxygen species,ROS)的酶基因上调表达,这暗示着转基因植株具有较高氧化态。差异表达的基因对我们进一步研究核黄素调控的代谢过程和防卫反应机制提供了线索。
3转核黄素受体基因植物抗病机制解析
基因表达谱的数据表明,转基因植株线粒体电子传递链的部分基因下调表达,而参与抗氧化体系中的有些基因上调表达,这暗示转基因植物可能具有较高氧化态。通过活性氧原位组织染色和叶片过氧化氢含量测定,发现转基因植株中的活性氧水平比野生型和沉默植株均高;喷施ROS供体百草枯(Paraquat)后,发现转基因植物对百草枯表现较敏感,表明转基因植物体内的氧化还原平衡被打破(具有较高的氧化态)。为了解析转基因植物抗病性与氧化还原平衡改变的关系,以及氧化平衡改变是否受体内核黄素含量升高的影响,我们通过注射过氧化氢清除剂Catalase及核黄素,并结合DC3000接种,检测不同处理中植物的氧爆发、胼胝质积累和细胞坏死这三种细胞防卫反应的产生情况,并对植物抗病性和菌落生长数量进行观测。结果表明,转基因植物体内的氧化还原改变对引发植物抗病防卫反应是必需的,而且植物体内核黄素含量的变化是引起植物体内氧化还原状态改变的原因。我们又利用本实验室产生的转基因植物与基本防卫信号通路突变体npr1-1、etr1-1、jar1-1和abi1-1杂交或转基因获得的双突变体,解析内源核黄素介导的抗病性所依赖的信号通路。结果发现,双突变体均具有较高的氧化态,但接种后,npr1-1中没有显著的活性氧积累,也没有出现胼胝质积累和细胞坏死,而其他双突变体均产生增强的细胞防卫反应,这表明內源核黄素引发抗病防卫反应需要NPR1,但不依赖于乙烯、茉莉酸和脱落酸信号通路。本章的研究结果表明,转基因植物内高水平的核黄素引起植物体内ROS积累及较高的氧化态,使得植物进入引发状态,当接种病原物时,转基因植物能够表现快速增强的细胞和分子防卫反应,从而引发对病原菌的增强抗性,而且引发防卫反应过程需要NPR1的参与。
4核黄素引发抗病防卫信号传导机制研究
转核黄素受体基因拟南芥RIRA11中氧化还原平衡状态的改变和ROS的积累在植物抗病性中是必需的。为了证明外施核黄素是否导致体內氧化还原态的改变并且这一改变在引发抗病防卫反应中的作用,我们检测了核黄素处理拟南芥5天内的氧化还原动态变化。结果发现,在0小时至5天內,外源核黄素处理植物激发体内的ROS积累且在2小时的达到高峰值,5天后恢复到原来水平;我们通过DAB染色、过氧化氢含量测定、百草枯(PQ)敏感性测定,发现核黄素处理拟南芥后导致氧化还原态的改变,致使体内的氧化态升高。核黄素喷施植物后再注射Catalase,体內的氧化态降低;而且5天后接种DC3000后,植物体内没有出现细胞防卫反应,其抗病性与喷施核黄素植株相比显著降低,这表明,核黄素处理拟南芥导致还原状态的改变对核黄素诱导的抗病性是必需的。根据转基因植物表达谱信息,我们选取线粒体电子传递链复合Ⅰ上的两个基因,利用Real-time PCR技术检测核黄素处理过程中的这两个基因的表达动态变化,发现两个基因的表达明显受抑制且在6小时表达量最低,这表明核黄素可能通过抑制线粒体电子传递链而导致ROS积累并打破胞内正常的氧化还原平衡,但也不能排除是线粒体行使ROS动态平衡初始变化的第一个转播站并且将信号放大的结果。核黄素处理导致体內氧化还原平衡的改变,使植物对外来刺激更加敏感并进入引发状态,当病原菌侵染时,植物能够表现快速增强的细胞防卫反应,这可能是核黄素引发防卫反应的细胞机制。
5防卫反应引发激发子引发植物抗病的生产应用
研究表明,水稻细菌性条斑病菌(Xanthomonas oryzae pv.oryzicola)的HpaG_(xooc)功能片段HpaG_(10-42)在引发水稻防卫反应中的活性最强。通过浓度/植物处理时期组合试验发现,在水稻苗期喷施一次和大田移栽后喷施三次浓度为6μg/ml的HpaG_(10-42)后,同对照处理相比,处理的籼稻和粳稻上水稻白叶枯病(X.oryzae pv.oryzae)和穗颈瘟(Magnaporthe grisea)的病情指数均显著降低;而且,该浓度的蛋白在水稻苗期,返青期、分蘖后期、始穗期单独处理一次,均可高效引发水稻在该时期的抗病性;与常规农事操作相比,水稻生长的四个时期施用6μg/ml的蛋白处理后,两种病害的病情指数显著降低,在9个测试水稻品种上的诱导抗病效果也很显著。结果表明,该激发子可以高效引发大田植物的抗病性,为其在田间作物上的大规模应用提供了基础。
6总结
本研究利用外源喷施核黄素及內源核黄素调控两种手段,对核黄素引发植物防卫反应的信号传导机制进行了初步解析,同时利用基因表达谱技术,分析了內源核黄素含量调控所影响的生理过程和代谢途径,还对防卫反应激发子HpaG_(10-42)引发田间水稻抗病性进行了研究.研究发现:第一,引发是核黄素诱导抗病防卫反应的细胞机制,引发病原菌刺激时产生的细胞和分子防卫反应依赖于NPR1,但不依赖于SA.第二,核黄素通过引起植物体內氧化还原平衡改变而使植物进入引发状态,但氧化还原状态的改变不依赖于NPR1。第三,内源核黄素影响了次级代谢、物质运输、转录调控等多种生理代谢过程以及激素、非激素信号传导信号通路,这为解析核黄素调控植物生长和防卫的机制及与激素、非激素信号通路的交叉对话提供了有益的线索。第四,核黄素可能通过作用于线粒体电子传递链而激发活性氧积累,并因此改变了植物体内的氧化还原平衡。第五,HpaG_(10-42)可以高效引发田间水稻的抗病性。
Riboflavin (vitamin B_2) biosynthetic and functional pathways affect plant growth, development, and defensive responses by multiple mechanisms. Riboflavin is involved in anti-oxidation and peroxidation. Both processes affect the production of reactive oxygen species (ROS) in oxidative burst. Our previous studies suggest that riboflavin is a novel elicitor of systemic acquired resistance (SAR) in plants and activates a distinct defense signaling pathway from several known ones, but the underlying molecular mechanism remains unclear. Endogenous-modulated riboflavin also triggers plant disease resistance in Arabidopsis expressing the riboflavin receptor protein encoding gene of soft-shelled turtle (Trionyx sinensis japonicus). However, the mechanism of disease resistance in transgenetic plants is still unknown. Studies in this Ph.D thesis aim at determination of signaling pathways and components in plant responses to exogenous and endogenous riboflavin, as well as the physiological processes and metabolic pathways, which are affected by endogenous riboflavin with higher levels. The results here will provide basic clues to explore the riboflavin mediated plant defense and growth pathways and crosstalk with hormonal and non-hormonal signaling pathways.
1. Riboflavin-induced priming for pathogen responses in Arabidopsis requires hydrogen peroxide and NPR1
Besides having a pivotal biological function as a component of coenzymes, riboflavin appears as an elicitor of systemic acquired resistance (SAR) in plants, but the underlying molecular mechanism remains unclear. SAR is associated with the ability to induce cellular defense responses more rapidly and to a greater degree than in non-induced plants, a process called "priming." Here we report that the application of riboflavin to Arabidopsis thaliana induces priming of defense responses toward infection with virulent Psedumonas syringae pv. tomato DC3000 (Pst). Induced plant resistance to the bacterial pathogen was mechanistically connected with the expression of defense response genes and cellular defensive events, including H_2O_2 burst, HCD, and callose deposition. Riboflavin treatment and inoculation of plants with Pst were neither active but both synergized to induce priming events. The defense-priming process needed NPR1 (essential regulator of systemic acquired resistance) and maintenance of H_2O_2 burst but was independent of salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA). Our results suggest that the role of riboflavin in priming defenses is subject to signaling process distinct from the known pathways of hormone signal transduction.
2. Genome-wide transcriptional profiling and metabolism analysis of transgenetic Arabidopsis plants expressing an oviparal riboflavin receptor gene
We have cloned the riboflavin receptor protein encoding gene RIR from soft-shelled turtle and transferred it into Arabidopsis and got several homozygous lines. We also constructed RIR-silencing vector, which was able to silence RIR in RIRA11 and got SiRB11, for further study on the roles of riboflavin in plant growth and defense regulation network. We used the Arabidopsis ATH1 Affymetrix chip to analyze the global transcriptional profiling. Based on the pre-hybridization and quality control results, our microarray experiments were successful and data we got was credible. Then we used the GCOS software to analyze the original data and pre-treated with robust multiarray analysis (RMA), and we got the differentially regulated genes between Col-0 and RIRA11 plants. Our choosing criterion was based on the FDR < 0.1, p < 0.05, Permutation P<0.05. Further data analysis was carried out by selecting for the genes exhibiting >2-fold differences. There were 320 genes found to be significantly up-regulated and 630 down-regulated. We then performed RT-PCR and Real-time PCR on a select group of genes and compared the results with those obtained from the array. Although the ratios from the PCR data are not the same as those in the chip, the correlation between the two groups of data are very good. Subsequently, Gene ontology analysis was carried out on the Arabidopsis Biological Research Center. To analyze the metabolism processes changed in RIRA11, we used the MapMan software to visualize the metabolic pathway assigned from the significantly regulated genes. The results suggested that there are some genes involved in secondary metabolism, transport, transcription and mitochondrial electron transport, redox homeostasis. Meanwhile, some genes involved in plant defense response, hormonal signaling pathway and protein kinase were analyzed in the text. To our great interesting, some genes in the mitochondrial electron transport chain were depressed but some ROS detoxification genes were up-regulated, suggesting that there is escalated oxidative state in RIRA11.These results provide us the insights into the effect of riboflavin on plants and explore a list of candidate genes that may act to regulate plant defense and development, hormonal and non-hormonal signaling pathways.
3. Modulated riboflavin may activate the mitochondrial pathway of ROS signaling and primes pathogen defense response in transgenetic Arabidopsis plants
Compared with Col-0 and SiRB11 plants, RIRA11 contains higher endogenous riboflavin than that in Col-0 and SiRB11. Moreover, RIRA11 exhibits alleviative symptoms and reduced bacterial propagation after DC3000 infection, but the underlying mechanisms are unclear. Based on the microarray data, we deduced that the inhibition of the mitochondrial electron transport chain may result in the escalated oxidative state in RIRA11.Then we detected the ROS levels by DAB and DCFH-DA staining and H_2O_2 content measuring, as well as the sensitivity of the plants to the extra oxidative stresses, generated by Paraquat (PQ), the results suggested that there was escalated oxidative state in RIRA11. Combined with catalase, riboflavin, and DC3000 inoculation, we analyzed the cellular and molecular defense responses. Thus, our results suggested that riboflavin may inactive the mitochondrial electron transport chain resulting in the escalated oxidative state and shifted the plants to the primed state, which plays a pivotal role in augmented defense response in RIRA11 when infected by DC3000. Endogenous riboflavin-induced priming is the mechanism of disease resistance in RIRA11. Then we analyzed the signaling pathways required in endogenous riboflavin-induced priming using the mutants npr1-1、etr1-1、jar1-、and abi1-1, each of which has the RIR gene by the methods of gene transferring and crossing with RIRA11. The results show that endogenous riboflavin-induced priming requires NPR1, but is independent of ET, JA and ABA signaling pathways.
4. Priming of pathogen defense signal transduction by riboflavin in Arabidopsis
Our previously studies suggest that the disturbed redox homeostasis plays a pivotal role in endogenous riboflavin-mediated priming. To explore whether it also functions in the exogenous riboflavin-induced priming, we detected the ROS accumulation in plants from the beginning of riboflavin sprayed till 5 dpt. The results showed that riboflavin trigger ROS accumulation in plants during the period tested and the levels of ROS reach the highest at 2 hpt, but restore to the original level at 5dpt. Meanwhile, the riboflavin-treated plants are more sensitive to the extra oxidative stresses, generated by Paraquat, suggesting that the plants have escalated oxidative state. Combined with catalase and DC3000 inoculation, we analyzed the cellular and molecular defense responses. Catalse, which infiltrated at 30min after riboflavin treatment, nullifies the escalated oxidative state and the augmented ROS accumulation when infected by Pst. Moreover, the disease resistance is also abolished in riboflavin pretreated but catalase treated plants, which suggest that the disrupted redox homeostasis is required in riboflavin-induced priming. However, the disrupted redox homeostasis is independent of NPR1. Based on the microarray data, we then analyzed the two genes involved in mitochondrial electron transport with Real-time PCR technology. Both of the genes were depressed during the course of riboflavin treatment. Therefore, the results here suggest that disrupted redox homeostasis plays a pivotal role in riboflavin-induced priming and may connect with functional inhabitation of mitochondria.
5. Practical use of defense priming by harpin in rice
HpaG_(10-42), which generated from truncating the Xanthomonas oryzae pv. oryzicola HpaG_(Xooc) protein, is active in priming defense responses in rice. When 6μg/ml HpaG_(10-42) was applied once to seedling nursery and three times to transplanting fields of indica and japonica rice varieties, bacterial blight caused by X. oryzae pv. oryzae and panicle blast caused by Magnaporthe grisea were both less severe, relative to controls. Meanwhile, when HpaG_(10-42) applied once at the four stages of rice growth, the effects on decreasing disease severities were also significant. HpaG_(10-42) treatment was similar to local agronomic measures, including use of chemicals, in decreasing disease severities of 9 rice varieties. Hence, results here provide an example for effective use of beneficial pathogen defense priming agents to control diseases in the staple food crop.
Conclusive remarks
Results described above have provided us with further understanding on the mechanisms of riboflavin-mediated pathogen defense in plants. Firstly, priming is an important cellular mechanism in SAR by riboflavin and requires hydrogen peroxide and intact NPR1. Secondly, disrupted redox homeostasis induced by riboflavin, which is independent of NPR1, plays a pivotal role in shifting the plants to primed state. Thirdly, Endogenous riboflavin dose affect many physiological processes, such as secondary metabolism, transport, transcription, redox metabolism, as well as hormonal and non-hormonal signaling pathways, which provide us the cues to explore the mechanisms of riboflavin mediated plant defense and development, the crosstalk between riboflavin signaling with hormonal and non-hormonal signaling pathways. Fourthly, riboflavin may inactivate mitochondrial electron transport, resulting in ROS accumulation and disrupted redox homeostasis in plants. Fifthly, HpaG_(10-42), a selected fragment of HpaG_(Xooc), could prime disease resistance of rice effectively in fields.
引文
1.Agrawal AA(1998) Induced responses to herbivory and increased plant performance.Science 279:1201-1202
2.Ahlfors R,Lang S,Overmyer K,Jaspers P,Brosche M,Tauriainen A,Kollist H,Tuominen H,Belles-Boix E,Piippo M(2004) Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid,ethylene,and methyl jasmonate responses.Plant Cell 16:1925-1937
3.Ahn IP,Kim S,Lee YH(2005) Vitamin B1 functions as an activator of plant disease resistance.Plant Physiol 138:1505-1515
4.Ahn IP,Kim S,Lee YH,Suh SC(2007) Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis.Plant Physiol 143:838-848
5.Ahn IP,Lee SW,Suh SC(2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene,jasmonic acid,and NPR1.Mol Plant Microbe Interact 20:759-768
6.Alvarez ME,Pennell RI,Meijer,P-J,Ishikawa A,Dixon RA,Lamb C(1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.Cell 92:773-784
7.Amirsadeghi S,Robson CA,Vanlerberghe GC(2007) The role of the mitochondrion in plant responses to biotic stress.Physiologia Plantarum 159:2539-266
8.Apel K,Hirt H(2004) Reactive oxygen species:metabolism,oxidative stress,and signal transduction.Annu Rev Plant Biol 55:373-399
9.Auh C-K,Murphy TM(1995) Plasma membrane redox enzyme is involved in the synthesis of O_2~- and H_2O_2 by Phytophthora elicitor-stimulated rose cells.Plant Physiol 107:1241-1247
10.Avdiushiko SA,Ye XS,Hildebrand DF(1993) Induction of lipoxygenasa activity in immunized cucumber plants.Physiol Mol Plant Patho 142:83
11.Aver'yanov AA,Lapikova VP,Nikolaev ON,Stepanov AI(2000) Active oxygen-associated control of rice blast disease by riboflavin and roseoflavin.Biochemistry(Mosc) 65:1292-1298
12.Baker CJ,Orlandi EW,Mock NM(1993) Harpin,an elicitor of the hypersensitive response in tobacco caused by Erwinia amylovora,elicits active oxygen production in suspension cells.Plant Physiol 102:1341-1344
13.Baldwin IT(1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations.Proc Natl Acad Sci USA 95:8113-8118
14.Banze M,Follmann H(2000) Organelle-specific NADPH thioredoxin reductase in plant mitochondria.J Plant Physiol 156:126-129
15.Barrientos A,Moraes CT(1999) Titrating the effects of mitochondrial complex I impairment in the cell physiology.J Biol Chem 274:16188-16197
16.Beckers GJ,Conrath U(2007) Priming for stress resistance:from the lab to the field.Curt Opin Plant Biol 10:425-31
17.Beckman KB,Ames BN(1997) Oxidative decay of DNA.J Biol Chem 272:19633-19636
18.Benhamou N,Kloepper JW,Quadt-Hallman A,Tuzun S(1996) Induction of defense-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria.Plant Physiol 112:919-929
19.Berlett BS,Stadtman ER(1997) Protein oxidation in aging disease,and oxidative stress.J Biol Chem 272:20313-20316
20.Berna A,Bernier F(1997) Regulated expression of a wheat germin gene in tobacoo:oxalate oxidase activity and apoplastic localization of the heterologous protein.Plant Mol Bio 33:417-429
21.Bernier F,Berna A(2001) Germins and germin-like proteins:plant do-all proteins.But what do they do exactly?Plant Physiol Biochem 39:545-554
22.Bethke PC Jones RL(2001) Cell death of barley aleurone protoplastsis mediated by reactive oxygen species.Plant J 25:19-29
23.Blume B,Nurnberger T,Nass N,Scheel D(2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley.Plant Cell 12:1425-1440
24.Bolwell GP,Davies DR,Gerrish C,Auh CK,Murphy TM(1998) Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms.Plant Physiol 116:1379-1385
25.Bowler C,Fluhr R(2000) The role of calcium and activated oxygen as signals for controlling cross-tolerance.Trends Plant Sci 5:241-245
26.Brian Olszak,FGMa,Peter Brodersen,Morten Grell,Henfiette Giese,Morten Petersen,John Mundy(2006) A putative flavin-containing mono-oxygenase as a marker for certain defense and cell death pathways.Plant Sci 170:614-623
27.Bright J,Desikan R,Hancock JT,Weir IS,Neill SJ(2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H_2O_2 synthesis.Plant J 45:113-122
28.Buhot N,Gomes E,Milat ML,Ponchet M,Marion D,Lequeu J,Delrot S,Coutos-Thevenot P,Blein JP(2004)Modulation of the biological activity of a tobacco LTP1 by lipid complexation.Mol Biol Cell 15:5047-5052
29.Can H,Bowling SA,Gordon AS,Dong X(1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance.Plant Cell 8:1583-1592
30.Carter C,Graham RA,Thornburg RW(1998) Arabidopsis thaliana contains a large family of germin-like proteins:characterization of cDNA and genomic sequences encoding 12 unique family members.Plant Mol Biol 38:929-943
31.Cashman JR(2002) Human and plant flavin-containing monooxygenase Noxygenation of amines:detoxication vs.bioactivatiort,Drug.Metab Rev 34:513-521
32.Chamnongpol S,Willfkens H,Moeder W,Langebartels C,Sandermannj H,Vanmontagu M,Inze D,VAN Cam PW(1998) Defense activation and enhanced pathogen tolerance induced by H_2O_2 intransgenic plants.Proc Natl Acad Sci USA 95:5818-5823
33.Chen S,Dickman MB(2004) Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides.J Exp Bot 55:2617-2623
34.Chen TY,Lei MG,Suzuki T,Morrison DC(1992) Lipopolysaccharide receptors and signal transduction pathways in mononuclear phagocytes.Curr Top Micro Immunol 181:169-188
35.Chen Z,Silva H,Klessig DF(1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.Science 262:1883-1886
36.Chisholm ST,Mahajan SK,Whitman SA,Yamamoto ML,Carrington,JC(2000) Cloning of the Arabidopsis RTM1gene,which controls restriction of long-distance movement of tobacco etch virus.Proc Nail Acad Sci USA 97:489-494
37.Clarke SF,Guy PL,Burritt DJ,Jameson PE(2002) Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment.Physiol Plant 114:157-164
38.Conrath U,Beckers GJ,Flors V,Garcia-Agustin P,Jakab G.Mauch F,Newman MA,Pieterse CM,Poinssot B,Pozo MJ,Pugin A,Schaffrath U,Ton J,Wendehenne D,Zimmerli L,Mauch-Mani B(2006) Priming:getting ready for battle.Mol Plant-Microbe Interact 19:1062-1071
39.Cortrath U,Pieterse CM,Mauch-Mani B(2002) Priming in plant-pathogen interactions.Trends Plant Sci 7:210-216
40.Danon A,Miersch O,Felix G,op den Camp RGL,Apel K(2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana.Plant J 41:68-80
41.Dat JF,Pellinen R,Beeckman T,Van De Cotte B,Langebartels C,Kangasjarvi J,Inze D,Van Breusegem F(2003)Changes in hydrogen peroxide homeostasis triger an active cell death process in tobacco.Plant J 33:621-632
42.Davey MW,Gilot C,Persiau G,Ostergaard J,Han Y(1999) Ascorbate biosynthesis in Arabidopsis cells uspension cultures.Plant Physiol 121:535-543
43.De Luca V,St-Pierre B(2000) The cell and developmental biology of alkaloid biosynthesis.Trends Plant Sci 5:168-173
44.Dean M,Rzhetsky A,Allikmets R(2001) The human ATP-binding cassette(ABC) transporter superfamily.Genome Res 11:1156-1166
45.Delaney TP(1997) Genetic dissection of acquired resistance to disease.Plant Physiol 113:5-12
46.Delaney TP,Friedrich L,Ryals J(1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.Proc Natl Acad Sci USA 92:6602-6606
47.Delaney TP,Uknes S,Vemooij B,Friedrich L,Weymann K,Negrotto D,Gaffney T,Gut-Rella M,Kessmann H,Ward E,Ryals J(1994) A central role of salicylic acid in plant disease resistance.Science 266:1247-1250
48.Delledonne M,Zeier J,Marocco A,Lamb CJ(2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response.Proc Natl Acad Sci USA 98:13454-13459
49.Dempsey DA,Shah J,Klessig DF(1999) Salicylic acid and disease resistance in plants.Crit Rev Plant Sci 18:547-575
50.Desikan R,Cheung MK,Bright J,Henson D,Hancock JT,Neill SJ(2004) ABA,hydrogen peroxide and nitric oxide signalling in stomatal guard cells.J Exp Bot 55:205-212
51.Desikan R,Hancock JT,Bright J,Harrison J,Weir I,Hooley R,Neill SJ(2005) A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells.Plant Physiol 137:831-834
52.Desikan R,Hancock JT,Ichimura K,Shinozaki K,Neill SJ(2001) Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6.Plant Physiol 126:1579-1587
53.Desikan R,Mackerness SAH,Hancock JT,Neill SJ(2001) Regulation of the Arabidopsis transcriptome by oxidative stress.Plant Physiol 127:159-172
54.Desikan R,Reynolds A,Hancock JT,Neill SJ(1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defense gene expression in Arabidopsis suspension cultures.Biochem J 330:115-120
55.Doke N(1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of phytophthora infestans and to the hyphal wall components.Physiol Plant Pathol 23:345-357
56.Dong HS,Beer SV(2000) Riboflavin induces disease resistance in plants by activating a novel signal transduction pathway.Phytopathology 90:801-811
57.Dorey S,Kopp M,Geoffroy P,Fritig B,Kauffrnann S(1999) Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction,phenylalanine ammonia lyase stimulation,salicylic acid accumulation or scopoletin consumption in cultured tobacco cells treated with elicitor.Plant Physiol 121:163-173
58.Durner J,Klessig DF(1995) Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses.Proc Natl Acad Sci USA 92:11312-11316
59.Durrant WE,Dong X(2004) Systemic acquired resistance.Annu Rev Phytopathol 42:185-209
60.Epple P,Mack AA,Morris VRF,Dangl JL(2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related,plant specific zinc finger proteins.Proc Natl Acad Sci USA 100:6831-6836
61.Eshdat Y,Holland D,Faltin Z,Benhayyim G(1997) Plant glutathione peroxidases.Physiol Plant 100:234-240
62.Etienne P,Petitot AS,Houot V,Blein JP,Suty L(2000) Induction of tcI7,a gene encoding a β-subunit of proteasome,in tobacco plants treated with elicitin,salicylic acid or hydrogen peroxide.FEBS Lett 466:213-218
63.Fowler S,Thomashow MF(2002) Arabidopsis transeriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway.The Plant Cell 14:1675-1690
64.Foyer CH,Lopez-delgado H,Dat JF,Scitt IM(1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling.Physiol Plant 100:241-254
65.Foyer CH,Noctor G(2005) Redox homeostasis and antioxidant signaling:a metabolic interface between stress perception and physiological responses.Plant Cell 17:1866-1875
66.Friedrich L,Lawton K,Ruess W,Masner P,Specker N,Gut-Rella M.Meier B,Dincher S,Staub T,Uknes S,Kessmaun H,Ryals J(1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco.Plant J 10:61-70
67.Friedrich L,Lawton K,RuessW,Masher P,Specker N,RellaMG,Meier B,Gachomo WE,Shonukan OO,Kotchoni OS(2003) The molecular initiation and subsequent acquisition of disease resistance in plants.Afr J Biotechnol 2:26-32
68.Ge X,Chen J,Li N,Lin Y,Sun C,Cao K(2003) Resistance function of rice lipid transfer protein LTP110.J Biochem Mol Biol 36:603-607
69.Ge X,Li GJ,Wang SB,Zhu H,Zhu T,Wang X,Xia Y(2007) AtNUDT7,a negative regulator of basal immunity in Arabidopsis,modulates two distinct defense response pathways and is involved in maintaining redox homeostasis.Plant Physiol 145:204-215
70.Gerhardt P,Murray RGE,Costilow RN,Nester EW,Wood WA,Krieg NR,Phillips GB(1981) Manual of Methods for General Bacteriology.American Society for Microbiology,Washington,D.C
71.Gothel SF,Marahiel MA(1999) Peptidyl-prolyl cis-trans isomerases,a superfamily of ubiquitous folding catalysts.Cell Mol Life Sci 55:423-436
72.Govrin E,Levine A(2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea.Curr Biol 10:751-757
73.Grant JJ,Loake GJ(2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance.Plant Physiol 124:21-29
74.Grant JJ,Yun BW,Loake GJ(2000) Oxidative burst and cognate redox signaling reported by luciferase imaging:identification of a signal network that functions independently of ethylene,SA and Me-JA but is dependent on MAPKK activity.Plant J 24:569-582
75.Green R,Fluhr R(1995) UV-B-induced PR-1 accumulation is mediated by active oxygen species.Plant Cell 7:203-212
76.Grivermikova VG,Vinogradov AD(2006) Generation of superoxide by the mitochondrial Complex I.Biochim Biophys Acta 1757:553-561
77.Guanl M,Scandallos JG(2000) Hydrogen peroxide-mediated catalase gene expression in response to wounding.Free Radical Biology and Medicine 28:1182-1190
78.Hahlbrock K,Scheel D(1989) Physiology and molecular biology of phenylpropanoid metabolism.Annu Rev Plant Physiol Plant Mol Biol 40:347-369
79.Hamiduzzaman MM,Jakab G,Barnavon L,Neuhaus JM,Mauch-Mani B(2005) β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling.Mol Plant-Microbe Interact 18:819-829
80.Hase S,Van Pelt JA,Van Loon LC,Pieterse CMJ(2003) Colonization of Arabidopsis roots by Pseudomonas fluorescens primes the plant to produce higher levels of ethylene upon pathogen infection.Physiol Mol Plant Pathol 62:219-226
81.Hayes MP,Enterline JC,Gerrard TL,Zoon KC(1991) Priming of human monocytes for enhanced lipopolysaccharide responses:Expression of α-interferon,interferon regulatory factors,and tumor necrosis factor.J Leukoc Biol 50:176-181
82.Hayes MP,Freeman SL,DonnelIy RP(1995b) IFN-γ priming of monocytes enhances LPS-induced TNF production by augmenting both transcription and mRNA stability.Cytokine 7:427-435
83.Hayes MP,Wang J,Norcross MA(1995a) Regulation of interleukin expression in human monocytes:Selective priming by interferon-gamma of lipopolysaccharide-inducible p35 and p40 genes.Blood 86:646-650
84.He SY,Bauer DW,Collmer A(1994) Hypersensitive response elicited by Erwinia arnylovora harpin requires active plant metabolism.Mol Plant-Microbe Interact 7:289-292
85.He Z,Li L,Luan S(2004) Immunophilins and parvulins.Superfamily of peptidyl prolyl isomerases in Arabidopsis.Plant Physiol 134:1248-1267
86.Heil M,Kost C(2006) Priming of indirect defences.Ecol Lett 9:813-817
87.Heintzen C,Fischer R,Melzer S,Kappeler K,Apel K,Staiger D(1994) Circadian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L.Plant Physiol 106:905-915
88.Hoefnagel MHN,Millar AH,Wiskich JT,Day DA(1995) Cytochrome and alternative respiratory pathways compete for electrons in the presence of pyruvate in soybean mitochondria.Arch Biochem Biophys 318:394-400
89.Hofius D,Tsitsigiannis DI,Jones JD,Mundy J(2007) Inducible cell death in plant immunity.Semin Cancer Biol 17:166-187
90.Huckelhoven R,Kogel KH(2003) Reactive oxygen intermediates in plant-microbe interactions:Who is who in powdery mildew resistance? Planta 216:891-902
91.Hukkanen AT,Kokko HI,Buchala AJ,McDougall GJ,Stewart D,Karenlampi SO,Karjalalnen RO(2007)Benzothiadiazole induces the accumulation of phenolics and improves resistance to powdery mildew in strawberries.J Agric Food Chem 55:1862-1870
92.Jabs T,Tschope M,Colling C,Hahlbrock K,Scheel D(1997) Elicitor-stimulated ion fluex and O_2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley.Proc Natl Acad Sci USA 94:4800-4805
93.Jacobson MD,Weil M,Raff MC(1997) Programmed cell death in animal development.Cell 88:347-354
94.Jakab G,Cottier V,Toquin V,Rigoli G,Zimmerli L,Metraux JP,Mauch-Mani B(2001) β-Aminobutyric acid-induced resistance in plants.Eur J Plant Pathol 107:29-37
95.Jakab G,Ton J,Flors V,Zimmerli L,Metraux JP,Mauch-Mani B(2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses.Plant Physiol 139:267-274
96.Japes T(1999) Reactive oxynen intermediates as mediators of programmed cell death in plants and animals. Biochern Phrurnacol 57:231-245
97.Jarosch B,Jansen M,Schaffrath U(2003) Acquired resistance functions in mlo barley,which is hypersusceptible to Magnaporthe grisea.Mol Plant-Microbe Interact 16:107-114
98.Jiang M,Zhang J(2001) Effect of abscisic acid on active oxygen species,antioxidative defense system and oxidative damage in leaves of maize seedlings.Plant Cell Physiol 42:1265-1273
99.Jimenez A,Hernandez JA,Delrio LA,Sevilla F(1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves.Plant Physiol 114:275-284
I00.Kang CH,Jung WY,Kang YH,Kirn JY,Kim DG,Jeong JC,Back DW,Jin JB,Lee JY,Kim MO(2006) AtBAG6,a novel calmodulin-binding protein,induces programmed cell death in yeast and plants.Cell Death Differ 13:84-95
101.Kariola T,Brader G,Li J,Palva ET(2005) Chlorophyllase l,a damagecontrol enzyme,affects the balance between defense pathways in plants.Plant Cell 17:282-294
102.Karpinski S,Gabrys H,Mateo A,Karpinska B,Mullineaux PM(2003) Light perception in plant disease defense signalling.Curt Opin Plant Biol 6:390-396
103.Karpinski S,Reynolds H Karpinska B,Wingsle G,Creissen G,Mullineaux P(1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis.Science 284:654-657
104.Karpova OV,Kuzmin EV,Elthon TE,Newton KJ(2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants.Plant Cell 14:3271-3284
105.Katz V,Fuchs A,Conrath U(2002) Pretreatment with salicylic acid primes parsley cells for enhanced ion transport following elicitation.FEBS Lett 520:53-57
106.Katz VA,Thulke OU,Conrath U(1998) A benzothiadiazole primes parsley cells for augmented elicitation of defense responses.Plant Physiol 117:1333-1339
107.Kauss H,Franke K,Krause K,Conrath U,Jeblick W,Grimmig B,Matern U(1993) Conditioning of Parsley (Petroselinum crispum L.) Suspension cells increases elicitor-induced incorporation of cell wall phenolics.Plant Physiol 102:459-466
108.Kauss H,Krause K,Jeblick W(1992) Methyl jasmonate conditions parsley suspension cells for increased elicitation of phenylpropanoid defense responses.Biochem Biophys Res Commun 189:304-308
109.Kauss H,Theisinger-Hinkel E,Mindermann K,Conrath U(1992) Dichloroisonicotinic and salicylic acid,inducers of systemic acquired resistance,enhance fungal elicitor responses in parsley cells.Plant J 2:655-660
110.Kawaguchi R,Girke T,Bray EA,Bailey-Serres JN(2004) Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana.Plant J 38:823-839
111.Kazufumi Yazaki(2006) ABC transporters involved in the transport of plant secondary metabolites.FEBS Letters 580:1183-1191
112.Keppler LD,Baker CJ,Atkinson MM(1989) Active oxygen production during a bacteria induced hypersensitive reaction in tobacco suspension cells.Phytopathology 79:974-978
113.Kessler A,Halitschke R,Diezel C,Baldwin IT(2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata.Oecologia 148:280-292
114.Khuri S,Bakker FT,Dunwell JM(2001) Phylogeny,function,and evolution of the cupins,a structurally conserved,functionally diverse superfamily of proteins.Mol Biol Evol 18:593-605
115.Kieffer F,Simo N,Plas F,Maume BF(1997) Tobacco cells contain a protein immuologically related to the neutrophil small G protein Rac2 and involved in elicitor-induced oxidation burst.FEB S Letter 403:149
116.Kim HJ,Triplett BA(2004) Cotton fiber germin-like protein.I.Molecular cloning and gene expression.Planta 218: 516-524
117. Kinal H, Park CM, Berry JO, Koltin Y, Bruenn JA (1995) Processing and secretion of a virally encoded antifungal toxin in transgenic tobacco plants: evidence for a Kex2p pathway in plants. Plant cell 7: 677-685
118. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97: 8849-8855
119. Klessig DF, Malamy J (1994) The salicylic acid signal in plants. Plant Mol Biol 26:1439-1458
120. Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugovieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130: 2152-2163
121. Koch M, Vorwerk S, Masur C, Sharifi-Sirchi G, Olivieri N, Schlaich NL (2006) A role for a flavin-containing mono-oxygenase in resistance against microbial pathogens in Arabidopsis. Plant J 47: 629-639
122. Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128: 1046-1056
123. Koncz C, Chua NH, Schell J (1992) Methods in Arabidopsis Research. World Scientific Press, Singapore.
124. Konrad A, Banze M, Follmann H (1996) Mitochondria of plant leaves contain two thioredoxins. Completion of the thioredoxin profile of higher plants. J Plant Physiol 149: 317-321
125. Krause M, Durner J (2004) Harpin inactivates mitochondria in Arabidopsis suspension cells. Mol Plant Microbe Interact 17:131-139
126. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141
127. Kuc J (1982) Induced immunity to plant disease. Bioscience 32: 854-860
128. Kuzniak E, Sklodowska M (2005) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222: 192-200
129. Kvaratskhelia M, George SJ, Thorneley RN (1997) Salicylic acid is a reducing substrate and not an effective inhibitor of ascorbate peroxidase. J Biol Chem 272:20998-21001
130. Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323-329
131. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275
132. Lane BG (2000) Oxalate oxidases and differentiating surface structure in wheat: germins. Biochem J 349:309-321
133. Lane BG, Bernier F, Dratewka-Kos E, Shafai R, Kennedy TD, Pyne C, Munro JR, Vaughan T, Walters D, Altomare F (1991) Homologies between members of the germin family in hexaploid wheat and similarities between these wheat germins and certain Physarum spherulins. J Biol Chem 266: 10461-10469
134. Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993) Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 268: 12239-12242
135. Langebartels C, Wohlgemuth H, Kschieschan S, Griin S, Sandermann H (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiol Biochem 40: 567-575
136. Laxa M, Konig J, Dietz KJ, Kandlbinder A (2007) Role of the cysteine residues in Arabidopsis thaliana cyclophilin CYP20-3 in peptidyl-prolyl cis-trans isomerase and redox-related functions. Biochem J 401: 287-297
137. Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression.Plant Cell 14:1235-1251
138.Legendre L,Reuter S,HeinsteinPF,Low PS(1993) Characterization of the oligogalacturodine-induced oxidative burst in cultured soybean(Glycine max) cells.Plant Physiol 102:223-240
139.Leon J,Lawton MA,Rasldn I(1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco.Plant Physiol 108:1673-1678
140.Levine A,Pennell R,Palmer R,Lamb CJ(1996) Calcium-mediated apoptosis in a plant hypersensitive response.Curt Biol 6:427437
141.Levine A,Tenhaken R,Dixon R,Lamb C(1994) H_2O_2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.Cell 79:583-593
142.Lin J,Wang Y,Wang G(2006) Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status.J Plant Physiol 163:731-739
143.Lorrain S,Vailleau F,Balague C,Roby D(2003) Lesion mimic mutants:keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263-271
144.Lou Y,Baldwin IT(2006) Silencing of a germin-like gene in Nicotiana attenuata improves performance of native herbivores.Plant Physiol 140:1126-36
145.Love AJ,Yun BW,Laval V,Loake GJ,Milner JL(2005) Cauliflower mosaic virus,a compatible pathogen of Arabidopsis,engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species.Plant Physiol 139:935-948
146.Mackernessa HS,Surplus SL,Blake P,John CF,Buchannan-wollaston V,Jordan BR,Thomas B(1999)Ultraviolet-B induced stress and changes in gene expression in Arabidopsis thaliana:role of signaling pathways controlled byjasmonic acid,ethylene and reactive oxygen species.Plant Cell and Env 22:1413-1423
147.Majande A,Finel M,Wikstrom M(1994) Dephenyleneiodonium inhibits reduction of iron-sulfur clusters in the mitochondrial NADH-ubiquonone oxidoreductase(Complex Ⅰ).J Biol Chem 269:21037-21042
148.Maldonado AM,Doerner P,Dixon RA,Lamb CJ,Cameron RK(2002) A putative lipid transfer protein involved in systemic resistance signaling in Arabidopsis.Nature 419:399-403
149.Manners JM,Penninckx IA,Vermaere K,Kazan K,Brown RL,Morgan A,Maclean DJ,Curtis MD,Cammue BP,Broekaert WF(1998) The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid.Plant Mol Biol 38:1071-1080
150.Marrsk A(1996) The functions and regulation of glutathione S-transferases in plants.Annu Rev Plant Physiol Plant Mol Bio 47:127-158
151.Mateo A,Muhlenbock P,Rusterucci C,Chi-Chen Chang C,Miszalski Z,Karpinska B,Parker JE,Mullineaux PM,Karpinski S(2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy.Plant Physiol 136:2818-2830
152.Mehdy MC(1994)Active oxygen species in plant defense against pathogens.Plant Physiol 105:467-472
153.Meloa MP,Roberts TH,Mφller IM(1996) Evidence for the presence of two rotenone-insensitive NAD(P)H dehydrogenases on the inner surface of the inner membrane of potato tuber mitochondria.Biochim Biophys Acta 1276:133-139
154.Membre N,Berna A,Neutelings G,David A,David H,Staiger D,Saez Vasquez J,Raynal M,Delseny M,Bernier F (1997) cDNA sequence,genomic organization and differential expression of three Arabidopsis genes for germin/oxalate oxidase-like proteins.Plant Mol Biol 35:459469
155.Membre N,Bernier F,Staiger D,Berna A(2000) Arabidopsis thaliana germin-like proteins:common and specific features point to a variety of functions. Planta 3: 345-54
156. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
157. Moeder W, Yoshioka K, Klessig DF (2005) Involvement of the small GTPase Rac in the defense responses of tobacco to pathogens. Mol Plant-Microbe Interact 18: 116-124
158. M(?)ller IM (2001) Plant mitochondrial and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561-591
159. M(?)ller IM (2002) A new dawn for plant mitochondrial NAD(P)H dehydrogenases. Trends Plant Sci 7: 235-7
160. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944
161. Mur, LAJ, Brown IR, Darby RM, Bestwick CS, Bi YM, Mansfield JW, Draper J (1996) Salicylic acid potentiates defense gene expression in tissue exhibiting acquired resistance to pathogen attack. Plant J 9: 559-571
162. Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Neuenschwander U, Vernooij B, Friedrich L, Uknes S, Kessmann H, Ryals J (1995) Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant J 8: 227-233
163. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237-1247
164. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53:1283-1304
165. Nurnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6: 372-379
166. Ono M, Sage-Ono K, Inoue M, Kamada H, Harada H (1996) Transient increase in the level of mRNA for a germin-like protein in leaves of the short-day plant Pharbitis nil during the photoperiodic induction of flowering. Plant Cell Physiol 37: 855-861
167. op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15: 2320-2332
168. Opassiri R, Pomthong B, Onkoksoong T, Akiyama T, Esen A, Ketudat Cairns JR (2006) Analysis of rice glycosyl hydrolase family 1 and expression of Os4bglu12 β-glucosidase. BMC Plant Biol 6: 33
169. Orozco-cardenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell13: 179-191
170. Overmyer K, Brosche M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinanen M, Saarma M, Scheel D, Kangasjarvi J (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol 137:1092-1104
171. Pare PW, Farag MA, Krishnamachari V, Zhang H, Ryu CM, Kloepper JW (2005) Elicitors and priming agents initiate plant defense responses. Photosynth Res 85: 149-159
172. Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139: 1291-1303
173. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406: 731-734
174. Peng M, Kuc J (1992) Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks.Phytopathology 82:696-699
175.Peng JL,Zhao J,Pan XM,Zhao JF,Dong HS,Wang JS(2002) Riboflavin activates growth signal transduction pathway in plants.J Nanjing Agric Univ 25:33-36
176.Pennell RI,Lamb C(1997) Programmed cell death in plants.Plant Cell 9:1157-1168
177.Piacenza L,Irigoin F,Alvarez MN,Peluffo G,Taylor MC,Kelly JM,Wilkinson SR,Radi R(2007) Mitochondrial superoxide radicals mediate programmed cell death in Trypanosoma cruzi:cytoprotective action of mitochondrial iron superoxide dismutase overexpression.Biochem J 403:323-334
178.Pieterse CM,Schaller A,Mauch-Mani B,Conrath U(2006) Signaling in plant resistance responses:divergence and cross-talk of defense Pathways.In:Tuzun S,Bent E,editors.Multigenic and induced systemic resistance in plants,Springer Science+Business Media,Inc,New York.
179.Pieterse CMJ,Van Pelt JA,Ton J,Parchmann S,Mueller MJ,Buchala AJ,Metraux JP,Van Loon LC(2000)Rhizobacteria-mediated induced systemic resistance(ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production.Physiol Mol Plant Pathol 57:123-134
180.Pieterse CMJ,Van Wees SCM,Ton J,Van Pelt JA,Van Loon LC(2002) Signaling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana.Plant Biol.4:535-544
181.Pieterse,CMJ,Van Wees SCM,Van Pelt JA,Knoester M,Laan R,Gerrits H,Weisbeek PJ,Van Loon LC(1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis.Plant Cell 10:1571-1580
182.Polidoros AN,Mylona PV,Scandalios JP(2001) Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress.Transgenic Res 10:555-569
183.Polle A(2001) Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling:computer simulations as a step towards flux analysis.Plant Physiol 126:445-462
184.Pourcel L,Routaboul JM,Cheynier V,Lepiniec L,Debeaujon I(2007) Flavonoid oxidation in plants:from biochemical properties to physiological functions.Trends Plant Sci 12:29-36
185.Pozo MJ,Cordier C,Dumas-Gaudot E,Gianinazzi,S,Barea JM,Azc6n-Aguilar C(2002) Localized vs.systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants.J Exp Bot 53:525-534
186.Pozo Mr,Van Loon,LC,Pieterse CMJ(2005) Jasmonates signals in plant-microbe interactions.J P/ant Growth Regul 23:211-222
187.Purvis AC,Shesfelt RL(1993) Does the alternative pathway ameliorate chilling injury insensitive plant tissues.Physiol Plant 88:712-718
188.Ramputh AI,Arnason JT,Cass L,Simmonds JA(2002) Reduced herbivory of the European tom borer(Ostrinia nubilalis) on corn transformedwith germin,a wheat oxalate oxidase gene.Plant Sci 162:431-440
189.Ran MV,Davis KR(2001) The physiology of ozone induced cell death.Planta 213:682-690
190.Rasmusson AG,Heiser VV,Zabaleta E,Brennicke A,Grohmann L(1998) Physiological,biochemical and molecular aspects of mitochondrial complex I in plants.Biochim Biophys Acta 1364:101-111
191.Ren D,Yang H,Zhang S(2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis.J Biol Chem 277:559-565
192.Reuber TL,Plotnikova JM,Dewdney J,Rogers EE,Wood W,Ausubel FM(1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants.Plant J 16:473-485
193.Rhoads DM,Umbach AL,Subbaiah CC,Siedow JN(2006) Mitochondrial reactive oxygen species.Contribution to oxidative stress and interorganellar signaling.Plant Physiol 141:357-366
194.Robson CA,Vanlerberghe GC(2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and-independent pathways of programmed cell death.Plant Physiol 129:1908-1920
195.Roje S(2007) Vitamin B biosynthesis in plants.Phytochemistry 68:1904-1921
196.Ryals,JA,Neuenschwander UH,Willits MG,Molina A,Steiner HY,Hunt M(1996) Systemic acquired resistance.Plant Cell 8:1809-1819
197.Ryu CM,Farag,MA,Hu CH,Reddy MS,Kloepper JW,Pare PW(2004) Bacterial volatiles induce systemic resistance in Arabidopsis.Plant Physiol 134:1017-1026
198.Samuel MA,Ellis BE(2002) Double jeopardy:both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive.Plant Cell 14:2059-2069
199.Scandalios JC(1993) Oxygen stress and superoxide dismutases.Plant Physiol 101:7-12
200.Schultheiss H,Dechert C,Kogel KH,Huckelhoven R(2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus.Plant J 36:589-601
201.Seki M,Ishida J,Narusaka M,Fujita M,Nanjo T,Umezawa T,Kamiya A,Nakajima M,Enju A,Sakurai T,Satou M,Akiyama K,Yamagnchi-Shinozaki K,Caminci P,Kawai J,Hayashizaki Y,Shinozaki K(2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray.Funct Integr Genomics 2:282-291
202.Sharma YK,Leon J,Raskin I,Davis KR(1996) Ozone-induced responses in Arabidopsis thaliana:the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance.Proc Natl Acad Sci USA 93:5595-5599
203.Shirasu K,Nakajima H,Rajasekhar VK,Dixon RA,Lamb CJ(1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms.Plant Cell 9:261-270
204.Shoresh M,Yedidia I,Chet I(2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203.Phytopathol 95:76-84
205.Stadnik M J,Buchenauer H(2000) Inhibition of phenylalanine ammonialyase suppresses the resistance induced by benzothiadiazole in wheat to Blumeria grarainis f.sp.tritici.Physiol Mol Plant Pathol 57:25-34
206.Staiger D,Apel K,Trepp G(1999) The Atger3 promoter confers circadian clock-regulated transcription with peak expression at the beginning of the night.Plant Mol Biol 40:873-882
207.Sticher L,Mauch-Mani B,Metraux JP(1997) Systemic acquired resistance.Annu Rev Phytopathol 35:235-270
208.Taheri P,Hofte M(2006) Riboflavin induces resistance in rice against Rhizoctonia sheath diseases by activating signal transduction pathways leading to upregulation of rice cationic peroxidase and formation of lignin as a structural barrier.Commun Agric Appl Biol Sci 71:255-258
209.Taipalensuu J,Falk A,Rask L(1996) A wound-and methyljasmonate-inducible transcript coding for a myrosinase-associated protein with similarities to an early nodulin.Plant Physiol 110:471-483
210.Tatiana E,Mishina,Jurgen Z(2006) The Arabidopsis flavin-dependent monooxygenase FMOl is an essential component of biologically induced systemic acquired resistance.Plant Physiol 141:1666-1675
211.Tobena-Santamaria R,Bliek M,Ljung K,Sandberg G,Mol JNM,Souer E,Koes R(2002) FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture.Genes Dev 16:753-763
212.Ton J,Jakab G,Toquin V,Flors V,Iavicoli A,Maeder MN,Metraux JP,Mauch-Mani B(2005) Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis.Plant Cell 17:987-999
213.Ton J,Mauch-Mani B(2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose.Plant J 38:119-130
214.Torres MA,Dangl JL(2005) Functions of the respiratory burst oxidase in biotic interactions,abiotic stress and development.Curr Opin Plant Biol 8:397403
215.Tortes MA,Jones JD,Dangl JL(2005) Pathogen-induced,NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana.Nat Genet 37:1130-1134
216.Truman W,Bennett MH,Kubigsteltig I,Turnbull C,Grant M(2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates.Proc Nail Acad Sci USA 104:1075-1080
217.Uhmsov T,Ohmiya A,Ha G,Guifoyle T(1995) The soybean GH2/4 gene that encode a glutathione S-transferase has a promoter that is activated by a wide range of chemical agents.Plant Physiol 108:919-927
218.Vallelian-bindschedler L,Mosinger E,Metraux JP,Schweizer P(1998) Structure,expression and localization of a germin-like protein in barley(Hordeura vulgare L.) that is insolubilized in stressed leaves.Plant Mol Biol 37:297-308
219.Van Breusegem F,Dat JF(2006) Reactive oxygen species in plant cell death.Plant Physiol 141:384-390
220.van der Merwe JA,Dubery IA(2006) Benzothiadiazole inhibits mitochondrial NADH:ubiquinone oxidoreductase in tobacco.J Plant Physiol 163:877-882
221.van Hulten M,Pelser M,van Loon LC,Pieterse CM,Ton J(2006) Costs and benefits of priming for defense in Arabidopsis.Proc Natl Acad Sci USA 103:5602-5607
222.Van Loon LC,Bakker PAHM,Pieterse CMJ(1998) Systemic resistance induced by rhizosphere bacteria.Annu Rev Phytopatho136:453-483
223.van Loon LC,van Strein EA(1999) The families of pathogenesis-related proteins,their activities,and comparative analysis of PR-1 type proteins.Physiol Mol Plant Pathol 55:85-97
224.Van Peer R,Niemann GJ,Schippers B(1991) Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp.strain WCS417r.Phytopathology 81:728-734
225.Vanlerberghe GC,Mcintosh L(1997) Alternative oxidase:from gene to function.Annu Rev Plant Physiol Plant Molec Biol 48:703-34
226.Verhagen BWM,Glazebrook J,Zhu T,Chang HS,van Loon LC,Pieterse,CMJ(2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis.Mol Plant-Microbe Interact 17:895-908
227.Vranova E,Langebartels C,Vanmontagu M,Inze D,Van cam PW(2000) Oxidative stress,heat shock and drought differentially affect expression of a tobacco protein phosphatase 2C.J Exp B or 51:1763-1764
228.Wagner AM(1995) A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells.FEBS Lett 368:339-342
229.Wagner D,Przybyla D,op den Camp R,Kim C,Landgraf F,Lee KP,Wusch M,Laloi C,Nater M,Hideg E(2004)The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana.Science 306:1183-1185
230.Wang Z,Xie W,Chi F,Li C(2005) Identification of non-specific lipid transfer protein-1 as a calmodulin-binding protein in Arabidopsis.FEBS Lett 579:1683-1687
231.Xie Z,Chen Z(1999) Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells.Plant Physiol 120:217-226
232.Xie Z,Chen Z(2000) Harpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells.Mol Plant-Microbe Interact 13:183-190
233.Xing T,Higgins VJ,Blumwal DE(1997) Race specific elicitors of Cladosporium fulvum promote translocation of eytosolie components of NADPH oxidase to the plasm membrane of tomato cell.Plant Cell 9:249-259
234.Xu Z,Escamilla-Trevino L,Zeng L,Lalgondar M,Bevan D,Winkel B,Mohamed A,Cheng CL,Shih MC,Poulton J,Esen A(2004) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1.Plant Mol Biol 55:343-367
235.Yao N,Eisfelder BJ,Marvin J,Greenberg JT(2004) The mitochondrion-an organelle commonly involved in programmed cell death in Arabidopsis thaliana.Plant J 40:596-610
236.Yao N,Tada Y,Sakamoto M,Nakayashiki H,Park P,Tosa Y,Mayama S(2002) Mitochondrial oxidative burst involved in apoptotic response in oats.Plant J 30:567-579
237.Yoshinaga K,Arimura SI,Niwa Y,Tsutsumi N,Uchimiya H,Kawai-Yamada M(2005) Mitochondrial behaviour in the early stages of ROS stress leading to cell death in Arabidopsis thaliana.Ann Bot(Lond) 96:337-342
238.Zago E,Morsa S,Dat JF,Alard P,Ferrarini A,Inze' D,Delledonne M,Van Breusegem F(2006) Nitric oxide-and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco.Plant Physiol 141:404-411
239.Zeier J,Delledonne M,Mishina T,Severi E,Sonoda M,Lamb CJ(2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions.Plant Physiol 136:2875-2886
240.Zhang Q,Mischis L,Wiskich JT(1996) Respiratory responses of pea and wheat seedlings to chloramphenicol treatment.Aust J Plant Physiol 23:683-692
241.Zhang Z,Collinge DB,Thordal-Christensen H(1995) Germin-like OxO,a H_2O_2-producing enzyme,accumulates in barley attacked by the powery mildew fungus.Plant J 8:139-145
242.Zhao Y,Christensen SK,Fankhauser C,Cashman JR,Cohen JD,Weigel D,Chory J(2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis.Science 291:306-309
243.Zhou F,Zhang Z,Gregersen PL,Mikkelsen JD,de Neergaard E,Collinge D,Thordal-Christensen H(1998)Molecular characterization of the oxalate oxidase involved in the response of barley to the powery mildew fungus.Plant Physiol 117:33-41
244.杜秀敏,殷文璇,赵彦修(2001)植物中活性氧的产生和清除.中同生物技术杂志17:121-125
245.方中达(1998)植病研究方法.中国农业出版社
246.贾琴(2007)核黄素受体蛋白对植物开花转型和抗病防卫调控作用的初步研究.硕士学位论文,南京农业大学
247.彭建令(2003)两类激发子(harpins和核黄素)启动植物抗病防卫和生长信号传导的分子遗传学解析.博士学位论文,南京农业大学
248.王颖(2004)中华鳖核黄素受体基因的克隆和在转基因植物中的表达.硕士学位论文,南京农业大学
249.闻伟刚(2001)水稻黄单胞菌过敏性反应激发子的研究.博士学位论文,南京农业大学
250.夏侯珍珠(2007)核黄素受体蛋白与HpaG_(Xoo)蛋白对植物生长与防卫反应的影响.硕士学位论文,南京农业大学
2.Ahlfors R,Lang S,Overmyer K,Jaspers P,Brosche M,Tauriainen A,Kollist H,Tuominen H,Belles-Boix E,Piippo M(2004) Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid,ethylene,and methyl jasmonate responses.Plant Cell 16:1925-1937
3.Ahn IP,Kim S,Lee YH(2005) Vitamin B1 functions as an activator of plant disease resistance.Plant Physiol 138:1505-1515
4.Ahn IP,Kim S,Lee YH,Suh SC(2007) Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis.Plant Physiol 143:838-848
5.Ahn IP,Lee SW,Suh SC(2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene,jasmonic acid,and NPR1.Mol Plant Microbe Interact 20:759-768
6.Alvarez ME,Pennell RI,Meijer,P-J,Ishikawa A,Dixon RA,Lamb C(1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.Cell 92:773-784
7.Amirsadeghi S,Robson CA,Vanlerberghe GC(2007) The role of the mitochondrion in plant responses to biotic stress.Physiologia Plantarum 159:2539-266
8.Apel K,Hirt H(2004) Reactive oxygen species:metabolism,oxidative stress,and signal transduction.Annu Rev Plant Biol 55:373-399
9.Auh C-K,Murphy TM(1995) Plasma membrane redox enzyme is involved in the synthesis of O_2~- and H_2O_2 by Phytophthora elicitor-stimulated rose cells.Plant Physiol 107:1241-1247
10.Avdiushiko SA,Ye XS,Hildebrand DF(1993) Induction of lipoxygenasa activity in immunized cucumber plants.Physiol Mol Plant Patho 142:83
11.Aver'yanov AA,Lapikova VP,Nikolaev ON,Stepanov AI(2000) Active oxygen-associated control of rice blast disease by riboflavin and roseoflavin.Biochemistry(Mosc) 65:1292-1298
12.Baker CJ,Orlandi EW,Mock NM(1993) Harpin,an elicitor of the hypersensitive response in tobacco caused by Erwinia amylovora,elicits active oxygen production in suspension cells.Plant Physiol 102:1341-1344
13.Baldwin IT(1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations.Proc Natl Acad Sci USA 95:8113-8118
14.Banze M,Follmann H(2000) Organelle-specific NADPH thioredoxin reductase in plant mitochondria.J Plant Physiol 156:126-129
15.Barrientos A,Moraes CT(1999) Titrating the effects of mitochondrial complex I impairment in the cell physiology.J Biol Chem 274:16188-16197
16.Beckers GJ,Conrath U(2007) Priming for stress resistance:from the lab to the field.Curt Opin Plant Biol 10:425-31
17.Beckman KB,Ames BN(1997) Oxidative decay of DNA.J Biol Chem 272:19633-19636
18.Benhamou N,Kloepper JW,Quadt-Hallman A,Tuzun S(1996) Induction of defense-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria.Plant Physiol 112:919-929
19.Berlett BS,Stadtman ER(1997) Protein oxidation in aging disease,and oxidative stress.J Biol Chem 272:20313-20316
20.Berna A,Bernier F(1997) Regulated expression of a wheat germin gene in tobacoo:oxalate oxidase activity and apoplastic localization of the heterologous protein.Plant Mol Bio 33:417-429
21.Bernier F,Berna A(2001) Germins and germin-like proteins:plant do-all proteins.But what do they do exactly?Plant Physiol Biochem 39:545-554
22.Bethke PC Jones RL(2001) Cell death of barley aleurone protoplastsis mediated by reactive oxygen species.Plant J 25:19-29
23.Blume B,Nurnberger T,Nass N,Scheel D(2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley.Plant Cell 12:1425-1440
24.Bolwell GP,Davies DR,Gerrish C,Auh CK,Murphy TM(1998) Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms.Plant Physiol 116:1379-1385
25.Bowler C,Fluhr R(2000) The role of calcium and activated oxygen as signals for controlling cross-tolerance.Trends Plant Sci 5:241-245
26.Brian Olszak,FGMa,Peter Brodersen,Morten Grell,Henfiette Giese,Morten Petersen,John Mundy(2006) A putative flavin-containing mono-oxygenase as a marker for certain defense and cell death pathways.Plant Sci 170:614-623
27.Bright J,Desikan R,Hancock JT,Weir IS,Neill SJ(2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H_2O_2 synthesis.Plant J 45:113-122
28.Buhot N,Gomes E,Milat ML,Ponchet M,Marion D,Lequeu J,Delrot S,Coutos-Thevenot P,Blein JP(2004)Modulation of the biological activity of a tobacco LTP1 by lipid complexation.Mol Biol Cell 15:5047-5052
29.Can H,Bowling SA,Gordon AS,Dong X(1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance.Plant Cell 8:1583-1592
30.Carter C,Graham RA,Thornburg RW(1998) Arabidopsis thaliana contains a large family of germin-like proteins:characterization of cDNA and genomic sequences encoding 12 unique family members.Plant Mol Biol 38:929-943
31.Cashman JR(2002) Human and plant flavin-containing monooxygenase Noxygenation of amines:detoxication vs.bioactivatiort,Drug.Metab Rev 34:513-521
32.Chamnongpol S,Willfkens H,Moeder W,Langebartels C,Sandermannj H,Vanmontagu M,Inze D,VAN Cam PW(1998) Defense activation and enhanced pathogen tolerance induced by H_2O_2 intransgenic plants.Proc Natl Acad Sci USA 95:5818-5823
33.Chen S,Dickman MB(2004) Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides.J Exp Bot 55:2617-2623
34.Chen TY,Lei MG,Suzuki T,Morrison DC(1992) Lipopolysaccharide receptors and signal transduction pathways in mononuclear phagocytes.Curr Top Micro Immunol 181:169-188
35.Chen Z,Silva H,Klessig DF(1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.Science 262:1883-1886
36.Chisholm ST,Mahajan SK,Whitman SA,Yamamoto ML,Carrington,JC(2000) Cloning of the Arabidopsis RTM1gene,which controls restriction of long-distance movement of tobacco etch virus.Proc Nail Acad Sci USA 97:489-494
37.Clarke SF,Guy PL,Burritt DJ,Jameson PE(2002) Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment.Physiol Plant 114:157-164
38.Conrath U,Beckers GJ,Flors V,Garcia-Agustin P,Jakab G.Mauch F,Newman MA,Pieterse CM,Poinssot B,Pozo MJ,Pugin A,Schaffrath U,Ton J,Wendehenne D,Zimmerli L,Mauch-Mani B(2006) Priming:getting ready for battle.Mol Plant-Microbe Interact 19:1062-1071
39.Cortrath U,Pieterse CM,Mauch-Mani B(2002) Priming in plant-pathogen interactions.Trends Plant Sci 7:210-216
40.Danon A,Miersch O,Felix G,op den Camp RGL,Apel K(2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana.Plant J 41:68-80
41.Dat JF,Pellinen R,Beeckman T,Van De Cotte B,Langebartels C,Kangasjarvi J,Inze D,Van Breusegem F(2003)Changes in hydrogen peroxide homeostasis triger an active cell death process in tobacco.Plant J 33:621-632
42.Davey MW,Gilot C,Persiau G,Ostergaard J,Han Y(1999) Ascorbate biosynthesis in Arabidopsis cells uspension cultures.Plant Physiol 121:535-543
43.De Luca V,St-Pierre B(2000) The cell and developmental biology of alkaloid biosynthesis.Trends Plant Sci 5:168-173
44.Dean M,Rzhetsky A,Allikmets R(2001) The human ATP-binding cassette(ABC) transporter superfamily.Genome Res 11:1156-1166
45.Delaney TP(1997) Genetic dissection of acquired resistance to disease.Plant Physiol 113:5-12
46.Delaney TP,Friedrich L,Ryals J(1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.Proc Natl Acad Sci USA 92:6602-6606
47.Delaney TP,Uknes S,Vemooij B,Friedrich L,Weymann K,Negrotto D,Gaffney T,Gut-Rella M,Kessmann H,Ward E,Ryals J(1994) A central role of salicylic acid in plant disease resistance.Science 266:1247-1250
48.Delledonne M,Zeier J,Marocco A,Lamb CJ(2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response.Proc Natl Acad Sci USA 98:13454-13459
49.Dempsey DA,Shah J,Klessig DF(1999) Salicylic acid and disease resistance in plants.Crit Rev Plant Sci 18:547-575
50.Desikan R,Cheung MK,Bright J,Henson D,Hancock JT,Neill SJ(2004) ABA,hydrogen peroxide and nitric oxide signalling in stomatal guard cells.J Exp Bot 55:205-212
51.Desikan R,Hancock JT,Bright J,Harrison J,Weir I,Hooley R,Neill SJ(2005) A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells.Plant Physiol 137:831-834
52.Desikan R,Hancock JT,Ichimura K,Shinozaki K,Neill SJ(2001) Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6.Plant Physiol 126:1579-1587
53.Desikan R,Mackerness SAH,Hancock JT,Neill SJ(2001) Regulation of the Arabidopsis transcriptome by oxidative stress.Plant Physiol 127:159-172
54.Desikan R,Reynolds A,Hancock JT,Neill SJ(1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defense gene expression in Arabidopsis suspension cultures.Biochem J 330:115-120
55.Doke N(1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of phytophthora infestans and to the hyphal wall components.Physiol Plant Pathol 23:345-357
56.Dong HS,Beer SV(2000) Riboflavin induces disease resistance in plants by activating a novel signal transduction pathway.Phytopathology 90:801-811
57.Dorey S,Kopp M,Geoffroy P,Fritig B,Kauffrnann S(1999) Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction,phenylalanine ammonia lyase stimulation,salicylic acid accumulation or scopoletin consumption in cultured tobacco cells treated with elicitor.Plant Physiol 121:163-173
58.Durner J,Klessig DF(1995) Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses.Proc Natl Acad Sci USA 92:11312-11316
59.Durrant WE,Dong X(2004) Systemic acquired resistance.Annu Rev Phytopathol 42:185-209
60.Epple P,Mack AA,Morris VRF,Dangl JL(2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related,plant specific zinc finger proteins.Proc Natl Acad Sci USA 100:6831-6836
61.Eshdat Y,Holland D,Faltin Z,Benhayyim G(1997) Plant glutathione peroxidases.Physiol Plant 100:234-240
62.Etienne P,Petitot AS,Houot V,Blein JP,Suty L(2000) Induction of tcI7,a gene encoding a β-subunit of proteasome,in tobacco plants treated with elicitin,salicylic acid or hydrogen peroxide.FEBS Lett 466:213-218
63.Fowler S,Thomashow MF(2002) Arabidopsis transeriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway.The Plant Cell 14:1675-1690
64.Foyer CH,Lopez-delgado H,Dat JF,Scitt IM(1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling.Physiol Plant 100:241-254
65.Foyer CH,Noctor G(2005) Redox homeostasis and antioxidant signaling:a metabolic interface between stress perception and physiological responses.Plant Cell 17:1866-1875
66.Friedrich L,Lawton K,Ruess W,Masner P,Specker N,Gut-Rella M.Meier B,Dincher S,Staub T,Uknes S,Kessmaun H,Ryals J(1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco.Plant J 10:61-70
67.Friedrich L,Lawton K,RuessW,Masher P,Specker N,RellaMG,Meier B,Gachomo WE,Shonukan OO,Kotchoni OS(2003) The molecular initiation and subsequent acquisition of disease resistance in plants.Afr J Biotechnol 2:26-32
68.Ge X,Chen J,Li N,Lin Y,Sun C,Cao K(2003) Resistance function of rice lipid transfer protein LTP110.J Biochem Mol Biol 36:603-607
69.Ge X,Li GJ,Wang SB,Zhu H,Zhu T,Wang X,Xia Y(2007) AtNUDT7,a negative regulator of basal immunity in Arabidopsis,modulates two distinct defense response pathways and is involved in maintaining redox homeostasis.Plant Physiol 145:204-215
70.Gerhardt P,Murray RGE,Costilow RN,Nester EW,Wood WA,Krieg NR,Phillips GB(1981) Manual of Methods for General Bacteriology.American Society for Microbiology,Washington,D.C
71.Gothel SF,Marahiel MA(1999) Peptidyl-prolyl cis-trans isomerases,a superfamily of ubiquitous folding catalysts.Cell Mol Life Sci 55:423-436
72.Govrin E,Levine A(2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea.Curr Biol 10:751-757
73.Grant JJ,Loake GJ(2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance.Plant Physiol 124:21-29
74.Grant JJ,Yun BW,Loake GJ(2000) Oxidative burst and cognate redox signaling reported by luciferase imaging:identification of a signal network that functions independently of ethylene,SA and Me-JA but is dependent on MAPKK activity.Plant J 24:569-582
75.Green R,Fluhr R(1995) UV-B-induced PR-1 accumulation is mediated by active oxygen species.Plant Cell 7:203-212
76.Grivermikova VG,Vinogradov AD(2006) Generation of superoxide by the mitochondrial Complex I.Biochim Biophys Acta 1757:553-561
77.Guanl M,Scandallos JG(2000) Hydrogen peroxide-mediated catalase gene expression in response to wounding.Free Radical Biology and Medicine 28:1182-1190
78.Hahlbrock K,Scheel D(1989) Physiology and molecular biology of phenylpropanoid metabolism.Annu Rev Plant Physiol Plant Mol Biol 40:347-369
79.Hamiduzzaman MM,Jakab G,Barnavon L,Neuhaus JM,Mauch-Mani B(2005) β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling.Mol Plant-Microbe Interact 18:819-829
80.Hase S,Van Pelt JA,Van Loon LC,Pieterse CMJ(2003) Colonization of Arabidopsis roots by Pseudomonas fluorescens primes the plant to produce higher levels of ethylene upon pathogen infection.Physiol Mol Plant Pathol 62:219-226
81.Hayes MP,Enterline JC,Gerrard TL,Zoon KC(1991) Priming of human monocytes for enhanced lipopolysaccharide responses:Expression of α-interferon,interferon regulatory factors,and tumor necrosis factor.J Leukoc Biol 50:176-181
82.Hayes MP,Freeman SL,DonnelIy RP(1995b) IFN-γ priming of monocytes enhances LPS-induced TNF production by augmenting both transcription and mRNA stability.Cytokine 7:427-435
83.Hayes MP,Wang J,Norcross MA(1995a) Regulation of interleukin expression in human monocytes:Selective priming by interferon-gamma of lipopolysaccharide-inducible p35 and p40 genes.Blood 86:646-650
84.He SY,Bauer DW,Collmer A(1994) Hypersensitive response elicited by Erwinia arnylovora harpin requires active plant metabolism.Mol Plant-Microbe Interact 7:289-292
85.He Z,Li L,Luan S(2004) Immunophilins and parvulins.Superfamily of peptidyl prolyl isomerases in Arabidopsis.Plant Physiol 134:1248-1267
86.Heil M,Kost C(2006) Priming of indirect defences.Ecol Lett 9:813-817
87.Heintzen C,Fischer R,Melzer S,Kappeler K,Apel K,Staiger D(1994) Circadian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L.Plant Physiol 106:905-915
88.Hoefnagel MHN,Millar AH,Wiskich JT,Day DA(1995) Cytochrome and alternative respiratory pathways compete for electrons in the presence of pyruvate in soybean mitochondria.Arch Biochem Biophys 318:394-400
89.Hofius D,Tsitsigiannis DI,Jones JD,Mundy J(2007) Inducible cell death in plant immunity.Semin Cancer Biol 17:166-187
90.Huckelhoven R,Kogel KH(2003) Reactive oxygen intermediates in plant-microbe interactions:Who is who in powdery mildew resistance? Planta 216:891-902
91.Hukkanen AT,Kokko HI,Buchala AJ,McDougall GJ,Stewart D,Karenlampi SO,Karjalalnen RO(2007)Benzothiadiazole induces the accumulation of phenolics and improves resistance to powdery mildew in strawberries.J Agric Food Chem 55:1862-1870
92.Jabs T,Tschope M,Colling C,Hahlbrock K,Scheel D(1997) Elicitor-stimulated ion fluex and O_2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley.Proc Natl Acad Sci USA 94:4800-4805
93.Jacobson MD,Weil M,Raff MC(1997) Programmed cell death in animal development.Cell 88:347-354
94.Jakab G,Cottier V,Toquin V,Rigoli G,Zimmerli L,Metraux JP,Mauch-Mani B(2001) β-Aminobutyric acid-induced resistance in plants.Eur J Plant Pathol 107:29-37
95.Jakab G,Ton J,Flors V,Zimmerli L,Metraux JP,Mauch-Mani B(2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses.Plant Physiol 139:267-274
96.Japes T(1999) Reactive oxynen intermediates as mediators of programmed cell death in plants and animals. Biochern Phrurnacol 57:231-245
97.Jarosch B,Jansen M,Schaffrath U(2003) Acquired resistance functions in mlo barley,which is hypersusceptible to Magnaporthe grisea.Mol Plant-Microbe Interact 16:107-114
98.Jiang M,Zhang J(2001) Effect of abscisic acid on active oxygen species,antioxidative defense system and oxidative damage in leaves of maize seedlings.Plant Cell Physiol 42:1265-1273
99.Jimenez A,Hernandez JA,Delrio LA,Sevilla F(1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves.Plant Physiol 114:275-284
I00.Kang CH,Jung WY,Kang YH,Kirn JY,Kim DG,Jeong JC,Back DW,Jin JB,Lee JY,Kim MO(2006) AtBAG6,a novel calmodulin-binding protein,induces programmed cell death in yeast and plants.Cell Death Differ 13:84-95
101.Kariola T,Brader G,Li J,Palva ET(2005) Chlorophyllase l,a damagecontrol enzyme,affects the balance between defense pathways in plants.Plant Cell 17:282-294
102.Karpinski S,Gabrys H,Mateo A,Karpinska B,Mullineaux PM(2003) Light perception in plant disease defense signalling.Curt Opin Plant Biol 6:390-396
103.Karpinski S,Reynolds H Karpinska B,Wingsle G,Creissen G,Mullineaux P(1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis.Science 284:654-657
104.Karpova OV,Kuzmin EV,Elthon TE,Newton KJ(2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants.Plant Cell 14:3271-3284
105.Katz V,Fuchs A,Conrath U(2002) Pretreatment with salicylic acid primes parsley cells for enhanced ion transport following elicitation.FEBS Lett 520:53-57
106.Katz VA,Thulke OU,Conrath U(1998) A benzothiadiazole primes parsley cells for augmented elicitation of defense responses.Plant Physiol 117:1333-1339
107.Kauss H,Franke K,Krause K,Conrath U,Jeblick W,Grimmig B,Matern U(1993) Conditioning of Parsley (Petroselinum crispum L.) Suspension cells increases elicitor-induced incorporation of cell wall phenolics.Plant Physiol 102:459-466
108.Kauss H,Krause K,Jeblick W(1992) Methyl jasmonate conditions parsley suspension cells for increased elicitation of phenylpropanoid defense responses.Biochem Biophys Res Commun 189:304-308
109.Kauss H,Theisinger-Hinkel E,Mindermann K,Conrath U(1992) Dichloroisonicotinic and salicylic acid,inducers of systemic acquired resistance,enhance fungal elicitor responses in parsley cells.Plant J 2:655-660
110.Kawaguchi R,Girke T,Bray EA,Bailey-Serres JN(2004) Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana.Plant J 38:823-839
111.Kazufumi Yazaki(2006) ABC transporters involved in the transport of plant secondary metabolites.FEBS Letters 580:1183-1191
112.Keppler LD,Baker CJ,Atkinson MM(1989) Active oxygen production during a bacteria induced hypersensitive reaction in tobacco suspension cells.Phytopathology 79:974-978
113.Kessler A,Halitschke R,Diezel C,Baldwin IT(2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata.Oecologia 148:280-292
114.Khuri S,Bakker FT,Dunwell JM(2001) Phylogeny,function,and evolution of the cupins,a structurally conserved,functionally diverse superfamily of proteins.Mol Biol Evol 18:593-605
115.Kieffer F,Simo N,Plas F,Maume BF(1997) Tobacco cells contain a protein immuologically related to the neutrophil small G protein Rac2 and involved in elicitor-induced oxidation burst.FEB S Letter 403:149
116.Kim HJ,Triplett BA(2004) Cotton fiber germin-like protein.I.Molecular cloning and gene expression.Planta 218: 516-524
117. Kinal H, Park CM, Berry JO, Koltin Y, Bruenn JA (1995) Processing and secretion of a virally encoded antifungal toxin in transgenic tobacco plants: evidence for a Kex2p pathway in plants. Plant cell 7: 677-685
118. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97: 8849-8855
119. Klessig DF, Malamy J (1994) The salicylic acid signal in plants. Plant Mol Biol 26:1439-1458
120. Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugovieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130: 2152-2163
121. Koch M, Vorwerk S, Masur C, Sharifi-Sirchi G, Olivieri N, Schlaich NL (2006) A role for a flavin-containing mono-oxygenase in resistance against microbial pathogens in Arabidopsis. Plant J 47: 629-639
122. Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128: 1046-1056
123. Koncz C, Chua NH, Schell J (1992) Methods in Arabidopsis Research. World Scientific Press, Singapore.
124. Konrad A, Banze M, Follmann H (1996) Mitochondria of plant leaves contain two thioredoxins. Completion of the thioredoxin profile of higher plants. J Plant Physiol 149: 317-321
125. Krause M, Durner J (2004) Harpin inactivates mitochondria in Arabidopsis suspension cells. Mol Plant Microbe Interact 17:131-139
126. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141
127. Kuc J (1982) Induced immunity to plant disease. Bioscience 32: 854-860
128. Kuzniak E, Sklodowska M (2005) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222: 192-200
129. Kvaratskhelia M, George SJ, Thorneley RN (1997) Salicylic acid is a reducing substrate and not an effective inhibitor of ascorbate peroxidase. J Biol Chem 272:20998-21001
130. Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323-329
131. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275
132. Lane BG (2000) Oxalate oxidases and differentiating surface structure in wheat: germins. Biochem J 349:309-321
133. Lane BG, Bernier F, Dratewka-Kos E, Shafai R, Kennedy TD, Pyne C, Munro JR, Vaughan T, Walters D, Altomare F (1991) Homologies between members of the germin family in hexaploid wheat and similarities between these wheat germins and certain Physarum spherulins. J Biol Chem 266: 10461-10469
134. Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993) Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 268: 12239-12242
135. Langebartels C, Wohlgemuth H, Kschieschan S, Griin S, Sandermann H (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiol Biochem 40: 567-575
136. Laxa M, Konig J, Dietz KJ, Kandlbinder A (2007) Role of the cysteine residues in Arabidopsis thaliana cyclophilin CYP20-3 in peptidyl-prolyl cis-trans isomerase and redox-related functions. Biochem J 401: 287-297
137. Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression.Plant Cell 14:1235-1251
138.Legendre L,Reuter S,HeinsteinPF,Low PS(1993) Characterization of the oligogalacturodine-induced oxidative burst in cultured soybean(Glycine max) cells.Plant Physiol 102:223-240
139.Leon J,Lawton MA,Rasldn I(1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco.Plant Physiol 108:1673-1678
140.Levine A,Pennell R,Palmer R,Lamb CJ(1996) Calcium-mediated apoptosis in a plant hypersensitive response.Curt Biol 6:427437
141.Levine A,Tenhaken R,Dixon R,Lamb C(1994) H_2O_2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.Cell 79:583-593
142.Lin J,Wang Y,Wang G(2006) Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status.J Plant Physiol 163:731-739
143.Lorrain S,Vailleau F,Balague C,Roby D(2003) Lesion mimic mutants:keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263-271
144.Lou Y,Baldwin IT(2006) Silencing of a germin-like gene in Nicotiana attenuata improves performance of native herbivores.Plant Physiol 140:1126-36
145.Love AJ,Yun BW,Laval V,Loake GJ,Milner JL(2005) Cauliflower mosaic virus,a compatible pathogen of Arabidopsis,engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species.Plant Physiol 139:935-948
146.Mackernessa HS,Surplus SL,Blake P,John CF,Buchannan-wollaston V,Jordan BR,Thomas B(1999)Ultraviolet-B induced stress and changes in gene expression in Arabidopsis thaliana:role of signaling pathways controlled byjasmonic acid,ethylene and reactive oxygen species.Plant Cell and Env 22:1413-1423
147.Majande A,Finel M,Wikstrom M(1994) Dephenyleneiodonium inhibits reduction of iron-sulfur clusters in the mitochondrial NADH-ubiquonone oxidoreductase(Complex Ⅰ).J Biol Chem 269:21037-21042
148.Maldonado AM,Doerner P,Dixon RA,Lamb CJ,Cameron RK(2002) A putative lipid transfer protein involved in systemic resistance signaling in Arabidopsis.Nature 419:399-403
149.Manners JM,Penninckx IA,Vermaere K,Kazan K,Brown RL,Morgan A,Maclean DJ,Curtis MD,Cammue BP,Broekaert WF(1998) The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid.Plant Mol Biol 38:1071-1080
150.Marrsk A(1996) The functions and regulation of glutathione S-transferases in plants.Annu Rev Plant Physiol Plant Mol Bio 47:127-158
151.Mateo A,Muhlenbock P,Rusterucci C,Chi-Chen Chang C,Miszalski Z,Karpinska B,Parker JE,Mullineaux PM,Karpinski S(2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy.Plant Physiol 136:2818-2830
152.Mehdy MC(1994)Active oxygen species in plant defense against pathogens.Plant Physiol 105:467-472
153.Meloa MP,Roberts TH,Mφller IM(1996) Evidence for the presence of two rotenone-insensitive NAD(P)H dehydrogenases on the inner surface of the inner membrane of potato tuber mitochondria.Biochim Biophys Acta 1276:133-139
154.Membre N,Berna A,Neutelings G,David A,David H,Staiger D,Saez Vasquez J,Raynal M,Delseny M,Bernier F (1997) cDNA sequence,genomic organization and differential expression of three Arabidopsis genes for germin/oxalate oxidase-like proteins.Plant Mol Biol 35:459469
155.Membre N,Bernier F,Staiger D,Berna A(2000) Arabidopsis thaliana germin-like proteins:common and specific features point to a variety of functions. Planta 3: 345-54
156. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
157. Moeder W, Yoshioka K, Klessig DF (2005) Involvement of the small GTPase Rac in the defense responses of tobacco to pathogens. Mol Plant-Microbe Interact 18: 116-124
158. M(?)ller IM (2001) Plant mitochondrial and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561-591
159. M(?)ller IM (2002) A new dawn for plant mitochondrial NAD(P)H dehydrogenases. Trends Plant Sci 7: 235-7
160. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944
161. Mur, LAJ, Brown IR, Darby RM, Bestwick CS, Bi YM, Mansfield JW, Draper J (1996) Salicylic acid potentiates defense gene expression in tissue exhibiting acquired resistance to pathogen attack. Plant J 9: 559-571
162. Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Neuenschwander U, Vernooij B, Friedrich L, Uknes S, Kessmann H, Ryals J (1995) Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant J 8: 227-233
163. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237-1247
164. Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53:1283-1304
165. Nurnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6: 372-379
166. Ono M, Sage-Ono K, Inoue M, Kamada H, Harada H (1996) Transient increase in the level of mRNA for a germin-like protein in leaves of the short-day plant Pharbitis nil during the photoperiodic induction of flowering. Plant Cell Physiol 37: 855-861
167. op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15: 2320-2332
168. Opassiri R, Pomthong B, Onkoksoong T, Akiyama T, Esen A, Ketudat Cairns JR (2006) Analysis of rice glycosyl hydrolase family 1 and expression of Os4bglu12 β-glucosidase. BMC Plant Biol 6: 33
169. Orozco-cardenas ML, Narvaez-Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell13: 179-191
170. Overmyer K, Brosche M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinanen M, Saarma M, Scheel D, Kangasjarvi J (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol 137:1092-1104
171. Pare PW, Farag MA, Krishnamachari V, Zhang H, Ryu CM, Kloepper JW (2005) Elicitors and priming agents initiate plant defense responses. Photosynth Res 85: 149-159
172. Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139: 1291-1303
173. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406: 731-734
174. Peng M, Kuc J (1992) Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks.Phytopathology 82:696-699
175.Peng JL,Zhao J,Pan XM,Zhao JF,Dong HS,Wang JS(2002) Riboflavin activates growth signal transduction pathway in plants.J Nanjing Agric Univ 25:33-36
176.Pennell RI,Lamb C(1997) Programmed cell death in plants.Plant Cell 9:1157-1168
177.Piacenza L,Irigoin F,Alvarez MN,Peluffo G,Taylor MC,Kelly JM,Wilkinson SR,Radi R(2007) Mitochondrial superoxide radicals mediate programmed cell death in Trypanosoma cruzi:cytoprotective action of mitochondrial iron superoxide dismutase overexpression.Biochem J 403:323-334
178.Pieterse CM,Schaller A,Mauch-Mani B,Conrath U(2006) Signaling in plant resistance responses:divergence and cross-talk of defense Pathways.In:Tuzun S,Bent E,editors.Multigenic and induced systemic resistance in plants,Springer Science+Business Media,Inc,New York.
179.Pieterse CMJ,Van Pelt JA,Ton J,Parchmann S,Mueller MJ,Buchala AJ,Metraux JP,Van Loon LC(2000)Rhizobacteria-mediated induced systemic resistance(ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production.Physiol Mol Plant Pathol 57:123-134
180.Pieterse CMJ,Van Wees SCM,Ton J,Van Pelt JA,Van Loon LC(2002) Signaling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana.Plant Biol.4:535-544
181.Pieterse,CMJ,Van Wees SCM,Van Pelt JA,Knoester M,Laan R,Gerrits H,Weisbeek PJ,Van Loon LC(1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis.Plant Cell 10:1571-1580
182.Polidoros AN,Mylona PV,Scandalios JP(2001) Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress.Transgenic Res 10:555-569
183.Polle A(2001) Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling:computer simulations as a step towards flux analysis.Plant Physiol 126:445-462
184.Pourcel L,Routaboul JM,Cheynier V,Lepiniec L,Debeaujon I(2007) Flavonoid oxidation in plants:from biochemical properties to physiological functions.Trends Plant Sci 12:29-36
185.Pozo MJ,Cordier C,Dumas-Gaudot E,Gianinazzi,S,Barea JM,Azc6n-Aguilar C(2002) Localized vs.systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants.J Exp Bot 53:525-534
186.Pozo Mr,Van Loon,LC,Pieterse CMJ(2005) Jasmonates signals in plant-microbe interactions.J P/ant Growth Regul 23:211-222
187.Purvis AC,Shesfelt RL(1993) Does the alternative pathway ameliorate chilling injury insensitive plant tissues.Physiol Plant 88:712-718
188.Ramputh AI,Arnason JT,Cass L,Simmonds JA(2002) Reduced herbivory of the European tom borer(Ostrinia nubilalis) on corn transformedwith germin,a wheat oxalate oxidase gene.Plant Sci 162:431-440
189.Ran MV,Davis KR(2001) The physiology of ozone induced cell death.Planta 213:682-690
190.Rasmusson AG,Heiser VV,Zabaleta E,Brennicke A,Grohmann L(1998) Physiological,biochemical and molecular aspects of mitochondrial complex I in plants.Biochim Biophys Acta 1364:101-111
191.Ren D,Yang H,Zhang S(2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis.J Biol Chem 277:559-565
192.Reuber TL,Plotnikova JM,Dewdney J,Rogers EE,Wood W,Ausubel FM(1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants.Plant J 16:473-485
193.Rhoads DM,Umbach AL,Subbaiah CC,Siedow JN(2006) Mitochondrial reactive oxygen species.Contribution to oxidative stress and interorganellar signaling.Plant Physiol 141:357-366
194.Robson CA,Vanlerberghe GC(2002) Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondria-dependent and-independent pathways of programmed cell death.Plant Physiol 129:1908-1920
195.Roje S(2007) Vitamin B biosynthesis in plants.Phytochemistry 68:1904-1921
196.Ryals,JA,Neuenschwander UH,Willits MG,Molina A,Steiner HY,Hunt M(1996) Systemic acquired resistance.Plant Cell 8:1809-1819
197.Ryu CM,Farag,MA,Hu CH,Reddy MS,Kloepper JW,Pare PW(2004) Bacterial volatiles induce systemic resistance in Arabidopsis.Plant Physiol 134:1017-1026
198.Samuel MA,Ellis BE(2002) Double jeopardy:both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive.Plant Cell 14:2059-2069
199.Scandalios JC(1993) Oxygen stress and superoxide dismutases.Plant Physiol 101:7-12
200.Schultheiss H,Dechert C,Kogel KH,Huckelhoven R(2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus.Plant J 36:589-601
201.Seki M,Ishida J,Narusaka M,Fujita M,Nanjo T,Umezawa T,Kamiya A,Nakajima M,Enju A,Sakurai T,Satou M,Akiyama K,Yamagnchi-Shinozaki K,Caminci P,Kawai J,Hayashizaki Y,Shinozaki K(2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray.Funct Integr Genomics 2:282-291
202.Sharma YK,Leon J,Raskin I,Davis KR(1996) Ozone-induced responses in Arabidopsis thaliana:the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance.Proc Natl Acad Sci USA 93:5595-5599
203.Shirasu K,Nakajima H,Rajasekhar VK,Dixon RA,Lamb CJ(1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms.Plant Cell 9:261-270
204.Shoresh M,Yedidia I,Chet I(2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203.Phytopathol 95:76-84
205.Stadnik M J,Buchenauer H(2000) Inhibition of phenylalanine ammonialyase suppresses the resistance induced by benzothiadiazole in wheat to Blumeria grarainis f.sp.tritici.Physiol Mol Plant Pathol 57:25-34
206.Staiger D,Apel K,Trepp G(1999) The Atger3 promoter confers circadian clock-regulated transcription with peak expression at the beginning of the night.Plant Mol Biol 40:873-882
207.Sticher L,Mauch-Mani B,Metraux JP(1997) Systemic acquired resistance.Annu Rev Phytopathol 35:235-270
208.Taheri P,Hofte M(2006) Riboflavin induces resistance in rice against Rhizoctonia sheath diseases by activating signal transduction pathways leading to upregulation of rice cationic peroxidase and formation of lignin as a structural barrier.Commun Agric Appl Biol Sci 71:255-258
209.Taipalensuu J,Falk A,Rask L(1996) A wound-and methyljasmonate-inducible transcript coding for a myrosinase-associated protein with similarities to an early nodulin.Plant Physiol 110:471-483
210.Tatiana E,Mishina,Jurgen Z(2006) The Arabidopsis flavin-dependent monooxygenase FMOl is an essential component of biologically induced systemic acquired resistance.Plant Physiol 141:1666-1675
211.Tobena-Santamaria R,Bliek M,Ljung K,Sandberg G,Mol JNM,Souer E,Koes R(2002) FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture.Genes Dev 16:753-763
212.Ton J,Jakab G,Toquin V,Flors V,Iavicoli A,Maeder MN,Metraux JP,Mauch-Mani B(2005) Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis.Plant Cell 17:987-999
213.Ton J,Mauch-Mani B(2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose.Plant J 38:119-130
214.Torres MA,Dangl JL(2005) Functions of the respiratory burst oxidase in biotic interactions,abiotic stress and development.Curr Opin Plant Biol 8:397403
215.Tortes MA,Jones JD,Dangl JL(2005) Pathogen-induced,NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana.Nat Genet 37:1130-1134
216.Truman W,Bennett MH,Kubigsteltig I,Turnbull C,Grant M(2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates.Proc Nail Acad Sci USA 104:1075-1080
217.Uhmsov T,Ohmiya A,Ha G,Guifoyle T(1995) The soybean GH2/4 gene that encode a glutathione S-transferase has a promoter that is activated by a wide range of chemical agents.Plant Physiol 108:919-927
218.Vallelian-bindschedler L,Mosinger E,Metraux JP,Schweizer P(1998) Structure,expression and localization of a germin-like protein in barley(Hordeura vulgare L.) that is insolubilized in stressed leaves.Plant Mol Biol 37:297-308
219.Van Breusegem F,Dat JF(2006) Reactive oxygen species in plant cell death.Plant Physiol 141:384-390
220.van der Merwe JA,Dubery IA(2006) Benzothiadiazole inhibits mitochondrial NADH:ubiquinone oxidoreductase in tobacco.J Plant Physiol 163:877-882
221.van Hulten M,Pelser M,van Loon LC,Pieterse CM,Ton J(2006) Costs and benefits of priming for defense in Arabidopsis.Proc Natl Acad Sci USA 103:5602-5607
222.Van Loon LC,Bakker PAHM,Pieterse CMJ(1998) Systemic resistance induced by rhizosphere bacteria.Annu Rev Phytopatho136:453-483
223.van Loon LC,van Strein EA(1999) The families of pathogenesis-related proteins,their activities,and comparative analysis of PR-1 type proteins.Physiol Mol Plant Pathol 55:85-97
224.Van Peer R,Niemann GJ,Schippers B(1991) Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp.strain WCS417r.Phytopathology 81:728-734
225.Vanlerberghe GC,Mcintosh L(1997) Alternative oxidase:from gene to function.Annu Rev Plant Physiol Plant Molec Biol 48:703-34
226.Verhagen BWM,Glazebrook J,Zhu T,Chang HS,van Loon LC,Pieterse,CMJ(2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis.Mol Plant-Microbe Interact 17:895-908
227.Vranova E,Langebartels C,Vanmontagu M,Inze D,Van cam PW(2000) Oxidative stress,heat shock and drought differentially affect expression of a tobacco protein phosphatase 2C.J Exp B or 51:1763-1764
228.Wagner AM(1995) A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells.FEBS Lett 368:339-342
229.Wagner D,Przybyla D,op den Camp R,Kim C,Landgraf F,Lee KP,Wusch M,Laloi C,Nater M,Hideg E(2004)The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana.Science 306:1183-1185
230.Wang Z,Xie W,Chi F,Li C(2005) Identification of non-specific lipid transfer protein-1 as a calmodulin-binding protein in Arabidopsis.FEBS Lett 579:1683-1687
231.Xie Z,Chen Z(1999) Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells.Plant Physiol 120:217-226
232.Xie Z,Chen Z(2000) Harpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells.Mol Plant-Microbe Interact 13:183-190
233.Xing T,Higgins VJ,Blumwal DE(1997) Race specific elicitors of Cladosporium fulvum promote translocation of eytosolie components of NADPH oxidase to the plasm membrane of tomato cell.Plant Cell 9:249-259
234.Xu Z,Escamilla-Trevino L,Zeng L,Lalgondar M,Bevan D,Winkel B,Mohamed A,Cheng CL,Shih MC,Poulton J,Esen A(2004) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1.Plant Mol Biol 55:343-367
235.Yao N,Eisfelder BJ,Marvin J,Greenberg JT(2004) The mitochondrion-an organelle commonly involved in programmed cell death in Arabidopsis thaliana.Plant J 40:596-610
236.Yao N,Tada Y,Sakamoto M,Nakayashiki H,Park P,Tosa Y,Mayama S(2002) Mitochondrial oxidative burst involved in apoptotic response in oats.Plant J 30:567-579
237.Yoshinaga K,Arimura SI,Niwa Y,Tsutsumi N,Uchimiya H,Kawai-Yamada M(2005) Mitochondrial behaviour in the early stages of ROS stress leading to cell death in Arabidopsis thaliana.Ann Bot(Lond) 96:337-342
238.Zago E,Morsa S,Dat JF,Alard P,Ferrarini A,Inze' D,Delledonne M,Van Breusegem F(2006) Nitric oxide-and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco.Plant Physiol 141:404-411
239.Zeier J,Delledonne M,Mishina T,Severi E,Sonoda M,Lamb CJ(2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions.Plant Physiol 136:2875-2886
240.Zhang Q,Mischis L,Wiskich JT(1996) Respiratory responses of pea and wheat seedlings to chloramphenicol treatment.Aust J Plant Physiol 23:683-692
241.Zhang Z,Collinge DB,Thordal-Christensen H(1995) Germin-like OxO,a H_2O_2-producing enzyme,accumulates in barley attacked by the powery mildew fungus.Plant J 8:139-145
242.Zhao Y,Christensen SK,Fankhauser C,Cashman JR,Cohen JD,Weigel D,Chory J(2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis.Science 291:306-309
243.Zhou F,Zhang Z,Gregersen PL,Mikkelsen JD,de Neergaard E,Collinge D,Thordal-Christensen H(1998)Molecular characterization of the oxalate oxidase involved in the response of barley to the powery mildew fungus.Plant Physiol 117:33-41
244.杜秀敏,殷文璇,赵彦修(2001)植物中活性氧的产生和清除.中同生物技术杂志17:121-125
245.方中达(1998)植病研究方法.中国农业出版社
246.贾琴(2007)核黄素受体蛋白对植物开花转型和抗病防卫调控作用的初步研究.硕士学位论文,南京农业大学
247.彭建令(2003)两类激发子(harpins和核黄素)启动植物抗病防卫和生长信号传导的分子遗传学解析.博士学位论文,南京农业大学
248.王颖(2004)中华鳖核黄素受体基因的克隆和在转基因植物中的表达.硕士学位论文,南京农业大学
249.闻伟刚(2001)水稻黄单胞菌过敏性反应激发子的研究.博士学位论文,南京农业大学
250.夏侯珍珠(2007)核黄素受体蛋白与HpaG_(Xoo)蛋白对植物生长与防卫反应的影响.硕士学位论文,南京农业大学