血红素加氧酶/一氧化碳信号系统介导拟南芥和小麦对盐、渗透和UV-C胁迫适应性的分子机理
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摘要
动物中的研究表明,血红素加氧酶/一氧化碳(heme oxygenase/carbon monoxide, HO/CO)是一种内源信号系统,HO(EC 1.14.99.3)产生的CO起着生理信号分子或生物活性小分子的功能,影响着细胞的繁殖和各种生长因子的合成。
在植物中,HO参与了光敏色素发色团的生物合成。先前我们通过研究发现,盐胁迫下小麦幼苗根部HO活性上升并导致内源CO含量增加,CO通过NO信号介导的上调根部抗氧化防护和维持离子稳态来提高小麦幼苗耐盐性,但还不清楚HO诱导与盐适应性之间的关系。我们进一步的研究发现,低浓度NaCl预处理(25 mM)不仅能激活小麦HO-1基因的表达和活性提高,还能诱导产生盐适应现象；200mM NaC1处理则能导致相反的结果。进一步探讨了HO-1上调在小麦幼苗获得性耐盐性(盐适应)中的作用,发现HO-1专一性抑制剂锌原卟啉(zinc protoporphyrin IX, ZnPP)能够逆转盐适应的产生,而200 mMNaCl产生的毒害效应能被外加HO-1诱导剂haemin部分逆转,这说明盐适应过程与HO-1上调有关。此外,CO(HO的催化产物之一)处理能模拟低浓度NaCl诱导产生的盐适应现象。CO预处理能重建活性氧(reactive oxygen species,ROS)稳态平衡,这一过程是通过上调超氧化物歧化酶(superoxide dismutase, SOD)、抗坏血酸过氧化物酶(ascorbate peroxidase, APX)和胞内过氧化物酶(peroxidase,POD)的转录本、总酶活和同工酶活性,下调NADPH氧化酶和细胞壁POD总酶活以及同工酶活性来实现的。同时也发现,过氧化氢(hydrogen peroxide, H2O2)稳态的维持是HO-1介导的盐适应所必需。上述结果表明,HO-1是通过维持ROS稳态来介导小麦幼苗盐适应性。
在拟南芥中,共有四个基因编码HO,它们分别是HY1、HO2, HO3和HO4。为了阐明各HO基因在盐适应过程中的功能,进一步利用遗传突变体研究HO介导盐适应性产生中的具体机制。首先比较了拟南芥野生型和四个HO单突变体(hy1-100、ho2、ho3和ho4)在NaCl胁迫下的萌发率和主根生长差异。结果表明,hy1-100对NaCl最敏感,且没有盐适应表型；而HYl过表达株系(35S：HYl-1/2/3/4)对NaCl则更具抗性。进一步研究发现,低浓度NaCl能激活NADPH氧化酶D(respiratory burst oxidase homologues, RbohD)转录本,其产生的ROS呈双峰诱导(峰Ⅰ和峰Ⅱ),ROS介导了低盐胁迫下HY1的诱导表达和其产生的盐适应现象；虽然hy1-100突变体的HY1无法正常表达,但依然检测到了ROS峰Ⅰ存在,这说明ROS峰Ⅰ的产生不依赖于HY1。我们还研究了受haemin诱导的HY1表达与RbohD产生的ROS峰Ⅱ对盐适应产生的影响。在atrbohD突变体中,haemin预处理能诱导HYl的表达,但无法诱导ROS和盐适应的产生；在hy1-100突变体中,haemin预处理既不能诱导HY1基因表达,RbohD产生的ROS峰Ⅱ也无法形成。上述结果说明,HY1在盐适应信号中起着重要作用,其功能的发挥需要RbohD产生的ROS峰Ⅱ参与。
由于渗透胁迫和盐胁迫存在诸多共性,因此进一步比较了拟南芥野生型Col-0、hy1-00突变体和HY1过表达突变体35s：HY1-3/1-4对渗透胁迫和盐胁迫的应答差异。结果表明,与野生型相比,hy1-100突变体的萌发受抑对mannitol和NaCl更敏感,而35s：HY1-3/1-4对mannitol和NaCl不敏感。HO-1活性诱导剂haemin和专一性抑制剂ZnPP能不同程度地缓解或更加抑制拟南芥野生型在渗透和盐胁迫下的鲜重累积和主根生长受抑；haemin不影响hy1-100突变体在胁迫下的表型,而ZnPP在一定程度上加剧了胁迫下hy1-100突变体的受抑程度。通过外源添加HO各催化产物发现,CO和胆红素(bilirubin, BR)是HY1调节拟南芥在胁迫下主根和侧根生长发育中的有效产物。与野生型相比,虽然hy1-100的生长受抑对渗透胁迫和盐胁迫均表现为超敏感,但hy1-100突变体在渗透胁迫均能存活,而盐胁迫下存活率较野生型则显著下降,这暗示着HY1在盐胁迫和渗透胁迫信号转导中功能可能存在差异。接着检测了渗透胁迫和盐胁迫下野生型和hy1-100突变体胁迫应答基因和脱落酸(abscisic acid, ABA)合成基因的表达,发现在渗透胁迫下,上述两类基因在hy1-100突变体中的诱导程度显著高于野生型的；而在盐胁迫下的结果则恰相反。同时,ABA能诱导HYl基因表达,hy1-100突变体的萌发受抑对外源ABA超敏感,35s：HYl-3/1-4过表达突变体则对ABA不敏感。自然干旱实验的结果表明,hy1-100突变体较野生型更耐旱,而35s：HY1-3过表达突变体不耐旱。进一步实验证明这可能是由于各材料气孔的开关对ABA响应的敏感性不同引起的,HY1可能通过调节气孔开放和关闭来改变耐旱性。
一氧化氮(nitric oxide, NO)是植物逆境信号转导的重要信号分子,还不清楚HY1与NO信号在耐盐信号转导中的关系。进一步的实验从遗传学角度继续研究了盐胁迫下NO产生的来源,并初步探讨了HY1与硝酸还原酶(nitrate reductase, NR)途径产生的NO之间的关系。NR抑制剂钨酸钠(tungstate)和动物NOS抑制剂NG-硝基-L-精氨酸甲酯(NG-nitro-L-arginine methyl ester hydrochloride, L-NAME)均能抑制NaCl诱导的NO产生,同时NaCl引起的拟南芥主根生长减缓和鲜重累积下降更受抑制；NaCl诱导了拟南芥根部两个NR的编码基因NIA1和NIA2及一氧化氮相关蛋白1(nitric oxide associated 1, NOA1)转录水平的提高,这些结果说明NR和L-Arg途径对盐胁迫诱导的NO产生均有贡献。遗传学的证据还表明,NaCl无法诱导NR突变体nial-1/2-5、NOA1突变体noal和nial-1/2-5/noal突变体根部NO含量的提高,而外源NO供体硝普钠(sodium nitroprusside, SNP)能同时增加各突变体的NO含量,说明NaCl诱导拟南芥根部NO的产生与NIA1、NIA2和NOA1均有关。同时,与野生型相比,nial-1/2-5、noal和nial-1/2-5/noal突变体的生长抑制均对NaCl表现为超敏感。进一步还比较了盐胁迫下拟南芥野生型、hy1-100, ho2, ho3和ho4突变体根部NO产生的差异。结果显示,hy1-100突变体在盐胁迫下产生更多的NO；NO供体二乙胺/一氧化氮复合物(diethylamine/nitric oxide adduct, NONOate)无法缓解hy11-100突变体萌发对NaCl超敏的现象,而NO清除剂2-苯-4,4,5,5-四甲基咪唑-1-氧-3-氧化物(2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt, PTIO)逆转了35s：HYl-3更抗盐的表型；HO-1诱导剂haemin能缓解NaCl胁迫下拟南芥野生型的萌发和子叶张开绿化受抑,但haemin对noal突变体的缓解效应则明显趋弱,haemin无法缓解nial-1/2-5和nial-1/2-5/noal突变体生长抑制对NaCl的超敏现象。这些结果暗示,盐胁迫信号转导途径中HY1可能与NR产生的NO存在互作,它们都是耐盐信号转导途径所必需的组分。
先前的研究表明,大豆血红素加氧酶响应紫外(ultraviolet, UV)辐射,HO的诱导能缓解UV-B胁迫引起的氧化伤害,且这一过程可能与ROS有关。由于缺乏遗传学证据,还不清楚HO调节紫外胁迫的具体机理。本论文从遗传学角度探讨了拟南芥HO各基因对UV-C的应答变化,并比较了UV-C辐射下野生型和hy1-100突变体类黄酮合成代谢途径和抗氧化防御系统的差异。结果发现,UV-C辐射胁迫下,拟南芥根部HY1、H02、HO3和H04均受诱导,其中以HYl的诱导最为剧烈。同时,与野生型相比,hy1-100突变体的生长抑制对UV-C辐射胁迫表现为超敏感。进一步实验结果表明这与其类黄酮代谢水平降低有关：与野生型相比,hy1-100突变体紫外吸收物质含量显著降低,类黄酮代谢途径4个重要代谢酶查尔酮合酶(chalcone synthase, CHS)、查尔酮异构酶(chalcone isomerase, CHI)、黄烷酮3-羟化酶(flavonoid 3-hydroxylase,F3H)和黄酮醇合成酶(flavonol synthase, FLS)的表达也有所降低。此外,UV-C辐射显著诱导了上述4个关键基因的表达；hy1-100突变体的CHI和FLS受诱导程度则部分受抑制,而CHS的表达则明显受抑制。hy1-100突变体上述基因诱导受抑是由其UV信号转导受阻引起的：UV-C辐射显著诱导了野生型根部类调控黄酮代谢的相关转录因子的表达；与之相对的是,HYl突变后,UV-C辐射对相关转录因子的诱导表达明显受到抑制。此外,抗氧化酶基因定量PCR的结果显示,hy-100突变体对UV-C辐射超敏感还与其抗氧化防护系统无法有效诱导有关。
Recent studies suggested that the heme oxygenase/carbon monoxide (HO/CO) is an endogenous siganlling system in modulating inflammatory reactions, influencing cell proliferation and production of growth factors in animals. It was also confirmed that carbon monoxide (CO), mainly generated by heme oxygenase enzymes (HOs, EC 1.14.99.3), functions as a physiological messenger or bioactive molecule in animal cells.
The major role of HO in phytochrome chromophore biosynthesis was discovered in plants. Our previous result showed that salt stress induced an increase in endogenous CO production and the activity of the CO synthetic enzyme HO in wheat seedling roots. CO might confer an increased tolerance to salinity stress by maintaining ion homeostasis and enhancing antioxidant system parameters in wheat seedling roots, both of which were partially mediated by NO signal. However, little was known about the relationship between HO induction and salt acclimation in plants. In this study, HO-1 up-regulation and its role in acquired salt tolerance (salinity acclimation) were also investigated in wheat plants. We discovered that pretreatment with a low concentration of NaCl (25 mM) followed by the transfer to 200 mM NaCl stress, not only led to the induction of wheat HO-1 protein and gene expression as well as the increased HO activity in seedling roots, but also induced salinity acclimatory response. Opposite phenomenon were observed in seedling plants upon 200 mM NaCl stress. The effect is specific for HO-1 since the potent HO-1 inhibitor zinc protoporphyrin IX (ZnPP) blocked the above cytoprotective actions, and the cytotoxic responses conferred by 200 mM NaCl were reversed partially when HO-1 inducer haemin was added. Furthermore, the HO's catalytic product CO aqueous solution pretreatment mimicked the low concentration of NaCl-induced salinity acclimatory responses. Meanwhile, the reestablishment of ROS homeostasis triggered by CO pretreatment followed by salinity stress was mainly guaranteed by the induction of total and isozymatic activities, or corresponding transcripts of superoxide dismutase (SOD), ascorbate peroxidase (APX), and cytosolic peroxidase (POD), as well as the down-regulation of NADPH oxidase expression and decreased cell-wall POD activity. A requirement of H2O2 homeostasis for HO-1-mediated salinity acclimation was also discovered. Taken together, the above results suggested that up-regulation of HO-1 expression was responsible for salinity acclimation through the regulation of ROS homeostasis.
In Arabidopsis thaliana, a family of four genes(HYl, HO2, HO3 and HO4) encodes haem oxygenase (HO), and their major role in phytochrome chromophore biosynthesis was discovered. We further characterize the detailed mechasim of HY1 mediated salt acclimation by using mutant analyses. To characterise the contribution of different HO isoforms involved in salt acclimation, effects of NaCl on seed germination and primary root growth in Arabidopsis wild-type and four HO mutants(hy1-100, ho2, ho3 and ho4) were compared. Among the four HO mutants, hy1-100 displayed maximal sensitivity to salinity and provided no acclimatory response. Whereas, HY1-over-expressing plants (35S:HY1) displayed tolerance characteristics. Mild salt-stress stimulated a biphasic change in RbohD transcripts and a consequent increase in its derived reactive oxygen species (ROS, peak I and II) production in wild-type. Furthermore, ROS peak I-mediated HY1 induction and thereafter salt acclimation were observed, while only the ROS peak I appeared in hy1-100 mutant. In a subsequent test, haemin-induced HY1 expression and RbohD-derived ROS peak II formation, confirmed their causal relationship with salt acclimation. Meanwhile, in atrbohD mutants, haemin pretreatment resulted in the induction of HY1 expression, whereas no similar response appeared in hyl-100, and neither peak II of ROS nor any following salt acclimatory responses were observed. Together, the above findings suggest that HY1 plays an important role in salt acclimation signalling, which required participation of RbohD-derived ROS peak II.
As both salt and osmotic stresses share common characterics, we further compared responses of Arabidopsis wild type Col-0, hyl-100 mutant and HY1 over-expressing lines 35s:HY1-3/1-4 to osmotic and salt stresses. Further results showed that, compared with wild type, hy1-100 mutant displayed hypersensitive phynotype, whereas 35s:HY1-3/1-4 was insensitive to exogenous NaCl and mannitol. Application of the HO-1 inducer haemin and potent inhibitor ZnPP can alleviate or aggravate the osmotic or salt, stress-induced inhibition of fresh weight and primary root growth. No significant response of hy1-100 mutant was obsereved when haemin was added upon stress conditions. Meanwhile, ZnPP slightly aggravates growth inhibition of hy1-100 mutant upon both osmotic and salt stresses. Further analysis discovered that both CO and BR were the effective by-product of HO modulating primary and latral root development when Arabidopsis seedlings were exposed to stresses. Interestingly, althought hy1-100 mutant exhibited hypersensitive phenotyes, different survive rates under osmotic and salt stresses were oberseved. By using real-time PCR analyses, we found that the inductions of both stress response and ABA metabolism genes expression were much higher in hy1-100 mutant than those of wild type under osmotic stress. Whereas opposite phenonmen were observed in salt stress condition. Additionally, ABA treatment results in the induction of HY1 expression, and the germination inhibition of hy1-100 was hypersensitive to exogenous ABA. Oppssite results were also found in 35s:HY1-3/1-4 plants. Finally, we also noticed that enhanced drought resistance of hy1-100 mutant plants was due to an efficient stomatal closure and inhibition of opening induced by ABA.
Former results showed that HY1 is a key component of the Arabidopsis salt acclimation. hy1-100 mutant displayed hypersensitive to salt stress, whereas the HY1 over expression line (35S:HY1) showed salt tolerant phenotype. Nitric oxide (NO) has been demonstrated to play an important role in salt stress signaling. However, the relationship between HY1 and endogenous NO function under salt stress was still unknown. In this chapter, we studied the origin of NO under salt stress by combined using pharmacological and genetic approaches, and the relationship between HY1 and nitrate reductase (NR)-derived NO production were also discussed. The results showed that the both NR and L-argine (L-Arg) pathway were responsible for NaCl-triggered NO generation. NR inihibitor tungstate and mammalian nitric oxide synthase (NOS) inihibitor NG-nitro-L-arginine methyl ester hydrochloride (L-NAME) were able to block the NO generation induced by NaCl; meanwhile, root growth inhibition and fresh weight accumulation of wild-type induced by NaCl were also aggravated. The transcription levels of NIA1, NIA2 and nitric oxide associated 1 (NOA1) in wild-type roots were also induced by NaCl treatment. By contrast, NR mutant nia1-1/2-5, NOA1 mutant noal and nia1-1/2-5/noal failed to accumulate NO under salt stress, whereas the application of NO donor sodium nitroprusside (SNP) could increase NO production. Above results indicated that NO generation in Arabidopsis roots induced by NaCl is related to NR and NOA1 up-regulation. Moreover, nia1-1/2-5, noa1 and nia1-1/2-5/noa1 are all hypersensitive to NaCl stress, which could be partially rescued by exogenous NO donor diethylamine/nitric oxide adduct (NONOate). We next compared the differences of NO generation between WT, hy1-100, ho2, ho3 mutant under salt stress. The results showed that more NO production could be observed in hy1-100 mutant seedling root under salt stress. Interestingly, NO donor NONOate failed to alleviate the hypersensitivity phenotype of hy1-100 mutant upon NaCl during germination period, whereas the NO scavenger 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (PTIO) reversed the salt tolerance phenotype of 35S:HY1-3. HO-1 inducer haemin could alleviate germination and cotyledon opening inhibition of WT seeds under salt stress. Whereas weak alleviation can be observed in noal mutant seedlings, and haemin failed to alleviate hypersensitivity phenotype of nia1-1/2-5 and nia1-1/2-5/noa1 mutants under salt stress. These results indicate that a cross-talk might exist between NR-derived NO and HY1 function during salt stress signaling, both of which are necessary for Arabidopsis salt tolerance.
Previous research demonstrated that the soybean HO can respond to ultraviolet (UV) radiation. The induction of HO can alleviate oxidative damage caused by UV-B radiation, the ROS may be involved in this process (Yannarelli et al.,2006). However, detailed genetic evidence is required for further investigating the mechanism of HO in regulating UV-B radiation response. In this chapter, we examined the responses of four HO genes under UV-C radiation in Arabidopsis. The difference between wild-type and hy1-100 mutant for flavonoid biosynthetic metabolism and antioxidant defence system in response to UV-C was also studied. The results showed that, compared with the wild type, the hypersensitivity of hy1-100 mutant in response to UV-C radiation appeared, and this was due to its low level of flavonoid biosynthetic metabolism. Compared with the wild-type, hy1-100 contained less UV-absorbing compounds, and the down-regulating of the transcripts of four key enzymes for the flavonoid biosynthetic metabolism (chalcone synthase (CHS), chalcone isomerase(CHI), flavonoid 3-hydroxylase (F3H), and flavonol synthase (FLS)) were also found, respectively. Moreover, four key genes in the Arabidopsis wild-type flavonoid biosynthetic metabolism were significantly induced after UV-C radiation, whereas in the hy1-100 mutant, the induction of CHS and FLS is partially blocked and CHS expression is reversed significantly. We further hypothesis that this suppression of hy1-100 mutant might due to its interruption of the UV signal perception. For example, the expression of transduction factor HY5, HYH (HY5 homolog), MYB11 and MYB12 in the root of wild-type can be markedly induced by UV-C radiation, whereas partially inhibited in hyl-100 mutant. Furthermore, the results of real-time PCR analysis indicated that the hyper-sensitivity of the hy1-100 mutant in response to UV-C radiation may also be contributed to the failure in induction of the antioxidant defence genes expression, such as CSD1 (Cu/Zn superoxide dismutase 1), CAT1 (catalasel), CAT2 (catalase2), FSDl (Fe superoxide dismutase), cAPXl (cytosolic ascorbate peroxidase 1), and cAPX2 (cytosolic ascorbate peroxidase 2).
在植物中,HO参与了光敏色素发色团的生物合成。先前我们通过研究发现,盐胁迫下小麦幼苗根部HO活性上升并导致内源CO含量增加,CO通过NO信号介导的上调根部抗氧化防护和维持离子稳态来提高小麦幼苗耐盐性,但还不清楚HO诱导与盐适应性之间的关系。我们进一步的研究发现,低浓度NaCl预处理(25 mM)不仅能激活小麦HO-1基因的表达和活性提高,还能诱导产生盐适应现象；200mM NaC1处理则能导致相反的结果。进一步探讨了HO-1上调在小麦幼苗获得性耐盐性(盐适应)中的作用,发现HO-1专一性抑制剂锌原卟啉(zinc protoporphyrin IX, ZnPP)能够逆转盐适应的产生,而200 mMNaCl产生的毒害效应能被外加HO-1诱导剂haemin部分逆转,这说明盐适应过程与HO-1上调有关。此外,CO(HO的催化产物之一)处理能模拟低浓度NaCl诱导产生的盐适应现象。CO预处理能重建活性氧(reactive oxygen species,ROS)稳态平衡,这一过程是通过上调超氧化物歧化酶(superoxide dismutase, SOD)、抗坏血酸过氧化物酶(ascorbate peroxidase, APX)和胞内过氧化物酶(peroxidase,POD)的转录本、总酶活和同工酶活性,下调NADPH氧化酶和细胞壁POD总酶活以及同工酶活性来实现的。同时也发现,过氧化氢(hydrogen peroxide, H2O2)稳态的维持是HO-1介导的盐适应所必需。上述结果表明,HO-1是通过维持ROS稳态来介导小麦幼苗盐适应性。
在拟南芥中,共有四个基因编码HO,它们分别是HY1、HO2, HO3和HO4。为了阐明各HO基因在盐适应过程中的功能,进一步利用遗传突变体研究HO介导盐适应性产生中的具体机制。首先比较了拟南芥野生型和四个HO单突变体(hy1-100、ho2、ho3和ho4)在NaCl胁迫下的萌发率和主根生长差异。结果表明,hy1-100对NaCl最敏感,且没有盐适应表型；而HYl过表达株系(35S：HYl-1/2/3/4)对NaCl则更具抗性。进一步研究发现,低浓度NaCl能激活NADPH氧化酶D(respiratory burst oxidase homologues, RbohD)转录本,其产生的ROS呈双峰诱导(峰Ⅰ和峰Ⅱ),ROS介导了低盐胁迫下HY1的诱导表达和其产生的盐适应现象；虽然hy1-100突变体的HY1无法正常表达,但依然检测到了ROS峰Ⅰ存在,这说明ROS峰Ⅰ的产生不依赖于HY1。我们还研究了受haemin诱导的HY1表达与RbohD产生的ROS峰Ⅱ对盐适应产生的影响。在atrbohD突变体中,haemin预处理能诱导HYl的表达,但无法诱导ROS和盐适应的产生；在hy1-100突变体中,haemin预处理既不能诱导HY1基因表达,RbohD产生的ROS峰Ⅱ也无法形成。上述结果说明,HY1在盐适应信号中起着重要作用,其功能的发挥需要RbohD产生的ROS峰Ⅱ参与。
由于渗透胁迫和盐胁迫存在诸多共性,因此进一步比较了拟南芥野生型Col-0、hy1-00突变体和HY1过表达突变体35s：HY1-3/1-4对渗透胁迫和盐胁迫的应答差异。结果表明,与野生型相比,hy1-100突变体的萌发受抑对mannitol和NaCl更敏感,而35s：HY1-3/1-4对mannitol和NaCl不敏感。HO-1活性诱导剂haemin和专一性抑制剂ZnPP能不同程度地缓解或更加抑制拟南芥野生型在渗透和盐胁迫下的鲜重累积和主根生长受抑；haemin不影响hy1-100突变体在胁迫下的表型,而ZnPP在一定程度上加剧了胁迫下hy1-100突变体的受抑程度。通过外源添加HO各催化产物发现,CO和胆红素(bilirubin, BR)是HY1调节拟南芥在胁迫下主根和侧根生长发育中的有效产物。与野生型相比,虽然hy1-100的生长受抑对渗透胁迫和盐胁迫均表现为超敏感,但hy1-100突变体在渗透胁迫均能存活,而盐胁迫下存活率较野生型则显著下降,这暗示着HY1在盐胁迫和渗透胁迫信号转导中功能可能存在差异。接着检测了渗透胁迫和盐胁迫下野生型和hy1-100突变体胁迫应答基因和脱落酸(abscisic acid, ABA)合成基因的表达,发现在渗透胁迫下,上述两类基因在hy1-100突变体中的诱导程度显著高于野生型的；而在盐胁迫下的结果则恰相反。同时,ABA能诱导HYl基因表达,hy1-100突变体的萌发受抑对外源ABA超敏感,35s：HYl-3/1-4过表达突变体则对ABA不敏感。自然干旱实验的结果表明,hy1-100突变体较野生型更耐旱,而35s：HY1-3过表达突变体不耐旱。进一步实验证明这可能是由于各材料气孔的开关对ABA响应的敏感性不同引起的,HY1可能通过调节气孔开放和关闭来改变耐旱性。
一氧化氮(nitric oxide, NO)是植物逆境信号转导的重要信号分子,还不清楚HY1与NO信号在耐盐信号转导中的关系。进一步的实验从遗传学角度继续研究了盐胁迫下NO产生的来源,并初步探讨了HY1与硝酸还原酶(nitrate reductase, NR)途径产生的NO之间的关系。NR抑制剂钨酸钠(tungstate)和动物NOS抑制剂NG-硝基-L-精氨酸甲酯(NG-nitro-L-arginine methyl ester hydrochloride, L-NAME)均能抑制NaCl诱导的NO产生,同时NaCl引起的拟南芥主根生长减缓和鲜重累积下降更受抑制；NaCl诱导了拟南芥根部两个NR的编码基因NIA1和NIA2及一氧化氮相关蛋白1(nitric oxide associated 1, NOA1)转录水平的提高,这些结果说明NR和L-Arg途径对盐胁迫诱导的NO产生均有贡献。遗传学的证据还表明,NaCl无法诱导NR突变体nial-1/2-5、NOA1突变体noal和nial-1/2-5/noal突变体根部NO含量的提高,而外源NO供体硝普钠(sodium nitroprusside, SNP)能同时增加各突变体的NO含量,说明NaCl诱导拟南芥根部NO的产生与NIA1、NIA2和NOA1均有关。同时,与野生型相比,nial-1/2-5、noal和nial-1/2-5/noal突变体的生长抑制均对NaCl表现为超敏感。进一步还比较了盐胁迫下拟南芥野生型、hy1-100, ho2, ho3和ho4突变体根部NO产生的差异。结果显示,hy1-100突变体在盐胁迫下产生更多的NO；NO供体二乙胺/一氧化氮复合物(diethylamine/nitric oxide adduct, NONOate)无法缓解hy11-100突变体萌发对NaCl超敏的现象,而NO清除剂2-苯-4,4,5,5-四甲基咪唑-1-氧-3-氧化物(2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt, PTIO)逆转了35s：HYl-3更抗盐的表型；HO-1诱导剂haemin能缓解NaCl胁迫下拟南芥野生型的萌发和子叶张开绿化受抑,但haemin对noal突变体的缓解效应则明显趋弱,haemin无法缓解nial-1/2-5和nial-1/2-5/noal突变体生长抑制对NaCl的超敏现象。这些结果暗示,盐胁迫信号转导途径中HY1可能与NR产生的NO存在互作,它们都是耐盐信号转导途径所必需的组分。
先前的研究表明,大豆血红素加氧酶响应紫外(ultraviolet, UV)辐射,HO的诱导能缓解UV-B胁迫引起的氧化伤害,且这一过程可能与ROS有关。由于缺乏遗传学证据,还不清楚HO调节紫外胁迫的具体机理。本论文从遗传学角度探讨了拟南芥HO各基因对UV-C的应答变化,并比较了UV-C辐射下野生型和hy1-100突变体类黄酮合成代谢途径和抗氧化防御系统的差异。结果发现,UV-C辐射胁迫下,拟南芥根部HY1、H02、HO3和H04均受诱导,其中以HYl的诱导最为剧烈。同时,与野生型相比,hy1-100突变体的生长抑制对UV-C辐射胁迫表现为超敏感。进一步实验结果表明这与其类黄酮代谢水平降低有关：与野生型相比,hy1-100突变体紫外吸收物质含量显著降低,类黄酮代谢途径4个重要代谢酶查尔酮合酶(chalcone synthase, CHS)、查尔酮异构酶(chalcone isomerase, CHI)、黄烷酮3-羟化酶(flavonoid 3-hydroxylase,F3H)和黄酮醇合成酶(flavonol synthase, FLS)的表达也有所降低。此外,UV-C辐射显著诱导了上述4个关键基因的表达；hy1-100突变体的CHI和FLS受诱导程度则部分受抑制,而CHS的表达则明显受抑制。hy1-100突变体上述基因诱导受抑是由其UV信号转导受阻引起的：UV-C辐射显著诱导了野生型根部类调控黄酮代谢的相关转录因子的表达；与之相对的是,HYl突变后,UV-C辐射对相关转录因子的诱导表达明显受到抑制。此外,抗氧化酶基因定量PCR的结果显示,hy-100突变体对UV-C辐射超敏感还与其抗氧化防护系统无法有效诱导有关。
Recent studies suggested that the heme oxygenase/carbon monoxide (HO/CO) is an endogenous siganlling system in modulating inflammatory reactions, influencing cell proliferation and production of growth factors in animals. It was also confirmed that carbon monoxide (CO), mainly generated by heme oxygenase enzymes (HOs, EC 1.14.99.3), functions as a physiological messenger or bioactive molecule in animal cells.
The major role of HO in phytochrome chromophore biosynthesis was discovered in plants. Our previous result showed that salt stress induced an increase in endogenous CO production and the activity of the CO synthetic enzyme HO in wheat seedling roots. CO might confer an increased tolerance to salinity stress by maintaining ion homeostasis and enhancing antioxidant system parameters in wheat seedling roots, both of which were partially mediated by NO signal. However, little was known about the relationship between HO induction and salt acclimation in plants. In this study, HO-1 up-regulation and its role in acquired salt tolerance (salinity acclimation) were also investigated in wheat plants. We discovered that pretreatment with a low concentration of NaCl (25 mM) followed by the transfer to 200 mM NaCl stress, not only led to the induction of wheat HO-1 protein and gene expression as well as the increased HO activity in seedling roots, but also induced salinity acclimatory response. Opposite phenomenon were observed in seedling plants upon 200 mM NaCl stress. The effect is specific for HO-1 since the potent HO-1 inhibitor zinc protoporphyrin IX (ZnPP) blocked the above cytoprotective actions, and the cytotoxic responses conferred by 200 mM NaCl were reversed partially when HO-1 inducer haemin was added. Furthermore, the HO's catalytic product CO aqueous solution pretreatment mimicked the low concentration of NaCl-induced salinity acclimatory responses. Meanwhile, the reestablishment of ROS homeostasis triggered by CO pretreatment followed by salinity stress was mainly guaranteed by the induction of total and isozymatic activities, or corresponding transcripts of superoxide dismutase (SOD), ascorbate peroxidase (APX), and cytosolic peroxidase (POD), as well as the down-regulation of NADPH oxidase expression and decreased cell-wall POD activity. A requirement of H2O2 homeostasis for HO-1-mediated salinity acclimation was also discovered. Taken together, the above results suggested that up-regulation of HO-1 expression was responsible for salinity acclimation through the regulation of ROS homeostasis.
In Arabidopsis thaliana, a family of four genes(HYl, HO2, HO3 and HO4) encodes haem oxygenase (HO), and their major role in phytochrome chromophore biosynthesis was discovered. We further characterize the detailed mechasim of HY1 mediated salt acclimation by using mutant analyses. To characterise the contribution of different HO isoforms involved in salt acclimation, effects of NaCl on seed germination and primary root growth in Arabidopsis wild-type and four HO mutants(hy1-100, ho2, ho3 and ho4) were compared. Among the four HO mutants, hy1-100 displayed maximal sensitivity to salinity and provided no acclimatory response. Whereas, HY1-over-expressing plants (35S:HY1) displayed tolerance characteristics. Mild salt-stress stimulated a biphasic change in RbohD transcripts and a consequent increase in its derived reactive oxygen species (ROS, peak I and II) production in wild-type. Furthermore, ROS peak I-mediated HY1 induction and thereafter salt acclimation were observed, while only the ROS peak I appeared in hy1-100 mutant. In a subsequent test, haemin-induced HY1 expression and RbohD-derived ROS peak II formation, confirmed their causal relationship with salt acclimation. Meanwhile, in atrbohD mutants, haemin pretreatment resulted in the induction of HY1 expression, whereas no similar response appeared in hyl-100, and neither peak II of ROS nor any following salt acclimatory responses were observed. Together, the above findings suggest that HY1 plays an important role in salt acclimation signalling, which required participation of RbohD-derived ROS peak II.
As both salt and osmotic stresses share common characterics, we further compared responses of Arabidopsis wild type Col-0, hyl-100 mutant and HY1 over-expressing lines 35s:HY1-3/1-4 to osmotic and salt stresses. Further results showed that, compared with wild type, hy1-100 mutant displayed hypersensitive phynotype, whereas 35s:HY1-3/1-4 was insensitive to exogenous NaCl and mannitol. Application of the HO-1 inducer haemin and potent inhibitor ZnPP can alleviate or aggravate the osmotic or salt, stress-induced inhibition of fresh weight and primary root growth. No significant response of hy1-100 mutant was obsereved when haemin was added upon stress conditions. Meanwhile, ZnPP slightly aggravates growth inhibition of hy1-100 mutant upon both osmotic and salt stresses. Further analysis discovered that both CO and BR were the effective by-product of HO modulating primary and latral root development when Arabidopsis seedlings were exposed to stresses. Interestingly, althought hy1-100 mutant exhibited hypersensitive phenotyes, different survive rates under osmotic and salt stresses were oberseved. By using real-time PCR analyses, we found that the inductions of both stress response and ABA metabolism genes expression were much higher in hy1-100 mutant than those of wild type under osmotic stress. Whereas opposite phenonmen were observed in salt stress condition. Additionally, ABA treatment results in the induction of HY1 expression, and the germination inhibition of hy1-100 was hypersensitive to exogenous ABA. Oppssite results were also found in 35s:HY1-3/1-4 plants. Finally, we also noticed that enhanced drought resistance of hy1-100 mutant plants was due to an efficient stomatal closure and inhibition of opening induced by ABA.
Former results showed that HY1 is a key component of the Arabidopsis salt acclimation. hy1-100 mutant displayed hypersensitive to salt stress, whereas the HY1 over expression line (35S:HY1) showed salt tolerant phenotype. Nitric oxide (NO) has been demonstrated to play an important role in salt stress signaling. However, the relationship between HY1 and endogenous NO function under salt stress was still unknown. In this chapter, we studied the origin of NO under salt stress by combined using pharmacological and genetic approaches, and the relationship between HY1 and nitrate reductase (NR)-derived NO production were also discussed. The results showed that the both NR and L-argine (L-Arg) pathway were responsible for NaCl-triggered NO generation. NR inihibitor tungstate and mammalian nitric oxide synthase (NOS) inihibitor NG-nitro-L-arginine methyl ester hydrochloride (L-NAME) were able to block the NO generation induced by NaCl; meanwhile, root growth inhibition and fresh weight accumulation of wild-type induced by NaCl were also aggravated. The transcription levels of NIA1, NIA2 and nitric oxide associated 1 (NOA1) in wild-type roots were also induced by NaCl treatment. By contrast, NR mutant nia1-1/2-5, NOA1 mutant noal and nia1-1/2-5/noal failed to accumulate NO under salt stress, whereas the application of NO donor sodium nitroprusside (SNP) could increase NO production. Above results indicated that NO generation in Arabidopsis roots induced by NaCl is related to NR and NOA1 up-regulation. Moreover, nia1-1/2-5, noa1 and nia1-1/2-5/noa1 are all hypersensitive to NaCl stress, which could be partially rescued by exogenous NO donor diethylamine/nitric oxide adduct (NONOate). We next compared the differences of NO generation between WT, hy1-100, ho2, ho3 mutant under salt stress. The results showed that more NO production could be observed in hy1-100 mutant seedling root under salt stress. Interestingly, NO donor NONOate failed to alleviate the hypersensitivity phenotype of hy1-100 mutant upon NaCl during germination period, whereas the NO scavenger 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (PTIO) reversed the salt tolerance phenotype of 35S:HY1-3. HO-1 inducer haemin could alleviate germination and cotyledon opening inhibition of WT seeds under salt stress. Whereas weak alleviation can be observed in noal mutant seedlings, and haemin failed to alleviate hypersensitivity phenotype of nia1-1/2-5 and nia1-1/2-5/noa1 mutants under salt stress. These results indicate that a cross-talk might exist between NR-derived NO and HY1 function during salt stress signaling, both of which are necessary for Arabidopsis salt tolerance.
Previous research demonstrated that the soybean HO can respond to ultraviolet (UV) radiation. The induction of HO can alleviate oxidative damage caused by UV-B radiation, the ROS may be involved in this process (Yannarelli et al.,2006). However, detailed genetic evidence is required for further investigating the mechanism of HO in regulating UV-B radiation response. In this chapter, we examined the responses of four HO genes under UV-C radiation in Arabidopsis. The difference between wild-type and hy1-100 mutant for flavonoid biosynthetic metabolism and antioxidant defence system in response to UV-C was also studied. The results showed that, compared with the wild type, the hypersensitivity of hy1-100 mutant in response to UV-C radiation appeared, and this was due to its low level of flavonoid biosynthetic metabolism. Compared with the wild-type, hy1-100 contained less UV-absorbing compounds, and the down-regulating of the transcripts of four key enzymes for the flavonoid biosynthetic metabolism (chalcone synthase (CHS), chalcone isomerase(CHI), flavonoid 3-hydroxylase (F3H), and flavonol synthase (FLS)) were also found, respectively. Moreover, four key genes in the Arabidopsis wild-type flavonoid biosynthetic metabolism were significantly induced after UV-C radiation, whereas in the hy1-100 mutant, the induction of CHS and FLS is partially blocked and CHS expression is reversed significantly. We further hypothesis that this suppression of hy1-100 mutant might due to its interruption of the UV signal perception. For example, the expression of transduction factor HY5, HYH (HY5 homolog), MYB11 and MYB12 in the root of wild-type can be markedly induced by UV-C radiation, whereas partially inhibited in hyl-100 mutant. Furthermore, the results of real-time PCR analysis indicated that the hyper-sensitivity of the hy1-100 mutant in response to UV-C radiation may also be contributed to the failure in induction of the antioxidant defence genes expression, such as CSD1 (Cu/Zn superoxide dismutase 1), CAT1 (catalasel), CAT2 (catalase2), FSDl (Fe superoxide dismutase), cAPXl (cytosolic ascorbate peroxidase 1), and cAPX2 (cytosolic ascorbate peroxidase 2).
引文
曹鸣庆.植物的耐盐性及其改良[M].北京：中国农业出版社,1989.
林栖凤.耐盐植物研究[M].北京：科学出版社,2004.
赵可夫.作物抗性生理[M].北京：农业出版社,1990.
赵可夫.盐分胁迫和水分胁迫对盐生和非盐生植物细胞膜脂过氧化作用的效应[J].植物学报,1993,35(7)：519-523.
赵可夫,李法曾.中国盐生植物[M].北京：科学出版社,1999.
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K.. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acidsignaling. Plant Cell, 2003;15:63-78.
Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell, 1997; 9:1859-1868.
Ahanger AA, Prawez S, Leo MD, et al. Pro-healing potential of hemin: an inducer of heme oxygenase-1. Eur J Pharmacol,2010; 645:165-170.
Amzallag G.N, Lerner HR, Poljakoff-Mayber A. Induction of increased salt tolerance in Sorghum bicolor by NaCl pretreatment. J Exp Bot,1990; 41:29-34.
Anand B, Surana P, Bhogaraju S, Pahari S, Prakash B. Circularly permuted GTPase YqeH binds 30S ribosomal subunit: implications for its role in ribosome assemble. Biochem Biophys Res Commmun,2009; 386:602-606.
Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell,1998; 1:213-222.
Arnaud N, Murgia I, Boucherez J, Briat JF, Cellier F,Gaymard F. An iron-induced nitric oxide burst precedes ubiquitin-dependent protein degradation for Arabidopsis AtFerl ferritin gene expression. J Biol Chem,2006; 281:23579-23588.
Asai S and Yoshioka H. Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botryis cinerea in Nicotiana benthamiana. Mol Plant Microbe Interact,2009; 22:619-629.
Aubert S, Hennion F, Bouchereau A, et al. Subcellular compartmentation of proline in the leaves of the subantartic Kerguelen cabbage Pringlea antiscorbutica R.Br. in vivo 13C-NMR study. Plant Cell Environ,1999; 22:255-259.
Azevedo H, Amorim-Silva V, Tavaers RM. Effect of salt on ROS homeostasis, lipid peroxidation and antioxidant mechanisms in Pinus pinaster suspension cells. Ann For Sci,2009; 66:211.
Balestrasse KB, Noriega GO, Batlle AMC, Tomaro ML. Involvement of heme oxygenase as antioxidant defence in soybean nodules. Free Rad Res,2005; 39:145-151.
Balestrasse KB, Zilli CG, Tomaro ML. Signal transduction patyways and haem oxygenase induction in soybean leaves subjected to salt stress. Redox Rep,2008; 13:255-262.
Baranano DE, Rao M, Ferris CD, Snydern SH. Biliverdin reductase:a major physiologic cytoprotectant. Proc Natl Acad Sci USA,2002; 99:16093-16098.
Bauer, M., Huse, K., Settmacher, U. and Claus, R.A. (2008) The heme oxygenase-carbon monoxide system: regulation and role in stress response and organ failure. Intensive Care Med,2008; 34: 640-648.
Beauchamp C, Fridovich I. Superoxide dismutase:improved assays and an assay applicable to acrylamide gels. Anal Biochem,1971; 44:276-287.
Bellincampi D, Dipierro N, Salvi G, Cervone F, De Lorenzo G. Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol,2000; 122:1379-1386.
Bethke PC, Badger MR, Jones RL. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell,2004; 16:332-341.
Bethke PC, Drew MC. Stomatal and nonstomatal components to inhibition of photosynthesis in leaves of Capsicum annuum during progressive exposure to NaCl salinity. Plant Physiol,1992; 99:219-226.
Besson-Bard A, Griveau S, Bedioui F, Wendehenne D. Real-time electrochemical detection of extracellular nitric oxide in tobacco cells exposed to cryptogein, an elicitor of defence responses. J Exp Bot,2008a; 59:3407-3414.
Besson-Bard A, Pugin A, Wendehenne D. New insights into nitric oxide signaling in plants. Annu Rev Plant Biol,2008b; 59:21-39.
Boczkowski J, Poderoso JJ, Motterlini R. CO-metal interaction: vital signaling from a lethal gas. Trends Biochem Sci,2006; 31:614-621.
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J. Growth stage-based phenotypic analysis of Arabidopsis:a model for high throughput functional genomics in plants. Plant Cell,2001; 13:1499-1510.
Blumwald E. Sodium transport and salt tolerance in plants. Curr Opin Cell Biol,2000; 12:431-434.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem,1976; 72:248-54.
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ. ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J,2006; 45:113-122.
Cao ZY, Huang BK, Wang QY, Xuan W, Ling TF, et al. Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway. Chin Sci Bull,2007a; 52:2365-2373.
Cao Z, Xuan W, Liu Z, Li X, Zhao N, Xu P, Wang Z, Guan R, Shen W. Carbon monoxide promotes lateral root formation in rapeseed. J Integr Plant Biol,2007b; 49:1070-1079.
Carmi A, Staden JV. Role of roots in regulating the growth rate and cytokinin content in leaves. Plant Physiol,1983; 73:76-78.
Castells E, Molinier J, Drevensek S, Genschik P, Barneche F, Bowler C. detl-1-induced UV-C hyposensitivity through UVR3 and PHR1 photolyase gene over-expression. Plant J,2010,63: 392-404.
Chandok MR, Ytterberg AJ, van Wijk KJ, Klessig DF. The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex. Cell,2003; 113: 469-482.
Chen XY, Ding X, Xu S, Wang R, Xuan W, Cao ZY, Chen J, Wu HH, Ye MB, Shen WB. Endogenous hydrogen peroxide plays a positive role in the upregulation of heme oxygenase and acclimation to oxidative stress in wheat seedling leaves. J Integr Plant Biol,2009; 51:951-960.
Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L. Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA, 2008; 105:4495-4500.
Chinnusamy, V., Schumaker, K. and Zhu, J.K. Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot,2004; 55:225-236.
Clough SJ, Bent AF. Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J,1998; 16:735-743.
Crawford NM. Nitrate: nutrient and signal for plant growth. Plant Cell,1995; 7:859-868.
Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A. Plant nitric oxide synthase:back to square one-response. Trends Plant Sci,2006; 11:526-527.
Cordoba-Pedregosa MC, Gonzalez-Reyes JA, Canadillas M, Navas P, Cordoba F. Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol,1996; 112: 1119-1125.
Corpas FJ, Chaki M, Fernandez-Ocana A, et al. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol,2008; 49:1711-1722.
Cui W, Fu GEQ Wu H, Shen W. Cadmium-induced heme oxygenase-1 gene expression is associated with the depletion of glutathione in the roots of Medicago sativa. Biometals,2011; 24:93-103.
Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U. Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil,2006; 284:363-373.
Davis SJ, Bhoo SH, Durski AM, Walker JM, Vierstra RD. The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol,2001; 126:656-669.
Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F. Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci,2000; 57:779-795.
D'Autreaux B, Toledano MB. ROS as signaling molecules:mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol,2007; 8:813-824.
Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V, Schlauch, K. and Mittler, R. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell,2005; 17:268-281.
de Azevedo Neto AD, Prisco JT, Eneas-Filho J, Medeiros JR, Gomes-Filho E. Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. J Plant Physiol,2005; 162: 1114-1122.
Dean JV and Harper JE. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol,1988; 88:389-395.
De Michele E, Vurro E, Rigo C, et al. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol,2009; 150:217-228.
Delledonne M, Xia Y, Dixon RA, Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature,1998; 394:585-588.
Desikan R, Griffiths R, Hancock J, Neill S. A new role for an old enzyme:nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA,2002; 99:16314-16318.
Ding M, Hou P, Shen X, et al. Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol,2010; 73:251-269.
Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U. Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil,2006; 284:363-373.
Dolan L and Davies J. Cell expansion in roots. Curr Opin Plant Biol,2004; 7:33-39.
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. OsDREB genes in rice, Oryza sativa L, encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant Journal,2003; 33: 751-763.
Dulak J, Jozkowicz A. Carbon monoxide-a "new" gaseous modulator of gene expression. Acta Biochim Pol,2003; 50:31-47.
Durner J, Wendehenne D, Klessig DF. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA,1998; 95:10328-10333.
Emborg TJ, Walker JM, Noh B, Vierstra RD. Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiol,2006; 140: 856-868.
Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM. The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell,1998; 10:1043-1054.
Flores-Perez U, Sauret-Gueto S, Gas E, Jarvis P, Rodriguez-Concepcion M. A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell,2008; 20:1303-1315.
Foreman J, Demidchik V, Bothwell JH, et al, Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature,2003; 422:442-446.
Frahry G, Schopfer P. NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta,2001; 212:175-1783.
Frankel D, Mehindate K, Schipper HM. Role of heme oxygenase-1 in the regulation of manganese superoxide dismutase gene expression in oxidatively challenged astroglia. J Cell Physiol,2000; 185: 80-86.
Gao L, Mann GE. Vascular NAD(P)H oxidase activation in diabetes:a double-edged sword in redox signaling. Cardiovasc Res,2009; 82:9-20.
Gaupels F, Furch ACU, Will T, Mur LAJ, Kogel K H, Van Bel AJE. Nitric oxide generation in Vicia faba phloem cells reveals them to be sensitive detectors as well as possible systemic transducers of stress signals. New Phytol,2008; 178:634-646.
Gisk B, Yasui Y, Kohchi T, Frankenberg-Dinkel N. Characterization of the haem oxygenase protein family in Arabidopsis thaliana reveals a diversity of functions. Biochem J,2010; 425:425-434.
Gniazdowska A, Krasuska U, Debska K, Andryka P, Bogatek R. The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta,2010; 232:999-1005.
Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol, 1980; 31:149-190.
Gulick P, Dvorak J. Gene induction and repression by salt treatment in roots of the salinity-sensitive Chinese Spring wheat and the salinity-tolerant Chinese Spring wheat x Elytrigia elongate amphiploid. Proc Natl Acad Sci USA,1987; 84:99-103.
Guo FQ and Crawford NM. Arabidopsis nitric oxide synthase 1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell,2005; 1.7:3436-3450.
Guo FQ, Okamoto M, Crawford NM. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science,2003; 302:100-103.
Guo K, Kong WW, Yang ZM. Carbon monoxide promotes root hair development in tomato. Plant Cell Environ,2009; 32:1033-1045.
Han Y, Zhang J, Chen X, Gao Z, Xuan W, Xu S, Ding X, Shen W. Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytol,2008; 177:155-166.
Han Y, Xuan W, Yu T, et al. Exogenous hematin alleviates mercury-induced oxidative damage in the roots of Medicago sativa. J Integr Plant Biol,2007; 49:1703-1713.
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. Plant cellular and molecular responses to high salinity. Annu Rev of Plant Physiol Plant Mol Biol,2000; 51:463-499.
He JM, Bai XL, Wang RB, Cao B, She XP. The involvement of nitric oxide in ultraviolet-B-inhibited pollen germination and tube growth of Paulownia tomentosa in vitro. Physiol Plant,2007; 131: 273-282.
Huang BK, Xu S, Xuan W, et al. Carbon monoxide alleviates salt-induced oxidative damage in wheat seedling leaves. J Integr Plant Biol,2006; 48:249-254.
Huang JJ, Han B, Xu S, Zhou MX, Shen WB. Heme oxygenase-1 is involved in the cytokinin-induced alleviation of senescence in detached wheat leaves during dark incubation. J Plant Physiol,2011; 168:768-775.
Jiang MY, Zhang JH. Involvement of plasma-membrane NADPH oxidase in abscisic acid-and water stress-induced antioxidant defense in leaves of maize seedlings. Planta,2002; 215:1022-1030.
Jenkins. Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol,2009; 60:407-430.
Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV. Different signaling and cell death roles of heterotrimeric G protein a and β subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell,2005; 17:957-970.
Jubany-Mari T, Munne-Bosch S, Lopez-Carbonell M, Alegre L. Hydrogen peroxide is involved in the acclimation of the Mediterranean shrub, Cistus albidus L., to summer drought. J Exp Bot,2009; 60: 107-120.
Kacperska A. Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol Plant,2004; 122:159-168.
Kim HP, Ryter SW, Choi AMK. CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol,2006; 46:411-449.
Kliebenstein DJ, Lim JE, Landry LG, Last RL. Arabidopsis UVR8 regulates Ultraviolet-B signal transduction and tolerance and contains sequence similarity to human Regulator of Chromatin Condenssation 1. Plant Physiol,2002; 130:234-243.
Kolbert Z, Bartha B, Erdei L. Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol,2008; 165:967-975.
Kopyra M, Gwozdz EA. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem,2003; 41: 1011-1017.
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R. ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem,2008; 283:34197-34203.
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidpsis. EMBO J,2003; 22:2623-2633.
Laloi C, Apel K, Danon A. Reactive oxygen signalling: the latest news. Curr Opin Plant Biol,2004; 7: 323-328.
Lambeth JD. Nox enzymes and the biology of reactive oxygen. Nature Rev Immunol,2004; 4:181-189.
Leshem Y, Seri L, Levine A. Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J,2007; 51:185-197.
Limam F, Chahed K, Ouelhazi N, Ghrir R, Ouelhazi L. Phytohormone regulation of isoperoxidases in Catharanthus roseus suspension cultures. Phytochem,1998; 49:1219-1225.
Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J. Exp. Bot,2009; 60:3221-3238.
Lin CC, Kao CH. Cell wall peroxidase against ferulic acid, lignin, and NaCl-reduced root growth of rice seedlings. J Plant Physiol,2001; 158:667-671.
Ling T, Zhang B, Cui W, Wu M, Lin J, et al. Carbon monoxide mitigates salt-induced inhibition of root growth and suppresses programmed cell death in wheat primary roots by inhibiting superoxide anion overproduction. Plant Sci,2009; 177:331-340.
Liu KL, Xu S, Xuan W, et al. Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa. Plant Sci,2007; 172:544-555.
Liu Y, Wu R, Wan Q, Xie G, Bi Y. Glucose-6-phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. Plant Cell Physiol,2007; 48:511-522.
Liu YH, Xu S, Ling TF, Xu LL, Shen WB. Heme oxygenase/carbon monoxide system participates in regulating wheat seed germination under osmotic stress involving the nitric oxide pathway. J Plant Physiol,2010; 167:1371-1379.
Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D. Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J,2008; 56:575-589.
Matsumoto H, Ishikawa K, Itabe H, Maruyama Y. Carbon monoxide and bilirubin from heme oxygenase-1 suppresses reactive oxygen species generation and plasminogen activator inhibitor-1 induction. Mol Cell Biochem,2006; 291:21-28.
Mazel, A., Leshem, Y., Tiwari, B.S. and Levine, A. Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7(AtRabG3e). Plant Physiol, 2004; 134:118-128.
Meloni DA, Oliva MA, Martinez CA, Cambraia J. Photosynthesis and activity of superoxide dismutase, peroxidase and glutat hione reductase in cotton under salt stress. Environ Exp Bot,2003; 49:69-76.
Millar AA, Jacobsen JV, Ross JJ, Helliwell CA, Poole AT, Scofield G, Reid JB. Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8'-hydroxylase. Plant J,2005; 45: 942-954.
Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal,2009; 2:ra45.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ,2010; 33:453-167.
Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci,2002; 7:405-410.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci,2004; 9:490-498.
Modolo LV, Augusto O, Almeida IMG, Pinto-Maglio CAF, Oliveira HC, Seligman K, Salgado I. Decreased arginine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Sci, 2006;171:34-40.
Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF. AtNOS/AtNOAl is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J Biol Chem,2008; 283:32957-32967.
Muller K, Carstens AC, Linkies A, Torres MA, Leubner-Metzger G. The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol,2009; 184:885-897.
Munns R and Tester. Mechanisms of Salinity tolerance. Annu Rev Plant Biol,2008; 59:651-681.
Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM. The Arabidopsis photomorphogenic mutant hyl is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell,1999; 11:335-348.
Muramoto T, Tsurui N, Terry MJ, Yokota A, Kohchi T. Expression and Biochemical Properties of a Ferredoxin-Dependent Heme Oxygenase Required for Phytochrome Chromophore Synthesis. Plant Physiol,2002; 130:1958-1966.
Murata Y, Pei ZM, Mori IC, Schroeder JI. Abscisic acidactivation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in dbil-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell,2001; 13:2513-2523.
Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell,2002; 14:3089-3099.
Nagahashi G, Leonard RT, Thomson WW. Purification of plasma membranes from roots of barley: specificity of the phosphotungstic acid-chromic acid strain. Plant Physiol,1978; 61:993-999.
Nanjo T, Kobayashi M, Yoshiba Y et al., Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J,1999; 18:185-193.
Nakahira K, Kim HP, Geng XH, et al. Carbon monoxide differentially inhibits TLR signaling pathway by regulating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med,2006; 203:2377-2389.
Neill SJ, Desikan R, Hancock JT. Hydrogen peroxide signalling. Curr Opin Plant Biol,2002; 5: 388-395.
Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I. Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot,2008; 59:165-176.
Noriega GO, Balestrasse KB, Batlle A, Tomaro ML. Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Biophys Res Commun,2004; 323:1003-1008.
Noriega GO, Yannarelli GG, Balestrasse KB, Batlle A, Tomaro ML. The effect of nitric oxide on heme oxygenase gene expression in soybean leaves. Planta,2007; 226:1155-1163.
Oliveira HC, Justino GC, Sodek L, Salgado I. Amino acid recovery does not prevent susceptibility to Pseudomonas syringae in nitrate reductase double-deficient Arabidopsis thaliana plants. Plant Sci, 2009; 176:105-111.
Oravecz A, Baumann A, Mate Z, et al. CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell,2006; 18:1975-1990.
Overmyer K, Brosche M, Kangasjarvi J. Reactive oxygen species and hormonal control of cell death. Trends Plant Sci,2003; 8:335-342.
Passardi F, Penel C, Dunand C. Performing the paradoxical:how plant peroxidases modify the cell wall. Trends Plant Sci,2004; 9:534-540.
Piantadosi CA. Carbon monoxide, reactive oxygen signaling, and oxidative stress. Free Radic Biol Med, 2008; 45:562-569.
Planchet E, Gupta KJ, Sonoda M, Kaiser WM. Nitric oxide emission from tobacco leaves and cell suspensions:rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J,2005; 41:732-743.
Pogany M, von Rad U, Grun S, Dong6 A, Pintye A, Simoneau P, Bahnweg G, Kiss L, Barna B, Durner J. Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol,2009; 151:1459-1475.
Pompella A, Maellaro E, Casini AF, Comporti M. Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Am J Pathol,1987; 129:295-301.
Quan LJ, Zhang B, Shi WW, Li HY. Hydrogen peroxide in plants:a versatile molecule of the reactive oxygen species network. J Integr Plant Biol,2008; 50:2-18.
Rhee SG. H2O2, a necessary evil for cell signaling. Science,2006; 312:1882-1883.
Ribeiro DM, Desikan R, Bright J, Confraria A, Harrison J, Hancock JT, Barros RS, Neill SJ, Wilson ID. Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ,2009; 32:46-57.
Rizzini L, Favory JJ, Cloix C, et al., Perception of UV-B by the Arabidopsis UVR8 protein. Science, 2011; 332:103-106.
Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot,2002; 53:103-110.
Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A,Corpas FJ, Gomez M, Del Rio LA, Sandalio LM. Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ,2006; 29:1532-1544.
Ruggiero B, Koiwa H, Manabe Y, et al., Uncoupling the effects of abscisic acid on plant growth and water relations. Analysis of stol/nced3, an abscisic acid-deficient byt salt stress-tolerant. Plant Physiol,2004; 136:3134-3147.
Rumer S, Gupta KJ, Kaiser WM. Plant cells oxidize hydroxylamines to NO. J Exp Bot,2009; 60: 2065-2072.
Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide:from basic science to therapeutic applications. Physiol Rev,2006; 86:583-650.
Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R. Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell,2004; 16:616-628.
Sakihama Y, Nakamura S, Yamasaki H. Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organism. Plant Cell Physiol,2002; 43:290-297.
Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M. Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. J Integr Plant Biol, 2008; 50:231-243.
Saito S, Yamamoto-KatouA, Yoshioka H, Doke N, Kawakita K. Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells. Plant Cell Physiol,2006; 47:689-697.
Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki KMonitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell,2001; 13:61-72.
Seligman K, Saviani EE, Oliveira HC, Pinto-Maglio CA, Salgado I. Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants. Plant Cell Physiol,2008; 49:1112-1121.
Shekhawat GS, Verma K. Haem oxygenase (HO):an overlooked enzyme of plant metabolism and defence. J Exp Bot,2010; 61:2255-2270.
Shi FM and Li YZ. Verticillium dahliae toxins-induced nitric oxide production in Arabidopsis is major dependent on nitrate reductase. BMB Rep,2009; 41:79-85.
Siegel SM, Renwick G, Roen LA. Formation of carbon monoxide during seed germination and seedling growth. Science,1962; 137:683-684.
Silveira JAG, Melo ARB, Viegas RA, Oliveira JTA. Salinity-induced effects on nitrogen assimilation related to growth in cowpea plants. Environ Exp Bot,2001; 46:171-179.
Simon-Plas F, Elmayan T, Blein JP. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J,2002; 31:137-147.
Srivastava N, Gonugunta VK, Puli MR, Raghavendra AS. Nitric oxide production occurs downstream of reactive oxygen species in guard cells during stomatal closure induced by chitosan in abaxial epidermis of Pisum sativum. Planta,2009; 229:757-765.
Stocker R. Antioxidant activities of bile pigment. Antioxid Redox Signal,2004; 6:841-849.
Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis seedling. Plant J,2007; 50:660-677.
Sudhamsu J, Lee GI, Klessig DF, Crane BR. The structure of YqeH. An AtNOSl/AtNOAl ortholog that couples GTP hydrolysis to molecular recognition. J Biol Chem,2008; 283:32968-32976.
Suttner DM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J,1999; 13:1800-1809.
Tischner R, Galli M, Heimer YM, Bielefeld S, Okamoto M, Mack A, Crawford NM. Interference with the citrulline-based nitric oxide synthase assay by argininosuccinate lyase activity in Arabidopsis extracts. FEBS J,2007; 274:4238-4245.
Torres MA, Dangl JL. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Cur Opin Plant Biol,2005; 8:397-403.
Torres MA, Dangl JL, Jones JD. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA,2002; 99:517-522.
Torres MA, Jones JDG, Dangl JL. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet,2005; 37: 1130-1134.
Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JDG. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91(phox)). Plant J,1998; 14: 365-370.
Toufighi K, Brady SM, Austin R, Ly E, and Provart NJ. The botany Array Resource:e-Northerns, Expression Angling, and promoter analyses. Plant J,2005; 43:153-163.
Tun NN, Livaja M, Kieber JJ, Scherer GF.Zeatin-induced nitric oxide (NO) biosynthesis in Arabidopsis thaliana mutants of NO biosynthesis and of two-component signaling genes. New Phytol,2008; 178: 515-531.
Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol, 2006; 47:346-354.
Turkseven S, Kruger A, Mingone CJ, et al. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol,2005; 289:701-707.
Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci,2002; 163:515-523.
Umezawa T, Shimizu K, Kato M, Ueda T. Enhancement of salt tolerance in soybean with NaCl pretreatment. Physiol Plant,2000; 110:59-63.
Umezawa T, Okamoto M, Kushiro T, Nambara E, Oono Y, Seki M, Kobayashi M, Koshiba T, Kamiya Y, Shinozaki K. CYP707A3, a major ABA 8'-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. Plant J,2006; 46:171-182.
Van Breusegem F, Bailey-Serres J, Mittler R. Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol,2008; 147:978-984.
Vinocur B and Altman A. Recent advances in engineering plant tolerance to abiotic stress:achievements and limitations. Curr Opin Biotech,2005; 16:123-132.
Wang R, Chen S, Zhou X, et al. Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol,2008a; 28:947-957.
Wang YH, Chen T, Zhang CY, et al. Nitric oxide modulates the influx of extracellular Ca2+ and actin filament organization during cell wall construction in Pinus bungeana pollen tubes. New Phytol, 2009;182:851-862.
Wang ZY, Li FM, Xiong YC, Xu BC. Soil-water threshold range of chemical signals and drought tolerance was mediated by ROS homeostasis in winter wheat during progressive soil drying. J Plant Growth Regul,2008b; 27:309-319.
Wilks A. Heme oxygenase:evolution, structure, and mechanism. Antioxid Redox Signal,2002; 4: 603-614.
Wilks S. Carbon monoxide in grenn plants. Science,1959; 129:964-966.
Wu M, Huang J, Xu S, Ling T, Xie Y, Shen W. Haem oxygenase delays programmed cell death in wheat aleurone layers by modulation of hydrogen peroxide metabolism. J Exp Bot,2011; 62:235-48.
Wu SJ, Qi JL, Zhang WJ, et al. Nitric oxide regulates shikonin formation in suspension-cultured Onosma paniculatum cells. Plant Cell Physiol,2009; 50:118-128.
Xie Y, Ling T, Han Y, et al. Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant Cell Environ,2008; 31:1864-1881.
Xie Y, Xu S, Han B, et al. Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J,2011; 66:280-292.
Xing T, Higgins VJ, Blumwald E. Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells. Plant Cell, 1997; 9:249-259.
Xu Q, Xu X, Zhao Y, et al. Salicylic acid, hydrogen peroxide and calcium-induced saline tolerance associated with endogenous hydrogen peroxide homeostasis in naked oat seedlings. Plant Growth Regul,2008; 54:249-259.
Xu S, Zhang B, Cao ZY, Ling TF, Shen WB. Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals,2011; 24:181-191.
Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, Ye MB, Shen WB. The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol,2008; 148:881-893.
Yamamoto-Katou A, Katou S, Yoshioka H, Doke N, Kawakita K. Nitrate reductase is responsible for elicitin-induced nitric oxide production in Nicotiana benthamiana. Plant Cell Physiol,2006; 47: 726-735.
Yamamoto Y, Kobayashi Y, Matsumoto H. Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol,2001; 125: 199-208.
Yamasaki H and Sakihama Y. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett, 2000; 468:89-92.
Yang Y, Xu S, An L, Chen N. NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. J Plant Physiol, 2007; 164:1429-1435.
Yannarelli GG, Noriega GO, Batlle A, Tomaro ML, Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta,2006; 224:1154-1162.
Yoshiba Y, Kiyosue T. Regulation of levels of proline as osmolyte in plants under water stress. Plant Cell Physiol,1997; 83:1095-1102.
Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J. Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci USA,2004; 101:15811-15816.
Zemojtel T, Frohlich A, Palmieri MC, et al. Plant nitric oxide synthase:a never-ending story? Trends Plant Sci,2006; 11:524-525.
Zhang JZ, Creelman RA, Zhu JK. From laboratory to field. Using information from Arabidopsis to engineer salt, cold and drought tolerance in crops. Plant Physiol,2004; 135:615-621.
Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta, 2006; 224:545-555.
Zhang Y, Zhu H, Zhang Q, et al. Phospholipase Dal and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell,2009; 21:2357-2377.
Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol,2004; 134:849-857.
Zhao MG, Tian QY, Zhang WH. Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol,2007; 144:206-217.
Zhu J, Liu J, Xiong L. Genetic analysis of salt tolerance in Arabidopsis:evidence for a critical role of potassium nutrition. Plant Cell,1998; 10:1181-1191.
Zhu JK. Plant salt tolerance. Trends Plant Sci,2001; 6:66-71.
Zhu JK. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol,2003; 6:441-445.
Zhu JK. Plant salt tolerance. Trends Plant Sci,2001; 6:66-71.
Zhu S, Yu X, Wang X, et al. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell,2007; 19:3019-3036.
Zhu X, Fan WG, Li DP, Lin MC, Kung H. Heme oxygenase-1 system and gastrointestinal tumors. World J Gastroenterol,2010; 16:2633-2637.
Zilli CG, Balestrasse KB, Yannarelli GG, Polizio AH, Santa-Cruz DM, Tomaro ML. Heme oxygenase up-regulation under salt stress protects nitrogen metabolism in nodules of soybean plants. Environ Exp Bot,2008; 64:83-89.
Zilli CG, Santa-Cruz DM, Yannarelli GG, Noriega GO, Tomaro ML, et al. Heme oxygenase contributes to alleviate salinity damage in Glycine max L. leaves. Int J Cell Biol,2009; 2009:1-9.
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol,2004; 136:2621-2632.
Zottini M, Costa A, De Michele R, Ruzzene M, Carimi F,Lo Schiavo F. Salicylic acid activates nitric oxide synthesis in Arabidopsis. J Exp Bot,2007; 58:1397-1405.
林栖凤.耐盐植物研究[M].北京：科学出版社,2004.
赵可夫.作物抗性生理[M].北京：农业出版社,1990.
赵可夫.盐分胁迫和水分胁迫对盐生和非盐生植物细胞膜脂过氧化作用的效应[J].植物学报,1993,35(7)：519-523.
赵可夫,李法曾.中国盐生植物[M].北京：科学出版社,1999.
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K.. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acidsignaling. Plant Cell, 2003;15:63-78.
Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell, 1997; 9:1859-1868.
Ahanger AA, Prawez S, Leo MD, et al. Pro-healing potential of hemin: an inducer of heme oxygenase-1. Eur J Pharmacol,2010; 645:165-170.
Amzallag G.N, Lerner HR, Poljakoff-Mayber A. Induction of increased salt tolerance in Sorghum bicolor by NaCl pretreatment. J Exp Bot,1990; 41:29-34.
Anand B, Surana P, Bhogaraju S, Pahari S, Prakash B. Circularly permuted GTPase YqeH binds 30S ribosomal subunit: implications for its role in ribosome assemble. Biochem Biophys Res Commmun,2009; 386:602-606.
Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell,1998; 1:213-222.
Arnaud N, Murgia I, Boucherez J, Briat JF, Cellier F,Gaymard F. An iron-induced nitric oxide burst precedes ubiquitin-dependent protein degradation for Arabidopsis AtFerl ferritin gene expression. J Biol Chem,2006; 281:23579-23588.
Asai S and Yoshioka H. Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botryis cinerea in Nicotiana benthamiana. Mol Plant Microbe Interact,2009; 22:619-629.
Aubert S, Hennion F, Bouchereau A, et al. Subcellular compartmentation of proline in the leaves of the subantartic Kerguelen cabbage Pringlea antiscorbutica R.Br. in vivo 13C-NMR study. Plant Cell Environ,1999; 22:255-259.
Azevedo H, Amorim-Silva V, Tavaers RM. Effect of salt on ROS homeostasis, lipid peroxidation and antioxidant mechanisms in Pinus pinaster suspension cells. Ann For Sci,2009; 66:211.
Balestrasse KB, Noriega GO, Batlle AMC, Tomaro ML. Involvement of heme oxygenase as antioxidant defence in soybean nodules. Free Rad Res,2005; 39:145-151.
Balestrasse KB, Zilli CG, Tomaro ML. Signal transduction patyways and haem oxygenase induction in soybean leaves subjected to salt stress. Redox Rep,2008; 13:255-262.
Baranano DE, Rao M, Ferris CD, Snydern SH. Biliverdin reductase:a major physiologic cytoprotectant. Proc Natl Acad Sci USA,2002; 99:16093-16098.
Bauer, M., Huse, K., Settmacher, U. and Claus, R.A. (2008) The heme oxygenase-carbon monoxide system: regulation and role in stress response and organ failure. Intensive Care Med,2008; 34: 640-648.
Beauchamp C, Fridovich I. Superoxide dismutase:improved assays and an assay applicable to acrylamide gels. Anal Biochem,1971; 44:276-287.
Bellincampi D, Dipierro N, Salvi G, Cervone F, De Lorenzo G. Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol,2000; 122:1379-1386.
Bethke PC, Badger MR, Jones RL. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell,2004; 16:332-341.
Bethke PC, Drew MC. Stomatal and nonstomatal components to inhibition of photosynthesis in leaves of Capsicum annuum during progressive exposure to NaCl salinity. Plant Physiol,1992; 99:219-226.
Besson-Bard A, Griveau S, Bedioui F, Wendehenne D. Real-time electrochemical detection of extracellular nitric oxide in tobacco cells exposed to cryptogein, an elicitor of defence responses. J Exp Bot,2008a; 59:3407-3414.
Besson-Bard A, Pugin A, Wendehenne D. New insights into nitric oxide signaling in plants. Annu Rev Plant Biol,2008b; 59:21-39.
Boczkowski J, Poderoso JJ, Motterlini R. CO-metal interaction: vital signaling from a lethal gas. Trends Biochem Sci,2006; 31:614-621.
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J. Growth stage-based phenotypic analysis of Arabidopsis:a model for high throughput functional genomics in plants. Plant Cell,2001; 13:1499-1510.
Blumwald E. Sodium transport and salt tolerance in plants. Curr Opin Cell Biol,2000; 12:431-434.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem,1976; 72:248-54.
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ. ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J,2006; 45:113-122.
Cao ZY, Huang BK, Wang QY, Xuan W, Ling TF, et al. Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway. Chin Sci Bull,2007a; 52:2365-2373.
Cao Z, Xuan W, Liu Z, Li X, Zhao N, Xu P, Wang Z, Guan R, Shen W. Carbon monoxide promotes lateral root formation in rapeseed. J Integr Plant Biol,2007b; 49:1070-1079.
Carmi A, Staden JV. Role of roots in regulating the growth rate and cytokinin content in leaves. Plant Physiol,1983; 73:76-78.
Castells E, Molinier J, Drevensek S, Genschik P, Barneche F, Bowler C. detl-1-induced UV-C hyposensitivity through UVR3 and PHR1 photolyase gene over-expression. Plant J,2010,63: 392-404.
Chandok MR, Ytterberg AJ, van Wijk KJ, Klessig DF. The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex. Cell,2003; 113: 469-482.
Chen XY, Ding X, Xu S, Wang R, Xuan W, Cao ZY, Chen J, Wu HH, Ye MB, Shen WB. Endogenous hydrogen peroxide plays a positive role in the upregulation of heme oxygenase and acclimation to oxidative stress in wheat seedling leaves. J Integr Plant Biol,2009; 51:951-960.
Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L. Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA, 2008; 105:4495-4500.
Chinnusamy, V., Schumaker, K. and Zhu, J.K. Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot,2004; 55:225-236.
Clough SJ, Bent AF. Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J,1998; 16:735-743.
Crawford NM. Nitrate: nutrient and signal for plant growth. Plant Cell,1995; 7:859-868.
Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A. Plant nitric oxide synthase:back to square one-response. Trends Plant Sci,2006; 11:526-527.
Cordoba-Pedregosa MC, Gonzalez-Reyes JA, Canadillas M, Navas P, Cordoba F. Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol,1996; 112: 1119-1125.
Corpas FJ, Chaki M, Fernandez-Ocana A, et al. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol,2008; 49:1711-1722.
Cui W, Fu GEQ Wu H, Shen W. Cadmium-induced heme oxygenase-1 gene expression is associated with the depletion of glutathione in the roots of Medicago sativa. Biometals,2011; 24:93-103.
Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U. Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil,2006; 284:363-373.
Davis SJ, Bhoo SH, Durski AM, Walker JM, Vierstra RD. The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol,2001; 126:656-669.
Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F. Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci,2000; 57:779-795.
D'Autreaux B, Toledano MB. ROS as signaling molecules:mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol,2007; 8:813-824.
Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V, Schlauch, K. and Mittler, R. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell,2005; 17:268-281.
de Azevedo Neto AD, Prisco JT, Eneas-Filho J, Medeiros JR, Gomes-Filho E. Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. J Plant Physiol,2005; 162: 1114-1122.
Dean JV and Harper JE. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol,1988; 88:389-395.
De Michele E, Vurro E, Rigo C, et al. Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol,2009; 150:217-228.
Delledonne M, Xia Y, Dixon RA, Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature,1998; 394:585-588.
Desikan R, Griffiths R, Hancock J, Neill S. A new role for an old enzyme:nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA,2002; 99:16314-16318.
Ding M, Hou P, Shen X, et al. Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol,2010; 73:251-269.
Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U. Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil,2006; 284:363-373.
Dolan L and Davies J. Cell expansion in roots. Curr Opin Plant Biol,2004; 7:33-39.
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. OsDREB genes in rice, Oryza sativa L, encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant Journal,2003; 33: 751-763.
Dulak J, Jozkowicz A. Carbon monoxide-a "new" gaseous modulator of gene expression. Acta Biochim Pol,2003; 50:31-47.
Durner J, Wendehenne D, Klessig DF. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA,1998; 95:10328-10333.
Emborg TJ, Walker JM, Noh B, Vierstra RD. Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiol,2006; 140: 856-868.
Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM. The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell,1998; 10:1043-1054.
Flores-Perez U, Sauret-Gueto S, Gas E, Jarvis P, Rodriguez-Concepcion M. A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell,2008; 20:1303-1315.
Foreman J, Demidchik V, Bothwell JH, et al, Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature,2003; 422:442-446.
Frahry G, Schopfer P. NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta,2001; 212:175-1783.
Frankel D, Mehindate K, Schipper HM. Role of heme oxygenase-1 in the regulation of manganese superoxide dismutase gene expression in oxidatively challenged astroglia. J Cell Physiol,2000; 185: 80-86.
Gao L, Mann GE. Vascular NAD(P)H oxidase activation in diabetes:a double-edged sword in redox signaling. Cardiovasc Res,2009; 82:9-20.
Gaupels F, Furch ACU, Will T, Mur LAJ, Kogel K H, Van Bel AJE. Nitric oxide generation in Vicia faba phloem cells reveals them to be sensitive detectors as well as possible systemic transducers of stress signals. New Phytol,2008; 178:634-646.
Gisk B, Yasui Y, Kohchi T, Frankenberg-Dinkel N. Characterization of the haem oxygenase protein family in Arabidopsis thaliana reveals a diversity of functions. Biochem J,2010; 425:425-434.
Gniazdowska A, Krasuska U, Debska K, Andryka P, Bogatek R. The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta,2010; 232:999-1005.
Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol, 1980; 31:149-190.
Gulick P, Dvorak J. Gene induction and repression by salt treatment in roots of the salinity-sensitive Chinese Spring wheat and the salinity-tolerant Chinese Spring wheat x Elytrigia elongate amphiploid. Proc Natl Acad Sci USA,1987; 84:99-103.
Guo FQ and Crawford NM. Arabidopsis nitric oxide synthase 1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell,2005; 1.7:3436-3450.
Guo FQ, Okamoto M, Crawford NM. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science,2003; 302:100-103.
Guo K, Kong WW, Yang ZM. Carbon monoxide promotes root hair development in tomato. Plant Cell Environ,2009; 32:1033-1045.
Han Y, Zhang J, Chen X, Gao Z, Xuan W, Xu S, Ding X, Shen W. Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytol,2008; 177:155-166.
Han Y, Xuan W, Yu T, et al. Exogenous hematin alleviates mercury-induced oxidative damage in the roots of Medicago sativa. J Integr Plant Biol,2007; 49:1703-1713.
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. Plant cellular and molecular responses to high salinity. Annu Rev of Plant Physiol Plant Mol Biol,2000; 51:463-499.
He JM, Bai XL, Wang RB, Cao B, She XP. The involvement of nitric oxide in ultraviolet-B-inhibited pollen germination and tube growth of Paulownia tomentosa in vitro. Physiol Plant,2007; 131: 273-282.
Huang BK, Xu S, Xuan W, et al. Carbon monoxide alleviates salt-induced oxidative damage in wheat seedling leaves. J Integr Plant Biol,2006; 48:249-254.
Huang JJ, Han B, Xu S, Zhou MX, Shen WB. Heme oxygenase-1 is involved in the cytokinin-induced alleviation of senescence in detached wheat leaves during dark incubation. J Plant Physiol,2011; 168:768-775.
Jiang MY, Zhang JH. Involvement of plasma-membrane NADPH oxidase in abscisic acid-and water stress-induced antioxidant defense in leaves of maize seedlings. Planta,2002; 215:1022-1030.
Jenkins. Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol,2009; 60:407-430.
Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV. Different signaling and cell death roles of heterotrimeric G protein a and β subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell,2005; 17:957-970.
Jubany-Mari T, Munne-Bosch S, Lopez-Carbonell M, Alegre L. Hydrogen peroxide is involved in the acclimation of the Mediterranean shrub, Cistus albidus L., to summer drought. J Exp Bot,2009; 60: 107-120.
Kacperska A. Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol Plant,2004; 122:159-168.
Kim HP, Ryter SW, Choi AMK. CO as a cellular signaling molecule. Annu Rev Pharmacol Toxicol,2006; 46:411-449.
Kliebenstein DJ, Lim JE, Landry LG, Last RL. Arabidopsis UVR8 regulates Ultraviolet-B signal transduction and tolerance and contains sequence similarity to human Regulator of Chromatin Condenssation 1. Plant Physiol,2002; 130:234-243.
Kolbert Z, Bartha B, Erdei L. Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol,2008; 165:967-975.
Kopyra M, Gwozdz EA. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem,2003; 41: 1011-1017.
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R. ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem,2008; 283:34197-34203.
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidpsis. EMBO J,2003; 22:2623-2633.
Laloi C, Apel K, Danon A. Reactive oxygen signalling: the latest news. Curr Opin Plant Biol,2004; 7: 323-328.
Lambeth JD. Nox enzymes and the biology of reactive oxygen. Nature Rev Immunol,2004; 4:181-189.
Leshem Y, Seri L, Levine A. Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J,2007; 51:185-197.
Limam F, Chahed K, Ouelhazi N, Ghrir R, Ouelhazi L. Phytohormone regulation of isoperoxidases in Catharanthus roseus suspension cultures. Phytochem,1998; 49:1219-1225.
Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J. Exp. Bot,2009; 60:3221-3238.
Lin CC, Kao CH. Cell wall peroxidase against ferulic acid, lignin, and NaCl-reduced root growth of rice seedlings. J Plant Physiol,2001; 158:667-671.
Ling T, Zhang B, Cui W, Wu M, Lin J, et al. Carbon monoxide mitigates salt-induced inhibition of root growth and suppresses programmed cell death in wheat primary roots by inhibiting superoxide anion overproduction. Plant Sci,2009; 177:331-340.
Liu KL, Xu S, Xuan W, et al. Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa. Plant Sci,2007; 172:544-555.
Liu Y, Wu R, Wan Q, Xie G, Bi Y. Glucose-6-phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. Plant Cell Physiol,2007; 48:511-522.
Liu YH, Xu S, Ling TF, Xu LL, Shen WB. Heme oxygenase/carbon monoxide system participates in regulating wheat seed germination under osmotic stress involving the nitric oxide pathway. J Plant Physiol,2010; 167:1371-1379.
Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D. Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J,2008; 56:575-589.
Matsumoto H, Ishikawa K, Itabe H, Maruyama Y. Carbon monoxide and bilirubin from heme oxygenase-1 suppresses reactive oxygen species generation and plasminogen activator inhibitor-1 induction. Mol Cell Biochem,2006; 291:21-28.
Mazel, A., Leshem, Y., Tiwari, B.S. and Levine, A. Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7(AtRabG3e). Plant Physiol, 2004; 134:118-128.
Meloni DA, Oliva MA, Martinez CA, Cambraia J. Photosynthesis and activity of superoxide dismutase, peroxidase and glutat hione reductase in cotton under salt stress. Environ Exp Bot,2003; 49:69-76.
Millar AA, Jacobsen JV, Ross JJ, Helliwell CA, Poole AT, Scofield G, Reid JB. Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8'-hydroxylase. Plant J,2005; 45: 942-954.
Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal,2009; 2:ra45.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ,2010; 33:453-167.
Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci,2002; 7:405-410.
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci,2004; 9:490-498.
Modolo LV, Augusto O, Almeida IMG, Pinto-Maglio CAF, Oliveira HC, Seligman K, Salgado I. Decreased arginine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Sci, 2006;171:34-40.
Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF. AtNOS/AtNOAl is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J Biol Chem,2008; 283:32957-32967.
Muller K, Carstens AC, Linkies A, Torres MA, Leubner-Metzger G. The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol,2009; 184:885-897.
Munns R and Tester. Mechanisms of Salinity tolerance. Annu Rev Plant Biol,2008; 59:651-681.
Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM. The Arabidopsis photomorphogenic mutant hyl is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell,1999; 11:335-348.
Muramoto T, Tsurui N, Terry MJ, Yokota A, Kohchi T. Expression and Biochemical Properties of a Ferredoxin-Dependent Heme Oxygenase Required for Phytochrome Chromophore Synthesis. Plant Physiol,2002; 130:1958-1966.
Murata Y, Pei ZM, Mori IC, Schroeder JI. Abscisic acidactivation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in dbil-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell,2001; 13:2513-2523.
Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell,2002; 14:3089-3099.
Nagahashi G, Leonard RT, Thomson WW. Purification of plasma membranes from roots of barley: specificity of the phosphotungstic acid-chromic acid strain. Plant Physiol,1978; 61:993-999.
Nanjo T, Kobayashi M, Yoshiba Y et al., Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J,1999; 18:185-193.
Nakahira K, Kim HP, Geng XH, et al. Carbon monoxide differentially inhibits TLR signaling pathway by regulating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med,2006; 203:2377-2389.
Neill SJ, Desikan R, Hancock JT. Hydrogen peroxide signalling. Curr Opin Plant Biol,2002; 5: 388-395.
Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I. Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot,2008; 59:165-176.
Noriega GO, Balestrasse KB, Batlle A, Tomaro ML. Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Biophys Res Commun,2004; 323:1003-1008.
Noriega GO, Yannarelli GG, Balestrasse KB, Batlle A, Tomaro ML. The effect of nitric oxide on heme oxygenase gene expression in soybean leaves. Planta,2007; 226:1155-1163.
Oliveira HC, Justino GC, Sodek L, Salgado I. Amino acid recovery does not prevent susceptibility to Pseudomonas syringae in nitrate reductase double-deficient Arabidopsis thaliana plants. Plant Sci, 2009; 176:105-111.
Oravecz A, Baumann A, Mate Z, et al. CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell,2006; 18:1975-1990.
Overmyer K, Brosche M, Kangasjarvi J. Reactive oxygen species and hormonal control of cell death. Trends Plant Sci,2003; 8:335-342.
Passardi F, Penel C, Dunand C. Performing the paradoxical:how plant peroxidases modify the cell wall. Trends Plant Sci,2004; 9:534-540.
Piantadosi CA. Carbon monoxide, reactive oxygen signaling, and oxidative stress. Free Radic Biol Med, 2008; 45:562-569.
Planchet E, Gupta KJ, Sonoda M, Kaiser WM. Nitric oxide emission from tobacco leaves and cell suspensions:rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J,2005; 41:732-743.
Pogany M, von Rad U, Grun S, Dong6 A, Pintye A, Simoneau P, Bahnweg G, Kiss L, Barna B, Durner J. Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol,2009; 151:1459-1475.
Pompella A, Maellaro E, Casini AF, Comporti M. Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Am J Pathol,1987; 129:295-301.
Quan LJ, Zhang B, Shi WW, Li HY. Hydrogen peroxide in plants:a versatile molecule of the reactive oxygen species network. J Integr Plant Biol,2008; 50:2-18.
Rhee SG. H2O2, a necessary evil for cell signaling. Science,2006; 312:1882-1883.
Ribeiro DM, Desikan R, Bright J, Confraria A, Harrison J, Hancock JT, Barros RS, Neill SJ, Wilson ID. Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ,2009; 32:46-57.
Rizzini L, Favory JJ, Cloix C, et al., Perception of UV-B by the Arabidopsis UVR8 protein. Science, 2011; 332:103-106.
Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot,2002; 53:103-110.
Rodriguez-Serrano M, Romero-Puertas MC, Zabalza A,Corpas FJ, Gomez M, Del Rio LA, Sandalio LM. Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ,2006; 29:1532-1544.
Ruggiero B, Koiwa H, Manabe Y, et al., Uncoupling the effects of abscisic acid on plant growth and water relations. Analysis of stol/nced3, an abscisic acid-deficient byt salt stress-tolerant. Plant Physiol,2004; 136:3134-3147.
Rumer S, Gupta KJ, Kaiser WM. Plant cells oxidize hydroxylamines to NO. J Exp Bot,2009; 60: 2065-2072.
Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide:from basic science to therapeutic applications. Physiol Rev,2006; 86:583-650.
Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R. Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell,2004; 16:616-628.
Sakihama Y, Nakamura S, Yamasaki H. Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organism. Plant Cell Physiol,2002; 43:290-297.
Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M. Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. J Integr Plant Biol, 2008; 50:231-243.
Saito S, Yamamoto-KatouA, Yoshioka H, Doke N, Kawakita K. Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells. Plant Cell Physiol,2006; 47:689-697.
Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki KMonitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell,2001; 13:61-72.
Seligman K, Saviani EE, Oliveira HC, Pinto-Maglio CA, Salgado I. Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants. Plant Cell Physiol,2008; 49:1112-1121.
Shekhawat GS, Verma K. Haem oxygenase (HO):an overlooked enzyme of plant metabolism and defence. J Exp Bot,2010; 61:2255-2270.
Shi FM and Li YZ. Verticillium dahliae toxins-induced nitric oxide production in Arabidopsis is major dependent on nitrate reductase. BMB Rep,2009; 41:79-85.
Siegel SM, Renwick G, Roen LA. Formation of carbon monoxide during seed germination and seedling growth. Science,1962; 137:683-684.
Silveira JAG, Melo ARB, Viegas RA, Oliveira JTA. Salinity-induced effects on nitrogen assimilation related to growth in cowpea plants. Environ Exp Bot,2001; 46:171-179.
Simon-Plas F, Elmayan T, Blein JP. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J,2002; 31:137-147.
Srivastava N, Gonugunta VK, Puli MR, Raghavendra AS. Nitric oxide production occurs downstream of reactive oxygen species in guard cells during stomatal closure induced by chitosan in abaxial epidermis of Pisum sativum. Planta,2009; 229:757-765.
Stocker R. Antioxidant activities of bile pigment. Antioxid Redox Signal,2004; 6:841-849.
Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis seedling. Plant J,2007; 50:660-677.
Sudhamsu J, Lee GI, Klessig DF, Crane BR. The structure of YqeH. An AtNOSl/AtNOAl ortholog that couples GTP hydrolysis to molecular recognition. J Biol Chem,2008; 283:32968-32976.
Suttner DM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J,1999; 13:1800-1809.
Tischner R, Galli M, Heimer YM, Bielefeld S, Okamoto M, Mack A, Crawford NM. Interference with the citrulline-based nitric oxide synthase assay by argininosuccinate lyase activity in Arabidopsis extracts. FEBS J,2007; 274:4238-4245.
Torres MA, Dangl JL. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Cur Opin Plant Biol,2005; 8:397-403.
Torres MA, Dangl JL, Jones JD. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA,2002; 99:517-522.
Torres MA, Jones JDG, Dangl JL. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet,2005; 37: 1130-1134.
Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JDG. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91(phox)). Plant J,1998; 14: 365-370.
Toufighi K, Brady SM, Austin R, Ly E, and Provart NJ. The botany Array Resource:e-Northerns, Expression Angling, and promoter analyses. Plant J,2005; 43:153-163.
Tun NN, Livaja M, Kieber JJ, Scherer GF.Zeatin-induced nitric oxide (NO) biosynthesis in Arabidopsis thaliana mutants of NO biosynthesis and of two-component signaling genes. New Phytol,2008; 178: 515-531.
Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol, 2006; 47:346-354.
Turkseven S, Kruger A, Mingone CJ, et al. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol,2005; 289:701-707.
Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci,2002; 163:515-523.
Umezawa T, Shimizu K, Kato M, Ueda T. Enhancement of salt tolerance in soybean with NaCl pretreatment. Physiol Plant,2000; 110:59-63.
Umezawa T, Okamoto M, Kushiro T, Nambara E, Oono Y, Seki M, Kobayashi M, Koshiba T, Kamiya Y, Shinozaki K. CYP707A3, a major ABA 8'-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. Plant J,2006; 46:171-182.
Van Breusegem F, Bailey-Serres J, Mittler R. Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol,2008; 147:978-984.
Vinocur B and Altman A. Recent advances in engineering plant tolerance to abiotic stress:achievements and limitations. Curr Opin Biotech,2005; 16:123-132.
Wang R, Chen S, Zhou X, et al. Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol,2008a; 28:947-957.
Wang YH, Chen T, Zhang CY, et al. Nitric oxide modulates the influx of extracellular Ca2+ and actin filament organization during cell wall construction in Pinus bungeana pollen tubes. New Phytol, 2009;182:851-862.
Wang ZY, Li FM, Xiong YC, Xu BC. Soil-water threshold range of chemical signals and drought tolerance was mediated by ROS homeostasis in winter wheat during progressive soil drying. J Plant Growth Regul,2008b; 27:309-319.
Wilks A. Heme oxygenase:evolution, structure, and mechanism. Antioxid Redox Signal,2002; 4: 603-614.
Wilks S. Carbon monoxide in grenn plants. Science,1959; 129:964-966.
Wu M, Huang J, Xu S, Ling T, Xie Y, Shen W. Haem oxygenase delays programmed cell death in wheat aleurone layers by modulation of hydrogen peroxide metabolism. J Exp Bot,2011; 62:235-48.
Wu SJ, Qi JL, Zhang WJ, et al. Nitric oxide regulates shikonin formation in suspension-cultured Onosma paniculatum cells. Plant Cell Physiol,2009; 50:118-128.
Xie Y, Ling T, Han Y, et al. Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant Cell Environ,2008; 31:1864-1881.
Xie Y, Xu S, Han B, et al. Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J,2011; 66:280-292.
Xing T, Higgins VJ, Blumwald E. Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells. Plant Cell, 1997; 9:249-259.
Xu Q, Xu X, Zhao Y, et al. Salicylic acid, hydrogen peroxide and calcium-induced saline tolerance associated with endogenous hydrogen peroxide homeostasis in naked oat seedlings. Plant Growth Regul,2008; 54:249-259.
Xu S, Zhang B, Cao ZY, Ling TF, Shen WB. Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals,2011; 24:181-191.
Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, Ye MB, Shen WB. The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol,2008; 148:881-893.
Yamamoto-Katou A, Katou S, Yoshioka H, Doke N, Kawakita K. Nitrate reductase is responsible for elicitin-induced nitric oxide production in Nicotiana benthamiana. Plant Cell Physiol,2006; 47: 726-735.
Yamamoto Y, Kobayashi Y, Matsumoto H. Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol,2001; 125: 199-208.
Yamasaki H and Sakihama Y. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett, 2000; 468:89-92.
Yang Y, Xu S, An L, Chen N. NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. J Plant Physiol, 2007; 164:1429-1435.
Yannarelli GG, Noriega GO, Batlle A, Tomaro ML, Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta,2006; 224:1154-1162.
Yoshiba Y, Kiyosue T. Regulation of levels of proline as osmolyte in plants under water stress. Plant Cell Physiol,1997; 83:1095-1102.
Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J. Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci USA,2004; 101:15811-15816.
Zemojtel T, Frohlich A, Palmieri MC, et al. Plant nitric oxide synthase:a never-ending story? Trends Plant Sci,2006; 11:524-525.
Zhang JZ, Creelman RA, Zhu JK. From laboratory to field. Using information from Arabidopsis to engineer salt, cold and drought tolerance in crops. Plant Physiol,2004; 135:615-621.
Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta, 2006; 224:545-555.
Zhang Y, Zhu H, Zhang Q, et al. Phospholipase Dal and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell,2009; 21:2357-2377.
Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol,2004; 134:849-857.
Zhao MG, Tian QY, Zhang WH. Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol,2007; 144:206-217.
Zhu J, Liu J, Xiong L. Genetic analysis of salt tolerance in Arabidopsis:evidence for a critical role of potassium nutrition. Plant Cell,1998; 10:1181-1191.
Zhu JK. Plant salt tolerance. Trends Plant Sci,2001; 6:66-71.
Zhu JK. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol,2003; 6:441-445.
Zhu JK. Plant salt tolerance. Trends Plant Sci,2001; 6:66-71.
Zhu S, Yu X, Wang X, et al. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell,2007; 19:3019-3036.
Zhu X, Fan WG, Li DP, Lin MC, Kung H. Heme oxygenase-1 system and gastrointestinal tumors. World J Gastroenterol,2010; 16:2633-2637.
Zilli CG, Balestrasse KB, Yannarelli GG, Polizio AH, Santa-Cruz DM, Tomaro ML. Heme oxygenase up-regulation under salt stress protects nitrogen metabolism in nodules of soybean plants. Environ Exp Bot,2008; 64:83-89.
Zilli CG, Santa-Cruz DM, Yannarelli GG, Noriega GO, Tomaro ML, et al. Heme oxygenase contributes to alleviate salinity damage in Glycine max L. leaves. Int J Cell Biol,2009; 2009:1-9.
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W. GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol,2004; 136:2621-2632.
Zottini M, Costa A, De Michele R, Ruzzene M, Carimi F,Lo Schiavo F. Salicylic acid activates nitric oxide synthesis in Arabidopsis. J Exp Bot,2007; 58:1397-1405.