油菜抗逆相关基因的鉴定和功能研究
|
摘要
油菜是重要的油料作物,种子的含油量占其干重的35%-45%。菜油也是非常好的食用油,含有丰富的脂肪酸。菜油也是重要的工业原料,是我国发展生物柴油的理想的原料来源之一。因此大力发展油菜,提高油菜含油量,不仅能为我国能源安全战略作出重要贡献,还将有助于保障我国的粮食安全,促进农民增收,具有十分重要的战略意义。然而,油菜经常受到高盐、干旱、低温和营养缺乏(如低磷、低钾)等不良非生物胁迫的严重破坏,造成油菜产量严重下降。通过基因工程手段将一些具有抗逆功能的基因导入植物基因组进而获得抗逆新品种,这为传统育种模式的改革带来了新的契机。
与拟南芥、水稻等传统模式植物相比,油菜中抗逆基因的鉴定和抗逆机制的研究还比较少。因此,筛选和鉴定油菜中与抗逆相关的基因,分析揭示其抗逆分子机制,可以为通过基因工程手段来改良油菜抗逆性提供了新的科学依据。本研究采用Macroarray技术,从油菜cDNA文库中筛选了参与高盐、干旱胁迫应答的基因,并对一些感兴趣的目标基因进行了深入的研究。主要结果如下：
1.通过Macroarray技术从油菜cDNA文库中筛选鉴定参与高盐、干旱胁迫应答的基因
采用Macroarray技术,从油菜cDNA文库中共筛选得到313个参与盐胁迫应答的基因(172个受到高盐胁迫的诱导,141受到高盐胁迫的抑制表达)；477个参与干旱胁迫应答的基因(288个受到干旱胁迫的诱导,189个受到干旱胁迫的抑制表达)；154个基因受到高盐和干旱两种胁迫的双重诱导；104个基因受到高盐和干旱两种胁迫的抑制表达。这也说明高盐胁迫和干旱胁迫之间存在着共同的调控系统或信号交叉。
2.高盐干旱胁迫应答基因的表达模式分析
从上述胁迫诱导表达的候选基因中选取了13个基因做进一步的研究。这些基因编码的蛋白分属于六个蛋白家族：蛋白激酶家族(MAPKKK和CIPK)、金属硫蛋白家族、生长素应答或抑制蛋白家族、脂类转运蛋白、直接和胁迫相关的蛋白、代谢酶类。实时定量RT-PCR分析了这13个基因在盐胁迫、干旱胁迫的表达模式,同时也分析了6个基因在ABA处理下的表达模式。结果如下：13个基因中,有7个基因的表达受到盐胁迫的诱导；12个基因的表达受到甘露醇(模拟干旱胁迫)的诱导,其中包括6个受盐胁迫诱导的基因；进一步的研究揭示5个受干旱胁迫诱导的基因也受ABA的显著诱导。这些结果进一步表明干旱和高盐胁迫信号、干旱与ABA信号通路之间存在着交叉。组织表达分析结果显示,这13个基因可能在油菜的不同组织器官发育中也发挥着重要的作用。
3.冷调节基因BnCOR25的表达分析及功能鉴定
我们从候选的288个干旱诱导的基因中,鉴定了一个新型的编码冷调节蛋白的基因,该基因编码蛋白的分子量为25KD,因此我们将其命名为BnCOR25 (GeneBank号为HM187577)。实时定量RT-PCR结果显示BnCOR25基因主要在下胚轴、子叶、茎和花中表达,但是在根和叶子中表达量较低。Northern杂交证实BnCOR25基因的表达受到干旱和冷胁迫的显著诱导。研究结果还揭示BnCOR25基因的表达是受ABA信号通路调节的。BnCOR25蛋白主要定位于细胞膜上和细胞质中。过量表达BnCOR25基因增强了裂殖酵母细胞在冷胁迫下的存活率；过量表达BnCOR25的转基因拟南芥增强了对冷胁迫的耐受性。这些结果暗示该基因可能在赋予植物对冷胁迫耐受性中起一定的作用。
4. BnCIPK6基因的表达鉴定和启动子活性分析
在154个受干旱和高盐胁迫诱导的候选基因中,其中有一个基因编码的蛋白和拟南芥CIPK蛋白激酶家族的成员CIPK6有很高的同源性,因而被命名为BnCIPK6。BnCIPK6基因的表达受到高盐胁迫、渗透胁迫、低磷胁迫、ABA和BL的显著诱导。组织表达分析结果显示,BnCIPK6基因主要在花中表达,在子叶中适度表达,而在其它组织中表达水平较低。我们分离得到了约850bp长度的BnCIPK6启动子片段,组织化学染色分析揭示12天苗龄的拟南芥小苗,下胚轴和子叶中均有很强的GUS信号,而在其它组织中很弱或者检测不到GUS信号；胁迫处理分析揭示BnCIPK6基因的启动子是受高盐、渗透胁迫、ABA和BL诱导的。
5. BnCIPK6互作蛋白的筛选及鉴定
酵母双杂交结果显示BnCIPK6可以与拟南芥的CBL1,CBL2, CBL3和CBL9发生相互作用。将BnCIPK6蛋白作为诱饵蛋白筛选油菜cDNA文库,得到27种与其相互作用蛋白,这些互作蛋白涉及到植物生长发育、代谢及信号转导等多个方面。其中包括两个CBL蛋白,分别与AtCBL1和AtCBL3蛋白同源,我们将和AtCBL1同源性较高的油菜CBL蛋白,命名为BnCBL1, BiFC实验也证明了BnCIPK6和BnCBLl蛋白在体内的相互作用。
6. BnCIPK6和BnCBL1蛋白的亚细胞定位及BnCIPK、BnCIPK6T182D蛋白的体外磷酸化分析
亚细胞定位研究显示BnCIPK6蛋白在细胞膜、细胞质及细胞核中均有分布,而BnCBL1蛋白定位于细胞膜上。体外激酶磷酸化分析揭示点突变的BnCIPK6T182D蛋白-BnCIPK6(M),相对BnCIPK6蛋白自磷酸化能力更强,表明182位的苏氨酸残基是蛋白激活的关键位点。
7. BnCIPK6、BnCIPK6(M)及BnCBL1过量表达转基因拟南芥均显著增强了对盐胁迫、低磷胁迫的耐受性
为研究BnCIPK6及BnCBLl基因的功能,我们分别构建了BnCIPK6、BnCIPK6(M)及BnCBLl过量表达载体并转化了拟南芥,筛选获得转基因植株。分别选取这些外源基因在拟南芥中表达量较高的纯合株系做表型分析及功能研究。结果显示BnCIPK6、BnCIPK6(M)及BnCBL1转基因拟南芥均显著增强了对盐胁迫、低磷胁迫的耐受性。结果说明BnCBL1-BnCIPK6可能通过功能性的相互作用来参与植物对高盐、低磷胁迫的应答。
8. BnCIPK6和BnCIPK6(M)的过量表达转基因拟南芥增强了对ABA的敏感性
我们分析了转基因植株对ABA的应答,结果显示BnCIPK6和BnCIPK6(M)的过量表达转基因拟南芥均增强了对ABA的敏感性,尤其是后者显示出了对ABA的超敏性。ABA相关的Marker基因包括RD29A, ABF3, ABF4在ABA处理后的BnCIPK6(M)的转基因拟南芥中的表达量显著升高。而我们并未观察到过量表达BnCBLl的转基因拟南芥对ABA应答的改变。上述结果表明BnCIPK6参与了对ABA的应答,而BnCBL1没有参与ABA的应答,暗示可能存在和BnCIPK6相互作用的其它CBL蛋白,参与并介导了对ABA的应答。
9. BnCIPK6(M)的过量表达转基因拟南芥植株对BR应答改变,且提高了对BR合成抑制剂BRZ的敏感性
BnCIPK6(M)过量表达转基因植株改变了对油菜素内酯(BR)的应答,提高了对BRZ的敏感性。而我们并未观察到BnCIPK6和BnCBLl过量表达转基因拟南芥对BR应答表型的改变。这说明激活形式的BnCIPK6可能参与了BR的信号,同样暗示可能存在和BnCIPK6相互作用的其它CBL蛋白,参与并介导了对BR的应答。
10.拟南芥cipk6功能缺失突变体减弱了对ABA的应答、对盐胁迫和低磷胁迫更加敏感
对拟南芥cipk6功能缺失突变体的研究发现,cipk6突变体对盐胁迫和低磷胁迫更加敏感,对ABA的敏感性下降,这也说明AtCIPK6基因参与了对盐、低磷胁迫及ABA的应答。
Brassica napus is an important oilseed plant, which contains oil content, accounting for 35%-45% of its dry weight. Rapeseed oil is also good edible oil that is rich in fatty acids. Rapeseed oil is also an important industrial raw material and is the optimal sourceoffeed for developing biodiesel. Therefore, developing rape and increasing oil content can not only make an important contribution to energy security strategy but also ensure food security and improve farmer income in china. However, Brassica napus often encounters abiotic stresses, such as high salinity, drought, cold and nutrient deficiency (such as P and k limitation), which result in plant growth retardation and reduce agricultural productivity. Transference of stress tolerance genes into plant genome by gene engineering strategies to produce new varieties of stress resistance will bring new chance for reform of conventional breeding.
Compared with model species such as Arabidopsis and rice, little is known about identification of abiotic stress-related genes and the molecular mechanism in response to abiotic stresses of Brassica napus. Hence, screening and identification of stress-related genes and study the molecular mechanism of stress tolerance could provide us the basis of effective genetic engineering strategies for improving stress tolerance of B. napus. In our study, over 500 genes related to high-salinity and drought stresses were identified from B. napus cDNA libraries using macroarray analysis, and some interested genes were chosen for further expression and functional study. The main results are as follows:
1. Screening and identification of high-salinity/drought-related genes from B. napus cDNA libraries by macroarray analysis
In total,313 high-salinity-responsive genes (including 172 up-regulated and 141 down-regulated genes), and 477 drought-responsive genes (including 288 up-regulated and 189 down-regulated genes) were identified by cDNA microarray.154 genes were induced by both high salinity and drought, whereas 104 genes were suppressed by both high salinity and drought, suggesting the existence of a substantial common regulatory system or a cross-talk between high-salinity and drought stresses.
2. Expression patterns of the 13 stress-induced genes
13 candidate genes were chosen for further study. These proteins of the 13 genes encoding belong to 6 protein families, including protein kinase (MAPKKK and CIPK), metallothionein proteins, auxin-responsive or-repressed proteins, lipid transfer protein, stress-related proteins and metabolic enzyme. The expression profiles of the 13 genes under salinity or drought stress were analyzed by real-time quantitative RT-PCR.6 genes were selected for analyzing expressions under ABA treatment. The results are as follows:among 13 genes, the expressions of 7 genes were induced by salt stress; 12 of the selected 13 genes were induced to up-express by treatment with 200 mM mannitol, of which 6 genes were induced by high-salinity stress simultaneously; further study revealed that 5 manitol-inducible genes were also induced by ABA, suggesting that a significant cross-talk may occur between drought and high-salinity stress signaling and between drought and ABA responses. Expression patterns of the 13 genes in different tissues/organs of B. napus suggest that these genes may play important roles in tissues/organs development.
3. Expression analysis and functional identification of cold regulated gene BnCOR25
Among 288 clones identified to be putative drought-responsive genes, one gene (cDNA) encodes putative novel cold-regulated protein with a calculated molecular mass of 25 kDa, and consequently designated as BnCOR25 (accession number in GenBank:HM 187577). The results of Real time RT-PCR displayed that BnCOR25 was mainly expressed in hypocotyls, cotyledons, stems, and flowers, but its mRNA was found at low levels in roots and leaves. Northern blotting indicated that BnCOR25 expression is significantly induced in roots by osmotic and drought stresses. The data also revealed that BnCOR25 gene expression may be mediated by ABA-dependent pathway. BnCOR25 protein may be chiefly localized on cell plasma membrane and cytoplasm. Overexpression of BnCOR25 in yeast enhanced the cell survival probability under cold stress, and overexpression of BnCOR25 in Arabidopsis enhances plant tolerance to cold stress. These results suggested that the BnCOR25 gene may play an important role in conferring freezing/cold tolerance in plants.
4. Expression analysis of BnCIPK6 gene and histochemical assay of BnCIPK6 promoter activities
Among 154 genes identified to be putative induced by both high salinity and drought stress, one gene (cDNA) with deduced amino acid sequence homology to CBL-interacting protein kinases 6, and consequently designated as BnCIPK6, was chosen for further analysis. Transcripts of BnCIPK6 gene were induced by high salinity, osmotic stress, low phosphate, ABA and BL treatment. The results of the RT-PCR showed that BnCIPK6 was mainly expressed in flowers, at moderate level in cotyledons, but its mRNA was found at low levels in other tissues. We isolated the 850bp promoter of BnCIPK6, Histochemical assay revealed that the GUS staining was detected at relatively high level in hypocotyls and cotyledons in 12-day-old seedlings, but weak or no GUS signals in other tissues. The results of stress and hormone treatments revealed that the BnCIPK6 promoter is salt-/osmotic-/ABA-/BL-inducible.
5. Screening and identification of BnCIPK6-interacting proteins
Yeast two-hybrid analysis showed that BnCIPK6 interacts strongly and specifically with AtCBL1, AtCBL2, AtCBL3 and AtCBL9. Yeast two-hybrid analysis was performed using the BnCIPK6 as bait to screen the two-hybrid library of Brassica napus cDNAs constructed on the prey vector.27 unique proteins were identified as positive clones. The BnCIPK6-interacting proteins were related to various aspects of plant development, metabolism and signal transduction. The identified proteins included two calcineurin B-like proteins that are homologous to AtCBL1 and AtCBL3, respectively. The protein homologous to AtCBL1, designated as BnCBL1, was chosen for further study. BiFC assays also confirmed BnCIPK6 protein interaction with BnCBLl protein in vivo.
6. Subcellular localization of BnCIPK6 and BnCBL1 protein and phosphorylation activities of BnCIPK6 and BnCIPK6T182D proteins in vitro
The results of subcellular localization showed that BnCIPK6:eGFP fusion protein can be observed at the plasma membrane, in the nucleus and cytosol, whereas BnCBL1 is plasma membrane-localized protein. The results of phosphorylation activities in vitro revealed that the BnCIPK6(M) mutant protein exhibited higher autophosphorylation activity, compared with BnCIPK6 protein, suggesting that the 182nd threonine residue in BnCIPK6 could be a critical target site for activation.
7. Overexpression of the BnCIPK6, BnCIPK6(M) and BnCBL1 in Arabidopsis enhance plant tolerance to salt and low phosphate stress To study the function of BnCIPK6 and BnCBL1, the coding region of the BnCIPK6, BnCIPK6(M) and BnCBL1 were fused to the CaMV 35S promoter and used to transform Arabidopsis plants. Several transgenic plants were obtained by screening and identification. Transgenic lines with higher gene expression were selected for analyzing their phenotypes under various treatment conditions. The results showed that BnCIPK6, BnCIPK6(M) and BnCBL1 transgenic plants all enhance plant tolerance to salt and low phosphate stress. These results suggest that BnCBL1-BnCIPK6 may functionally interact with each other and that are involved in salt and low Pi (LP) stresses response in plant.
8. BnCIPK6 and BnCIPK6(M) transgenic Arabidopsis were sensitive to abscisic acid (ABA)
We tested the transgenic lines under ABA treatment. The results showed that overexpression of BnCIPK6 and BnCIPK6(M) increased plant sensitivity to ABA, especially the latter that show hypersensitivity to ABA. The expression of ABA-responsive Marker genes, such asABF3, ABF4 and RD29A, in the BnCIPK6(M) transgenic plants was remarkably higher than that in wild type under ABA treatment although there was no significant difference in expression levels of those genes between the transgenic plants and wild type in absence of ABA. We did not observe the obvious phenotype changes of BnCBL1 transgenic plants in response to ABA, compared to wild type plants. The results showed that BnCIPK6, but not BnCBL1, is involved in ABA response, suggesting that there may be another BnCIPK6 interaction CBL(s) involved in ABA signaling.
9. BnCIPK6(M) overexpression transgenic plants show altered BR response phenotypes and increase plant sensitivity to BRZ
The results revealed that overexpression of the constitutively active BnCIPK6 in Arabidopsis alters plants response to BR and increases plant sensitivity to BRZ. However, we did not observe the obvious phenotype changes of BnCBLl and BnCIPK6 transgenic plants in response to BR. The results revealed that the constitutively active BnCIPK6, which has higher kinase activity, may be involved in BR signaling pathway, suggesting that there may be another BnCIPK6 interaction CBL(s) involved inBR signaling.
10. Arabidopsis cipk6 loss of function mutant shows less ABA sensitivity than the WT, but is more sensitive to salt and low phosphate stresses
The studies on Arabidopsis cipk6 loss of function mutant revealed that silencing of AtCIPK6 confers ABA insensitive growth phenotypes and enhances sensitivity to low phosphate stress, suggesting the AtCIPK6 gene is involved in response to salt, low phosphate and ABA. However, we did not observe obvious phenotypic changes under exogenous BL treatment.
与拟南芥、水稻等传统模式植物相比,油菜中抗逆基因的鉴定和抗逆机制的研究还比较少。因此,筛选和鉴定油菜中与抗逆相关的基因,分析揭示其抗逆分子机制,可以为通过基因工程手段来改良油菜抗逆性提供了新的科学依据。本研究采用Macroarray技术,从油菜cDNA文库中筛选了参与高盐、干旱胁迫应答的基因,并对一些感兴趣的目标基因进行了深入的研究。主要结果如下：
1.通过Macroarray技术从油菜cDNA文库中筛选鉴定参与高盐、干旱胁迫应答的基因
采用Macroarray技术,从油菜cDNA文库中共筛选得到313个参与盐胁迫应答的基因(172个受到高盐胁迫的诱导,141受到高盐胁迫的抑制表达)；477个参与干旱胁迫应答的基因(288个受到干旱胁迫的诱导,189个受到干旱胁迫的抑制表达)；154个基因受到高盐和干旱两种胁迫的双重诱导；104个基因受到高盐和干旱两种胁迫的抑制表达。这也说明高盐胁迫和干旱胁迫之间存在着共同的调控系统或信号交叉。
2.高盐干旱胁迫应答基因的表达模式分析
从上述胁迫诱导表达的候选基因中选取了13个基因做进一步的研究。这些基因编码的蛋白分属于六个蛋白家族：蛋白激酶家族(MAPKKK和CIPK)、金属硫蛋白家族、生长素应答或抑制蛋白家族、脂类转运蛋白、直接和胁迫相关的蛋白、代谢酶类。实时定量RT-PCR分析了这13个基因在盐胁迫、干旱胁迫的表达模式,同时也分析了6个基因在ABA处理下的表达模式。结果如下：13个基因中,有7个基因的表达受到盐胁迫的诱导；12个基因的表达受到甘露醇(模拟干旱胁迫)的诱导,其中包括6个受盐胁迫诱导的基因；进一步的研究揭示5个受干旱胁迫诱导的基因也受ABA的显著诱导。这些结果进一步表明干旱和高盐胁迫信号、干旱与ABA信号通路之间存在着交叉。组织表达分析结果显示,这13个基因可能在油菜的不同组织器官发育中也发挥着重要的作用。
3.冷调节基因BnCOR25的表达分析及功能鉴定
我们从候选的288个干旱诱导的基因中,鉴定了一个新型的编码冷调节蛋白的基因,该基因编码蛋白的分子量为25KD,因此我们将其命名为BnCOR25 (GeneBank号为HM187577)。实时定量RT-PCR结果显示BnCOR25基因主要在下胚轴、子叶、茎和花中表达,但是在根和叶子中表达量较低。Northern杂交证实BnCOR25基因的表达受到干旱和冷胁迫的显著诱导。研究结果还揭示BnCOR25基因的表达是受ABA信号通路调节的。BnCOR25蛋白主要定位于细胞膜上和细胞质中。过量表达BnCOR25基因增强了裂殖酵母细胞在冷胁迫下的存活率；过量表达BnCOR25的转基因拟南芥增强了对冷胁迫的耐受性。这些结果暗示该基因可能在赋予植物对冷胁迫耐受性中起一定的作用。
4. BnCIPK6基因的表达鉴定和启动子活性分析
在154个受干旱和高盐胁迫诱导的候选基因中,其中有一个基因编码的蛋白和拟南芥CIPK蛋白激酶家族的成员CIPK6有很高的同源性,因而被命名为BnCIPK6。BnCIPK6基因的表达受到高盐胁迫、渗透胁迫、低磷胁迫、ABA和BL的显著诱导。组织表达分析结果显示,BnCIPK6基因主要在花中表达,在子叶中适度表达,而在其它组织中表达水平较低。我们分离得到了约850bp长度的BnCIPK6启动子片段,组织化学染色分析揭示12天苗龄的拟南芥小苗,下胚轴和子叶中均有很强的GUS信号,而在其它组织中很弱或者检测不到GUS信号；胁迫处理分析揭示BnCIPK6基因的启动子是受高盐、渗透胁迫、ABA和BL诱导的。
5. BnCIPK6互作蛋白的筛选及鉴定
酵母双杂交结果显示BnCIPK6可以与拟南芥的CBL1,CBL2, CBL3和CBL9发生相互作用。将BnCIPK6蛋白作为诱饵蛋白筛选油菜cDNA文库,得到27种与其相互作用蛋白,这些互作蛋白涉及到植物生长发育、代谢及信号转导等多个方面。其中包括两个CBL蛋白,分别与AtCBL1和AtCBL3蛋白同源,我们将和AtCBL1同源性较高的油菜CBL蛋白,命名为BnCBL1, BiFC实验也证明了BnCIPK6和BnCBLl蛋白在体内的相互作用。
6. BnCIPK6和BnCBL1蛋白的亚细胞定位及BnCIPK、BnCIPK6T182D蛋白的体外磷酸化分析
亚细胞定位研究显示BnCIPK6蛋白在细胞膜、细胞质及细胞核中均有分布,而BnCBL1蛋白定位于细胞膜上。体外激酶磷酸化分析揭示点突变的BnCIPK6T182D蛋白-BnCIPK6(M),相对BnCIPK6蛋白自磷酸化能力更强,表明182位的苏氨酸残基是蛋白激活的关键位点。
7. BnCIPK6、BnCIPK6(M)及BnCBL1过量表达转基因拟南芥均显著增强了对盐胁迫、低磷胁迫的耐受性
为研究BnCIPK6及BnCBLl基因的功能,我们分别构建了BnCIPK6、BnCIPK6(M)及BnCBLl过量表达载体并转化了拟南芥,筛选获得转基因植株。分别选取这些外源基因在拟南芥中表达量较高的纯合株系做表型分析及功能研究。结果显示BnCIPK6、BnCIPK6(M)及BnCBL1转基因拟南芥均显著增强了对盐胁迫、低磷胁迫的耐受性。结果说明BnCBL1-BnCIPK6可能通过功能性的相互作用来参与植物对高盐、低磷胁迫的应答。
8. BnCIPK6和BnCIPK6(M)的过量表达转基因拟南芥增强了对ABA的敏感性
我们分析了转基因植株对ABA的应答,结果显示BnCIPK6和BnCIPK6(M)的过量表达转基因拟南芥均增强了对ABA的敏感性,尤其是后者显示出了对ABA的超敏性。ABA相关的Marker基因包括RD29A, ABF3, ABF4在ABA处理后的BnCIPK6(M)的转基因拟南芥中的表达量显著升高。而我们并未观察到过量表达BnCBLl的转基因拟南芥对ABA应答的改变。上述结果表明BnCIPK6参与了对ABA的应答,而BnCBL1没有参与ABA的应答,暗示可能存在和BnCIPK6相互作用的其它CBL蛋白,参与并介导了对ABA的应答。
9. BnCIPK6(M)的过量表达转基因拟南芥植株对BR应答改变,且提高了对BR合成抑制剂BRZ的敏感性
BnCIPK6(M)过量表达转基因植株改变了对油菜素内酯(BR)的应答,提高了对BRZ的敏感性。而我们并未观察到BnCIPK6和BnCBLl过量表达转基因拟南芥对BR应答表型的改变。这说明激活形式的BnCIPK6可能参与了BR的信号,同样暗示可能存在和BnCIPK6相互作用的其它CBL蛋白,参与并介导了对BR的应答。
10.拟南芥cipk6功能缺失突变体减弱了对ABA的应答、对盐胁迫和低磷胁迫更加敏感
对拟南芥cipk6功能缺失突变体的研究发现,cipk6突变体对盐胁迫和低磷胁迫更加敏感,对ABA的敏感性下降,这也说明AtCIPK6基因参与了对盐、低磷胁迫及ABA的应答。
Brassica napus is an important oilseed plant, which contains oil content, accounting for 35%-45% of its dry weight. Rapeseed oil is also good edible oil that is rich in fatty acids. Rapeseed oil is also an important industrial raw material and is the optimal sourceoffeed for developing biodiesel. Therefore, developing rape and increasing oil content can not only make an important contribution to energy security strategy but also ensure food security and improve farmer income in china. However, Brassica napus often encounters abiotic stresses, such as high salinity, drought, cold and nutrient deficiency (such as P and k limitation), which result in plant growth retardation and reduce agricultural productivity. Transference of stress tolerance genes into plant genome by gene engineering strategies to produce new varieties of stress resistance will bring new chance for reform of conventional breeding.
Compared with model species such as Arabidopsis and rice, little is known about identification of abiotic stress-related genes and the molecular mechanism in response to abiotic stresses of Brassica napus. Hence, screening and identification of stress-related genes and study the molecular mechanism of stress tolerance could provide us the basis of effective genetic engineering strategies for improving stress tolerance of B. napus. In our study, over 500 genes related to high-salinity and drought stresses were identified from B. napus cDNA libraries using macroarray analysis, and some interested genes were chosen for further expression and functional study. The main results are as follows:
1. Screening and identification of high-salinity/drought-related genes from B. napus cDNA libraries by macroarray analysis
In total,313 high-salinity-responsive genes (including 172 up-regulated and 141 down-regulated genes), and 477 drought-responsive genes (including 288 up-regulated and 189 down-regulated genes) were identified by cDNA microarray.154 genes were induced by both high salinity and drought, whereas 104 genes were suppressed by both high salinity and drought, suggesting the existence of a substantial common regulatory system or a cross-talk between high-salinity and drought stresses.
2. Expression patterns of the 13 stress-induced genes
13 candidate genes were chosen for further study. These proteins of the 13 genes encoding belong to 6 protein families, including protein kinase (MAPKKK and CIPK), metallothionein proteins, auxin-responsive or-repressed proteins, lipid transfer protein, stress-related proteins and metabolic enzyme. The expression profiles of the 13 genes under salinity or drought stress were analyzed by real-time quantitative RT-PCR.6 genes were selected for analyzing expressions under ABA treatment. The results are as follows:among 13 genes, the expressions of 7 genes were induced by salt stress; 12 of the selected 13 genes were induced to up-express by treatment with 200 mM mannitol, of which 6 genes were induced by high-salinity stress simultaneously; further study revealed that 5 manitol-inducible genes were also induced by ABA, suggesting that a significant cross-talk may occur between drought and high-salinity stress signaling and between drought and ABA responses. Expression patterns of the 13 genes in different tissues/organs of B. napus suggest that these genes may play important roles in tissues/organs development.
3. Expression analysis and functional identification of cold regulated gene BnCOR25
Among 288 clones identified to be putative drought-responsive genes, one gene (cDNA) encodes putative novel cold-regulated protein with a calculated molecular mass of 25 kDa, and consequently designated as BnCOR25 (accession number in GenBank:HM 187577). The results of Real time RT-PCR displayed that BnCOR25 was mainly expressed in hypocotyls, cotyledons, stems, and flowers, but its mRNA was found at low levels in roots and leaves. Northern blotting indicated that BnCOR25 expression is significantly induced in roots by osmotic and drought stresses. The data also revealed that BnCOR25 gene expression may be mediated by ABA-dependent pathway. BnCOR25 protein may be chiefly localized on cell plasma membrane and cytoplasm. Overexpression of BnCOR25 in yeast enhanced the cell survival probability under cold stress, and overexpression of BnCOR25 in Arabidopsis enhances plant tolerance to cold stress. These results suggested that the BnCOR25 gene may play an important role in conferring freezing/cold tolerance in plants.
4. Expression analysis of BnCIPK6 gene and histochemical assay of BnCIPK6 promoter activities
Among 154 genes identified to be putative induced by both high salinity and drought stress, one gene (cDNA) with deduced amino acid sequence homology to CBL-interacting protein kinases 6, and consequently designated as BnCIPK6, was chosen for further analysis. Transcripts of BnCIPK6 gene were induced by high salinity, osmotic stress, low phosphate, ABA and BL treatment. The results of the RT-PCR showed that BnCIPK6 was mainly expressed in flowers, at moderate level in cotyledons, but its mRNA was found at low levels in other tissues. We isolated the 850bp promoter of BnCIPK6, Histochemical assay revealed that the GUS staining was detected at relatively high level in hypocotyls and cotyledons in 12-day-old seedlings, but weak or no GUS signals in other tissues. The results of stress and hormone treatments revealed that the BnCIPK6 promoter is salt-/osmotic-/ABA-/BL-inducible.
5. Screening and identification of BnCIPK6-interacting proteins
Yeast two-hybrid analysis showed that BnCIPK6 interacts strongly and specifically with AtCBL1, AtCBL2, AtCBL3 and AtCBL9. Yeast two-hybrid analysis was performed using the BnCIPK6 as bait to screen the two-hybrid library of Brassica napus cDNAs constructed on the prey vector.27 unique proteins were identified as positive clones. The BnCIPK6-interacting proteins were related to various aspects of plant development, metabolism and signal transduction. The identified proteins included two calcineurin B-like proteins that are homologous to AtCBL1 and AtCBL3, respectively. The protein homologous to AtCBL1, designated as BnCBL1, was chosen for further study. BiFC assays also confirmed BnCIPK6 protein interaction with BnCBLl protein in vivo.
6. Subcellular localization of BnCIPK6 and BnCBL1 protein and phosphorylation activities of BnCIPK6 and BnCIPK6T182D proteins in vitro
The results of subcellular localization showed that BnCIPK6:eGFP fusion protein can be observed at the plasma membrane, in the nucleus and cytosol, whereas BnCBL1 is plasma membrane-localized protein. The results of phosphorylation activities in vitro revealed that the BnCIPK6(M) mutant protein exhibited higher autophosphorylation activity, compared with BnCIPK6 protein, suggesting that the 182nd threonine residue in BnCIPK6 could be a critical target site for activation.
7. Overexpression of the BnCIPK6, BnCIPK6(M) and BnCBL1 in Arabidopsis enhance plant tolerance to salt and low phosphate stress To study the function of BnCIPK6 and BnCBL1, the coding region of the BnCIPK6, BnCIPK6(M) and BnCBL1 were fused to the CaMV 35S promoter and used to transform Arabidopsis plants. Several transgenic plants were obtained by screening and identification. Transgenic lines with higher gene expression were selected for analyzing their phenotypes under various treatment conditions. The results showed that BnCIPK6, BnCIPK6(M) and BnCBL1 transgenic plants all enhance plant tolerance to salt and low phosphate stress. These results suggest that BnCBL1-BnCIPK6 may functionally interact with each other and that are involved in salt and low Pi (LP) stresses response in plant.
8. BnCIPK6 and BnCIPK6(M) transgenic Arabidopsis were sensitive to abscisic acid (ABA)
We tested the transgenic lines under ABA treatment. The results showed that overexpression of BnCIPK6 and BnCIPK6(M) increased plant sensitivity to ABA, especially the latter that show hypersensitivity to ABA. The expression of ABA-responsive Marker genes, such asABF3, ABF4 and RD29A, in the BnCIPK6(M) transgenic plants was remarkably higher than that in wild type under ABA treatment although there was no significant difference in expression levels of those genes between the transgenic plants and wild type in absence of ABA. We did not observe the obvious phenotype changes of BnCBL1 transgenic plants in response to ABA, compared to wild type plants. The results showed that BnCIPK6, but not BnCBL1, is involved in ABA response, suggesting that there may be another BnCIPK6 interaction CBL(s) involved in ABA signaling.
9. BnCIPK6(M) overexpression transgenic plants show altered BR response phenotypes and increase plant sensitivity to BRZ
The results revealed that overexpression of the constitutively active BnCIPK6 in Arabidopsis alters plants response to BR and increases plant sensitivity to BRZ. However, we did not observe the obvious phenotype changes of BnCBLl and BnCIPK6 transgenic plants in response to BR. The results revealed that the constitutively active BnCIPK6, which has higher kinase activity, may be involved in BR signaling pathway, suggesting that there may be another BnCIPK6 interaction CBL(s) involved inBR signaling.
10. Arabidopsis cipk6 loss of function mutant shows less ABA sensitivity than the WT, but is more sensitive to salt and low phosphate stresses
The studies on Arabidopsis cipk6 loss of function mutant revealed that silencing of AtCIPK6 confers ABA insensitive growth phenotypes and enhances sensitivity to low phosphate stress, suggesting the AtCIPK6 gene is involved in response to salt, low phosphate and ABA. However, we did not observe obvious phenotypic changes under exogenous BL treatment.
引文
1.戴秀玉,王忆琴,杨波,周坚(2001)大肠杆菌海藻糖合成酶基因对提高烟草抗逆性能的研究。微生物学报41：427-431.
2.胡红红(2006)水稻逆境相关转录因子的分离和功能鉴定。博士学位论文武汉：华中师范大学图书馆.
3.王汉中(2005)实施油菜生物柴油计划建造永不枯竭的“绿色油田”。农业科技通讯10：11.
4.张慧,董伟,周峻马等(1998)果聚糖蔗糖转移酶基因的克隆及耐盐转基因烟草的培育。生物工程学报14：741-745.
5. Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 55:541-552.
6. Aitken A, Howell S, Jones D, Madrazo J, Patel Y (1995) 14-3-3 alpha and delta are the phosphorylated forms of raf-activating 14-3-3 beta and zeta. In vivo stoichiometric phosphorylation in brain at a Ser-Pro-Glu-Lys MOTIF. J Biol Chem 270:5706-5709.
7. Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein-protein interaction module conserved in Ca2--regulated kinases. The EMBO Journal 20: 1051-1063.
8. APel K, Hirt H (2004) Reactive oxygen species:metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373-399.
9. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na-/H+ antiport in Arabidopsis. Science 285:1256-1258.
10. Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. PNAS 93:13404-13409.
11. Bargmann BO, Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9:515-522.
12. Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915-924.
13. Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plant specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435-466.
14. Boudsocq M, Sheen J (2010) Stress Signaling II:Calcium Sensing and Signaling. Abiotic Stress Adaptation in Plants. Physiological Molecular and Genomic Foundation, pp.75-90.
15. Boursiac Y, Chen S, Luu D, Sorieul M, Deies N, Maurel C (2005) Early Effects of Salinity on Water Transport in Arabidopsis Roots. Molecular and Cellular Features of Aquaporin Expression. Plant Physiol 139:790-805.
16. Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Knal. Plant Physiol 143:1918-1928.
17. Chatthai M, Kaukinen KH, Tranbarger TJ, Gupta PK and Misra S (1997) The isolation of a novel metal lothionein-related cDNA expressed in somatic and zygotic embryos of douglas-fir: regulation by ABA, osmoticum, and metal ions. Plant Mol Biol 34:243-254.
18. Chen L, Ren F, Zhong H, Jiang WM, Li XB (2010) Identification and expression analysis of genes induced by high-salinity and drought stresses in Brassica napus. Acta Biochim Biophys Sin 42:154-164.
19. Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21:3554-3566.
20. Cheng LH, Zhang B, Xu ZQ (2007) Genetic transformation of buckwheat (Fagopyrum esculentum Moench) with AtNHX1 gene and regeneration of salt-tolerant transgenic plants. Sheng Wu Gong Cheng Xue Bao 23:51-60.
21. Cheng NH, Pittman JK, Zhu JK, Hirschi KD (2004) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922-2926.
22. Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases: The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469-485.
23. Cheong YH, Pandey GK, Grant J, Batistic O, Li L, Lee SC, Kim BG, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223-239.
24. Chevalier C, Bourgeois E, Pradet A and Raymond P (1995) Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips. Plant Mol Biol 28:473-485.
25. Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICEI:a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043-1054.
26. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends plant Sci 12:444-451
27. Choe S, Schmitz RJ, Fujioka S, Takatsuto S, Lee MO, Yoshida S, Feldmann KA and Tax FE (2002) Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3beta-like kinase. Plant Physiol 130:1506-1515.
28. Choi D, Kim HM, Yun HK, Park JA, Kim WT and Bok SH (1996) Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L and its induction by wounding and tobacco mosaic virus infection. Plant Physiol 112:353-359.
29. Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binging factors. J Biol Chem 275:1723-1730.
30. Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang Ⅰ, Kim SY (2005a) Arabidopsis calcium dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750-1761.
31. Clouse SD (1996) Molecular genetic studies confirm the role of brassinosteroids in plant growth and development. Plant J 10:1-8
32. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735-743.
33. Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Lenohardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regultates stomatal movements and plant drought tolerance. Curr Biol 15:1196-1200.
34. D' Angelo C, Weinl S, Batistic O, Pandey G, Sch(?)ultke YHCS, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid dependent and independent stress responses in Arabidopsis. Plant J 48:857-872.
35. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21: 972-984.
36. Ershov PV, Reshetova OS, Trofimova MS, Babakov AV (2005) Activity of ion transporters and salt tolerance in barley. Russian Journal of Plant Physiology 6:765-773.
37. Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19: 1617-1634.
38. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway, Plant J 39:863-876.
39. Fusaro A, Mangeon A, Magrani-Junqueira R, Bem'cio-Rocha CA, Cardoso-Coutinho T, Margis R, Sachetto-Martins G (2001) Classification, expression pattern and comparative analysis of sugarcane expressed sequences tags (ESTs) encoding glycine rich proteins (GRPs). Genet Mol Biol 24:263-273
40. Garcia AB, Engler J, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants on NaCl stress in rice. Plant Physiol 115:159-169
41. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Nati Acad Sci USA 99:15898-15903.
42. Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459-471.
43. Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13-21.
44. Gong D, Guo Y, Jagendorf AT, Zhu JK (2002a) Biochemical characterization of the Arabidopsis protein kinase SOS2 that functions in salt tolerance. Plant Physiol 130:256-264.
45. Gong D, Gong Z, Guo Y, Chen X, Zhu JK (2002b) Biochemical and functional characterization of PKS11, a novel Arabidopsis protein kinase. J Biol Chem 277:28340-28350.
46. Gong D, Zhang C, Chen X, Gong Z, Zhu JK (2002c) Constitutive activation and transgenic evaluation of the function of an Arabidopsis PKS protein kinase. J Biol Chem 277:42088-42096.
47. Gong D, Guo Y, Schurnaker K, Zhu JK (2004) The SOS3 family of calcium sensors and SOS2 family of protein kinases in Arabidopsis. Plant Physiol 134:919-926.
48. Guo Y, Halfter U, Ishitani M, Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383-1399.
49. Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK (2002) A calcium sensor and its interacting protein kinase are globar regulators of abscisic acid signaling in Arabidopsis. Developmental Cell 3:233-244.
50. Gupta A, Heinen J, Holaday A, Burke J, Allen R (1993) Increased resistance to oxidative stress in transgenic Plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci USA 90:1629-1633.
51. Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639-648.
52. Halfter U, Ishitani M, Zhu J K (2000)The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium2+binding protein SOS3. Proc Natl Acad Sci USA 97:3735-3740.
53. Harmon AC, Gribskov M, Harper J F (2000) CDPKs:A kinase for every Ca2+ signal? Trends Plant Sci 5:317-319.
54. Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263-288.
55. Hayashi, H., Mustardy, L., Deshnium, P., Ida, M. & Murata, N(1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase:accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12:133-142.
56. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903-916.
57. Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53:383-397.
58. Hidenori H (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase:accumulation of glycinebetaine and enhanced tolerance to salt and stress. Planta 12: 133-142.
59. Hirt H (1997). Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci 2: 11-15.
60. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138: 1184-1194.
61. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 32:666-680.
62. Hsieh HM, Liu WK and Huang PC (1995) A novel stress-inducible metallothionein-like gene from rice. Plant Mol Biol 28: 381-389.
63. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264-278.
64. Huang DQ, Wu WR, Abrams SR and Cutler AJ (2008) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59: 2991-3007.
65. Hwang Ⅰ, Sze H, Harper JF (2000) A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc Natl Acad Sci USA 97:6224-6229.
66. Jeroni G, Alicia P, Maria Mar A, Magdalena T, Hipolito M, Jaume F (2007) Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.):relationship with ecophysiological status. Planta 226:671-681.
67. Johansson Ⅰ, Larsson C, Ek B, Kjellbom P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8:1181-1191.
68. Johasson Ⅰ, Karisson M, Shukla V, Chrispeels M, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin RM28A is regulated by phosphorylation. Plant Cell 10:451-459.
69. Jonak C, Kiegerl S, Ligterink W, Baker PJ, Huskisson NS and Hirt H (1996) Stress signaling in plants:a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274-11279.
70. Kader MA, Seidel T, Golldack D, Lindberg S (2006) Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot 57:4257-4268.
71. Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343-357.
72. Kim BG, Waadt R, Cheong Y, Pandey G, Dominguez-Solis J, Sch(?)ultke S, Lee S, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473-484.
73. Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Lee MH, Moon J, Lee I, Kim J (2004)A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36:167-171.
74. Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO, Cho MJ (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 25:247-259.
75. Kim KN, Cheong Y, Pandey G, Grant J, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411-423.
76. Kishor PBK, Hong Z, Miao GH, Hu CAA, Verma DPS(1995) Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants. Plant Physiol 108:1387-1394.
77. Knight H and Knight MR (2001) Abiotic stress signalling pathways:specificity and cross-talk. Trends Plant Sci 6:262-267.
78. Knight H, Veale EL, Warren GJ, Knight MR (2005) The sfi-6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell 11: 875-886.
79. Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases:genomics of the Arabidopsis and rice CBLCIPK signaling networks. Plant Physiol 134:43-58.
80. Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B (1998) Towards functional characterization of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263-276.
81. Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289-297.
82. Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci U S A 96: 4718-4723.
83. Kudla J, Batistic O, Hashimoto K (2010) Calcium Signals:The Lead Currency of Plant Information Processing. Plant Cell 22:541-563.
84. Lee SH, Johnson JD, Walsh MP, Van Lierop JE, Sutherland C, Xu A, Snedden WA, Kosk-Kosicka D, Fromm H, Narayanan N, Cho MJ (2000) Differential regulation of Ca2+/calmodulin-dependent enzymes by plant calmodulin isoforms and free Ca2+ concentration. Biochem J 350:299-306.
85. Lee H, Xiong LM, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulates nucleo—cytoplasmic partitioning. Genes Dev 15:912-924.
86. Lee JH, Van Montagu M, Verbruggen N (1999) A highly conserved kinase is an essential component for stress tolerance in yeast and plant cells. PNAS 96:5873-5877.
87. Lee KW, Chen PW, Lu CA, Chen S, Ho TH, Yu SM (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61.
88. Lee SC, Lan WZ, Kim BG, Li L, Cheong YH, Pandey GK, Lu G, Buchanan BB, Luan S(2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci USA 104:15959-15964.
89. Li B, Liu HT, Sun DY, Zhou RG (2004) Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant Cell Physiol 45:627-634.
90. Li DD, Tai FJ, Zhang ZT, Li Y, Zheng Y, Wu YF, Li XB (2009) A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. Gene 438:26-32.
91. Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625-12630.
92. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929-938.
93. Li J and Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295:1299-1301.
94. Lilius G, Holmberg N and Bulow L (1996) Enhanced NaCl stress tolerance in transgenic tobacco expressing bacterial choline dehydrogenase. Biotechnol 14:177-180.
95. Lin C, Thomashow MF (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis COR 15 and characterization of the COR 15 polypeptide. Plant Physiol 115:171-180.
96. Liu HT, Li B, Shang ZL, Li XZ, Mu RL, Sun DY, Zhou RG (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol 132:1186-1195.
97. Liu J and Zhu JK (1997) Proline accumulation and salt-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591-596.
98. Liu J, Zhu J K (1998) A calcium sensor homolog required for plant salt tolerance. Science 280: 1943-1945.
99. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K(1998) Two transcription factors, DREB1 and DREB2, with an ERRBP/AP2 DNA binging domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant cell 10:1391-1406.
100. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins:calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389-S400.
101.Luoni L, Bonza MC, de Michelis MI (2006) Calmodulin/Ca2+-ATPase interaction at the Arabidopsis thaliana plasma membrane is dependent on calmodulin isoform showing isoform-specific Ca2+ dependencies. Physiol Plant 126:175-186.
102. Ma QB, Dai XY, Xu YY, Guo J, Liu YJ, Chen N, Xiao J, Zhang DJ, Xu ZH, Zhang XS, Chong K (2009) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol 150:244-256.
103. Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mo1 Biol 65:9511-518.
104. Mahajan S and Tuteja N (2005) Cold, Salinity and drought stresses:An overview. Arch Biochem Biophys 44: 139-158.
105. Mahajan S, Sopory SK, Tuteja N (2006) Cloning and characterization of CBL-CIPK signaling components from a legume (Pisum sativum). FEBS J 273:907-925.
106. Martmez-Atienza J, Jiang X, Garciadeblas B, Mendoza Ⅰ, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the Salt Overly Sensitive Pathway in Rice. Plant Physiol 143:1001-1012.
107. Maurel C (2007) Plant aquaporins:Novel functions and regulation properties. FEBS Lett 581: 2227-2236.
108. McCormack E and Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159:585-598.
109. Meissner RC, Jin H, Cominelli E, Denekamp M, Fuertes A, Greco R, Kranz H D, Penfield S, Petroni K, Urzainqui A, Martin C, Paz-Ares J, Smeekens S, Tonelli C, Weisshaar B, Baumann E,Klimyuk V, Jones JJ (1999) Function search in a large transcription factor gene family in Arabidopsis:assessing the potential of reverse genetics to identify insertional mutations in R2R3 MYB genes. Plant Cell 11:1827-1840.
110. Mikolajczyk M, Awotunde OS, Muszynska G, Klessig DF and Dobrowolska G (2000).Osmotic stress induces rapid activation of a salicylic acid induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12:165-178.
111. Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002a) Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the coda gene are highly tolerant to salt stress. Theor APP1 Genet,106:51-57.
112. Mohanty D, Colah RB, Gorakshakar AC, Nadkarni AH, Phanasgaonkar SP, Shetty S, Ghosh K, Mukherjee MB (2002b) Genetic disorders in haematological Practice in India. Community Genet 5:197-200.
113. Monroy AF, Sarhan F, Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression-evidence for a role of calcium. Plant Physiol 102: 1227-1235.
114. Munnik T, LigterinkW, Meskiene I, Calderini O, Beyerly J, Musgrave A and Hirt H (1999) Distinct osmo-sensing protein kinase pathways are involved in signaling moderate and severe hyper-osmotic stress. Plant J 20:381-388.
115. Nagae M, Nozawa A, Koizumi N, Sano H, Hashimoto H, Sato M, Shimizu T (2003). The crystal structure of the novel calcium-binding protein AtCBL2 from Arabidopsis thaliana. J Biol Chem. 278:42240-42246.
116. Narusaka Y, Nakashinma K, Shinwari Z K, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137-148.
117. NDong C, Danyluk J, Wilson KE, Pocock T, Huner NPA, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129:1368-1381.
118. Nozawa A, Koizumi N, Sano H (2001) An Arabidopsis SNF1-related protein kinase, AtSRl, interacts with a calcium-binding protein, AtCBL2, of which transcripts respond to light. Plant Cell Physiol 42:976-981.
119. Oh SJ, Song SI, Kim YS, Jang HJ, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341-351.
120. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Haysashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive Analysis of NAC Family Genes in Oryza sativa and Arabidopsis thaliana. DNA Research 10:239-247.
121. Pandey G, Cheong YH, Kim KN, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912-1924.
122. Pandey G, Grant J, Cheong YH, Kim BG, Li L, Luan S (2008) Calcineurin B-like protein CBL9 interactes with target kinase CIPK3 in the regulation of ABA response in seed germination. Molecular Plant 2:38-248.
123. Pandey GK, Cheong YH, Kim BG, Grant JJ, Li L, Luan S (2007) CIPK9:a calcium sensor-interacting protein kinase required for low-potassium tolerance in Arabidopsis. Cell Research 17:411-421.
124. Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J and Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282:10036-10046.
125. Perl A, Perl-Treves R, Galili S, Aviv D, Shalgi E, Malkin S, Galun E (1993) Enhanced oxidative-stress defense in transgenic potato expressing tomato Cu/Zn superoxide dismutase. Theor Appl Genet 85:568-576.
126. Perruc E, Charpenteau M, Ramirez BC, Jauneau A, Galaud JP, Ranjeva R, Ranty B (2004) A novel calmodulin-binding protein functions as a negative regulator of osmotic stress tolerance in Arabidopsis thaliana seedlings. Plant J 38:410-420.
127. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Nat/Ht exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Nat1 Acad Sci USA 99:8436-8441.
128. Qiu QS, Guo Y, Quintero FJ, Pardo JM, Schumaker KS and Zhu JK (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the SOS pathway. J Biol Chem 279: 207-215.
129. Quan R, Lin H, Mendosa I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo J, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415-1431.
130. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755-1767.
131.Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mo1 Biol 50:665-693.
132. Reddy VS, Reddy ASN (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65: 1745-1776.
133. Riechmann JL, Heard J, Martin G, Reubuer L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Ghandehari D, Sherman B K, Yu G. (2000) Arabidopsis Transcription factors:genome-wide comparative analysis among eukaryotes. Science 290:2105-2110.
134. Reid SJ and Ross GS (1997) Up-regulation of two cDNA clones encoding metallothionein-like proteins in apple fruit during cool storage. Physiol Plant 100:183-189.
135. Rodriguez HG Boberts JKM, Jordan WR, Drew MC (1997) Growth, water relation, and accumulation of organic solutes in roots of Maize seedling during salt stress. Plant Physiol 113: 881-893.
136. Rodriguez Milla MA, Uno Y, Chang IF, Townsend J, Maher EA, Quilici D, Cushman JC (2006) A novel yeast twohybrid approach to identify CDPK substrates:characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein. FEBS Lett 580:904-911.
137. Romero C, Belles JM, Vaya JL, Serrano R, Culianez-Macia FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants:pleiotropic phenotypes include drought tolerance. Planta 201:293-297.
138. Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physio1 41: 1229-1234.
139. Ryu HS, Han M, Lee SK, Cho JI, Ryoo N, Heu S, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A Comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836-847.
140. Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319-327.
141. Sairam RK, Srivastava GC (2002) Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 362: 897-904.
142. Sanders D, Pelloux J, Brownlee C, Harper J (2002) Calcium at the crossroads of signaling. Plant Cell 14:401-417.
143. Scrase-Field SA, Knight MR (2003) Calcium:just a chemical switch? Curr Opin Plant Biol 6: 500-506.
144. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292.
145. Seki M, Kamei A, Yamaguchi-Shinozaki K. Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biontechnol 14:194-199.
146. Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661-671.
147. Sharma P, Sharma N, Deswal R (2005) The molecular biology of the low temperature response in plants. BioEssays 27:1048-1059.
148. Sheen J (1996) Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900-1902.
149. Shi H, Ishitani M, Kim CS, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896-6901.
150. Shi H, Xiong L, Stevenson B, Lu T, Zhu JK (2002) The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for Vitamin B6 in plant salt tolerance. Plant Cell,14:575-588.
151. Shi H, Kim Y, Guo Y, Stevenson B, Zhu JK (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15: 19-32.
152. Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calceneurin B-like calcium sensors in Arabidopsis. Plant Cell 11: 2393-2405.
153. Shimamura C, Ohno R, Nakamura C, Takumi S (2006) Improvement of freezing tolerance in tobacco plants expressing a cold responsive and chloroplast-targeting protein WCOR15 of wheat. J Plant Physiol 163:213-219. Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular response to drought and cold stress. Curr Opin Biotechnol 7:161-167.
154. Shinozaki K and Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature:differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217-223.
155. Shinozaki K, Yamaguchi-Shinozaki K (2003) Molecular responses to dehydration and low temperature:differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 6:410-417.
156. Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430-436.
157. Smirnoff N, Bryant J A (1999). DREB takes the stress out of growing up. Nat Biotechnol 17: 229-230.
158. Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384-2396.
159. Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543-584.
160. Suzuki K and Shinshi H (1995) Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with a fungal elicitor. Plant Cell 7:639-647.
161.Talame V, Ozturk NZ, Bohnert HJ and Tuberosa R (2007) Barley transcript profiles under dehydration shock and drought stress treatments:a comparative analysis. J Exp Bot 58:229-240.
162. Tarezynski M, Jensen RG and Bohnert H (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259:508-510.
163. Thomas JC (1995) Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant Cell Environ. 18:801-806.
164. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571-599.
165. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481-2498.
166. Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plant. Plant J 58:778-790.
167. Uner Kolukisaoglu, Stefan Weinl, Dragica Blazevic, Oliver Batistic, and Jorg Kudla Calcium Sensors and Their Interacting Protein Kinases:Genomics of the Arabidopsis and Rice CBL-CIPK Signaling Networks Kim KN, Cheong Y, Pandey G, Grant J, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411-423.
168. Van Camp W, Willekens H, Bowler C, van Montagu M, Inze D, Reupold-Popp P, Samdermann H, Langebartels C (1994) Elevated levels of superoxide dismutase protect transgenic plants against ozone damage. Bio/Techno.12:165-168.
169. Vinocur B and Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotech 16:123-132.
170. Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313:1118-1122.
171. Wang YJ, Zhang ZG, He XJ, Zhou HL, Wen YX, Dai JX, Zhang JS, Chen SY (2003) A rice transcription factor OsbHLH1 is involved in cold stress response. Theor Appl Genet 107: 1402-1409.
172. Wei W, Huang J, Hao YJ, Zou HF, Wang HW, Zhao JY, Liu XY, Zhang WK, Ma B, Zhang JS, Chen SY (2009) Soybean GmPHD-type transcription regulators improve stress tolerance in transgenic Arabidopsis plants. PLoS One 4:e7209.
173. Weinl S and Kudla J (2009) The CBL-CIPK Ca2+-decoding signaling network:function and perspectives. New Phytologist 184:517-528.
174. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487-511.
175. White TC, Simmonds D, Donaldson P, Singh J (1994) Regulation of BN115, a low-temperature responsive gene from winter Brassica napus. Plant Physiol 106:917-928.
176. Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9-26.
177. Xiong L, Yang Y (2003) Disease resistence and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745-759.
178. Xing Y, Jia WS, Zhang JH (2007) AtMEK1 mediates stress induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J Exp Bot 58:2969-2981.
179. Xing Y, Jia WS, Zhang JH (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440-451.
180. Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought and salt stress. Plant Cell 14:S165-S183.
181. Xiong LZ and Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen activated protein kinase. Plant Cell 15: 745-759.
182. Xiong Y, Liu T, Tran C, Sun S, Li J, Chen M (2005) Transcription factors in rice:a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191-203.
183. Xu D (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barely confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249-257.
184. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006). A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125: 1347-1360.
185. Yakovlev IA, Asante DK, Fossdal CG, Partanen J, Junttila O, Johnsen O (2008) Dehydrins expression related to timing of bud burst in Norway spruce. Planta 228:A59-472.
186. Yamaguchi-Shinozaki K and Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88-94.
187. Yamakawa H, Katou S, Seo S, Mitsuhara I, Kamada H, Ohashi Y (2004) Plant MAPK phosphatase interacts with calmodulins. J Biol Chem 279:928-936.
188. Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis:activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 99:4097-4102.
189. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8: 505-512.
190. Yang Y, Qin Y, Xie C, Zhao F, Zhao J, Liu D, Chen S, Fuglsang AT, Palmgren MG, Schumaker KS, Deng XW, Guo Y (2010) The Arabidopsis chaperone J3 regulates the plasma membrane H+-ATPase through interaction with the PKS5 kinase. Plant Cell 22:1313-1332.
191. Yoo JH, Park CY, Kim JC, Heo WD, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH, Lee JH, Kim HS, Lee SM, Yoon HW, Lim CO, Yun DJ, Lee SY, Chung WS, Cho MJ (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem 280:3697-3706.
192. Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558-579.
193. Yu XC, Zhu SY, Gao GF, Wang XJ, Zhao R, Zou KQ, Wang XF, Zhang XY, Wu FQ, Peng CC, Zhang DP (2007) Expression of a grape calcium-dependent protein kinase ACPK1 in Arabidopsis thaliana promotes plant growth and confers abscisic acid-hypersensitivity in germination, post-germination growth, and stomatal movement. Plant Mol Biol 64:531-538.
194. Zhang HX, Blumwald E (2001a) Transgenic salt-tolerance tomato plants accumulate salt in foliage but not in fruit. Nature Biotech 19:765-768.
195. Zhang HX, Hodson JN, Williams JP, Blumwald E (2001b) Engineering salt-tolerant brassica plants:characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc.Natl.Acad.Sci. USA 98:12832-12836.
196. Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009). Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889-1901.
197. Zhu B, Su J, Chang M, Verma D, Fan Y, Wu R (1998) Overexpression of a A1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice. Plant Sci 139:41-48.
198. Zhu JK. Salt and drought stress signal transduction in plants (2002) Annu Rev Plant Biol 53: 247-273.
199. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019-3036.
2.胡红红(2006)水稻逆境相关转录因子的分离和功能鉴定。博士学位论文武汉：华中师范大学图书馆.
3.王汉中(2005)实施油菜生物柴油计划建造永不枯竭的“绿色油田”。农业科技通讯10：11.
4.张慧,董伟,周峻马等(1998)果聚糖蔗糖转移酶基因的克隆及耐盐转基因烟草的培育。生物工程学报14：741-745.
5. Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 55:541-552.
6. Aitken A, Howell S, Jones D, Madrazo J, Patel Y (1995) 14-3-3 alpha and delta are the phosphorylated forms of raf-activating 14-3-3 beta and zeta. In vivo stoichiometric phosphorylation in brain at a Ser-Pro-Glu-Lys MOTIF. J Biol Chem 270:5706-5709.
7. Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein-protein interaction module conserved in Ca2--regulated kinases. The EMBO Journal 20: 1051-1063.
8. APel K, Hirt H (2004) Reactive oxygen species:metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373-399.
9. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na-/H+ antiport in Arabidopsis. Science 285:1256-1258.
10. Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. PNAS 93:13404-13409.
11. Bargmann BO, Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9:515-522.
12. Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915-924.
13. Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plant specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435-466.
14. Boudsocq M, Sheen J (2010) Stress Signaling II:Calcium Sensing and Signaling. Abiotic Stress Adaptation in Plants. Physiological Molecular and Genomic Foundation, pp.75-90.
15. Boursiac Y, Chen S, Luu D, Sorieul M, Deies N, Maurel C (2005) Early Effects of Salinity on Water Transport in Arabidopsis Roots. Molecular and Cellular Features of Aquaporin Expression. Plant Physiol 139:790-805.
16. Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Knal. Plant Physiol 143:1918-1928.
17. Chatthai M, Kaukinen KH, Tranbarger TJ, Gupta PK and Misra S (1997) The isolation of a novel metal lothionein-related cDNA expressed in somatic and zygotic embryos of douglas-fir: regulation by ABA, osmoticum, and metal ions. Plant Mol Biol 34:243-254.
18. Chen L, Ren F, Zhong H, Jiang WM, Li XB (2010) Identification and expression analysis of genes induced by high-salinity and drought stresses in Brassica napus. Acta Biochim Biophys Sin 42:154-164.
19. Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21:3554-3566.
20. Cheng LH, Zhang B, Xu ZQ (2007) Genetic transformation of buckwheat (Fagopyrum esculentum Moench) with AtNHX1 gene and regeneration of salt-tolerant transgenic plants. Sheng Wu Gong Cheng Xue Bao 23:51-60.
21. Cheng NH, Pittman JK, Zhu JK, Hirschi KD (2004) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922-2926.
22. Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases: The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469-485.
23. Cheong YH, Pandey GK, Grant J, Batistic O, Li L, Lee SC, Kim BG, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223-239.
24. Chevalier C, Bourgeois E, Pradet A and Raymond P (1995) Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips. Plant Mol Biol 28:473-485.
25. Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICEI:a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043-1054.
26. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends plant Sci 12:444-451
27. Choe S, Schmitz RJ, Fujioka S, Takatsuto S, Lee MO, Yoshida S, Feldmann KA and Tax FE (2002) Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3beta-like kinase. Plant Physiol 130:1506-1515.
28. Choi D, Kim HM, Yun HK, Park JA, Kim WT and Bok SH (1996) Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L and its induction by wounding and tobacco mosaic virus infection. Plant Physiol 112:353-359.
29. Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binging factors. J Biol Chem 275:1723-1730.
30. Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang Ⅰ, Kim SY (2005a) Arabidopsis calcium dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750-1761.
31. Clouse SD (1996) Molecular genetic studies confirm the role of brassinosteroids in plant growth and development. Plant J 10:1-8
32. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735-743.
33. Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Lenohardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regultates stomatal movements and plant drought tolerance. Curr Biol 15:1196-1200.
34. D' Angelo C, Weinl S, Batistic O, Pandey G, Sch(?)ultke YHCS, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid dependent and independent stress responses in Arabidopsis. Plant J 48:857-872.
35. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21: 972-984.
36. Ershov PV, Reshetova OS, Trofimova MS, Babakov AV (2005) Activity of ion transporters and salt tolerance in barley. Russian Journal of Plant Physiology 6:765-773.
37. Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19: 1617-1634.
38. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway, Plant J 39:863-876.
39. Fusaro A, Mangeon A, Magrani-Junqueira R, Bem'cio-Rocha CA, Cardoso-Coutinho T, Margis R, Sachetto-Martins G (2001) Classification, expression pattern and comparative analysis of sugarcane expressed sequences tags (ESTs) encoding glycine rich proteins (GRPs). Genet Mol Biol 24:263-273
40. Garcia AB, Engler J, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants on NaCl stress in rice. Plant Physiol 115:159-169
41. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Nati Acad Sci USA 99:15898-15903.
42. Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459-471.
43. Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13-21.
44. Gong D, Guo Y, Jagendorf AT, Zhu JK (2002a) Biochemical characterization of the Arabidopsis protein kinase SOS2 that functions in salt tolerance. Plant Physiol 130:256-264.
45. Gong D, Gong Z, Guo Y, Chen X, Zhu JK (2002b) Biochemical and functional characterization of PKS11, a novel Arabidopsis protein kinase. J Biol Chem 277:28340-28350.
46. Gong D, Zhang C, Chen X, Gong Z, Zhu JK (2002c) Constitutive activation and transgenic evaluation of the function of an Arabidopsis PKS protein kinase. J Biol Chem 277:42088-42096.
47. Gong D, Guo Y, Schurnaker K, Zhu JK (2004) The SOS3 family of calcium sensors and SOS2 family of protein kinases in Arabidopsis. Plant Physiol 134:919-926.
48. Guo Y, Halfter U, Ishitani M, Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383-1399.
49. Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK (2002) A calcium sensor and its interacting protein kinase are globar regulators of abscisic acid signaling in Arabidopsis. Developmental Cell 3:233-244.
50. Gupta A, Heinen J, Holaday A, Burke J, Allen R (1993) Increased resistance to oxidative stress in transgenic Plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci USA 90:1629-1633.
51. Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639-648.
52. Halfter U, Ishitani M, Zhu J K (2000)The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium2+binding protein SOS3. Proc Natl Acad Sci USA 97:3735-3740.
53. Harmon AC, Gribskov M, Harper J F (2000) CDPKs:A kinase for every Ca2+ signal? Trends Plant Sci 5:317-319.
54. Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263-288.
55. Hayashi, H., Mustardy, L., Deshnium, P., Ida, M. & Murata, N(1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase:accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12:133-142.
56. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903-916.
57. Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53:383-397.
58. Hidenori H (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase:accumulation of glycinebetaine and enhanced tolerance to salt and stress. Planta 12: 133-142.
59. Hirt H (1997). Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci 2: 11-15.
60. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138: 1184-1194.
61. Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 32:666-680.
62. Hsieh HM, Liu WK and Huang PC (1995) A novel stress-inducible metallothionein-like gene from rice. Plant Mol Biol 28: 381-389.
63. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264-278.
64. Huang DQ, Wu WR, Abrams SR and Cutler AJ (2008) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59: 2991-3007.
65. Hwang Ⅰ, Sze H, Harper JF (2000) A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc Natl Acad Sci USA 97:6224-6229.
66. Jeroni G, Alicia P, Maria Mar A, Magdalena T, Hipolito M, Jaume F (2007) Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.):relationship with ecophysiological status. Planta 226:671-681.
67. Johansson Ⅰ, Larsson C, Ek B, Kjellbom P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8:1181-1191.
68. Johasson Ⅰ, Karisson M, Shukla V, Chrispeels M, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin RM28A is regulated by phosphorylation. Plant Cell 10:451-459.
69. Jonak C, Kiegerl S, Ligterink W, Baker PJ, Huskisson NS and Hirt H (1996) Stress signaling in plants:a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274-11279.
70. Kader MA, Seidel T, Golldack D, Lindberg S (2006) Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot 57:4257-4268.
71. Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343-357.
72. Kim BG, Waadt R, Cheong Y, Pandey G, Dominguez-Solis J, Sch(?)ultke S, Lee S, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473-484.
73. Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Lee MH, Moon J, Lee I, Kim J (2004)A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36:167-171.
74. Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO, Cho MJ (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 25:247-259.
75. Kim KN, Cheong Y, Pandey G, Grant J, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411-423.
76. Kishor PBK, Hong Z, Miao GH, Hu CAA, Verma DPS(1995) Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants. Plant Physiol 108:1387-1394.
77. Knight H and Knight MR (2001) Abiotic stress signalling pathways:specificity and cross-talk. Trends Plant Sci 6:262-267.
78. Knight H, Veale EL, Warren GJ, Knight MR (2005) The sfi-6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell 11: 875-886.
79. Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases:genomics of the Arabidopsis and rice CBLCIPK signaling networks. Plant Physiol 134:43-58.
80. Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B (1998) Towards functional characterization of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263-276.
81. Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289-297.
82. Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci U S A 96: 4718-4723.
83. Kudla J, Batistic O, Hashimoto K (2010) Calcium Signals:The Lead Currency of Plant Information Processing. Plant Cell 22:541-563.
84. Lee SH, Johnson JD, Walsh MP, Van Lierop JE, Sutherland C, Xu A, Snedden WA, Kosk-Kosicka D, Fromm H, Narayanan N, Cho MJ (2000) Differential regulation of Ca2+/calmodulin-dependent enzymes by plant calmodulin isoforms and free Ca2+ concentration. Biochem J 350:299-306.
85. Lee H, Xiong LM, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulates nucleo—cytoplasmic partitioning. Genes Dev 15:912-924.
86. Lee JH, Van Montagu M, Verbruggen N (1999) A highly conserved kinase is an essential component for stress tolerance in yeast and plant cells. PNAS 96:5873-5877.
87. Lee KW, Chen PW, Lu CA, Chen S, Ho TH, Yu SM (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61.
88. Lee SC, Lan WZ, Kim BG, Li L, Cheong YH, Pandey GK, Lu G, Buchanan BB, Luan S(2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci USA 104:15959-15964.
89. Li B, Liu HT, Sun DY, Zhou RG (2004) Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant Cell Physiol 45:627-634.
90. Li DD, Tai FJ, Zhang ZT, Li Y, Zheng Y, Wu YF, Li XB (2009) A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. Gene 438:26-32.
91. Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625-12630.
92. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929-938.
93. Li J and Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295:1299-1301.
94. Lilius G, Holmberg N and Bulow L (1996) Enhanced NaCl stress tolerance in transgenic tobacco expressing bacterial choline dehydrogenase. Biotechnol 14:177-180.
95. Lin C, Thomashow MF (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis COR 15 and characterization of the COR 15 polypeptide. Plant Physiol 115:171-180.
96. Liu HT, Li B, Shang ZL, Li XZ, Mu RL, Sun DY, Zhou RG (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol 132:1186-1195.
97. Liu J and Zhu JK (1997) Proline accumulation and salt-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591-596.
98. Liu J, Zhu J K (1998) A calcium sensor homolog required for plant salt tolerance. Science 280: 1943-1945.
99. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K(1998) Two transcription factors, DREB1 and DREB2, with an ERRBP/AP2 DNA binging domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant cell 10:1391-1406.
100. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins:calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389-S400.
101.Luoni L, Bonza MC, de Michelis MI (2006) Calmodulin/Ca2+-ATPase interaction at the Arabidopsis thaliana plasma membrane is dependent on calmodulin isoform showing isoform-specific Ca2+ dependencies. Physiol Plant 126:175-186.
102. Ma QB, Dai XY, Xu YY, Guo J, Liu YJ, Chen N, Xiao J, Zhang DJ, Xu ZH, Zhang XS, Chong K (2009) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol 150:244-256.
103. Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mo1 Biol 65:9511-518.
104. Mahajan S and Tuteja N (2005) Cold, Salinity and drought stresses:An overview. Arch Biochem Biophys 44: 139-158.
105. Mahajan S, Sopory SK, Tuteja N (2006) Cloning and characterization of CBL-CIPK signaling components from a legume (Pisum sativum). FEBS J 273:907-925.
106. Martmez-Atienza J, Jiang X, Garciadeblas B, Mendoza Ⅰ, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the Salt Overly Sensitive Pathway in Rice. Plant Physiol 143:1001-1012.
107. Maurel C (2007) Plant aquaporins:Novel functions and regulation properties. FEBS Lett 581: 2227-2236.
108. McCormack E and Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159:585-598.
109. Meissner RC, Jin H, Cominelli E, Denekamp M, Fuertes A, Greco R, Kranz H D, Penfield S, Petroni K, Urzainqui A, Martin C, Paz-Ares J, Smeekens S, Tonelli C, Weisshaar B, Baumann E,Klimyuk V, Jones JJ (1999) Function search in a large transcription factor gene family in Arabidopsis:assessing the potential of reverse genetics to identify insertional mutations in R2R3 MYB genes. Plant Cell 11:1827-1840.
110. Mikolajczyk M, Awotunde OS, Muszynska G, Klessig DF and Dobrowolska G (2000).Osmotic stress induces rapid activation of a salicylic acid induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12:165-178.
111. Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002a) Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the coda gene are highly tolerant to salt stress. Theor APP1 Genet,106:51-57.
112. Mohanty D, Colah RB, Gorakshakar AC, Nadkarni AH, Phanasgaonkar SP, Shetty S, Ghosh K, Mukherjee MB (2002b) Genetic disorders in haematological Practice in India. Community Genet 5:197-200.
113. Monroy AF, Sarhan F, Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression-evidence for a role of calcium. Plant Physiol 102: 1227-1235.
114. Munnik T, LigterinkW, Meskiene I, Calderini O, Beyerly J, Musgrave A and Hirt H (1999) Distinct osmo-sensing protein kinase pathways are involved in signaling moderate and severe hyper-osmotic stress. Plant J 20:381-388.
115. Nagae M, Nozawa A, Koizumi N, Sano H, Hashimoto H, Sato M, Shimizu T (2003). The crystal structure of the novel calcium-binding protein AtCBL2 from Arabidopsis thaliana. J Biol Chem. 278:42240-42246.
116. Narusaka Y, Nakashinma K, Shinwari Z K, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137-148.
117. NDong C, Danyluk J, Wilson KE, Pocock T, Huner NPA, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129:1368-1381.
118. Nozawa A, Koizumi N, Sano H (2001) An Arabidopsis SNF1-related protein kinase, AtSRl, interacts with a calcium-binding protein, AtCBL2, of which transcripts respond to light. Plant Cell Physiol 42:976-981.
119. Oh SJ, Song SI, Kim YS, Jang HJ, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341-351.
120. Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Haysashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive Analysis of NAC Family Genes in Oryza sativa and Arabidopsis thaliana. DNA Research 10:239-247.
121. Pandey G, Cheong YH, Kim KN, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912-1924.
122. Pandey G, Grant J, Cheong YH, Kim BG, Li L, Luan S (2008) Calcineurin B-like protein CBL9 interactes with target kinase CIPK3 in the regulation of ABA response in seed germination. Molecular Plant 2:38-248.
123. Pandey GK, Cheong YH, Kim BG, Grant JJ, Li L, Luan S (2007) CIPK9:a calcium sensor-interacting protein kinase required for low-potassium tolerance in Arabidopsis. Cell Research 17:411-421.
124. Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J and Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282:10036-10046.
125. Perl A, Perl-Treves R, Galili S, Aviv D, Shalgi E, Malkin S, Galun E (1993) Enhanced oxidative-stress defense in transgenic potato expressing tomato Cu/Zn superoxide dismutase. Theor Appl Genet 85:568-576.
126. Perruc E, Charpenteau M, Ramirez BC, Jauneau A, Galaud JP, Ranjeva R, Ranty B (2004) A novel calmodulin-binding protein functions as a negative regulator of osmotic stress tolerance in Arabidopsis thaliana seedlings. Plant J 38:410-420.
127. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Nat/Ht exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Nat1 Acad Sci USA 99:8436-8441.
128. Qiu QS, Guo Y, Quintero FJ, Pardo JM, Schumaker KS and Zhu JK (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the SOS pathway. J Biol Chem 279: 207-215.
129. Quan R, Lin H, Mendosa I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo J, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415-1431.
130. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755-1767.
131.Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mo1 Biol 50:665-693.
132. Reddy VS, Reddy ASN (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65: 1745-1776.
133. Riechmann JL, Heard J, Martin G, Reubuer L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Ghandehari D, Sherman B K, Yu G. (2000) Arabidopsis Transcription factors:genome-wide comparative analysis among eukaryotes. Science 290:2105-2110.
134. Reid SJ and Ross GS (1997) Up-regulation of two cDNA clones encoding metallothionein-like proteins in apple fruit during cool storage. Physiol Plant 100:183-189.
135. Rodriguez HG Boberts JKM, Jordan WR, Drew MC (1997) Growth, water relation, and accumulation of organic solutes in roots of Maize seedling during salt stress. Plant Physiol 113: 881-893.
136. Rodriguez Milla MA, Uno Y, Chang IF, Townsend J, Maher EA, Quilici D, Cushman JC (2006) A novel yeast twohybrid approach to identify CDPK substrates:characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein. FEBS Lett 580:904-911.
137. Romero C, Belles JM, Vaya JL, Serrano R, Culianez-Macia FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants:pleiotropic phenotypes include drought tolerance. Planta 201:293-297.
138. Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physio1 41: 1229-1234.
139. Ryu HS, Han M, Lee SK, Cho JI, Ryoo N, Heu S, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A Comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836-847.
140. Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319-327.
141. Sairam RK, Srivastava GC (2002) Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 362: 897-904.
142. Sanders D, Pelloux J, Brownlee C, Harper J (2002) Calcium at the crossroads of signaling. Plant Cell 14:401-417.
143. Scrase-Field SA, Knight MR (2003) Calcium:just a chemical switch? Curr Opin Plant Biol 6: 500-506.
144. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292.
145. Seki M, Kamei A, Yamaguchi-Shinozaki K. Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biontechnol 14:194-199.
146. Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661-671.
147. Sharma P, Sharma N, Deswal R (2005) The molecular biology of the low temperature response in plants. BioEssays 27:1048-1059.
148. Sheen J (1996) Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900-1902.
149. Shi H, Ishitani M, Kim CS, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896-6901.
150. Shi H, Xiong L, Stevenson B, Lu T, Zhu JK (2002) The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for Vitamin B6 in plant salt tolerance. Plant Cell,14:575-588.
151. Shi H, Kim Y, Guo Y, Stevenson B, Zhu JK (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15: 19-32.
152. Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calceneurin B-like calcium sensors in Arabidopsis. Plant Cell 11: 2393-2405.
153. Shimamura C, Ohno R, Nakamura C, Takumi S (2006) Improvement of freezing tolerance in tobacco plants expressing a cold responsive and chloroplast-targeting protein WCOR15 of wheat. J Plant Physiol 163:213-219. Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular response to drought and cold stress. Curr Opin Biotechnol 7:161-167.
154. Shinozaki K and Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature:differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217-223.
155. Shinozaki K, Yamaguchi-Shinozaki K (2003) Molecular responses to dehydration and low temperature:differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 6:410-417.
156. Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430-436.
157. Smirnoff N, Bryant J A (1999). DREB takes the stress out of growing up. Nat Biotechnol 17: 229-230.
158. Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384-2396.
159. Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543-584.
160. Suzuki K and Shinshi H (1995) Transient activation and tyrosine phosphorylation of a protein kinase in tobacco cells treated with a fungal elicitor. Plant Cell 7:639-647.
161.Talame V, Ozturk NZ, Bohnert HJ and Tuberosa R (2007) Barley transcript profiles under dehydration shock and drought stress treatments:a comparative analysis. J Exp Bot 58:229-240.
162. Tarezynski M, Jensen RG and Bohnert H (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259:508-510.
163. Thomas JC (1995) Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant Cell Environ. 18:801-806.
164. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571-599.
165. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481-2498.
166. Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plant. Plant J 58:778-790.
167. Uner Kolukisaoglu, Stefan Weinl, Dragica Blazevic, Oliver Batistic, and Jorg Kudla Calcium Sensors and Their Interacting Protein Kinases:Genomics of the Arabidopsis and Rice CBL-CIPK Signaling Networks Kim KN, Cheong Y, Pandey G, Grant J, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411-423.
168. Van Camp W, Willekens H, Bowler C, van Montagu M, Inze D, Reupold-Popp P, Samdermann H, Langebartels C (1994) Elevated levels of superoxide dismutase protect transgenic plants against ozone damage. Bio/Techno.12:165-168.
169. Vinocur B and Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotech 16:123-132.
170. Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313:1118-1122.
171. Wang YJ, Zhang ZG, He XJ, Zhou HL, Wen YX, Dai JX, Zhang JS, Chen SY (2003) A rice transcription factor OsbHLH1 is involved in cold stress response. Theor Appl Genet 107: 1402-1409.
172. Wei W, Huang J, Hao YJ, Zou HF, Wang HW, Zhao JY, Liu XY, Zhang WK, Ma B, Zhang JS, Chen SY (2009) Soybean GmPHD-type transcription regulators improve stress tolerance in transgenic Arabidopsis plants. PLoS One 4:e7209.
173. Weinl S and Kudla J (2009) The CBL-CIPK Ca2+-decoding signaling network:function and perspectives. New Phytologist 184:517-528.
174. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487-511.
175. White TC, Simmonds D, Donaldson P, Singh J (1994) Regulation of BN115, a low-temperature responsive gene from winter Brassica napus. Plant Physiol 106:917-928.
176. Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9-26.
177. Xiong L, Yang Y (2003) Disease resistence and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745-759.
178. Xing Y, Jia WS, Zhang JH (2007) AtMEK1 mediates stress induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J Exp Bot 58:2969-2981.
179. Xing Y, Jia WS, Zhang JH (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440-451.
180. Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought and salt stress. Plant Cell 14:S165-S183.
181. Xiong LZ and Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen activated protein kinase. Plant Cell 15: 745-759.
182. Xiong Y, Liu T, Tran C, Sun S, Li J, Chen M (2005) Transcription factors in rice:a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191-203.
183. Xu D (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barely confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249-257.
184. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006). A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125: 1347-1360.
185. Yakovlev IA, Asante DK, Fossdal CG, Partanen J, Junttila O, Johnsen O (2008) Dehydrins expression related to timing of bud burst in Norway spruce. Planta 228:A59-472.
186. Yamaguchi-Shinozaki K and Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88-94.
187. Yamakawa H, Katou S, Seo S, Mitsuhara I, Kamada H, Ohashi Y (2004) Plant MAPK phosphatase interacts with calmodulins. J Biol Chem 279:928-936.
188. Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis:activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 99:4097-4102.
189. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8: 505-512.
190. Yang Y, Qin Y, Xie C, Zhao F, Zhao J, Liu D, Chen S, Fuglsang AT, Palmgren MG, Schumaker KS, Deng XW, Guo Y (2010) The Arabidopsis chaperone J3 regulates the plasma membrane H+-ATPase through interaction with the PKS5 kinase. Plant Cell 22:1313-1332.
191. Yoo JH, Park CY, Kim JC, Heo WD, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH, Lee JH, Kim HS, Lee SM, Yoon HW, Lim CO, Yun DJ, Lee SY, Chung WS, Cho MJ (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem 280:3697-3706.
192. Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558-579.
193. Yu XC, Zhu SY, Gao GF, Wang XJ, Zhao R, Zou KQ, Wang XF, Zhang XY, Wu FQ, Peng CC, Zhang DP (2007) Expression of a grape calcium-dependent protein kinase ACPK1 in Arabidopsis thaliana promotes plant growth and confers abscisic acid-hypersensitivity in germination, post-germination growth, and stomatal movement. Plant Mol Biol 64:531-538.
194. Zhang HX, Blumwald E (2001a) Transgenic salt-tolerance tomato plants accumulate salt in foliage but not in fruit. Nature Biotech 19:765-768.
195. Zhang HX, Hodson JN, Williams JP, Blumwald E (2001b) Engineering salt-tolerant brassica plants:characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc.Natl.Acad.Sci. USA 98:12832-12836.
196. Zhang SW, Li CH, Cao J, Zhang YC, Zhang SQ, Xia YF, Sun DY, Sun Y (2009). Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/OsGH3.13 activation. Plant Physiol 151:1889-1901.
197. Zhu B, Su J, Chang M, Verma D, Fan Y, Wu R (1998) Overexpression of a A1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice. Plant Sci 139:41-48.
198. Zhu JK. Salt and drought stress signal transduction in plants (2002) Annu Rev Plant Biol 53: 247-273.
199. Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019-3036.