小麦CBL基因CIPK基因的克隆及在非生物胁迫中的功能研究
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摘要
小麦是世界上最重要的粮食作物，其种植面积、总产量及总贸易额均居粮食作物之首。干旱、高盐等是严重影响小麦产量和品质的非生物逆境，研究小麦对逆境信号的感知、传导以及抗逆性的分子机制，对小麦抗逆分子育种研究与开发具有重要意义。Ca~(2+)作为第二信使介导植物对各种不同逆境胁迫的反应，这其中涉及到复杂的信号转导途径。类钙调磷酸酶B蛋白(Calcineurin B-Like, CBL)和其互作蛋白激酶（CBL-interacting protein kinase, CIPK）是与非生物逆境胁迫相关的Ca~(2+)信号转导中很重要的组分。然而到目前为止，除了发现一个小麦CIPK基因（WPK4）参与细胞分裂素以及光和营养胁迫信号转导外，对小麦CBL和CIPK基因的系统研究还未见报道。我们在对DFCI数据库和NCBI数据库中小麦CBL和CIPK基因相关EST序列的搜索和分析的基础上，利用RACE技术分别成功地克隆了7个CBL基因和8个CIPK基因，并对它们编码的蛋白质进行了系统的分析。利用酵母双杂交方法研究了CBL和CIPK之间特异的相互作用。利用RT-PCR和qRT-PCR技术分析了这些基因在不同非生物胁迫逆境处理下的表达水平。另外，进一步通过对转TaCIPK14基因和转TaCIPK29基因的烟草在非生物胁迫下的表型，生理生化指标与分子机制的分析，揭示了TaCIPK14和TaCIPK29在非生物胁迫中功能和作用机理，取得的主要研究结果如下：
1）小麦CBL和CIPK蛋白与水稻同源的CBL和CIPK蛋白的氨基酸序列和结构高度相似，这些CBL蛋白均含有四个能结合Ca~(2+)的EF-hands结构域和一个FPSF结构域；CIPK蛋白都含有激酶结构域，FISL结构域和PPI结构域。进化分析显示，小麦CBL蛋白和CIPK蛋白和水稻同源CBL蛋白和CIPK蛋白都归类于相同的亚族。
2）基因表达分析结果表明，小麦特定的CBL或CIPK基因对冷、盐、渗透胁迫和ABA处理的响应模式不同，而且同一处理能够被不同的CBL或CIPK基因感应，这说明小麦CBL和CIPK基因可能介导对不同胁迫信号的交联过程。
3）利用酵母双杂交技术分析发现，小麦不同的CBL和CIPK蛋白之间的相互作用的特异性和强度不同。一些重要的特异性的CBL-CIPK互作子如：TaCBL1-TaCIPK9,TaCBL1-TaCIPK23, TaCBL2-TaCIPK2, TaCBL3-TaCIPK2, TaCBL2-TaCIPK29和TaCBL3-TaCIPK29可能参与小麦对不同非生物胁迫的响应。这些结果表明，小麦CBL和CIPK对不同非生物胁迫的信号转导是通过形成不同的CBL-CIPK复合物来解码特定胁迫下产生的特异Ca~(2+)信号。
4）系统分析了TaCIPK14基因和TaCIPK29基因在非生物胁迫反应中的作用。TaCIPK14基因受冷、渗透胁迫和盐胁迫等非生物胁迫以及胁迫相关信号分子ABA、乙烯和H2O2诱导。证明了在烟草中过表达TaCIPK14基因可提高转基因烟草植株对冷和盐胁迫的抗性。TaCIPK14提高对冷和盐的抗性是通过调控一些抗氧化酶或胁迫相关基因如NtCAT, NtDREB3和NtLEA等的表达来实现的。增强的抗氧化酶的活性有助于清除逆境下产生的过量ROS，减轻ROS对细胞膜的损伤。同时，TaCIPK14能降低转基因烟草在盐胁迫下的Na+含量和提高细胞的K+/Na+比率，这也有助于植物对盐胁迫的抗性。
5）TaCIPK29基因能够被盐、冷、甲基紫晶（MV）、ABA和乙烯诱导。过表达TaCIPK29基因的烟草植株增强了对盐胁迫的抗性。TaCIPK29通过提高一些通道蛋白基因如NtSOS1，NtNHX2，NtNHX4和NtCAX3的表达来维持高的K+/Na+比和Ca~(2+)含量以及通过增强CAT和POD的表达和活性来减少H2O2对细胞膜的损伤来抵抗盐胁迫的伤害。TaCIPK29没有特定的定位信号，在整个细胞中都有分布。TaCIPK29不仅能够特异地与小麦的TaCBL2和TaCBL3互作，也能与烟草的NtCBL2和NtCBL3互作，说明TaCIPK29通过CBL2和CBL3传递Ca~(2+)信号。同时TaCIPK29还能与烟草的NtCAT1相互作用，增强其活性，这有助于清除过多的H2O2。因此，TaCIPK29是一个盐胁迫中的正调控因子，参与了盐胁迫下对离子和ROS的调控。综上所述，如同水稻和拟南芥中同源的CBL和CIPK基因一样，小麦CBL和CIPK基因也是非生物胁迫响应基因。不同的CBL和CIPK基因可能赋予植物对不同逆境的抗性。已鉴定的抗逆基因TaCIPK14和TaCIPK29可作为培育转基因抗逆小麦新品种的候选基因。本研究为深入研究小麦中这两个重要的基因家族的功能和分子机制奠定了基础，同时也有助于小麦抗逆分子育种研究与开发。
Wheat is a world staple crop, and its acreage, total production and trade ranks thefirst place among food crops. However, wheat production is often constrained by variousabiotic stresses, such as drought, salinity, and extreme temperatures. Understanding themolecular mechanism of the abiotic stress responses can facilitate the geneticimprovement of stress tolerance in wheat. Calcium, as a second messenger, is involved inthe mediation of various responses to different environmental stresses and related tohighly complex signal transduction pathways. Calcineurin B-like proteins (CBLs) andtheir target proteins, the CBL-interacting protein kinases (CIPKs), have emerged as keyCa~(2+)-mediated signaling components in response to various abiotic stresses in many plants.However, the CBL and CIPK genes in wheat have not yet been comprehensively studied todate，except one CIPK gene（WPK4）which has been reported to mediate cytokinesignaling transduction and the response to light and nutrient deprivation. In this study,seven CBL genes and eight CIPK genes were amplified from wheat genome using theRACE technique and their preferential interaction and differential responses to variousabiotic stresses were investigated. The roles of two wheat CIPK genes TaCIPK14andTaCIPK29in response to abiotic stresses were further inverstigated. The main results areas follows:
1) Wheat CBLs and CIPKs were found to be similar to their counterparts in rice in motifstructure and subgroup classifcation. These CBL proteins have four EF-hands andFPSF domains, while CIPK proteins contain kinase domain, FISL domain and PPIdomain.
2) The isolated wheat CBL and CIPK genes were found to be expressed differentially invarious tissues and in response to different abiotic stresses including cold, salt, andosmotic stresses and exposure to the phytohormone abscisic acid (ABA). Furthermore,we also found that one CBL or CIPK gene was able to respond to several treatments,and one treatment was sensed by multiple CBL or CIPK genes. Thus, TaCBLs andTaCIPKs were found to mediate crosstalk among different signaling pathways.
3) The preferential interactions of TaCBLs and TaCIPKs were identified using a yeast two-hybrid assay. Several important, specific CBL-CIPK interaction partners(TaCBL1-TaCIPK9, TaCBL1-TaCIPK23, TaCBL2-TaCIPK2, and TaCBL3-TaCIPK2,TaCBL2/TaCBL3-TaCIPK29) were found to be responsive to distinct abiotic stresses.These results suggest that wheat CBL and CIPK genes may collectively mediatecrosstalk of multiple stress signaling pathways through the formation of differentCBL-CIPK complexes to decode stress-specific Ca~(2+)signaling.
4) The roles of the TaCIPK14and TaCIPK29gene in response to various abiotic stresseswere further investigated. TaCIPK14gene was upregulated under cold or when treatedwith salt, PEG or exogenous stresses related signaling molecules including ABA,ethylene and H2O2.Subcellular localization assay revealed the presence of TaCIPK14throughout the cell. Phenotype analysis showed that overexpression of TaCIPK14intobacco enhanced cold and salt stress tolerance. Overexpression of TaCIPK14enhanced cold and salt stress tolerance by regulating the expression of antioxidantgenes or stress related genes such as NtCAT, NtDREB3, NtLEA5, etc and enhancingthe antioxidant system to reduce ROS accumulation and relieve membrane damage.Moreover, enhanced salt stress tolerance in TaCIPK14overexpressing plants was alsoattributed to decreased Na+content and elevated K+/Na+ratio.
5) TaCIPK29transcript was induced by NaCl, cold, methyl viologen (MV), ABA andethylene treatments. Overexpression of TaCIPK29in tobacco resulted in increased salttolerance. Further investigation showed that transgenic tobacco seedlings retained highK+/Na+ratio and Ca~(2+)content by up-regulating some transporter genes such as NtSOS1,NtNHX2, NtNHX4and NtCAX3and reduced H2O2accumulation and membranedamage through enhancing the activities and expression of CAT and POD under saltstress. Finally, TaCIPK29was localized throughout cells and it interacted withTaCBL2, TaCBL3, NtCBL2, NtCBL3and NtCAT1. Taken together, our resultsshowed that TaCIPK29functions as a positive factor under salt stress, involved in theregulation of ion and ROS homeostasis.
In conclusion, wheat CBL and CIPK genes were found to be abiotic stress responsivegenes as those in rice and Arabidopsis. Different CBL or CIPK genes may differentiallycontribute to the plants’ tolerance to distinct stresses. TaCIPK14and TaCIPK29gene maybe useful candidate genes for developing stress-tolerant crops including wheat. Our work may facilitate further functional studies of these two important gene families and isbeneficial for further molecular breeding in wheat.
1）小麦CBL和CIPK蛋白与水稻同源的CBL和CIPK蛋白的氨基酸序列和结构高度相似，这些CBL蛋白均含有四个能结合Ca~(2+)的EF-hands结构域和一个FPSF结构域；CIPK蛋白都含有激酶结构域，FISL结构域和PPI结构域。进化分析显示，小麦CBL蛋白和CIPK蛋白和水稻同源CBL蛋白和CIPK蛋白都归类于相同的亚族。
2）基因表达分析结果表明，小麦特定的CBL或CIPK基因对冷、盐、渗透胁迫和ABA处理的响应模式不同，而且同一处理能够被不同的CBL或CIPK基因感应，这说明小麦CBL和CIPK基因可能介导对不同胁迫信号的交联过程。
3）利用酵母双杂交技术分析发现，小麦不同的CBL和CIPK蛋白之间的相互作用的特异性和强度不同。一些重要的特异性的CBL-CIPK互作子如：TaCBL1-TaCIPK9,TaCBL1-TaCIPK23, TaCBL2-TaCIPK2, TaCBL3-TaCIPK2, TaCBL2-TaCIPK29和TaCBL3-TaCIPK29可能参与小麦对不同非生物胁迫的响应。这些结果表明，小麦CBL和CIPK对不同非生物胁迫的信号转导是通过形成不同的CBL-CIPK复合物来解码特定胁迫下产生的特异Ca~(2+)信号。
4）系统分析了TaCIPK14基因和TaCIPK29基因在非生物胁迫反应中的作用。TaCIPK14基因受冷、渗透胁迫和盐胁迫等非生物胁迫以及胁迫相关信号分子ABA、乙烯和H2O2诱导。证明了在烟草中过表达TaCIPK14基因可提高转基因烟草植株对冷和盐胁迫的抗性。TaCIPK14提高对冷和盐的抗性是通过调控一些抗氧化酶或胁迫相关基因如NtCAT, NtDREB3和NtLEA等的表达来实现的。增强的抗氧化酶的活性有助于清除逆境下产生的过量ROS，减轻ROS对细胞膜的损伤。同时，TaCIPK14能降低转基因烟草在盐胁迫下的Na+含量和提高细胞的K+/Na+比率，这也有助于植物对盐胁迫的抗性。
5）TaCIPK29基因能够被盐、冷、甲基紫晶（MV）、ABA和乙烯诱导。过表达TaCIPK29基因的烟草植株增强了对盐胁迫的抗性。TaCIPK29通过提高一些通道蛋白基因如NtSOS1，NtNHX2，NtNHX4和NtCAX3的表达来维持高的K+/Na+比和Ca~(2+)含量以及通过增强CAT和POD的表达和活性来减少H2O2对细胞膜的损伤来抵抗盐胁迫的伤害。TaCIPK29没有特定的定位信号，在整个细胞中都有分布。TaCIPK29不仅能够特异地与小麦的TaCBL2和TaCBL3互作，也能与烟草的NtCBL2和NtCBL3互作，说明TaCIPK29通过CBL2和CBL3传递Ca~(2+)信号。同时TaCIPK29还能与烟草的NtCAT1相互作用，增强其活性，这有助于清除过多的H2O2。因此，TaCIPK29是一个盐胁迫中的正调控因子，参与了盐胁迫下对离子和ROS的调控。综上所述，如同水稻和拟南芥中同源的CBL和CIPK基因一样，小麦CBL和CIPK基因也是非生物胁迫响应基因。不同的CBL和CIPK基因可能赋予植物对不同逆境的抗性。已鉴定的抗逆基因TaCIPK14和TaCIPK29可作为培育转基因抗逆小麦新品种的候选基因。本研究为深入研究小麦中这两个重要的基因家族的功能和分子机制奠定了基础，同时也有助于小麦抗逆分子育种研究与开发。
Wheat is a world staple crop, and its acreage, total production and trade ranks thefirst place among food crops. However, wheat production is often constrained by variousabiotic stresses, such as drought, salinity, and extreme temperatures. Understanding themolecular mechanism of the abiotic stress responses can facilitate the geneticimprovement of stress tolerance in wheat. Calcium, as a second messenger, is involved inthe mediation of various responses to different environmental stresses and related tohighly complex signal transduction pathways. Calcineurin B-like proteins (CBLs) andtheir target proteins, the CBL-interacting protein kinases (CIPKs), have emerged as keyCa~(2+)-mediated signaling components in response to various abiotic stresses in many plants.However, the CBL and CIPK genes in wheat have not yet been comprehensively studied todate，except one CIPK gene（WPK4）which has been reported to mediate cytokinesignaling transduction and the response to light and nutrient deprivation. In this study,seven CBL genes and eight CIPK genes were amplified from wheat genome using theRACE technique and their preferential interaction and differential responses to variousabiotic stresses were investigated. The roles of two wheat CIPK genes TaCIPK14andTaCIPK29in response to abiotic stresses were further inverstigated. The main results areas follows:
1) Wheat CBLs and CIPKs were found to be similar to their counterparts in rice in motifstructure and subgroup classifcation. These CBL proteins have four EF-hands andFPSF domains, while CIPK proteins contain kinase domain, FISL domain and PPIdomain.
2) The isolated wheat CBL and CIPK genes were found to be expressed differentially invarious tissues and in response to different abiotic stresses including cold, salt, andosmotic stresses and exposure to the phytohormone abscisic acid (ABA). Furthermore,we also found that one CBL or CIPK gene was able to respond to several treatments,and one treatment was sensed by multiple CBL or CIPK genes. Thus, TaCBLs andTaCIPKs were found to mediate crosstalk among different signaling pathways.
3) The preferential interactions of TaCBLs and TaCIPKs were identified using a yeast two-hybrid assay. Several important, specific CBL-CIPK interaction partners(TaCBL1-TaCIPK9, TaCBL1-TaCIPK23, TaCBL2-TaCIPK2, and TaCBL3-TaCIPK2,TaCBL2/TaCBL3-TaCIPK29) were found to be responsive to distinct abiotic stresses.These results suggest that wheat CBL and CIPK genes may collectively mediatecrosstalk of multiple stress signaling pathways through the formation of differentCBL-CIPK complexes to decode stress-specific Ca~(2+)signaling.
4) The roles of the TaCIPK14and TaCIPK29gene in response to various abiotic stresseswere further investigated. TaCIPK14gene was upregulated under cold or when treatedwith salt, PEG or exogenous stresses related signaling molecules including ABA,ethylene and H2O2.Subcellular localization assay revealed the presence of TaCIPK14throughout the cell. Phenotype analysis showed that overexpression of TaCIPK14intobacco enhanced cold and salt stress tolerance. Overexpression of TaCIPK14enhanced cold and salt stress tolerance by regulating the expression of antioxidantgenes or stress related genes such as NtCAT, NtDREB3, NtLEA5, etc and enhancingthe antioxidant system to reduce ROS accumulation and relieve membrane damage.Moreover, enhanced salt stress tolerance in TaCIPK14overexpressing plants was alsoattributed to decreased Na+content and elevated K+/Na+ratio.
5) TaCIPK29transcript was induced by NaCl, cold, methyl viologen (MV), ABA andethylene treatments. Overexpression of TaCIPK29in tobacco resulted in increased salttolerance. Further investigation showed that transgenic tobacco seedlings retained highK+/Na+ratio and Ca~(2+)content by up-regulating some transporter genes such as NtSOS1,NtNHX2, NtNHX4and NtCAX3and reduced H2O2accumulation and membranedamage through enhancing the activities and expression of CAT and POD under saltstress. Finally, TaCIPK29was localized throughout cells and it interacted withTaCBL2, TaCBL3, NtCBL2, NtCBL3and NtCAT1. Taken together, our resultsshowed that TaCIPK29functions as a positive factor under salt stress, involved in theregulation of ion and ROS homeostasis.
In conclusion, wheat CBL and CIPK genes were found to be abiotic stress responsivegenes as those in rice and Arabidopsis. Different CBL or CIPK genes may differentiallycontribute to the plants’ tolerance to distinct stresses. TaCIPK14and TaCIPK29gene maybe useful candidate genes for developing stress-tolerant crops including wheat. Our work may facilitate further functional studies of these two important gene families and isbeneficial for further molecular breeding in wheat.
引文
[1] Hepler PK. Calcium: a central regulator of plant growth and development. PlantCell.2005,17:2142-2155.
[2] Williamson RE, Ashley CC. Free Ca2+and cytoplasmic streaming in the alga Chara.Nature.1982,296(5858):647-50.
[3] Sanders D, Brownlee C, Harper JF. Communicating with calcium Plant Cell.1999,11(4):691-706.
[4] Kudla J, Batistic O, Hashimoto K. Calcium Signals: The Lead Currency of PlantInformation Processing. Plant Cell.2010,22,541-563.
[5] Dodd AN, Kudla J, Sanders D. The language of calcium signaling. Annu. Rev.Plant Biol.2010,61,593-620.
[6] Luan S. The CBL-CIPK network in plant calcium signaling. Trends Plant Sci.2009,14,37-42.
[7] Webb AAR, McAinsh MR, Taylor JE, et al. Calcium ions as intracellular secondmessengers in higher plants. Adv. Bot. Res.1996,22:45-96.
[8] Allen GJ, Chu SP, Schμmacher K, et al. Alteration of stimulus-specifc guard cellcalcium oscillations and stomatal closing in Arabidopsis det3mutant. Science.2000,289,2338-2342.
[9] Boudsocq M, Sheen J. CDPKs in immune and stress signaling. Trends Plant Sci.2013,18(1):30-40.
[10] Hashimoto K, Kudla J. Calcium decoding mechanisms in plants. Biochimie.2011,93(12):2054-9.
[11] Luan S, Kudla J, Rodriguez-Concepcion, M, et al. Calmodulins and calcineurinB-like proteins: calcium sensors for specifc signal response coupling in plants.Plant Cell.2002,14, S389-S400.
[12] McCormack E, Braam J. Calmodulins and related potential calcium sensors ofArabidopsis. New Phytol.2003,159,585-598.
[13] Chinpongpanich A, Limruengroj K, Phean-O-Pas S, et al. Expression analysis ofcalmodulin and calmodulin-like genes from rice, Oryza sativa L. BMC Res Notes.2012,5:625.
[14] Popescu SC, Popescu GV, Bachan S, et al. Differential binding ofcalmodulin-related proteins to their targets revealed through high-densityArabidopsis protein microarrays. PNAS.2007,104(11):4730-5.
[15] Reddy AS, Ben-Hur A, Day IS. Experimental and computational approaches forthe study of calmodulin interactions. Phytochemistry.2011,72(10):1007-19.
[16] Kushwaha R, Singh A, Chattopadhyay S. Calmodulin7plays an important role astranscriptional regulator in Arabidopsis seedling development. Plant Cell.2008,20(7):1747-59.
[17] Perochon A, Aldon D, Galaud JP, et al. Calmodulin and calmodulin-like proteins inplant calciμm signaling. Biochimie.2011,93(12):2048-53.
[18] Oh MH, Kim HS, Wu X, et al. Calcium/calmodulin inhibition of the ArabidopsisBRASSINOSTEROID-INSENSITIVE1receptor kinase provides a possible linkbetween calcium and brassinosteroid signalling. Biochem J.2012,443(2):515-23.
[19] Magnan F, Ranty B, Charpenteau M, et al. Mutations in AtCML9, acalmodulin-like protein from Arabidopsis thaliana, alter plant responses to abioticstress and abscisic acid. Plant J.2008,56(4):575-89.
[20] Leba LJ, Cheval C, Ortiz-Martín I, et al. CML9, an Arabidopsis calmodulin-likeprotein, contributes to plant innate immunity through a flagellin-dependentsignalling pathway. Plant J.2012,71(6):976-89.
[21] Delk NA, Johnson KA, Chowdhury NI, et al. CML24, regulated in expression bydiverse stimuli, encodes a potential Ca2+sensor that functions in responses toabscisic acid, daylength, and ion stress. Plant Physiol.2005,139(1):240-53.
[22] Tsai YC, Koo Y, Delk NA, et al. Calmodulin-related CML24interacts with ATG4band affects autophagy progression in Arabidopsis. Plant J.2012. doi:10.1111/tpj.12043.
[23] Hrabak EM, Chan CW, Gribskov M, et al. The Arabidopsis CDPK-SnRKsuperfamily of protein kinases. Plant Physiol.2003,132(2):666-80.
[24] Asano T, Tanaka N, Yang G, et al. Genome-wide identification of the ricecalcium-dependent protein kinase and its closely related kinase gene families:comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol.2005,46(2):356-66.
[25] Ma P, Liu J, Yang X, et al. Genome-Wide Identification of the MaizeCalcium-Dependent Protein Kinase Gene Family. Appl Biochem Biotechnol.2013.
[26]薛彬，夏新莉，尹伟伦.杨树钙依赖蛋白激酶基因家族生物信息学分析.经济林研究[J].2010,28(1):20-27.
[27] Li AL, Zhu YF, Tan XM, et al. Evolutionary and functional study of the CDPKgene family in wheat (Triticum aestivum L.). Plant Mol Biol.2008a,66(4):429-43.
[28] Li A, Wang X, Leseberg CH, et al. Biotic and abiotic stress responses throughcalcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivumL.). Plant Signal Behav.2008b,3(9):654-6.
[29] Cheng SH, Willmann MR, Chen HC, et al. Calcium signaling through proteinkinases. The Arabidopsis calcium-dependent protein kinase gene family. PlantPhysiol.2002,129(2):469-85.
[30] Harper JF, Breton G, Harmon A. Decoding Ca2+signals through plant proteinkinases. Annu. Rev. Plant Biol.2004,55:263-288.
[31] Ludwig AA, Romeis T, Jones JD. CDPK-mediated signalling pathways: specificityand cross-talk. J Exp Bot.2004,55(395):181-8.
[32] Boudsocq M, Droillard MJ, Regad L, et al. Characterization of Arabidopsiscalcium-dependent protein kinases: activated or not by calcium?. Biochem J.2012,15;447(2):291-9.
[33] Mori IC, Murata Y, Yang Y, et al. CDPKs CPK6and CPK3function in ABAregulation of guard cell S-type anion-and Ca2+-permeable channels and stomatalclosure. PLoS Biol.2006,4(10):e327.
[34] Geiger D, Scherzer S, Mumm P, et al. Guard cell anion channel SLAC1isregulated by CDPK protein kinases with distinct Ca2+affinities. PNAS.2010,107(17):8023-8.
[35] Geiger D, Maierhofer T, Al-Rasheid KA,et al. Stomatal closure by fast abscisicacid signaling is mediated by the guard cell anion channel SLAH3and the receptorRCAR1. Sci Signal.2011,4(173):ra32.
[36] Kobayashi M, Ohura I, Kawakita K, et al. Calcium-dependent protein kinasesregulate the production of reactive oxygen species by potato NADPH oxidase.Plant Cell.2007,19(3):1065-80.
[37] Asano T, Hayashi N, Kobayashi M, et al. A rice calcium-dependent protein kinaseOsCPK12oppositely modulates salt-stress tolerance and blast disease resistance.Plant J.2012,69(1):26-36.
[38] Ding Y, Cao J, Ni L, et al. ZmCPK11is involved in abscisic acid-inducedantioxidant defence and functions upstream of ZmMPK5in abscisic acid signallingin maize. J Exp Bot.2013,64(4):871-84.
[39] Choi HI, Park HJ, Park JH, et al. Arabidopsis calcium-dependent protein kinaseAtCPK32interacts with ABF4, a transcriptional regulator of abscisicacid-responsive gene expression, and modulates its activity. Plant Physiol.2005,139(4):1750-61.
[40] Zhu SY, Yu XC, Wang XJ, et al. Two calcium-dependent protein kinases, CPK4and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell.2007,19(10):3019-36.
[41] Kim H, Hwang H, Hong JW, et al. A rice orthologue of the ABA receptor,OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway inseed germination and early seedling growth. J Exp Bot.2012,63(2):1013-24.
[42] Ishida S, Yuasa T, Nakata M, et al. A tobacco calcium-dependent protein kinase,CDPK1, regulates the transcription factor REPRESSION OF SHOOT GROWTHin response to gibberellins. Plant Cell.2008,20(12):3273-88.
[43] Ho SL, Huang LF, Lu CA, et al. Sugar starvation-and GA-induciblecalcium-dependent protein kinase1feedback regulates GA biosynthesis andactivates a14-3-3protein to confer drought tolerance in rice seedlings. Plant Mol.Biol.2013,81(4-5):347-61.
[44] Matschi S, Werner S, Schulze WX, et al. Function of calcium-dependent proteinkinase CPK28of Arabidopsis thaliana in plant stem elongation and vasculardevelopment. Plant J.2012. doi:10.1111/tpj.12090.
[45] Liu J, Zhu JK. A calcium sensor homolog required for plant salt tolerance. Science.1998,280(5371):1943-5.
[46] Kudla J, Xu Q, Harter K, et al. Genes for calcineurin B-like proteins in Arabidopsisare differentially regulated by stress signals. PNAS.1999,96(8):4718-23.
[47] Batistic O, Kudla, J. Integration and channeling of calcium signaling through theCBL calcium sensor/CIPK protein kinase network. Planta.2004,219,915-924.
[48] Reddy VS, Reddy AS. Proteomics of calcium-signaling components in plants.Phytochemistry.2004,65(12):1745-76.
[49] Kolukisaoglu U, Weinl S, Blazevic D, et al. Calcium sensors and their interactingprotein kinases: genomics of the Arabidopsis and rice CBL-CIPK signalingnetworks. Plant Physiol.2004,134,43-58.
[50] Batistic O, Kudla J. Plant calcineurin B-like proteins and their interacting proteinkinases. Biochim. Biophys. Acta.2009,1793,985-992.
[51] Weinl S, Kudla J. The CBL-CIPK Ca2+-decoding signaling network: function andperspectives. New Phytol.2009,84,517-528.
[52] Xiang Y, Huang YM, Xiong LZ. Characterization of Stress-Responsive CIPKGenes in Rice for Stress Tolerance Improvement. Plant Physiol.2007,144,1416-1428.
[53] Gu ZM, Ma BJ, Jiang Y, et al. Expression analysis of the calcineurin B-like genefamily in rice (Oryza sativa L.) under environmental stresses. Gene.2008,415,1-12.
[54] Li LB, Zhang YR, Liu KC, et al. Identification and Bioinformatics Analysis ofSnRK2and CIPK Family Genes in Sorghum. Agri. Sci. China.2010,9,19-30.
[55] Zhang CX, Bian MD, Yu H, et al. Identifcation of alkaline stress-responsive genesof CBL family in sweet sorghum (Sorghum bicolor L.). Plant Physiol. Biochem.2011,49,1306-1312.
[56] Yu Y, Xia X, Yin W, et al. Comparative genomic analysis of CIPK gene family inArabidopsis and Populus. Plant Growth Regul.2007,52,101-110.
[57] Zhang HC, Yin WL, Xia XL. Calcineurin B-Like family in Populus: comparativegenome analysis and expression pattern under cold, drought and salt stresstreatment. Plant Growth Regul.2008,56,129-140.
[58] Pandey GK. Emergence of a novel calcium signaling pathway in plants:CBL-CIPK signaling network. Physiol. Mol. Biol. Plants.2008,14(1&2):51-68.
[59] Nagae M, Nozawa A, Koizumi N, et al. The crystal structure of the novelcalcium-binding protein AtCBL2from Arabidopsis thaliana. J Biol Chem.2003,278(43):42240-6.
[60] Lewit-Bentley A, Rety S. EF-hand calcium-binding proteins. Curr. Opin. Struct.Biol.2000,10,637-643.
[61] Batistic O, Kim Kyung-Nam, Kleist Thomas, et al. The CBL–CIPK Network forDecoding Calcium Signals in Plants. S. Luan (ed.), Coding and Decoding ofCalcium Signals in Plants, Signaling and Communication in Plants.2010b,10. doi10.1007/978-3-642-20829-4_12.
[62] Sanchez-Barrena MJ, Martinez-Ripoll M, Zhu JK, et al. The structure of theArabidopsis thaliana SOS3: molecular mechanism of sensing calcium for saltstress response. J Mol Biol.2005,345:1253-1264
[63] Batisti O, Rehers M, Akerman A, et al. S-acylation-dependent association of thecalcium sensor CBL2with the vacuolar membrane is essential for proper abscisicacid responses. Cell Res.2012,22(7):1155-68.
[64] Du WM, Lin HX, Chen S, et al. Phosphorylation of SOS3-Like Calcium-BindingProteins by Their Interacting SOS2-Like Protein Kinases Is a Common RegulatoryMechanism in Arabidopsis. Plant Physiol.2011,156,2235-2243.
[65] Hashimoto KJ, Eckert C, Anschutz U, et al. Phosphorylation of Calcineurin B-like(CBL) Calcium Sensor Proteins by Their CBL-interacting Protein Kinases (CIPKs)Is Required for Full Activity of CBL-CIPK Complexes toward Their TargetProteins. J. Biol. Chem.2012,287,7956-7968.
[66] Albrecht V, Ritz O, Linder S, et al. The NAF domain defnes a novelprotein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J.2001,20,1051-1063.
[67] Lee SC, Lan WZ, Kim BG, et al. A protein phosphorylation/dephosphorylationnetwork regulates a plant potassium channel. PNAS.2007,104,15959-15964.
[68] Guo Y, Halfter U, Ishitani M, et al. Molecular characterization of functionaldomains in the protein kinase SOS2that is required for plant salt tolerance. PlantCell.2001,13,1383-1400.
[69] Gong D, Guo Y, Jagendorf AT, et al. Biochemical characterization of theArabidopsis protein kinase SOS2that functions in salt tolerance. Plant Physiol.2002,130:256-264.
[70] Sanchez-Barrena MJ, Fujii H, Angulo I, et al. The structure of the C-terminaldomain of the protein kinase AtSOS2bound to the calcium sensor AtSOS3. Mol.Cell.2007,26,427-435.
[71] Batistic O, Waadt R, Steinhorst L, et al. CBL-mediated targeting of CIPKsfacilitates the decoding of calcium signals emanating from distinct cellular stores.Plant J.2010a,61(2):211-22.
[72] Kim BG, Waadt R, Cheong YH, et al. The calcium sensor CBL10mediates salttolerance by regulating ion homeostasis in Arabidopsis. Plant J.2007,52,473-484.
[73] Liu LL, Ren HM, Chen LQ, et al. A protein kinase, calcineurin B-likeprotein-interacting protein Kinase9, interacts with calcium sensor calcineurinB-like Protein3and regulates potassium homeostasis under low-potassium stress inArabidopsis. Plant Physiol.2013,161(1):266-77.
[74] Hwang YS, Bethke PC, Cheong YH, et al. A gibberellin-regulated calcineurin B inrice localizes to the tonoplast and is implicated in vacuole function. Plant Physiol.2005,138,1347-1358.
[75] Drerup MM, Schlücking K, Hashimoto K, et al. The calcineurin B-like calciumsensors CBL1and CBL9together with their interacting protein kinase CIPK26regulate the Arabidopsis NADPH oxidase RBOHF. Mol. Plant.2013,18.
[76] Waadt R, Schmidt LK, Lohse M, et al. Multicolor bimolecular fluorescencecomplementation reveals simultaneous formation of alternative CBL/CIPKcomplexes in planta. Plant J.2008,56(3):505-16.
[77] Xu J, Li HD, Chen LQ, et al. A Protein Kinase, Interacting with Two CalcineurinB-like Proteins, Regulates K+Transporter AKT1in Arabidopsis. Cell.2006,125,1347-1360.
[78] Zhao J, Sun Z, Zheng J, et al. Cloning and characterization of a novelCBL-interacting protein kinase from maize. Plant Mol. Biol.2009,69,661-674.
[79] Cheong YH, Pandey GK, Grant JJ, et al. Two calcineurin B-like calcium sensors,interacting with protein kinase CIPK23, regulate leaf transpiration and rootpotassium uptake in Arabidopsis. Plant J.2007,52,223-239.
[80] Martinez-Atienza J, Jiang XY, Garciadeblas B, et al. Conservation of the saltoverly sensitive pathway in rice. Plant physiol.2007,143,1001-1012.
[81] Kurusu T, Hamada J, Nokajima H, et al. Regulation of microbe-associatedmolecular pattern-induced hypersensitive cell death, phytoalexin production, anddefense gene expression by calcineurin B-like protein-interacting protein kinases,OsCIPK14/15, in rice cultured cells. Plant Physiol.2010,153(2):678-92.
[82] Yoona S, Parka J, Ryua M, et al. Calcineurin B-like proteins in rice can bind withcalcium ion and associate with the Arabidopsis CIPK family members. Plant Sci.2009,177(6):577-583
[83] Tripathi V, Parasuraman B, Laxmi A, et al. CIPK6, a CBL-interacting proteinkinase is required for development and salt tolerance in plants. Plant J.2009,58(5):778-90.
[84] Wang RK, Li LL, Cao ZH, et al. Molecular cloning and functional characterizationof a novel apple MdCIPK6L gene reveals its involvement in multiple abiotic stresstolerance in transgenic plants. Plant Mol. Biol.2012,79:123-135.
[85] Chen L, Ren F, Zhou L, et al. The Brassica napus calcineurin B-Like1/CBL-interacting protein kinase6(CBL1/CIPK6) component is involved in theplant response to abiotic stress and ABA signalling. J Exp. Bot.2012,63(17):6211-22.
[86] Lan WZ, Lee SC, Che YF, et al. Mechanistic analysis of AKT1regulation by theCBL-CIPK-PP2CA interactions. Mol. Plant.2011,4(3):527-36.
[87] Ren XL, Qi GN, Feng HQ, et al. Calcineurin B-like protein CBL10directlyinteracts with AKT1and modulates K+homeostasis in Arabidopsis. Plant J.2013,20.
[88] Oh SI, Park J, Yoon S, et al. The Arabidopsis calcium sensor calcineurin B-like3inhibits the5'-methylthioadenosine nucleosidase in a calcium-dependent manner.Plant Physiol.2008,148(4):1883-96.
[89] Albrecht V, Weinl S, Blazevic D, et al. The calcium sensor CBL1integrates plantresponses to abiotic stresses. Plant J.2003,36,457-470.
[90] Quan R, Lin H, Mendoza I, et al. SCABP8/CBL10, a putative calcium sensor,interacts with the protein kinase SOS2to protect Arabidopsis shoots from saltstress. Plant Cell.2007,19,1415-1431.
[91] Li RF, Zhang JW, Wu GY, et al. HbCIPK2, a novel CBL-interacting protein kinasefrom halophyte Hordeum brevisubulatum, confers salt and osmotic stress tolerance.Plant Cell Environ.2012,35(9):1582-1600.
[92] Halfter U, Ishitani M, Zhu JK. The Arabidopsis SOS2protein kinase physicallyinteracts with and is activated by the calcium-binding protein SOS3. PNAS.2000,97,735-740.
[93] Zhu JK. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol.2002,53,247-273.
[94] Zhu JK. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol.2003,6,441-445.
[95] Tang RJ, Liu H, Bao Y, et al. The woody plant poplar has a functionally conservedsalt overly sensitive pathway in response to salinity stress. Plant Mol. Biol.2010,74,367-380.
[96] Huertas R, Olías R, Eljakaoui Z, et al. Overexpression of SlSOS2(SlCIPK24)confers salt tolerance to transgenic tomato. Plant Cell Environ.2012,35:1467-1482.
[97] Roy SJ, Huang W, Wang XJ, et al. A novel protein kinase involved in Na+exclusion revealed from positional cloning. Plant Cell Environ.2013,36(3):553-68.
[98] Held K, Pascaud F, Eckert C, et al. Calcium-dependent modulation and plasmamembrane targeting of the AKT2potassium channel by the CBL4/CIPK6calciumsensor/protein kinase complex. Cell Res.2011,21(7):1116-30.
[99] Pandey GK,Cheong YH, Kim BG.,et al. CIPK9: a calcium sensor-interactingprotein kinase required for low-potassium tolerance in Arabidopsis. Cell Res.2007,17:411-421
[100] Cheong YH, Sung SJ, Kim BG, et al. Constitutive overexpression of the calciumsensor CBL5confers osmotic or drought stress tolerance in Arabidopsis. Mol.Cells.2010,29(2):159-65.
[101] Kim KN, Cheong YH, Grant JJ, et al. CIPK3, a calcium sensor-associated proteinkinase that regulates abscisic acid and cold signal transduction in Arabidopsis.Plant Cell.2003,15(2):411-23.
[102] Huang C, Ding S, Zhang H, et al. CIPK7is involved in cold response byinteracting with CBL1in Arabidopsis thaliana. Plant Sci.2011a,181:57-64
[103] Yang W, Kong Z, Omo-Ikerodah E, et al. Calcineurin B-like interacting proteinkinase OsCIPK23functions in pollination and drought stress responses in rice(Oryza sativa L.). J Genet. Genomics.2008,35(9):531-43, S1-2.
[104] Ho CH, Lin SH, Hu HC, et al. CHL1functions as a nitrate sensor in plants. Cell.2009,138(6):1184-94.
[105] Ho CH, Tsay YF. Nitrate, ammonium, and potassium sensing and signaling. Curr.Opin. Plant Biol.2010,13(5):604-10.
[106] Park SY, Fung P, Nishimura N, et al. Abscisic acid inhibits type2C proteinphosphatases via the PYR/PYL family of START proteins. Science.2009,324(5930):1068-71.
[107] Umezawa T, Nakashima K, Miyakawa T, et al. Molecular basis of the coreregulatory network in ABA responses: sensing, signaling and transport. Plant CellPhysiol.2010,51(11):1821-39.
[108] Soon FF, Ng LM, Zhou XE, et al. Molecular mimicry regulates ABA signaling bySnRK2kinases and PP2C phosphatases. Science.2012,335(6064):85-8.
[109] Pandey GK, Cheong YH, Kim KN, et al. The calcium sensor calcineurin B-like9modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell.2004,16,1912-1924.
[110] Pandey GK, Grant JJ, Cheong YH, et al. Calcineurin-B-like protein CBL9interactswith target kinase CIPK3in the regulation of ABA response in seed germination.Mol. Plant.2008,1,238-248.
[111] Guo Y, Xiong L, Song CP, et al. A calcium sensor and its interacting protein kinaseare global regulators of abscisic acid signaling in Arabidopsis. Dev. Cell.2002,3(2):233-44.
[112] Qin Y, Li X, Guo M, et al. Regulation of salt and ABA responses by CIPK14, acalcium sensor interacting protein kinase in Arabidopsis. Sci. China C. Life Sci.2008,51:391-401
[113] Zhu J, Fu X, Koo YD, et al. An enhancer mutant of Arabidopsis salt overlysensitive3mediates both ion homeostasis and the oxidative stress response. Mol.Cell Biol.2007,27(14):5214-24.
[114] Katiyar-Agarwal S, Zhu J, Kim K, et al. The plasma membrane Na+/H+antiporterSOS1interacts with RCD1and functions in oxidative stress tolerance inArabidopsis. PNAS.2006,103(49):18816-21.
[115] Kimura S, Kawarazaki T, Nibori H, et al. The CBL-interacting protein kinaseCIPK26is a novel interactor of Arabidopsis NADPH oxidase AtRbohF thatnegatively modulates its ROS-producing activity in a heterologous expressionsystem. J Bio chem.2013,153(2):191-5.
[116] Li ZY, Xu ZS, Chen Y, et al. A Novel Role for Arabidopsis CBL1in AffectingPlant Responses to Glucose and Gibberellin during Germination and SeedlingDevelopment. PLoS One.2013,8(2):e56412.
[117] Fuglsang AT, Guo Y, Cuin TA, et al. Arabidopsis protein kinase PKS5inhibits theplasma membrane H+-ATPase by preventing interaction with14-3-3protein. PlantCell.2007,19(5):1617-34.
[118] Liu LL, Ren HM, Chen LQ, et al. A protein kinase, calcineurin B-likeprotein-interacting protein Kinase9, interacts with calcium sensor calcineurinB-like Protein3and regulates potassium homeostasis under low-potassium stress inArabidopsis. Plant Physiol.2013,161(1):266-77.
[119] Tang RJ, Liu H, Yang Y, et al. Tonoplast calcium sensors CBL2and CBL3controlplant growth and ion homeostasis through regulating V-ATPase activity inArabidopsis. Cell Res.2012,22(12):1650-65.
[120] Lee KW, Chen PW, Lu CA, et al. Coordinated responses to oxygen and sugardeficiency allow rice seedlings to tolerate flooding. Sci. Signal.2009,2(91):ra61.
[121] Livaka KJ, Schmittgen TD. Analysis of relative gene expression data usingreal-time quantitative PCR and the2(-Delta Delta C(T)) Method. Methods.2001,25,402-408.
[122] Sano H, Youssefian S. Light and nutritional regulation of transcripts encoding awheat protein kinase homolog is mediated by cytokinins. PNAS.1994,91,2582-2586.
[123] Ikeda Y, Koizumi N, Kusano T, et al. Sucrose and Cytokinin Modulation of WPK4,a Gene Encoding a SNF1-Related Protein Kinase from Wheat. Plant Physiol.1999,121,813-820.
[124] Ohta M, Guo Y, Halfter U, et al. A novel domain in the protein kinase SOS2mediates interaction with the protein phosphatase2C ABI2. PNAS.2003,100:11771-11776
[125] Kim KN, Cheong YH, Gupta R, et al. Interaction specificity of Arabidopsiscalcineurin B-like calcium sensors and their target kinases. Plant Physiol.2000,124(4):1844-53.
[126] Gong DM, Guo Y, Schumaker KS, et al. The SOS3Family of Calcium Sensors andSOS2Family of Protein Kinases in Arabidopsis. Plant Physiol.2004,134,919-926.
[127] Piao HL, Xuan YH, Park SY, et al. OsCIPK31, a CBL interacting protein kinase isinvolved in germination and seedling growth under abiotic stress conditions in riceplants. Mol. Cell.2010,30,19-27.
[128] Brenchley R, Spannagl M, Pfeifer M, et al. Analysis of the bread wheat genomeusing whole-genome shotgun sequencing. Nature.2012,491(7426):705-10.
[129] Heath RL, Packer L. Photoperoxidation in isolated chloroplasts. I. Kinetics andstoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys.1968,25:189-198.
[130]张蜀秋，李云，武维华.植物生理学实验技术教程.科学出版社[M].2011.
[131] Jiang M, Zhang J. Effect of abscisic acid on active oxygen species, antioxidativedefence system and oxidative damage in leaves of maize seedlings.Plant CellPhysiol.2001,42:1265-1273.
[132] Kong X, Pan J, Zhang M, et al. ZmMKK4, a novel group C mitogen-activatedprotein kinase kinase in maize (Zea mays), confers salt and cold tolerance intransgenic Arabidopsis. Plant Cell Environ.2011,34:1291-1303
[133] Yang Q, Chen ZZ, Zhou XF, et al. Overexpression of SOS (Salt Overly Sensitive)Genes Increases Salt Tolerance in Transgenic Arabidopsis. Mol. Plant.2009,2:22-31.
[134] Maathuis FJM, Amtmann A. K+nutrition and Na+toxicity: the basis of cellular K+/Na+ratios. Ann. Bot.1999,84:123-133.
[135] Sairam RK, Tyagi A. Physiology and molecular biology of salinity stress tolerancein plants. Curr. Sci.2004,86:407-421.
[136] Munns R, Tester M. Mechanisms of Salinity Tolerance. Annu. Rev. Plant Biol.2008,59:651-681.
[137] Shi H, Lee BH, Wu SJ, et al. Overexpression of plasma membraneNa+/H+antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat.Biotechnol.2003,21:81-85.
[138] Mochida K, Kawaura K, Shimosaka E, et al. Tissue expression map of a largenumber of expressed sequence tags and its application to insilico screening ofstress response genes in common wheat. Mol. Genet. Genomics.2006,276:304-312.
[139] Huang XS, Liu JH, Chen XJ. Overexpression of PtrABF gene, a bZIP transcriptionfactor isolated from Poncirus trifoliata, enhances dehydration and droughttolerance in tobacco via scavenging ROS and modulating expression ofstress-responsive genes. BMC Plant Biol.2010,10,230.
[140] Couée I, Sulmon C, Gouesbet G, et al. Involvement of soluble sugars in reactiveoxygen species balance and responses to oxidative stress in plants. J Exp. Bot.2006,57:449-459.
[141] Zhu JK. Plant salt tolerance. Trends Plant Sci.2001,6:66-71.
[142] Sorrells ME, La Rota M, Bermudez-Kandianis CE, et al. Comparative DNASequence Analysis of Wheat and Rice Genomes. Genome Res.2003,13:1818-1827.
[143] Nelson BK, Cai X, Nebenführ A. A multicolored set of in vivo organelle markersfor co-localization studies in Arabidopsis and other plants. Plant J.2007,51:1126-1136.
[144] Shi H, Ishitani M, Kim C, et al. The Arabidopsis thaliana salt tolerance gene SOS1encodes a putative Na+/H+antiporter. PNAS.2000,97(12):6896-901.
[145] Rodríguez-Rosales MP, Jiang X, Gálvez FJ, et al. Overexpression of the tomatoK+/H+antiporter LeNHX2confers salt tolerance by improving potassiumcompartmentalization. New Phytol.2008,179,366-377.
[146] Rodríguez-Rosales MP, Gálvez FJ, Huertas R, et al. Plant NHX cation/protonantiporters. Plant Signal. Behav.2009,4,1-13.
[147] Cheng NH, Pittman JK, Shigaki T, et al. Functional Association of ArabidopsisCAX1and CAX3Is Required for Normal Growth and Ion Homeostasis. PlantPhysiol.2005,138:2048-2060.
[148] Zhao J, Barkla BJ, Marshall J, et al. The Arabidopsis cax3mutants display alteredsalt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity.Planta.2008,227:659-669.
[149] Gouiaa S, Khoudi H, Leidi EO, et al. Expression of wheat Na+/H+antiporterTNHXS1and H+-pyrophosphatase TVP1genes in tobacco from a bicistronictranscriptional unit improves salt tolerance. Plant Mol. Biol.2012,79:137-155
[150] Verslues PE, Batelli G, Grillo S, et al. Interaction of SOS2with nucleosidediphosphate kinase2and catalases reveals a point of connection between salt stressand H2O2signaling in Arabidopsis thaliana. Mol. Cell Biol.2007,27:7771-7780
[151] D'Angelo C, Weinl S, Batistic O, et al. Alternative complex formation of theCa-regulated protein kinase CIPK1controls abscisic acid-dependent andindependent stress responses in Arabidopsis. Plant J.2006,48(6):857-72.
[2] Williamson RE, Ashley CC. Free Ca2+and cytoplasmic streaming in the alga Chara.Nature.1982,296(5858):647-50.
[3] Sanders D, Brownlee C, Harper JF. Communicating with calcium Plant Cell.1999,11(4):691-706.
[4] Kudla J, Batistic O, Hashimoto K. Calcium Signals: The Lead Currency of PlantInformation Processing. Plant Cell.2010,22,541-563.
[5] Dodd AN, Kudla J, Sanders D. The language of calcium signaling. Annu. Rev.Plant Biol.2010,61,593-620.
[6] Luan S. The CBL-CIPK network in plant calcium signaling. Trends Plant Sci.2009,14,37-42.
[7] Webb AAR, McAinsh MR, Taylor JE, et al. Calcium ions as intracellular secondmessengers in higher plants. Adv. Bot. Res.1996,22:45-96.
[8] Allen GJ, Chu SP, Schμmacher K, et al. Alteration of stimulus-specifc guard cellcalcium oscillations and stomatal closing in Arabidopsis det3mutant. Science.2000,289,2338-2342.
[9] Boudsocq M, Sheen J. CDPKs in immune and stress signaling. Trends Plant Sci.2013,18(1):30-40.
[10] Hashimoto K, Kudla J. Calcium decoding mechanisms in plants. Biochimie.2011,93(12):2054-9.
[11] Luan S, Kudla J, Rodriguez-Concepcion, M, et al. Calmodulins and calcineurinB-like proteins: calcium sensors for specifc signal response coupling in plants.Plant Cell.2002,14, S389-S400.
[12] McCormack E, Braam J. Calmodulins and related potential calcium sensors ofArabidopsis. New Phytol.2003,159,585-598.
[13] Chinpongpanich A, Limruengroj K, Phean-O-Pas S, et al. Expression analysis ofcalmodulin and calmodulin-like genes from rice, Oryza sativa L. BMC Res Notes.2012,5:625.
[14] Popescu SC, Popescu GV, Bachan S, et al. Differential binding ofcalmodulin-related proteins to their targets revealed through high-densityArabidopsis protein microarrays. PNAS.2007,104(11):4730-5.
[15] Reddy AS, Ben-Hur A, Day IS. Experimental and computational approaches forthe study of calmodulin interactions. Phytochemistry.2011,72(10):1007-19.
[16] Kushwaha R, Singh A, Chattopadhyay S. Calmodulin7plays an important role astranscriptional regulator in Arabidopsis seedling development. Plant Cell.2008,20(7):1747-59.
[17] Perochon A, Aldon D, Galaud JP, et al. Calmodulin and calmodulin-like proteins inplant calciμm signaling. Biochimie.2011,93(12):2048-53.
[18] Oh MH, Kim HS, Wu X, et al. Calcium/calmodulin inhibition of the ArabidopsisBRASSINOSTEROID-INSENSITIVE1receptor kinase provides a possible linkbetween calcium and brassinosteroid signalling. Biochem J.2012,443(2):515-23.
[19] Magnan F, Ranty B, Charpenteau M, et al. Mutations in AtCML9, acalmodulin-like protein from Arabidopsis thaliana, alter plant responses to abioticstress and abscisic acid. Plant J.2008,56(4):575-89.
[20] Leba LJ, Cheval C, Ortiz-Martín I, et al. CML9, an Arabidopsis calmodulin-likeprotein, contributes to plant innate immunity through a flagellin-dependentsignalling pathway. Plant J.2012,71(6):976-89.
[21] Delk NA, Johnson KA, Chowdhury NI, et al. CML24, regulated in expression bydiverse stimuli, encodes a potential Ca2+sensor that functions in responses toabscisic acid, daylength, and ion stress. Plant Physiol.2005,139(1):240-53.
[22] Tsai YC, Koo Y, Delk NA, et al. Calmodulin-related CML24interacts with ATG4band affects autophagy progression in Arabidopsis. Plant J.2012. doi:10.1111/tpj.12043.
[23] Hrabak EM, Chan CW, Gribskov M, et al. The Arabidopsis CDPK-SnRKsuperfamily of protein kinases. Plant Physiol.2003,132(2):666-80.
[24] Asano T, Tanaka N, Yang G, et al. Genome-wide identification of the ricecalcium-dependent protein kinase and its closely related kinase gene families:comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol.2005,46(2):356-66.
[25] Ma P, Liu J, Yang X, et al. Genome-Wide Identification of the MaizeCalcium-Dependent Protein Kinase Gene Family. Appl Biochem Biotechnol.2013.
[26]薛彬，夏新莉，尹伟伦.杨树钙依赖蛋白激酶基因家族生物信息学分析.经济林研究[J].2010,28(1):20-27.
[27] Li AL, Zhu YF, Tan XM, et al. Evolutionary and functional study of the CDPKgene family in wheat (Triticum aestivum L.). Plant Mol Biol.2008a,66(4):429-43.
[28] Li A, Wang X, Leseberg CH, et al. Biotic and abiotic stress responses throughcalcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivumL.). Plant Signal Behav.2008b,3(9):654-6.
[29] Cheng SH, Willmann MR, Chen HC, et al. Calcium signaling through proteinkinases. The Arabidopsis calcium-dependent protein kinase gene family. PlantPhysiol.2002,129(2):469-85.
[30] Harper JF, Breton G, Harmon A. Decoding Ca2+signals through plant proteinkinases. Annu. Rev. Plant Biol.2004,55:263-288.
[31] Ludwig AA, Romeis T, Jones JD. CDPK-mediated signalling pathways: specificityand cross-talk. J Exp Bot.2004,55(395):181-8.
[32] Boudsocq M, Droillard MJ, Regad L, et al. Characterization of Arabidopsiscalcium-dependent protein kinases: activated or not by calcium?. Biochem J.2012,15;447(2):291-9.
[33] Mori IC, Murata Y, Yang Y, et al. CDPKs CPK6and CPK3function in ABAregulation of guard cell S-type anion-and Ca2+-permeable channels and stomatalclosure. PLoS Biol.2006,4(10):e327.
[34] Geiger D, Scherzer S, Mumm P, et al. Guard cell anion channel SLAC1isregulated by CDPK protein kinases with distinct Ca2+affinities. PNAS.2010,107(17):8023-8.
[35] Geiger D, Maierhofer T, Al-Rasheid KA,et al. Stomatal closure by fast abscisicacid signaling is mediated by the guard cell anion channel SLAH3and the receptorRCAR1. Sci Signal.2011,4(173):ra32.
[36] Kobayashi M, Ohura I, Kawakita K, et al. Calcium-dependent protein kinasesregulate the production of reactive oxygen species by potato NADPH oxidase.Plant Cell.2007,19(3):1065-80.
[37] Asano T, Hayashi N, Kobayashi M, et al. A rice calcium-dependent protein kinaseOsCPK12oppositely modulates salt-stress tolerance and blast disease resistance.Plant J.2012,69(1):26-36.
[38] Ding Y, Cao J, Ni L, et al. ZmCPK11is involved in abscisic acid-inducedantioxidant defence and functions upstream of ZmMPK5in abscisic acid signallingin maize. J Exp Bot.2013,64(4):871-84.
[39] Choi HI, Park HJ, Park JH, et al. Arabidopsis calcium-dependent protein kinaseAtCPK32interacts with ABF4, a transcriptional regulator of abscisicacid-responsive gene expression, and modulates its activity. Plant Physiol.2005,139(4):1750-61.
[40] Zhu SY, Yu XC, Wang XJ, et al. Two calcium-dependent protein kinases, CPK4and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell.2007,19(10):3019-36.
[41] Kim H, Hwang H, Hong JW, et al. A rice orthologue of the ABA receptor,OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway inseed germination and early seedling growth. J Exp Bot.2012,63(2):1013-24.
[42] Ishida S, Yuasa T, Nakata M, et al. A tobacco calcium-dependent protein kinase,CDPK1, regulates the transcription factor REPRESSION OF SHOOT GROWTHin response to gibberellins. Plant Cell.2008,20(12):3273-88.
[43] Ho SL, Huang LF, Lu CA, et al. Sugar starvation-and GA-induciblecalcium-dependent protein kinase1feedback regulates GA biosynthesis andactivates a14-3-3protein to confer drought tolerance in rice seedlings. Plant Mol.Biol.2013,81(4-5):347-61.
[44] Matschi S, Werner S, Schulze WX, et al. Function of calcium-dependent proteinkinase CPK28of Arabidopsis thaliana in plant stem elongation and vasculardevelopment. Plant J.2012. doi:10.1111/tpj.12090.
[45] Liu J, Zhu JK. A calcium sensor homolog required for plant salt tolerance. Science.1998,280(5371):1943-5.
[46] Kudla J, Xu Q, Harter K, et al. Genes for calcineurin B-like proteins in Arabidopsisare differentially regulated by stress signals. PNAS.1999,96(8):4718-23.
[47] Batistic O, Kudla, J. Integration and channeling of calcium signaling through theCBL calcium sensor/CIPK protein kinase network. Planta.2004,219,915-924.
[48] Reddy VS, Reddy AS. Proteomics of calcium-signaling components in plants.Phytochemistry.2004,65(12):1745-76.
[49] Kolukisaoglu U, Weinl S, Blazevic D, et al. Calcium sensors and their interactingprotein kinases: genomics of the Arabidopsis and rice CBL-CIPK signalingnetworks. Plant Physiol.2004,134,43-58.
[50] Batistic O, Kudla J. Plant calcineurin B-like proteins and their interacting proteinkinases. Biochim. Biophys. Acta.2009,1793,985-992.
[51] Weinl S, Kudla J. The CBL-CIPK Ca2+-decoding signaling network: function andperspectives. New Phytol.2009,84,517-528.
[52] Xiang Y, Huang YM, Xiong LZ. Characterization of Stress-Responsive CIPKGenes in Rice for Stress Tolerance Improvement. Plant Physiol.2007,144,1416-1428.
[53] Gu ZM, Ma BJ, Jiang Y, et al. Expression analysis of the calcineurin B-like genefamily in rice (Oryza sativa L.) under environmental stresses. Gene.2008,415,1-12.
[54] Li LB, Zhang YR, Liu KC, et al. Identification and Bioinformatics Analysis ofSnRK2and CIPK Family Genes in Sorghum. Agri. Sci. China.2010,9,19-30.
[55] Zhang CX, Bian MD, Yu H, et al. Identifcation of alkaline stress-responsive genesof CBL family in sweet sorghum (Sorghum bicolor L.). Plant Physiol. Biochem.2011,49,1306-1312.
[56] Yu Y, Xia X, Yin W, et al. Comparative genomic analysis of CIPK gene family inArabidopsis and Populus. Plant Growth Regul.2007,52,101-110.
[57] Zhang HC, Yin WL, Xia XL. Calcineurin B-Like family in Populus: comparativegenome analysis and expression pattern under cold, drought and salt stresstreatment. Plant Growth Regul.2008,56,129-140.
[58] Pandey GK. Emergence of a novel calcium signaling pathway in plants:CBL-CIPK signaling network. Physiol. Mol. Biol. Plants.2008,14(1&2):51-68.
[59] Nagae M, Nozawa A, Koizumi N, et al. The crystal structure of the novelcalcium-binding protein AtCBL2from Arabidopsis thaliana. J Biol Chem.2003,278(43):42240-6.
[60] Lewit-Bentley A, Rety S. EF-hand calcium-binding proteins. Curr. Opin. Struct.Biol.2000,10,637-643.
[61] Batistic O, Kim Kyung-Nam, Kleist Thomas, et al. The CBL–CIPK Network forDecoding Calcium Signals in Plants. S. Luan (ed.), Coding and Decoding ofCalcium Signals in Plants, Signaling and Communication in Plants.2010b,10. doi10.1007/978-3-642-20829-4_12.
[62] Sanchez-Barrena MJ, Martinez-Ripoll M, Zhu JK, et al. The structure of theArabidopsis thaliana SOS3: molecular mechanism of sensing calcium for saltstress response. J Mol Biol.2005,345:1253-1264
[63] Batisti O, Rehers M, Akerman A, et al. S-acylation-dependent association of thecalcium sensor CBL2with the vacuolar membrane is essential for proper abscisicacid responses. Cell Res.2012,22(7):1155-68.
[64] Du WM, Lin HX, Chen S, et al. Phosphorylation of SOS3-Like Calcium-BindingProteins by Their Interacting SOS2-Like Protein Kinases Is a Common RegulatoryMechanism in Arabidopsis. Plant Physiol.2011,156,2235-2243.
[65] Hashimoto KJ, Eckert C, Anschutz U, et al. Phosphorylation of Calcineurin B-like(CBL) Calcium Sensor Proteins by Their CBL-interacting Protein Kinases (CIPKs)Is Required for Full Activity of CBL-CIPK Complexes toward Their TargetProteins. J. Biol. Chem.2012,287,7956-7968.
[66] Albrecht V, Ritz O, Linder S, et al. The NAF domain defnes a novelprotein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J.2001,20,1051-1063.
[67] Lee SC, Lan WZ, Kim BG, et al. A protein phosphorylation/dephosphorylationnetwork regulates a plant potassium channel. PNAS.2007,104,15959-15964.
[68] Guo Y, Halfter U, Ishitani M, et al. Molecular characterization of functionaldomains in the protein kinase SOS2that is required for plant salt tolerance. PlantCell.2001,13,1383-1400.
[69] Gong D, Guo Y, Jagendorf AT, et al. Biochemical characterization of theArabidopsis protein kinase SOS2that functions in salt tolerance. Plant Physiol.2002,130:256-264.
[70] Sanchez-Barrena MJ, Fujii H, Angulo I, et al. The structure of the C-terminaldomain of the protein kinase AtSOS2bound to the calcium sensor AtSOS3. Mol.Cell.2007,26,427-435.
[71] Batistic O, Waadt R, Steinhorst L, et al. CBL-mediated targeting of CIPKsfacilitates the decoding of calcium signals emanating from distinct cellular stores.Plant J.2010a,61(2):211-22.
[72] Kim BG, Waadt R, Cheong YH, et al. The calcium sensor CBL10mediates salttolerance by regulating ion homeostasis in Arabidopsis. Plant J.2007,52,473-484.
[73] Liu LL, Ren HM, Chen LQ, et al. A protein kinase, calcineurin B-likeprotein-interacting protein Kinase9, interacts with calcium sensor calcineurinB-like Protein3and regulates potassium homeostasis under low-potassium stress inArabidopsis. Plant Physiol.2013,161(1):266-77.
[74] Hwang YS, Bethke PC, Cheong YH, et al. A gibberellin-regulated calcineurin B inrice localizes to the tonoplast and is implicated in vacuole function. Plant Physiol.2005,138,1347-1358.
[75] Drerup MM, Schlücking K, Hashimoto K, et al. The calcineurin B-like calciumsensors CBL1and CBL9together with their interacting protein kinase CIPK26regulate the Arabidopsis NADPH oxidase RBOHF. Mol. Plant.2013,18.
[76] Waadt R, Schmidt LK, Lohse M, et al. Multicolor bimolecular fluorescencecomplementation reveals simultaneous formation of alternative CBL/CIPKcomplexes in planta. Plant J.2008,56(3):505-16.
[77] Xu J, Li HD, Chen LQ, et al. A Protein Kinase, Interacting with Two CalcineurinB-like Proteins, Regulates K+Transporter AKT1in Arabidopsis. Cell.2006,125,1347-1360.
[78] Zhao J, Sun Z, Zheng J, et al. Cloning and characterization of a novelCBL-interacting protein kinase from maize. Plant Mol. Biol.2009,69,661-674.
[79] Cheong YH, Pandey GK, Grant JJ, et al. Two calcineurin B-like calcium sensors,interacting with protein kinase CIPK23, regulate leaf transpiration and rootpotassium uptake in Arabidopsis. Plant J.2007,52,223-239.
[80] Martinez-Atienza J, Jiang XY, Garciadeblas B, et al. Conservation of the saltoverly sensitive pathway in rice. Plant physiol.2007,143,1001-1012.
[81] Kurusu T, Hamada J, Nokajima H, et al. Regulation of microbe-associatedmolecular pattern-induced hypersensitive cell death, phytoalexin production, anddefense gene expression by calcineurin B-like protein-interacting protein kinases,OsCIPK14/15, in rice cultured cells. Plant Physiol.2010,153(2):678-92.
[82] Yoona S, Parka J, Ryua M, et al. Calcineurin B-like proteins in rice can bind withcalcium ion and associate with the Arabidopsis CIPK family members. Plant Sci.2009,177(6):577-583
[83] Tripathi V, Parasuraman B, Laxmi A, et al. CIPK6, a CBL-interacting proteinkinase is required for development and salt tolerance in plants. Plant J.2009,58(5):778-90.
[84] Wang RK, Li LL, Cao ZH, et al. Molecular cloning and functional characterizationof a novel apple MdCIPK6L gene reveals its involvement in multiple abiotic stresstolerance in transgenic plants. Plant Mol. Biol.2012,79:123-135.
[85] Chen L, Ren F, Zhou L, et al. The Brassica napus calcineurin B-Like1/CBL-interacting protein kinase6(CBL1/CIPK6) component is involved in theplant response to abiotic stress and ABA signalling. J Exp. Bot.2012,63(17):6211-22.
[86] Lan WZ, Lee SC, Che YF, et al. Mechanistic analysis of AKT1regulation by theCBL-CIPK-PP2CA interactions. Mol. Plant.2011,4(3):527-36.
[87] Ren XL, Qi GN, Feng HQ, et al. Calcineurin B-like protein CBL10directlyinteracts with AKT1and modulates K+homeostasis in Arabidopsis. Plant J.2013,20.
[88] Oh SI, Park J, Yoon S, et al. The Arabidopsis calcium sensor calcineurin B-like3inhibits the5'-methylthioadenosine nucleosidase in a calcium-dependent manner.Plant Physiol.2008,148(4):1883-96.
[89] Albrecht V, Weinl S, Blazevic D, et al. The calcium sensor CBL1integrates plantresponses to abiotic stresses. Plant J.2003,36,457-470.
[90] Quan R, Lin H, Mendoza I, et al. SCABP8/CBL10, a putative calcium sensor,interacts with the protein kinase SOS2to protect Arabidopsis shoots from saltstress. Plant Cell.2007,19,1415-1431.
[91] Li RF, Zhang JW, Wu GY, et al. HbCIPK2, a novel CBL-interacting protein kinasefrom halophyte Hordeum brevisubulatum, confers salt and osmotic stress tolerance.Plant Cell Environ.2012,35(9):1582-1600.
[92] Halfter U, Ishitani M, Zhu JK. The Arabidopsis SOS2protein kinase physicallyinteracts with and is activated by the calcium-binding protein SOS3. PNAS.2000,97,735-740.
[93] Zhu JK. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol.2002,53,247-273.
[94] Zhu JK. Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol.2003,6,441-445.
[95] Tang RJ, Liu H, Bao Y, et al. The woody plant poplar has a functionally conservedsalt overly sensitive pathway in response to salinity stress. Plant Mol. Biol.2010,74,367-380.
[96] Huertas R, Olías R, Eljakaoui Z, et al. Overexpression of SlSOS2(SlCIPK24)confers salt tolerance to transgenic tomato. Plant Cell Environ.2012,35:1467-1482.
[97] Roy SJ, Huang W, Wang XJ, et al. A novel protein kinase involved in Na+exclusion revealed from positional cloning. Plant Cell Environ.2013,36(3):553-68.
[98] Held K, Pascaud F, Eckert C, et al. Calcium-dependent modulation and plasmamembrane targeting of the AKT2potassium channel by the CBL4/CIPK6calciumsensor/protein kinase complex. Cell Res.2011,21(7):1116-30.
[99] Pandey GK,Cheong YH, Kim BG.,et al. CIPK9: a calcium sensor-interactingprotein kinase required for low-potassium tolerance in Arabidopsis. Cell Res.2007,17:411-421
[100] Cheong YH, Sung SJ, Kim BG, et al. Constitutive overexpression of the calciumsensor CBL5confers osmotic or drought stress tolerance in Arabidopsis. Mol.Cells.2010,29(2):159-65.
[101] Kim KN, Cheong YH, Grant JJ, et al. CIPK3, a calcium sensor-associated proteinkinase that regulates abscisic acid and cold signal transduction in Arabidopsis.Plant Cell.2003,15(2):411-23.
[102] Huang C, Ding S, Zhang H, et al. CIPK7is involved in cold response byinteracting with CBL1in Arabidopsis thaliana. Plant Sci.2011a,181:57-64
[103] Yang W, Kong Z, Omo-Ikerodah E, et al. Calcineurin B-like interacting proteinkinase OsCIPK23functions in pollination and drought stress responses in rice(Oryza sativa L.). J Genet. Genomics.2008,35(9):531-43, S1-2.
[104] Ho CH, Lin SH, Hu HC, et al. CHL1functions as a nitrate sensor in plants. Cell.2009,138(6):1184-94.
[105] Ho CH, Tsay YF. Nitrate, ammonium, and potassium sensing and signaling. Curr.Opin. Plant Biol.2010,13(5):604-10.
[106] Park SY, Fung P, Nishimura N, et al. Abscisic acid inhibits type2C proteinphosphatases via the PYR/PYL family of START proteins. Science.2009,324(5930):1068-71.
[107] Umezawa T, Nakashima K, Miyakawa T, et al. Molecular basis of the coreregulatory network in ABA responses: sensing, signaling and transport. Plant CellPhysiol.2010,51(11):1821-39.
[108] Soon FF, Ng LM, Zhou XE, et al. Molecular mimicry regulates ABA signaling bySnRK2kinases and PP2C phosphatases. Science.2012,335(6064):85-8.
[109] Pandey GK, Cheong YH, Kim KN, et al. The calcium sensor calcineurin B-like9modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell.2004,16,1912-1924.
[110] Pandey GK, Grant JJ, Cheong YH, et al. Calcineurin-B-like protein CBL9interactswith target kinase CIPK3in the regulation of ABA response in seed germination.Mol. Plant.2008,1,238-248.
[111] Guo Y, Xiong L, Song CP, et al. A calcium sensor and its interacting protein kinaseare global regulators of abscisic acid signaling in Arabidopsis. Dev. Cell.2002,3(2):233-44.
[112] Qin Y, Li X, Guo M, et al. Regulation of salt and ABA responses by CIPK14, acalcium sensor interacting protein kinase in Arabidopsis. Sci. China C. Life Sci.2008,51:391-401
[113] Zhu J, Fu X, Koo YD, et al. An enhancer mutant of Arabidopsis salt overlysensitive3mediates both ion homeostasis and the oxidative stress response. Mol.Cell Biol.2007,27(14):5214-24.
[114] Katiyar-Agarwal S, Zhu J, Kim K, et al. The plasma membrane Na+/H+antiporterSOS1interacts with RCD1and functions in oxidative stress tolerance inArabidopsis. PNAS.2006,103(49):18816-21.
[115] Kimura S, Kawarazaki T, Nibori H, et al. The CBL-interacting protein kinaseCIPK26is a novel interactor of Arabidopsis NADPH oxidase AtRbohF thatnegatively modulates its ROS-producing activity in a heterologous expressionsystem. J Bio chem.2013,153(2):191-5.
[116] Li ZY, Xu ZS, Chen Y, et al. A Novel Role for Arabidopsis CBL1in AffectingPlant Responses to Glucose and Gibberellin during Germination and SeedlingDevelopment. PLoS One.2013,8(2):e56412.
[117] Fuglsang AT, Guo Y, Cuin TA, et al. Arabidopsis protein kinase PKS5inhibits theplasma membrane H+-ATPase by preventing interaction with14-3-3protein. PlantCell.2007,19(5):1617-34.
[118] Liu LL, Ren HM, Chen LQ, et al. A protein kinase, calcineurin B-likeprotein-interacting protein Kinase9, interacts with calcium sensor calcineurinB-like Protein3and regulates potassium homeostasis under low-potassium stress inArabidopsis. Plant Physiol.2013,161(1):266-77.
[119] Tang RJ, Liu H, Yang Y, et al. Tonoplast calcium sensors CBL2and CBL3controlplant growth and ion homeostasis through regulating V-ATPase activity inArabidopsis. Cell Res.2012,22(12):1650-65.
[120] Lee KW, Chen PW, Lu CA, et al. Coordinated responses to oxygen and sugardeficiency allow rice seedlings to tolerate flooding. Sci. Signal.2009,2(91):ra61.
[121] Livaka KJ, Schmittgen TD. Analysis of relative gene expression data usingreal-time quantitative PCR and the2(-Delta Delta C(T)) Method. Methods.2001,25,402-408.
[122] Sano H, Youssefian S. Light and nutritional regulation of transcripts encoding awheat protein kinase homolog is mediated by cytokinins. PNAS.1994,91,2582-2586.
[123] Ikeda Y, Koizumi N, Kusano T, et al. Sucrose and Cytokinin Modulation of WPK4,a Gene Encoding a SNF1-Related Protein Kinase from Wheat. Plant Physiol.1999,121,813-820.
[124] Ohta M, Guo Y, Halfter U, et al. A novel domain in the protein kinase SOS2mediates interaction with the protein phosphatase2C ABI2. PNAS.2003,100:11771-11776
[125] Kim KN, Cheong YH, Gupta R, et al. Interaction specificity of Arabidopsiscalcineurin B-like calcium sensors and their target kinases. Plant Physiol.2000,124(4):1844-53.
[126] Gong DM, Guo Y, Schumaker KS, et al. The SOS3Family of Calcium Sensors andSOS2Family of Protein Kinases in Arabidopsis. Plant Physiol.2004,134,919-926.
[127] Piao HL, Xuan YH, Park SY, et al. OsCIPK31, a CBL interacting protein kinase isinvolved in germination and seedling growth under abiotic stress conditions in riceplants. Mol. Cell.2010,30,19-27.
[128] Brenchley R, Spannagl M, Pfeifer M, et al. Analysis of the bread wheat genomeusing whole-genome shotgun sequencing. Nature.2012,491(7426):705-10.
[129] Heath RL, Packer L. Photoperoxidation in isolated chloroplasts. I. Kinetics andstoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys.1968,25:189-198.
[130]张蜀秋，李云，武维华.植物生理学实验技术教程.科学出版社[M].2011.
[131] Jiang M, Zhang J. Effect of abscisic acid on active oxygen species, antioxidativedefence system and oxidative damage in leaves of maize seedlings.Plant CellPhysiol.2001,42:1265-1273.
[132] Kong X, Pan J, Zhang M, et al. ZmMKK4, a novel group C mitogen-activatedprotein kinase kinase in maize (Zea mays), confers salt and cold tolerance intransgenic Arabidopsis. Plant Cell Environ.2011,34:1291-1303
[133] Yang Q, Chen ZZ, Zhou XF, et al. Overexpression of SOS (Salt Overly Sensitive)Genes Increases Salt Tolerance in Transgenic Arabidopsis. Mol. Plant.2009,2:22-31.
[134] Maathuis FJM, Amtmann A. K+nutrition and Na+toxicity: the basis of cellular K+/Na+ratios. Ann. Bot.1999,84:123-133.
[135] Sairam RK, Tyagi A. Physiology and molecular biology of salinity stress tolerancein plants. Curr. Sci.2004,86:407-421.
[136] Munns R, Tester M. Mechanisms of Salinity Tolerance. Annu. Rev. Plant Biol.2008,59:651-681.
[137] Shi H, Lee BH, Wu SJ, et al. Overexpression of plasma membraneNa+/H+antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat.Biotechnol.2003,21:81-85.
[138] Mochida K, Kawaura K, Shimosaka E, et al. Tissue expression map of a largenumber of expressed sequence tags and its application to insilico screening ofstress response genes in common wheat. Mol. Genet. Genomics.2006,276:304-312.
[139] Huang XS, Liu JH, Chen XJ. Overexpression of PtrABF gene, a bZIP transcriptionfactor isolated from Poncirus trifoliata, enhances dehydration and droughttolerance in tobacco via scavenging ROS and modulating expression ofstress-responsive genes. BMC Plant Biol.2010,10,230.
[140] Couée I, Sulmon C, Gouesbet G, et al. Involvement of soluble sugars in reactiveoxygen species balance and responses to oxidative stress in plants. J Exp. Bot.2006,57:449-459.
[141] Zhu JK. Plant salt tolerance. Trends Plant Sci.2001,6:66-71.
[142] Sorrells ME, La Rota M, Bermudez-Kandianis CE, et al. Comparative DNASequence Analysis of Wheat and Rice Genomes. Genome Res.2003,13:1818-1827.
[143] Nelson BK, Cai X, Nebenführ A. A multicolored set of in vivo organelle markersfor co-localization studies in Arabidopsis and other plants. Plant J.2007,51:1126-1136.
[144] Shi H, Ishitani M, Kim C, et al. The Arabidopsis thaliana salt tolerance gene SOS1encodes a putative Na+/H+antiporter. PNAS.2000,97(12):6896-901.
[145] Rodríguez-Rosales MP, Jiang X, Gálvez FJ, et al. Overexpression of the tomatoK+/H+antiporter LeNHX2confers salt tolerance by improving potassiumcompartmentalization. New Phytol.2008,179,366-377.
[146] Rodríguez-Rosales MP, Gálvez FJ, Huertas R, et al. Plant NHX cation/protonantiporters. Plant Signal. Behav.2009,4,1-13.
[147] Cheng NH, Pittman JK, Shigaki T, et al. Functional Association of ArabidopsisCAX1and CAX3Is Required for Normal Growth and Ion Homeostasis. PlantPhysiol.2005,138:2048-2060.
[148] Zhao J, Barkla BJ, Marshall J, et al. The Arabidopsis cax3mutants display alteredsalt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity.Planta.2008,227:659-669.
[149] Gouiaa S, Khoudi H, Leidi EO, et al. Expression of wheat Na+/H+antiporterTNHXS1and H+-pyrophosphatase TVP1genes in tobacco from a bicistronictranscriptional unit improves salt tolerance. Plant Mol. Biol.2012,79:137-155
[150] Verslues PE, Batelli G, Grillo S, et al. Interaction of SOS2with nucleosidediphosphate kinase2and catalases reveals a point of connection between salt stressand H2O2signaling in Arabidopsis thaliana. Mol. Cell Biol.2007,27:7771-7780
[151] D'Angelo C, Weinl S, Batistic O, et al. Alternative complex formation of theCa-regulated protein kinase CIPK1controls abscisic acid-dependent andindependent stress responses in Arabidopsis. Plant J.2006,48(6):857-72.