摘要
在非生物胁迫下,许多植物适应环境的重要机制就是积累一些低分子量的相容性物质,如甜菜碱(GB, Glycine betaine)、脯氨酸、可溶性糖等。其中甜菜碱是一种有特殊功效的相容性物质。甜菜碱在提高植物环境逆境(例如盐胁迫或高温胁迫)的抗性方面有重要作用,并且甜菜碱提高植物耐受性的同时伴随着热激蛋白(HSP, heat shockprotein)的积累。甜菜碱提高抗逆性与信号转导和离子稳态有关。本研究在前期工作基础上利用转BADH基因的烟草和番茄材料,结合外源甜菜碱处理的方法,分析甜菜碱的作用与不同的逆境胁迫及不同遗传背景的关系,探究转基因植物耐受性获得中与热激蛋白和钙-钙调蛋白信号途径的关系,甜菜碱提高光合性能以及甜菜碱对活性氧清除系统的作用。研究结果和主要结论如下:
(1)利用非损伤微测技术,对外源甜菜碱处理和转BADH基因烟草(体内积累甜菜碱)进行钙离子(Ca2+)跨膜流速变化趋势的分析研究。实验结果表明:烟草根部的伸长区表皮细胞用NaCl处理后,产生一个瞬态Ca2+外流,高峰值在1-2分钟内。甜菜碱可降低这种外流的峰值。提高NaCl(50-100mM)浓度后,峰值不再升高,Ca2+-ATPase抑制剂(Eosin Y,Eryth-B和CPA)也没有显著影响Ca2+外流,表明这种瞬时的外流主要是细胞壁的阳离子交换;盐胁迫24小时后,Ca2+呈现内流趋势,与此同时低浓度的甜菜碱显著增加NaCl诱导的Ca2+内流值。药理学实验结果表明,胁迫条件下甜菜碱可通过LaCl3敏感的钙离子通道加强Ca2+内流。
(2)甜菜碱升高了胁迫下细胞内自由钙离子浓度([Ca2+]cyt)。激光共聚焦的实验结果证实,无论是外源还是内部合成甜菜碱都可适度升高胞质内自由钙离子浓度。非损伤微测技术和激光共聚焦的实验结果,从动态和静态两方面综合印证了盐胁迫条件下甜菜碱与钙离子之间的因果关系。
(3)甜菜碱提高了非生物胁迫下的植物体内钙的积累。进一步研究甜菜碱对Ca2+吸收的重要作用,对植物中的Ca2+含量进行分析比较表明,在长时间盐和高温胁迫下,甜菜碱预处理的和转基因植物中Ca2+含量明显高于野生型。
(4)甜菜碱增强钙调蛋白(CaM)和热激因子(HSF)基因的表达,从而诱导HSP的积累。实时定量PCR实验,从基因表达层面证实甜菜碱与钙-钙调蛋白(Ca2+-CaM)以及HSP的因果关系。药理实验证实Ca2+和CaM增加了HSFs和HSP基因表达水平,HSP70的Western杂交结果也证实了HSP的积累。Western杂交的药理学实验,从蛋白层面证明甜菜碱可以通过Ca2+-CaM信号途径诱导热激蛋白HSP70的合成积累。结果表明:甜菜碱作为辅助因子增强盐或热胁迫下Ca2+的吸收,并通过Ca2+-CaM的信号途径诱导HSP的转录和翻译。
(5)甜菜碱降低活性氧(ROS)的积累。过氧化氢(H2O2)和超氧阴离子自由基(O2-)在热激下积累,但是转BADH基因植株中积累量少于野生型。另一重要发现是外源添加甜菜碱在活体外不能清除H2O2和O2-,但酶抽提物能降低ROS的浓度,并且转基因植物中的明显清除能力强。这些结果表明在活体内积累甜菜碱不能直接清除ROS,而是通过体内的ROS清除系统发挥作用。
(6)甜菜碱提高植物的抗氧化酶活性,减轻膜伤害的。转BADH基因植物的抗氧化酶活性高于野生型,相对电导率(REC)和丙二醛(MDA)的含量低于野生型,表明甜菜碱积累可提高抗氧化酶活性,减轻膜伤害。
(7)甜菜碱提高ROS清除酶的基因表达,药理学实验证实Ca2+和CaM增加了CuSOD、APX1和CAT1基因的表达水平,从基因表达层面证实甜菜碱甜菜碱可以通过Ca2+-CaM途径影响一系列基因的表达。
(8)甜菜碱提高植物逆境胁迫下的光合能力,减轻光抑制。在42℃热激条件下观测叶绿素荧光表明转基因植物比野生型有较高的光合能力。表明积累甜菜碱可减轻热激引起的光抑制。在盐胁迫下也有类似的结果。同时D1蛋白的Western杂交结果表明甜菜碱提高了D1蛋白的含量,加快D1蛋白的周转,加速PSII的修复。
盐和高温是两种普遍的非生物胁迫,利用外源甜菜碱处理及两种转BADH基因材料,在非生物胁迫(高温和盐胁迫)下,研究甜菜碱在不同植物的遗传背景下的抗逆性机制,排除了材料差异和转基因事件引起的其他影响,更好地证实了甜菜碱的生物学功能。从钙信号转导、活性氧清除、光合机构的保护以及热激蛋白等相关基因表达等方面综合阐明:非生物胁迫产生活性氧的积累,形成变性蛋白,伤害细胞的正常生命活动,引起光合能力下降,影响生物量的积累。胁迫可引起Ca2+内流,[Ca2+]cyt适度升高,可以加快下游的信号转导,从而诱导HSP的转录,获得HSP的积累,减少伤害,是植物细胞一种积极的防御措施。甜菜碱的积累,无论是外源处理还是内部合成,都可加强这一信号,诱导胞质内钙离子浓度适度升高,并通过Ca2+-CaM的信号途径诱导较多HSP的转录和翻译,提高防御能力。甜菜碱通过钙离子信号系统,增加HSP的积累,发挥分子伴侣作用,帮助变性蛋白复性,减少变性蛋白的积累,从而提高植物抗逆性。另外甜菜碱可诱导活性氧清除酶的表达,提高抗氧化酶活性,减少活性氧的积累,从而减轻胁迫造成的伤害。
Glycine betaine (GB) is a substance with special efficiency of the compatibility. GBincrease plant tolerance at the same time accompanied by heat shock protein (HSP, heat shockprotein) accumulation in plants under abiotic stress. HSPs can act as chaperones of denaturedproteins and assist in the translocation and/or degradation of damaged proteins under variousstresses. GB improves salt resistance related to signal transduction and ion homeostasis.Based on the previous work, this study used these two kinds of genetically modified materialand processing method of exogenous betaine to analysis the role of GB and different adversitystress and the relationship between the different genetic background, to explore the transgenicplants for heat resistance and heat shock protein and calcium and calmodulin signalingpathways, the relationship between GB how to protect the photosynthetic mechanism andinfluence the expression of HSP and improve resistance and active oxygen removal system.
(1) To investigate the mechanism of how GB influences the expression of HSP, both theaccumulation of GB in vivo and exogenously applied GB in WT seedlings was studied duringNaCl stress. The elongation zone in tobacco root epidermal cells treated with NaCl. Atransient Ca2+efflux was found after NaCl treatment for1-2min in the epidermal cells of theelongation zone of tobacco roots. But increasing the NaCl concentration (50-100mM) did notsignificantly increase the speed of the outflow of calcium ions. In addition, Ca2+-ATPasemetabolic inhibitors (Eosin Y; eryth-B and CPA) had not significantly effect on Ca2+efflux,which indicated the transient NaCl-induced Ca2+efflux were likely produced by the cell wallcation exchange. After24h of NaCl treatment, an influx of Ca2+was observed, meanwhile lowconcentrations of GB significantly increased NaCl-induced Ca2+influx. Pharmacologyexperiments showed that GB can enhance Ca2+influx through the LaCl3sensitive calcium ionchannel under stress condition.
(2) GB increased intracellular free calcium ion concentration ([Ca2+]cyt) using LSCM,which proved whether foreign or internal composition GB can enhance [Ca2+]cyt.The resultsof non-invasive microelectrode ion flux measuring technique and LSCM proved there is the causal relationships between GB and calcium from two aspects of the static and dynamicunder salt stress and high temperature stress condition.
(3) GB increased the calcium content of tobacco plants under salt or heat stress. Tofurther investigate whether GB plays a role in Ca2+uptake, the calcium content of WT plantspre-treated with GB (WT+GB) and transgenic plants (T) were compared with that of WTplants. GB affected Ca2+acquisition in shoots and roots during long-time NaCl stress, and thecalcium content of WT plants pretreated with GB and that of T plants was higher than that ofuntreated WT plants. The results were consistent with the calcium content of leaves underheat stress.
(4) GB increased the intracellular free calcium ion concentration and enhanced theexpression of calmodulin (CaM) and heat shock factor (HSF) genes resulting in potentiatedlevels of heat shock proteins (HSPs). Pharmacological experiments confirmed that Ca2+andCaM increased the HSFs and HSPs gene expressions coincide with increased the levels ofHSP70accumulation. The causality of GB, calcium-calmodulin (Ca2+-CaM) and HSP isconfirmed from gene expression level by real-time quantitative PCR. It is proved that GB canenhance the levels of HSP70accumulation through the Ca2+-CaM signal pathway from thelevel of protein by Western blotting. A possible regulatory model of Ca2+-CaM in the signaltransduction pathway for induction of transcription and translation of the active HSPs is described.
(5) Significant accumulation of hydrogen peroxide (H2O2) and superoxide radical (O2-)were observed in wild type plants under heat stress; however, these accumulations were muchless in transgenic plants. An important finding reported herein is that exogenous GB cannotdirectly reduce the content of ROS. However, enzyme extraction from the WT can slightlyreduce ROS. In particular, enzyme extraction from transgenic plants greatly decreased theROS compared to the WT plants. These results also indicate that GB indirectly scavengesROS through antioxidative defense in vivo.
(6) GB increase ROS scavenging enzyme activities. Evidently, GB may enhance theactivities of these enzymes to quench ROS in vivo, resulting in a lower ROS concentration.The activities of antioxidant enzymes were also stronger in accordance with lower relativeelectrolyte conductivity (REC) and malondialdehyde (MDA) content in transgenic lines,indicating that the degree of membrane injury in transgenic plants was lower than that in wild type plants. In addition, GB enhanced the expression of antioxidant enzyme genes. The resultssuggested that the accumulation of GB in vivo cannot directly eliminate reactive oxygenspecies (ROS), rather, through maintaining higher activities of antioxidant enzymes to lessenthe accumulation of ROS in transgenic plants and decrease the degree of membrane injury.
(7) GB increase ROS scavenging enzyme (CuSOD, APX1and CAT1) gene expression.Pharmacological experiments confirmed that Ca2+and CaM increased these genes expressions.It is confirmed that GB can affect a series of gene expression through Ca2+-CaM pathway byreal-time quantitative PCR.
(8) The chlorophyll fluorescence analysis of wild type and transgenic plants exposed toheat treatment (42°C) showed that transgenic plants exhibited higher photosynthetic capacitythan wild type plants. This result suggests that the accumulation of GB increased the toleranceto heat-enhanced photoinhibition. This increased tolerance is associated with theimprovement of D1protein content, which accelerated the repair of photosystem II (PSII)from heat-enhanced photoinhibition. GB also increased the tolerance to NaCl-enhancedphotoinhibition.
GB is researched in different plant genetic background for salt stress resistance and hightemperature mechanism, to confirm biological function of GB. The relation of GB, HSP andCa2+-CaM signal transduction pathways is clarified from the heat shock protein accumulation,signal transduction, active oxygen removal, photosynthetic mechanism as well as theprotection of related gene expression. Environmental stresses generate ROS accumulation toformate denatured protein to affect normal metabolic activity. These results suggests thatstress signals are perceived by an unidentified receptor and GB applied exogenously oraccumulated in vivo in BADH-transgenic plants may act as a cofactor to activate Ca2+channels in the plasma membrane or intracellular Ca2+store membrane resulting in anincrease in [Ca2+]cyt. GB accumulation can strengthen this signal, This moderately elevatedlevel of [Ca2+]cytpromoted the expression of CaM1, which increased the DNA-bindingactivity of HSF. Activation of HSF initiated transcription and translation of HSP genes. Theelevated HSP, as molecular chaperone, assist in modified protein renaturation, reducedenatured protein accumulation, to improve plant resistance. In addition, GB induced theexpression of ROS scavenging enzyme, also reduce the accumulation of ROS to alleviate the damage caused by stress. Other pathways are possible including the regulation of HSFphosphorylation by regulation of CaM-dependent kinase, CDPK, MAPK activity, etc.; futurestudies may determine definitively which pathways are playing a role.
引文
陈忠,苏维埃,汤章城。豌豆热激蛋白Hsp60对酶的高温保护功能及其机理。科学通报,1999,44:2171-2174
樊志和,周人纲,李晓芝,自娟。钙-钙调素与小麦苗中热激蛋白的诱导。植物生理学报,2000,26:331-336
冯小燕,高世勇。甜菜碱通过钙通道升高鼠脾淋巴细胞内[Ca2+]i的研究。哈尔滨商业大学学报,2008,24:513-517
郭北海,张艳敏,李洪杰,杜立群,李银心,张劲松,陈受宜,朱至清。甜菜碱醛脱氢酶(BADH)基因转化小麦及其表达。植物学报,2000,42:279-283
李冰,周人刚。钙-钙调素信号系统参与热激信号转导的研究。西北植物学报,2004,24:1322-1328
刘凤华,郭岩,谷冬梅,肖岗,陈正华,陈受宜。转甜菜碱醛脱氢酶基因植物的耐盐性研究。遗传学报,1997,24:54-58
刘箭,庄野真理子。高温下线粒体小分子热激蛋白对柠檬酸合成酶、线粒体和花粉粒的保护作用。植物生理学报,2001,27:375-380
仝月澳,周厚基。果树营养诊断法。北京:农业出版社,1981,81-86
赵世杰,史国安,董新纯(主编)。植物生理学实验指导。北京:中国农业科学技术出版社,2002:58
邹琦(主编)。植物生理生化实验指导。北京:中国农业出版社,1995
Ahmad R., Kim M.D., Back K.H., Kim H.S., Lee H.S., Kwon S.Y., Murata N., Chung W.I.and Kwak S.S.. Stress-induced expression of choline oxidase in potato plant chloroplastsconfers enhanced tolerance to oxidative, salt, and drought stresses. Plant Cell Rep.,2008,27:687-698
Ahmad R., Kim Y.H., Kim M.D., Kwon S.Y., Cho K., Lee H.S. and Kwak S.S.. Simultaneousexpression of choline oxidase, superoxide dismutase and ascorbate peroxidase in potatoplant chloroplasts provides synergistically enhanced protection against various abioticstresses. Physiol. Plant,2010,138:520-533
Ahmad R., Lim C.J. and Kwon S.Y.. Glycine betaine: a versatile compound with greatpotential for gene pyramiding to improve crop plant performance against environmentalstresses. Plant Biotechnol. Rep.,2013,7:49-57
Alia, Sakamoto A., Nonaka H., Hayashi H., Saradhi P.P., Chen T.H.H. and Murata N..Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codAgene for a bacterial choline oxidase. Plant Mol. Biol.,1999,40:279-288
Allakhverdiev S.I., Feyziev Y.M., Ahmed A., Hayashi H., Alie J.A., Klimov V.V., Murata N.and Carpentier R.. Stabilization of oxygen evolution and primary electron transportreactions in photosystem II against heat stress with glycinebetaine and sucrose.Photochem. Photobiol.,1996,34:149-157
Allakhverdiev S.I., Hayashi H., Nishiyama Y., Ivanov A.G., Aliev J.A., Klimov V.V., MurataN. and Carpentier R.. Glycinebetaine protects the D1/D2/Cytb559complex ofphotosystem II against photo-induced and heat-induced inactivation. J. Plant Physiol.,2003,160:41-49
Allakhverdiev S.I., Los D.A., Mohanty P., Nishiyama Y., and Murata N.. Glycinebetainealleviates the inhibitory effect of moderate heat stress on the repair of photosystem IIduring photoinhibition. Biochim. Biophys. Acta,2007,1767:1363-1371
Allen G., Muir S. and Sanders D.. Release of Ca2+from individual plant vacuoles by bothInsP3and cyclic ADP-ribose. Science,1995,268:735
Al-Taweel K., Iwaki T., Yabuta Y., Shigeoka S., Murata N. and Wadano A.. A bacterialtransgene for catalase protects translation of D1protein during exposure of salt-stressedtobacco leaves to strong light. Plant Physiol.,2007,145:258-265
Al-Whaibi M.H.. Plant heat-shock proteins: A mini review. J. King Saud Univ. Sci.2011,23:139-150
Apel K. and Hirt H.. Reactive oxygen species: metabolism, oxidative stress, and signaltransduction. Annu. Rev. Plant Biol.,2004,55:373-399
Asada K.. The water-water cycle in chloroplasts: scavenging of active oxygen species anddissipation of excess photons. Ann. Rev. Plant Physiol. Plant Mol. Biol.,1999,50:601-639
Ashraf M. and Foolad M.R.. Role of glycine betaine and praline in improving plant abioticresistance. Environ. Exp. Bot.,2007,59:206-216
Ashraf M.Y., Akhtar K., Sarwar G. and Ashraf M.. Role of the rooting system in salt tolerancepotential of different guar accessions. Agron. Sustain. Dev.,2005,25:243-249
Bajji M., Lutts S. and Kinet J.M.. Water deficit effect on solution contribution to osmoticadjustment as a function of leaf ageing in three durum wheat (Triticum durum Desf)cultivars performing differently in arid conditions. Plant Sci.,2001,160:669-681
Banti V., Mafessoni F., Loreti E., Alpi A. and Perata P.. The heatinducible transcription factorHsfA2enhances anoxia tolerance in Arabidopsis. Plant Physiol.,2010,152:1471-1483
Basha E., Lee G.J., Breci L.A., Hausrath A.C., Buan N.R., Giese K.C. and Vierling E.. Theidentity of proteins associated with a small heat shock protein during heat stress in vivoindicates that these chaperones protect a wide range of cellular functions. J. Biol. Chem.,2004a,279:7566-7575
Basha E., Lee G.J., Demeler B. and Vierling E., Chaperone activity of cytosolic small heatshock proteins from wheat. Eur. J. Biochem.,2004b,271:1426-1436
Beffagna N., Buffoli B. and Busi C.. Modulation of reactive oxygen species production duringosmotic stress in Arabidopsis thaliana cultured cells: involvement of the plasmamembrane Ca2+-ATPase and H+-ATPase. Plant Cell Physiol.,2005,46:1326-1339
Blum A. and Ebercon A.. Cell membrane stability as measure of drought and heat tolerance inwheat. Crop Sci.,1981,21:43-47
Blume B., Ntkrnberger T., Nass N. and Scheel D.. Receptormediated increase in cytopIasmicfree calcium required for activation of pathogen defense in parsley. Plant Cell,2000,12:1425-1440
Bose J., Pottosin I.I., Shabala S.S., Palmgren M.G. and Shabala S.. Calcium efflux systems instress signaling and adaptation in plants. Front. Plant Sci.,2011,2:85
Bowler C., Montagu M.V. and Inze D.. Superoxide dismutase and stress tolerance. Annu RevPlant Physiol. Plant Mol. Biol.,1992,43:83-116
Braam J.. Regulated expression of the calmodulin related TCH genes in cultured Arabidopsiscells: Induction by calcium and heat shock. Proc. Natl. Acad. Sci. U.S.A.,1992,89:3213-3216
Buchner J.. Supervising the fold: functional principles of molecular chaperones. FASEB J.,1996,10:10-19
Chaidee A. and Pfeiffer W.. Parameters for cellular viability and membrane function inchenopodium cells show a specific response of extracellular pH to heat shock withextreme Q10. Plant Biol.,2006,8:42-51
Charng Y.Y., Liu H.C., Liu N.Y., Chi W.T., Wang C.N., Chang S.H. and Wang T.T.. Aheat-inducible transcription factor, HsfA2, is required for extension of acquiredthermotolerance in Arabidopsis. Plant Physiol.,2007,143:251-262
Chen S., Gollop N. and Heuer B.. Proteomic analysis of salt-stressed tomato (Solanumlycopersicum) seedlings: effect of genotype and exogenous application of glycinebetaine.J. Exp. Bot.,2009,60:2005-2019
Chen T.H.H. and Murata N.. Glycinebetaine protects plants against abiotic stress:mechanisms and biotechnological applications. Plant Cell Environ.,2011,34:1-20
Chen T.H.H. and Murata N.. Glycinebetaine: an effective protectant against abiotic stress inplants. Trends Plant Sci.,2008,13:499-505
Chen W.P., Li P.H. and Chen T.H.H.. Glycinebetaine increase chilling tolerance and reduceschilling-induced lipid peroxidation in Zea mays L. Plant Cell Environ.,2000,23:609-618
Chou M., Chen Y.M. and Lin C.Y.. Thermotolerance of isolated mitochondria associated withheat shock proteins. Plant Physiol.,1989,98:617-621
Clapham D.E.. Calcium signaling. Cell,1995,80:259-268
Cooke A., Cookson A. and Eamshaw M.J.. The mechanism of action on calcium in theinhibition on high temperature-induced leakage of betacyanin from beet root discs. NewPhytol.,1986,102:491-497
Craig E.A., Gambill B.D. and Nelson R.J.. Heat shock proteins molecular chaperones ofprotein biogenesis. Mictobiol. Rev.,1993,57:402-414
Cramer G.R. and Jones R.L.. Osmotic stress and abscisic acid reduce cytosolic calciumactivities in roots of Arabidopsis thaliana. Plant Cell Environ.,1996,19:1291-1298
Cuin Y.A. and Shabala S.. Compatible solutes reduce ROS-induced potassium efflux inArabidopsis roots. Plant Cell Environ.,2007,30:875-885
Davletova S., Schlauch K., Coutu J. and Mittler R.. The zinc-finger protein Zat12plays acentral role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol.,2005a,133:847-856
Davletova S., Rizhsky L., Liang H., Shengqiang Z., Oliver D.J., Coutu J., Shulaev V.,Schlauch K. and Mittler R.. Cytosolic ascorbate peroxidase1is a central component of thereactive oxygen gene network of Arabidopsis. Plant Cell,2005b,17:268-281
DeFalco T., Bender K. and Snedden W.. Breakingthecode: Ca2+sensors inplantsignalling.Biochem. J.,2010,425:27-40
Demidchik V., Shabala S.N., Coutts K.B., Tester M. and Davies J.M.. Free oxygen radicalsregulate plasma membrane Ca2+-and K+-permeable channels in plant root cells. J. CellSci.,2003,116:81-88
Dempsey D.A., Shah J. and Klessig D.F. Salicylic acid and disease resistance in plants. Crit.Rev. Plant Sci.,1999,18:547-575
Deshnium P., Gombos Z., Nishiyama Y. and Murata N.. The action in vivo of glycine betainein enhancement of tolerance of Synechococcus sp.strain PCC7942to low temperature. J.Biol. Chem.,1997,179:339-344
Dhanda S.S. and Munjal R.. Inheritance of cellular thermotolerance in bread wheat. PlantBreed.,2006,125:557-564
Dodd A.N., Kudla J. and Sanders D.. The language of calcium signaling. Annu. Rev. PlantBiol.,2010,61:593-620
Downs C.A., Coleman J.S. and Heckathorn S.A.. The chloroplast22-Ku heat-shock protein: aluminal protein that associates with the oxygen evolving complex and protectsphotosystemII during heat stress. J. Plant Physiol.,1999a,155:477-487
Downs C.A., Heckathorn S.A., Bryan J.K.. The methionine-rich low-molecular-weightcholoroplast heat-shock protein: evolutionary conservation and accumulation in relation tothermotolerance. Amer. J. Bot.,1998,85:175-183
Downs C.A., Jones L.R. and Heckathorn S.A.. Evidence for a novel set of small heat-shockproteins that associate with mitochondria of murine PC12nerve cells and protects NADH:ubiquinone oxidoreductase from heat stress and oxidative stress. Archives. Biochem.Biophysics.,1999b,365:344-350
Einset J., Nielsen E., Connolly E.L., Bones A., Sparstad T., Winge P. and Zhu J.K..Membrane-trafficking RabA4c involved in the effect of glycinebetaine on recovery fromchilling stress in Arabidopsis. Physiol. Plantarum,2007,130:511-518
Einset J.. Candidate effector and regulator genes activated by glycinebetainein Arabidopsis.Amer. soci. plant boil.,2002,653
Elstner F.F. and Heupel C.. Inhibition of nitrite formation from hydroxylammoniumchloride:a simple assay for superoxide dismutase. Anal. Biochem.,1976,70:616-620
Emanuel F., Sabrina A. and Jiri M.. Modulation of D1protein turnover under cadmium andheat stresses monitored by [35S] methionine incorporation. Plant Sci.,1999,144:53-61
Foyer C.H., Descourvieres P. and Kunea K.J.. Protection against oxygen radicals: animportant defense mechanism studied in transgenic plants. Plant Cell Environ.,1994,17:507-523
Gao M., Sakamoto A., Miura K., Murata N., Sugiura A. and Tao R.. Transformation ofJapanese persimmon (Diospyros kaki Thunb) with a bacterial gene for choline oxidase.Mol. Breed.,2000,6:501-510
Garg A.K., Kim J.K., Owens T.G., Ranwala A.P., Choi Y.D., Kochian L.V. and Wu R.J..Trehalose accumulation in rice plants confers high tolerance levels to different abioticstresses. Proc. Natl. Acad. Sci. U.S.A.,2002,99:15898-15903
Glover J.R. and Lindquist S.. Hsp104, hsp70and hsp40: a novel chaperone system thatrescues previously aggregated proteins. Cell,1998,94:73-82
Goel D., Singh A.K., Yadav V., Babbar S.B., Murata N. and Bansal K.C.. Transformation oftomato with a bacterial codA gene enhances tolerance to salt and water stresses. J. PlantPhysiol.,2011,168:1286-1294
Gong M. and Li Z.G.. Calmodulin-binding proteins from zea mays germs. Phytochemistry,1995,40:1335-1339
Gong M., Li Y.J., Dai X., Tian M. and Li Z.G.. Involvement of calcium and calmodulin in theacquisition of heat-shock induced thermotolerance in maize seedlings. J. Plant Physiol.,1997,150:615-621
Gong M., Vander L.A.H., Knight M.R. and Trewavas A.J.. Heat-shock-induced changes inintracellular Ca2+level in tobacco seedlings in relation to thermotolerance.Plant Physiol.,1998,116:429-437
Guy G.L. and Li Q.B.. The organization and evolution of the spinach stress70molecularchaperone gene family. Plant Cell,1998,10:539-556
Hakala M., Tuominen I., Ker nen M., Tyystj rvi T. and Tyystj rvi E.. Evidence for the roleof the oxygen-evolving manganese complex in photoinhibition of photosystemII.BBA-Bioenergetics,2005,1706:68-80
Hayashi H., Alia, Mustardy L., Deshnium P., Ida M. and Murata N.. Transformation ofArabidopsis thaliana with the codA gene for choline oxidase: accumulation ofglycinebetaine and enhanced tolerance to salt and cold stress. Plant J.,2003,12:133-142
Heber U., Lange O.L. and Shuvalov V.A.. Conservation and dissipation of light energy ascomplementary processes: homoiohydric and poikilohydric autotrophs. J. Exp. Bot.,2006,57:1211-1223
Heckathorn S.A., Down C.A., Sharkey T.D. and Coleman J.S.. The small, methinonine-richchloroplast heat-shock protein protects photosystem electron transport during heat stress.Plant Physiol.,1998,116:439-44
Heckathorn S.A., Ryan S.L., Baylis J.A. et al. Invivo evidence from an Agrostis stoloniferaselection genotype that chloroplast small heat-shock proteins can protect photosystemIIduring heat stress. Func. Plant Biol.,2002,29:933-944
Hermans C., Smeyers M., Rodriguez R.M., Eyletters M., Strasser R.J. and Delhaye J.P..Quality assessment of urban trees: A comparative study of physiological characterization,airborne imaging and on site fluorescence monitoring by the OJIP-test. J. Plant Physiol.,2003,160:81-90
Holmstrom K., Somersalo S., Mandal A., Palva T.E. and Welin B.. Improved tolerance tosalinity and low temperature in transgenic tobacco producing glycine betaine. J. Exp.Bot.,2000,51:177-185
Holmstr n K., Somersalo S., Mandal A., Palva T.E. and Welin B.. Improved tolerance tosalinity and low temperature in transgenic tobacco producing glycine betaine. J. Exp. Bot.,2000,51:177-185
Hoque M.A., Banu M.N.A., Nakamura Y., Shimoishi Y. and Murata Y.. Proline andglycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems andreduce NaCl-induced damage in cultured tobacco cells. J. Plant Physiol.,2008,165:813-824
Hsieh T.H., Lee J.T., Yang P.T., Chiu L.H., Charng Y.Y., Wang Y.C. and Chan M.T..Heterology expression of the Arabidopsis C-repeat/dehydration response elementbinding factor1gene confers elevated tolerance to chilling and oxidative stresses intransgenic tomato. Plant Physiol.,2002,129:1086-1094
Ito Y., Katsura K., Maruyama K., Taji T., Kobayashi M., Seki M., Shinozaki K. andYamaguchi-Shinozaki K.. Functional analysis of rice DREB1/CBF-type transcriptionfactors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol.,2006,47:141-153
Jagendorf A.T. and Takabe T.. Inducers of glycinebetaine synthesis in barley. Plant Physiol.,2001,127:1827-1835
Jakob U., Gaestel M., Engel K. and Buchner J.. Small heat shock proteins are molecularchaperones. J. Biol. Chem.1993,268:1517-1520
J rg K., Oliver B. and Kenji H.. Calcium Signals: The lead currency of plant informationprocessing. Plant Cell,2010,22:541-563
Karima H.A., Salama, Mohamed M.F., Mansour and Noaman S.H.. Choline primingimproves salt tolerance in wheat (Triticum aestivum L.). Aust. J. Basic. Appl. Sci.,2011,5:126-132
Kathuria H., Giri J., Nataraja K.N., Murata N., Udayakumar M. and Tyagi A.K..Glycinebetaine-induced water-stress tolerance in codA-expressing transgenic indica rice isassociated with up-regulation of several stress responsive genes. Plant Biotechnol. J.,2009,7:512-26
Kiang J.G., Carr F.E., Burns M.R. and McClain D.E.. HSP-72synthesis is promoted byincrease in [Ca2+]i or activation of G proteins but not pHi or cAMP. Amer. J. Physiol. CellPhysiol.,1994,267:104-114
Kiang J.G. and Tsokos G.C.. Cell signaling and heat shock protein expression. J. Biomed Sci.,1996,3:379-388
Kiegle E., Moore C.A., Haseloff J., Tester M.A. and Knight M.R.. Cell-type-specific calciumresponses to drought, salt and cold in the Arabidopsis root. Plant J.,2000,23:267-278
Kilstrup M., Jacobsen S., Hammer K. and Vogensen F.K.. Induction of heat shock proteinsDnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Appl. Environ. Microb.,1997,63:1826-1837
Kim B.H. and Sch ffl F.. Interaction between Arabidopsis heat shock transcription factor1and70kDa heat shock proteins. J. Exp. Bot.,2002,53:371-375
Klein J.D. and Ferguson I.B.. Effect of high temperature on calcium uptake bysuspention-cultured pear fruit cells. Plant Physiol.,1987,84:153-156
Kloppstech K., Meyer G. and Ohad I.. Synthesis, transport and localization of a nuclear coded22kDheat-shock protein in the chloroplast membranes of peas and chlamydomonasreinhardtii. EMBO J.,1985,4:1901-1909
Konigshofer H., Tromballa H.W., and Loppert H.G.. Early events in signallinghigh-temperature stress in tobacco BY2cells involve alterations in membrane fluidity andenhanced hydrogen peroxide production. Plant Cell Environ.,2008,31:1771-1780
Krause G.H. and Weis E.. Chlorophyll fluorescence and photosynthesis the basis. Annu. Rev.Plant Physiol. Plant Mol. Biol..,1991,42:313-349
Kudla J., Batisti O. and Hashimoto K.. Calcium signals: the lead currency of plantinformation processing. Plant Cell,2010,22:541-563
Larkindale J. and Huang B.. Thermotolerance and antioxidant systems in agrostis stolonifera:involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J.Plant Physiol.,2004,161:405-413
Larkindale J. and Knight M.R.. Protection against heat stressinduced oxidative damage inArabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol.,2002,128:682-695
Laurie S. and Stewart G.R.. The effects of compatible solutes on the heat stability ofglutamine synthetase from chickpeas grown under different nitrogen and temperatureregimes. J. Exp. Bot.,1990,41:1415-1422
Lee K., Thorneycroft D., Achuthan P., Hermjakob H. and Ideker T.. Mapping plantinteractomes using literature curated and predicted protein-protein interaction data sets.Plant Cell,2010,22:997-1005
Li B., Liu H.T., Sun D.Y. and Zhou R.G.. Ca2+and calmodulin modulate DNA-bindingactivity of maize heat shock transcription factor in vitro. Plant Cell Physiol.,2004,45:627-634
Li M.F., Ji L.S., Yang X.H., Meng Q.W. and Guo S.J.. The protective mechanisms ofCaHSP26in transgenic tobacco to alleviate photoinhibition of PSII during chilling stress.Plant Cell Rep.,2012,31:1969-1979
Li S.F., Li F., Wang J.W., Zhang W., Meng Q.W., Chen T.H.H., Murata N. and Yang X.H..Glycinebetaine enhances the tolerance of tomato plants to high temperature duringgermination of seeds and growth of seedlings. Plant Cell Environ.,2011,34:1931-1943
Liu H.T., Li B., Shang Z.L.. Camodulin is involvement in heat shock signal transduction inwheat. Plant Physiol.,2003,132:1186-1195
Liu H.T., Gao F., Han J.L., Li G.L., Liu D.L., Sun D.Y., and Zhou R.G.. Thecalmodulin-binding protein kinase3is part of heat shock signal transduction inArabidopsis thaliana. Plant J.,2008,5:760-773
Lopez C.M.L., Takahashi H. and Yamazaki S.. Plant-water relations of kidney bean plantstreated with NaCl and foliarly applied glycinebetaine. J. Agron. Crop Sci.,2002,188:73-80
Lv S.L., Yang A.F., Zhang K.W., Wang L. and Zhang J.R.. Increase of glycinebetainesynthesis improves drought tolerance in cotton. Mol. Breed.,2007,20:233-248
Lynch J., Polito V.S. and L uchli A.. Salinity reduces membrane-associated calcium in cornroot protoplasts. Plant Physiol.,1989,90:1271-1274
Ma W., Smigel A., Tsai Y.C., Braam J. and Berkowitz G.A.. Innate immunity signaling:cytosolic Ca2+elevation is linked to downstream nitric oxide generation through the actionof calmodulin or a calmodulin-like protein. Plant Physiol.,2008,148:818-828
Ma X.L., Wang Y.J., Xie S.L., Wang C. and Wang W.. Glycinebetaine application amelioranegative effects of drought stress in tobacco. Russ. J. Plant Physiol.,2007,54:472-479
M kel P., Peltonen-Sainio P., Jokinen K., Pehu E., Set l H., Hinkkanen R. and SomersaloS.. Uptake and translocation of foliar-applied glycine betaine in crop plants. Plant Sci.,1996,121:221-230
Mahmood T., Iqbal N., Raza H., Qasim M. and Ashraf M.Y.. Growth modulation and ionpartitioning in salt stressed sorghum (Sorghum bicolor L.) by exogenous supply ofsalicylic acid. Pak. J. Bot.,2010,42:3047-3054
McAinsh M.R. and Pittman J.K.. Shaping the calcium signature. New Phytol.,2009,181:275-294
McCue K.F. and Hanson A.D.. Salt-inducible betaine aldehyde dehydrogenase from sugarbeet: cDNA cloning and expression. Plant Mol. Biol.,1992,18:1-11
Miller G. and Miller R.. Could heat shock transcription factors function as hydrogen peroxidesensors in plants? Ann. Bot.,2006,98:279-288
Miller G., Suzuki N., Ciftci-Yilmaz S. and Mittler R.. Reactive oxygen species homeostasisand signaling during drought and salinity stresses. Plant Cell Environ.,2010,33:453-467
Mittler R.. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci.,2002,7:405-410
Mittler R. and Zilinskas B.A.. Molecular cloning and characterization of a gene encoding peacytosolic ascorbate peroxidase. J. Biol. Chem.,1992,267:21802-21807
Mohanty P.S., Hayashi H. and Papageorgiou G.C.. Stabilization of the Mn-cluster of theoxygen-evolving complex by glycinebetaine. BBA-Bioenergetics,1993,1144:92-96
Monroy A.F., Sarhan F. and Dhindsa.. Cold-induced changes in freezing tolerance proteinphosphorylation and gene expression. Plant Physiol.,1993,102:1227-1235
Moon B.Y., Higashi S.I., Gombos Z. and Murata N.. Unsaturation of the membrane lipids ofchloroplasts stabilizes the photosynthetic machinery against low-temperaturephotoinhibition in transgenic tobacco plants. Proc. Natl. Acad. Sci. U.S.A.,1995,92:6219-6223
Mori I.C. and Schroeder J.I.. Reactive oxygen species activation of plant Ca2+channels: asignaling mechanism in polar growth, hormone transduction, stress signaling, andhypothetically mechanotransduction. Plant Physiol.,2004,135:702-708
Mosser D.D., Kotzbauer P.T., Sarge K.D. and Morimoto R.I.. In vitro activation of heat shocktranscription factor DNA-binding by calcium and biochemical conditions that affectprotein conformation. Proc. Natl. Acad. Sci. USA,1990,87:3748-3752
Munns R. and Tester M.. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol.,2008,59:651-681
Murata N., Takahashi S., Nishiyama Y. and Allakhverdiev S.I.. Photoinhibition ofphotosystem II under environmental stress. BBA-Bioenergetics,2007,1767:414-421
Nakamoto H., Suzuki N. and Roy S.K.. Constitutive expression of a small heat-shock proteinconfers cellular thermotolerance and thermal protection to the photosynthetic apparatus incyanobacteria. FEBS Lett.,2000,483:169-174
Nemchinov L.G., Shabala L. and Shabala S.. Calcium efflux as a component of thehypersensitive reponse of Nicotiana benthamiana to Pseudomonas syringae. Plant CellPhysiol.,2008,49:40-46
Nicolas L.T., Tan Y.F,. Richard P.J. and Harvey M.A.. Abiotic environmental stress inducedchanges in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes.J. Proteomics,2009,72:367-378
Nishiyama Y., Allakhverdiev S.I. and Murata N.. Inhibition of the repair of photosystemII byoxidative stress in cyanobacteria. Photosynth. Res.,2005,84:1-7
Noctor G. and Foyer C.H.. Ascorbate and glutathione: keeping active oxygen under control.Annu. Rev. Plant Physiol. Plant Mol. Biol.,1998,49:249-279
Nollen E.A.A. and Morimoto R.I.. Chaperoning signaling pathways: molecular chaperones asstress-sensing “heat shock” proteins. J. Cell Sci.,2002,115:2809-2816
Nomura M., Hibino T., Takabe T., Sugiyama T., Yokota A., Miyake H. and Takabe T..Transgenically produced glycinebetaine protects ribulose1,5-bisphosphatecarboxylase/oxygenase from inactivation in Synechococcus sp. PCC7942under salt stress.Plant Cell Physiol.,1998,39:425-432
Ohnishi N. and Murata N.. Glycinebetaine counteracts the inhibitory effects of salt stress onthe degradation and synthesis of D1protein during photoinhibition in Synechococcus sp.PCC7942. Plant Physiol.,2006,141:758-765
Ohnishi N., Allakhverdiev S.I., Takahashi S., Higashi S.,Watanabe M., Nishiyama Y. andMurata N.. Two-step mechanism of photodamage to photosystem II: step1occurs at theoxygen-evolving complex and step2occurs at the photochemical reaction center.Biochemisty,2005,44:8494-8499
Okazaki Y., Kikuyama M., Hiramoto Y. and Iwasaki N.. Short-term regulation of cytosolicCa2+, cytosolic pH and vacuolar pH under NaCl stress in the charophyte alga nitellopsisobtusa. Plant Cell Environ.,1996,19:569-576
Panaretou B. and Zhai C.. The heat shock proteins: their roles as multi-component machinesfor protein folding. Fungal biol. rev.,2008,22:110-119
Pang C.H. and Wang B.S.. Oxidative stress and salt tolerance in plants. Prog. Bot.,2008,69:231-245
Papageorgiou G.C., Fujimura Y. and Murata N.. Protection of the oxygen-evolvingPhotosystemII complex by glycinebetaine. BBA-Bioenergetics,1991,1057:361-366
Papageorgiou G.C. and Murata N.. The unusually strong stabilizing effects of glycine betaineon the structure and function of the oxygen-evolving photosystemII complex. Photosynth.Res.,1995,44:243-252
Park E.J., Jeknic Z. and Chen T.H.H.. Exogenous application of glycinebetaine increaseschilling tolerance in tomato plants. Plant Cell Physiol.,2006,47:706-714
Park E.J., Jeknic Z., Pino M.T., Murata N. and Chen T.H.H.. Glycinebetaine accumulation ismore effective in chloroplasts than in the cytosol for protecting transgenic tomato plantsagainst abiotic stress. Plant Cell Environ.,2007,30:994-1005
Park E.J., Jeknic Z., Sakamoto A., DeNoma J., Yuwansiri R., Murata N. and Chen T.H.H..Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, andflowers from chilling damage. Plant J.,2004,40:474-487
Parsell L.. Small heat dhock proteins and stress tolerance in plants. BBA-Bioenergetics,2002,1577:1-9
Pei Z.M., Murata Y., Benning G., Thomine S., Klusener B., Allen G.J., Grill E. and SchroederJ.I.. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling inguard cells. Nature,2000,406:731-734
Plieth C., Sattelmacher B. and Hansen U.P.. Cytoplasmic Ca2+-H+-exchange buffers ingreenalgae. Protoplasma,1997,198:107-124
Pnueli L., Liang H., Rozenberg M. and Mittler R.. Growth suppression, altered stomatalresponses, and augmented induction of heat shock proteins in cytosolic ascorbateperoxidase (Apx1)-deficient Arabidopsis plants. Plant J.,2003,34:187-203
Prasad K.V.S.K., Sharmila P., Kumar P.A. and Pardha S.P.. Transformation of Brassica juncea(L.) Czern with bacterial coda gene enhances its tolerance to salt stress. Mol. Breed.,2000,6:489-499
Preczewski P., Heckathorn S.A., Downs C.A.. Photosynthetic thermotolerance is positivelyand quantitatively correlated with production of specific heat-shock proteins among ninegenotypes of tomato. Photosynthetica,2000,38:127-134
Rajendrakumar C.S., Suryanarayana T. and Reddy A.R.. DNA helix destabilization by prolineand betaine: possible role in the salinity tolerance process. FEBS Lett.,1997,410:201-205
Reddy A.S.N., Ali G.S., Celesnik H. and Day I.S.. Coping with stresses: roles of calcium-andcalcium/calmodulin-regulated gene expression. Plant Cell,2011,23:2010-2032
Rehman H., Malik S.A. and Saleem M.. Heat tolerance of upland cotton during fruiting stageevaluated using cellular membrane thermostability. Field Crops Res.,2004,85:149-158
Remacle J.,Raes M., Toussaint O., Renard P. and Rao G.. Low levels of reactive oxygenspecies as modulators of cell function. Mutation Res.,1995,316:103-122
Rentel M.C. and Knight M.R.. Oxidative stress-induced calcium signaling in Arabidopsis.Plant Physiol.,2004,135:1471-1479
Rhodes D. and Hanson A.D.. Quaternary ammonium and tertiary sulfonium compounds inhigher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol.,1993,44:357-384
Robinson S.P., and Jones G.P.. Accumulation of glycinebetaine in chloroplasts providesosmotic adjustment during salt stress. Aust J. Plant Physiol.,1986,13:659-668
Romani G., Bonza M.C., Filippini I., Cerana M., Beffagna N. and De Michelis M.I..Involvement of the plasma membrane Ca2+-ATPase in the short-term response of theArabidopsis thaliana cultured cells to oligalacturonides. Plantr. Biol.,2004,6:192-200
Saidi Y., Finka A. and Goloubinoff, P.. Heat perception and signalling in plants: a tortuouspath to thermotolerance. New Phytol.,2011,190:556-565
Saidi Y., Finka A., Muriset M., Bromberg Z., Weiss Y.G., Maathuis F.J. and Goloubinoff P.The heat shock response in moss plants is regulated by specific calcium-permeablechannels in the plasma membrane. Plant Cell,2009,21:2829-2843
Sakamoto A. and Murata N.. The role of glycine betaine in the protection of plants from stress:clues from transgenic plants. Plant Cell Environ.,2002,25:163-171
Sakamoto A. and Murata N.. Genetic engineering of glycinebetaine synthesis in plants:current status and implications for enhancement of stress tolerance. J. Exp. Bot.,2000,51:81-88
Sanders D., Brownlee C. and Harper J.F.. Communicating with calcium. Plant Cell,1999,11:691-706
Sanmiya K., Suzuki K., Egawa Y. and Shono M.. Mitochondrial small heat-shock proteinenhances thermotolerance in tobacco plants. FEBS Lett.,2004,557:265-268
Scandalios J.G.. Oxygen stress and superoxide dismutases. Plant Physiol.,1993,101:7-12
Schroda M., Vallon O., Wollman F.A. and Beck C.F.. A chloroplast-targeted heat shockprotein70(HSP70) contributes to the photoprotection and repair of photosystem duringand after photoinhibition. Plant Cell,1999,11:1165-1178
Schuster G., Even D., Kloppstech K.. Evidence for protection by heat-shock protein againstphotoinhibition during heat-shock. EMBO J.,1988,7:1-6
Shabala S., Baekgaard L., Shabala L., Fuglsang A., Babourina O., Palmgren M.G., Cuin T.A.,Rengel Z. and Nemchinov L.G.. Plasma membrane Ca2+transporters mediatevirus-induced acquired resistance to oxidative stress. Plant Cell Environ.,2011,34:406-417
Shabala S. and Newman I.. Salinity effects on the activity of plasma membrane H+and Ca2+transporters in bean leaf mesophyll: masking role of the cell wall. Ann. Bot.,2000,85:681-686
Snedden W.A. and Fromm H.. Calmodulin as a versatile calcium signal transducer in plants.New Phytol.,2001,151:35-66
Stevenson M.A., Calderwood S.K. and Hahn G.M.. Rapid increases in inositol trisphosphateand intracellular Ca2+after heat shock. Biochem. Biophys. Res. Commun.,1986,137:826-833
Storozhenko S., Pauw P.D., Montagu M.V., Inze′D. and Kushnir S.. The heat-shock elementis a functional component of the Arabidopsis APX1gene promoter. Plant Physiol.,1998,118:1005-1014
Strasser R.J., Srivastava A. and Govindjee.. Polyphasic chlorophyll a fluorescence transient inplants and cyanobacteria. Photochem. Photobiol.,1995,61:32-42
Su P. and Li H.. Arabidopsis stromal70-kD heat shock proteins are essential for plantdevelopment and important for thermotolerance of germinating seeds. Plant Physiol.,2008,146:1231-1241
Sudhakar C., Lakshmi A. and Giridarakumar S.. Changes in the antioxidant enzyme efficacyin two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. PlantSci.,2001,161:613-619
Sun J., Chen S., Dai S., Wang R., Li N., Shen X., Zhou X., Lu C., Zheng X,. Hu Z., Zhang Z.,Song J. and Xu Y.. NaCl-induced alternations of cellular and tissue ion fluxes in roots ofsalt resistant and salt-sensitive poplar species. Plant Physiol.,2009,149:1141-1153
Sun Q.P., Guo Y., Sun Y., Sun D.Y. and Wang X.J.. Influx of extracellular Ca2+involved injasmonic acid-induced elevation of [Ca2+]cytand JA expression in Arabidopsis thaliana. J.Plant Res.,2006,119:343-335
Sun X.T., Li B. and Zhou G.M.. Binding of the maize cytosolic HSP70to calmodulin,andidentification of calmodulin-binding site in HSP70. Plant Cell Physiol.,2000,41:804-810
Sung D.Y. and Guy C.. Physiological and molecular assessment of altered expression ofHsc70-1in Arabidopsis.evidence for pleiotropic consequences. Plant Physiol.,2003,132:979-987
Süss K.H. and Yordanov I.T.. Biosynthesis cause of in vivo acquired thermotolerance ofphotosynthetic light reaction and metabolic responses of chloroplasts to heat stress. PlantPhysiol.,1986,81:192-199
Takahashi F., Mizoguchi T., Yoshida R., Ichimura K. and Shinozaki K.. Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol. Cell,2011,41:649-660
Takahashi S. and Murata N.. How do environmental stresses accelerate photoinhibition?Trends Plant Sci.,2008,13:178-182
Takahashi S. and Murata N.. Glycerate-3-phosphate, produced by CO2fixation in the Calvincycle, is critical for the synthesis of the D1protein of photosystem II. BBA-Bioenergetics,2006,1757:198-205
Tan W., Meng Q.W., Brestic M., Olsovska K. and Yang X.H.. Photosynthesis is improved byexogenous calcium in heat-stressed tobacco plants. J. Plant Physiol.,2011,168:2063-2071
Tang L., Kwon S.Y., Kim S.H., Kim J.S., Choi J., Cho K., Sung C., Kwak S.S. and Lee H.S..Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase andascorbate peroxidase in chloroplasts against oxidative stress and high temperature. PlantCell Rep.,2006,25:1380-1386
Timperio A.M., Egidi M.G. and Zolla L.. Proteomics applied on plant abiotic stresses: Role ofheat shock proteins (HSP). J. Proteomics,2008,71:391-411
T r k Z, Goloubinoff P, Horvath I,. Synechocystis HSP17is an amphitropic protein thatstabilizes heatstressed membranes and binds denatured proteins for subsequentchaperone-mediated refolding. Proc. Natl Acad. Sci. U.S.A.,2001,98:3098-3103
Tracy F.E., Gilliham M., Dodd A.N., Webb A.A. and Tester M.. NaCl-induced changes incytosolic free Ca2+in Arabidopsis thaliana are heterogeneous and modified by externalionic composition. Plant Cell Environ.,2008,31:1063-1073
Tsvetkova N.M,. Horvath I., Trk Z.. Small heat-shock proteins regulate membrane lipidpolymorphism. Proc. Natl Acad. Sci. U.S.A.,2002,99:13504-13509
Vierling E.. The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol.Biol.,1991,42:579-620
Volkov R.A., Panchuk I.I., Mullineaux P.M. and Scho¨ffl F.. Heat stressinduced H2O2isrequired for effective expression of heat shock genes in Arabidopsis. Plant Mol. Biol.,2006,61:733-746
Wahid A., Gelani S., Ashraf M. and Foolad M.R.. Heat tolerance in plants: An overview.Environ. Exp. Bot.,2007,61:199-233
Wahid A., Perveen M., Gelani S. and Basra Shahzad M.A.. Pretreatment of seed with H2O2improves salt tolerance of wheat seedlings by alleviation of oxidative damage andexpression of stress proteins. J. Plant Physiol.,2007,164:283-294
Wahid A. and Shabbir A.. Induction of heat stress tolerance in barley seedlings by pre-sowingseed treatment with glycinebetaine. Plant Growth Regul.,2005,46:133-141
Wang G.P., Li F., Zhang J., Zhao M.R., Hui Z. and Wang W.. Overaccumulation of glycinebetaine enhances tolerance of the photosynthetic apparatus to drought and heat stress inwheat. Photosynthesis,2010,48:30-41
Waters E.R., Lee G.J. and Vierling E.. Evolution, structure and function of the small heatshock protein in plants. J. Exp. Bot.,1996,47:325-338
Weiss E.. The influence of metal cations and pH on the heat sensitivity of photosyntheticoxygen evolution and chlorophyll fluorescence in spinach chloroplasts. Planta,1982,154:41-47
White P.J. and Broadley M.R.. Calcium in Plants. Ann. Bot.,2003,92:487-511
Wu H.C., Luo D.L., Vignols F. and Jinn T.L.. Heat shock-induced biphasic Ca2+signature andOsCaM1-1nuclear localization mediate downstream signalling in acquisition ofthermotolerance in rice (Oryza sativa L.). Plant Cell Environ.,2012,35:1543-1557
Xiong L., Schumaker K.S. and Zhu J.K.. Cell signaling during cold, drought, and salt stress.Plant Cell,2002,14:165-183
Xu Y., and Huystee R.B.. Association of calcium and Calmodulin to peroxidase secretion andactivation. J. Plant Physiol.,1993,141:141-146
Yancey P.H.. Compatible and counteracting solutes. Cellul. Mol. Physiol. Cell Vol. Regul.,1994,81-109
Yang G., Rhodes D. and Joly R.J.. Effects of high temperature on membrane stability andchlorophyll fluorescence in glycinebetaine-deficient and glycinebetaine-containing maizelines. Aust. J. Plant Physiol.,1996,23:437-443
Yang X.H., Wen X.G., Gong H.M., Lu Q.T., Yang Z.P., Tang Y.L., Liang Z. and Lu C.M..Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance ofphotosystem II in tobacco plants. Planta,2007,225:719-733
Yang X.H., Liang Z. and Lu C.M.. Genetic engineering of the biosynthesis of glycinebetaineenhances photosynthesis against high temperature stress in transgenic tobacco plants.Plant Physiol.,2005a,138:2299-2309
Yang X.H., Liang Z., Wen X.G. and Lu.CM.. Genetic engineering of the biosynthesis ofglycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenictobacco plants. Plant Mol. Biol.,2008,66:73-86
Yang X.H. and Lu C.M.. Effects of exogenous glycinebetaine on growth, CO2assimilation,and photosystemII photochemistry of maize plants. Physiol. Plantarum,2006,127:593-602
Yang X.H. and Lu C.M.. Photosynthesis is improved by exogenous glycinebetaine insalt-stressed maize plants. Physiol. Plantarum,2005b,124:343-352
Yoshioka M., Uchida S., Mori H., Komayama K., Ohira S., Morita N., Nakanishi T. andYamamoto Y.. Quality control of photosystem II: Cleavage of reaction center D1proteinin spinach thylakoids by FtsH protease under moderate heat stress. J. Biol. Chem.,2006,281:21660-21669
Zarcinas B.A., Carwright B. and Spouncer L.R.. Nitric acid digestion and multi-elementanalysis of plant material by inductively coupled plasma spectrometry. Commun. Soil Sci.Plan.,1987,8:131-146
Zepeda-Jazo I., Velarde-Buendía A.M., Enríquez-Figueroa R., Bose J., Shabala S.,Mu iz-Murguía J. and Pottosin I.I.. Polyamines interact with hydroxyl radicals inactivating Ca2+and K+transport across the root epidermal plasma membranes. PlantPhysiol.,2011,157:2167-2180
Zhang N., Si H.J., Wen G., Du H.H., Liu B.L. and Wang D.. Enhanced drought and salinitytolerance in transgenic potato plants with a BADH gene from spinach. Plant Biotechnol.Rep.,2011,5:71-77
Zhang W., Fan L.M. and Wu W.H.. Osmo-sensitive and stretch activated calcium-permeablechannels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiol.,2007,143:1140-1151
Zhang W., Zhou R.G., Gao Y.J., Zheng S.Z., Xu P., Zhang S.Q. and Sun D.Y.. Molecular andgenetic evidence for the key role of AtCaM3in heat-shock signal transduction inArabidopsis. Plant Physiol.,2009,149:1773-1784
Zhao Y., Aspinal D. and Paleg L.G.. Protection of membrane integrity in Medicago sativa L.by glycinebetaine against the effects of freezing. J. Plant Physiol.,1992,140:541-543