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. 2008 Jun 15;14(1-2):155–166. doi: 10.1007/s12298-008-0014-2

Genetic engineering for heat tolerance in plants

Amanjot Singh 1, Anil Grover 1,
PMCID: PMC3550655  PMID: 23572882

Abstract

High temperature tolerance has been genetically engineered in plants mainly by over-expressing the heat shock protein genes or indirectly by altering levels of heat shock transcription factor proteins. Apart from heat shock proteins, thermotolerance has also been altered by elevating levels of osmolytes, increasing levels of cell detoxification enzymes and through altering membrane fluidity. It is suggested that Hsps may be directly implicated in thermotolerance as agents that minimize damage to cell proteins. The other three above approaches leading to thermotolerance in transgenic experiments though operate in their own specific ways but indirectly might be aiding in creation of more reductive and energy-rich cellular environment, thereby minimizing the accumulation of damaged proteins. Intervention in protein metabolism such that accumulation of damaged proteins is minimized thus appears to be the main target for genetically-engineering crops against high temperature stress.

Key words: Heat shock proteins, Heat shock factors, Protein metabolism, Thermotolerance, Transgenic plants

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References

  1. Agarwal M., Katiyar-Agarwal S., Grover A. Plant Hsp100 proteins: structure, function and regulation. Plant Sci. 2002;163:397–405. doi: 10.1016/S0168-9452(02)00209-1. [DOI] [Google Scholar]
  2. Agarwal M., Katiyar-Agarwal S., Sahi C., Gallie D.R., Grover A. Arabidopsis thaliana Hsp100 protein: kith and kin. Cell Stress Chap. 2001;6:219–224. doi: 10.1379/1466-1268(2001)006<0219:ATHPKA>2.0.CO;2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Agarwal M., Sarkar N., Grover A. Low molecular weight heat shock proteins in plants. J. Plant Biol. 2003;30:141–149. [Google Scholar]
  4. Alia, Hayashi H., Sakamoto A., Murata N. Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. Plant J. 1998;16:155–161. doi: 10.1046/j.1365-313x.1998.00284.x. [DOI] [PubMed] [Google Scholar]
  5. Alscher R.G., Erturk N., Heath L.S. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 2002;53:1331–1341. doi: 10.1093/jexbot/53.372.1331. [DOI] [PubMed] [Google Scholar]
  6. Barnett T.M., Altohuler C., McDaniel N., Mascarenhas J.P. Heat shock induced proteins in plant cells. Dev. Genet. 1980;1:331–340. doi: 10.1002/dvg.1020010406. [DOI] [Google Scholar]
  7. Batra G., Chauhan V.S., Singh A., Sarkar N.K., Grover A. Complexity of rice Hsp100 gene family: lessons from rice genome sequence data. J. Biosci. 2007;32:611–619. doi: 10.1007/s12038-007-0060-x. [DOI] [PubMed] [Google Scholar]
  8. Buchner J. Hsp90 & Co.: a holding for folding. Trends Biochem. Sci. 1999;24:136. doi: 10.1016/S0968-0004(99)01373-0. [DOI] [PubMed] [Google Scholar]
  9. Burke, J.J. and Chen, J. (2006). Changes in cellular and molecular processes in plant adaptation to heat stress. In: Plant-Environment Interactions (Ed. Huang, B.), CRC press, pp. 27–46.
  10. Charng Y.Y., Liu H.C., Liu N.Y., Chi W.T., Wang C.N., Chang S.H., Wang T.T. A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 2007;143:251–262. doi: 10.1104/pp.106.091322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Charng Y.Y., Liu H.C., Liu N.Y., Hsu F.C., Ko S.S. Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol. 2006;140:1297–1305. doi: 10.1104/pp.105.074898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen J., Burke J.J., Xin Z., Xu C., Velten J. Characterization of the Arabidopsis thermosensitive mutant atts02 reveals an important role for galactolipids in thermotolerance. Plant Cell Environ. 2006;29:1437–1448. doi: 10.1111/j.1365-3040.2006.01527.x. [DOI] [PubMed] [Google Scholar]
  13. Chen S., Vaghchhipawala Z., Li W., Asard H., Dickman M. B. Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by bax and oxidative stresses in yeast and plants. Plant Physiol. 2004;135:1630–1641. doi: 10.1104/pp.103.038091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Doyle S.M., Hoskins J.R., Wickner S. Collaboration between the ClpB AAA+ remodeling protein and the DnaK chaperone system. Proc Natl Acad Sci U S A. 2007;104:11138–11144. doi: 10.1073/pnas.0703980104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dragovic Z., Broadley S.A., Shomura Y., Bracher A., Hartl F.U. Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 2006;25:2519–2528. doi: 10.1038/sj.emboj.7601138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Feng, L., Wang, K., Li, Y., Tan, Y., Kong, J., Li, H. and Zhu, Y. (2007). Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep. DOI 10.1007/s00299-006-0299-y [DOI] [PubMed]
  17. Georgopoulos C., Welch P.A. Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol. 1993;9:601–634. doi: 10.1146/annurev.cb.09.110193.003125. [DOI] [PubMed] [Google Scholar]
  18. Gepstein S., Grover A., Blumwald E. Producing biopharmaceuticals in the desert: building an abiotic stress tolerance in plants for salt, heat and drought. In: Knablein J., Muller R.H., editors. Modern Biopharmaceuticals. Weinhaum: Wiley-VCH Verlag GmbH & Co.; 2005. pp. 967–994. [Google Scholar]
  19. Glover J.R., Lindquist S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell. 1998;94:73–82. doi: 10.1016/S0092-8674(00)81223-4. [DOI] [PubMed] [Google Scholar]
  20. Grover A. Molecular biology of stress responses. Cell Stress Chap. 2002;7:1–5. doi: 10.1379/1466-1268(2002)007<0001:MBOSR>2.0.CO;2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Grover A., Agarwal M., Katiyar-Agarwal S., Sahi C., Agarwal S. Production of high temperature tolerant transgenic plants through manipulation of photosynthetic membrane lipids. Curr. Sci. 2000;79:557–559. [Google Scholar]
  22. Grover A., Aggarwal P.K., Kapoor A., Katiyar-Agarwal S., Agarwal M., Chandramouli A. Addressing abiotic stresses in agriculture through transgenic technology. Curr Sci. 2003;84:355–367. [Google Scholar]
  23. Grover A., Kapoor A., Katiyar-Agarwal S., Agarwal M., Sahi C., Jain P., Satyalakshmi O., Agarwal S., Dubey H. Experimentation in biology of plant abiotic stress responses. Proc Indian Natl Acad Sci. 2001;B67:189–214. [Google Scholar]
  24. Grover A., Kapoor A., Satyalakshmi O., Agarwal S., Sahi C., Katiyar-Agarwal S., Agarwal M., Dubey H. Understanding molecular alphabets of the plant abiotic stress responses. Curr. Sci. 2001;80:206–216. [Google Scholar]
  25. Grover A., Pareek A., Singla S.L., Minhas D., Katiyar S., Ghawana S., Dubey H., Agarwal M., Rao G.U., Rathee J., Grover A. Engineering crops for tolerance against abiotic stresses through gene manipulation. Curr. Sci. 1998;75:689–696. [Google Scholar]
  26. Grover A., Sahi C., Sanan N., Grover A. Taming abiotic stresses in plants through genetic engineering: current strategies and perspective. Plant Sci. 1999;143:101–111. doi: 10.1016/S0168-9452(99)00025-4. [DOI] [Google Scholar]
  27. Hartl F.U., Hlodan R., Langer T. Molecular chaperones in protein folding: The art of avoiding sticky situations. Trends Biochem. Sci. 1994;19:20–25. doi: 10.1016/0968-0004(94)90169-4. [DOI] [PubMed] [Google Scholar]
  28. Hong S.W., Vierling E. Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci, U S A. 2000;97:4392–4397. doi: 10.1073/pnas.97.8.4392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hong S.W., Vierling E. Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J. 2001;27:25–35. doi: 10.1046/j.1365-313x.2001.01066.x. [DOI] [PubMed] [Google Scholar]
  30. Ignatova Z., Gierasch L.M. Inhibition of protein aggregation in vitro and in vivo by a natural osmoprotectant. Proc Natl Acad Sci, U S A. 2006;103:13357–13361. doi: 10.1073/pnas.0603772103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Katiyar-Agarwal S., Agarwal M., Grover A. Heat tolerant basmati rice engineered by overexpression of hsp101 gene. Plant Mol. Biol. 2003;51:677–686. doi: 10.1023/A:1022561926676. [DOI] [PubMed] [Google Scholar]
  32. Katiyar-Agarwal S., Agarwal M., Gallie D., Grover A. Search for the cellular functions of plant Hsp100/Clp family proteins. Crit. Rev. lant Sci. 2001;20:277–295. doi: 10.1016/S0735-2689(01)80043-5. [DOI] [Google Scholar]
  33. Kotak S., Larkindale J., Lee U., von Koskull-Doring P., Vierling E., Scharf K.D. Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 2007;10:310–316. doi: 10.1016/j.pbi.2007.04.011. [DOI] [PubMed] [Google Scholar]
  34. Krishna P., Gloor G. The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chap. 2001;6:238–246. doi: 10.1379/1466-1268(2001)006<0238:THFOPI>2.0.CO;2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kumar M.S., Kumar G., Srikanthbabu V., Udayakumar M. Assessment of variability in acquired thermotolerance: potential option to study genotypic response and the relevance of stress genes. J Plant Physiol. 2007;164:111–125. doi: 10.1016/j.jplph.2005.11.001. [DOI] [PubMed] [Google Scholar]
  36. Lee J.H., Schoffl F. An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF, and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol. Gen. Genet. 1996;252:11–19. doi: 10.1007/BF02173200. [DOI] [PubMed] [Google Scholar]
  37. Lee J.H., Hubel A., Schoffl F. Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. Plant J. 1995;8(4):603–612. doi: 10.1046/j.1365-313X.1995.8040603.x. [DOI] [PubMed] [Google Scholar]
  38. Lee U., Wie C., Escobar M., Williams B., Hong S.W., Vierling E. Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. Plant Cell. 2005;17:559–571. doi: 10.1105/tpc.104.027540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Li C., Chen Q., Gao X., Chen N., Xu S., Chen J., Wang X. AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci. China C Life Sci. 2005;48(6):540–550. doi: 10.1360/062005-119. [DOI] [PubMed] [Google Scholar]
  40. Low D., Brandle K., Nover L., Forreiter C. Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta. 2000;211:575–582. doi: 10.1007/s004250000315. [DOI] [PubMed] [Google Scholar]
  41. Malik M.K., Slovin J. P., Hwang C.H., Zimmerman J.L. Modified expression of a carrot small heat shock protein gene, hsp17.7, results in increased or decreased thermotolerance. Plant J. 1999;20:89–99. doi: 10.1046/j.1365-313X.1999.00581.x. [DOI] [PubMed] [Google Scholar]
  42. Mishra S.K., Tripp J., Winkelhaus S., Tschiersch B., Theres K., Nover L., Scharf K.D. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 2002;16:1555–1567. doi: 10.1101/gad.228802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Murakami T., Matsuba S., Funatsuki H., Kawaguchi K., Saruyama H., Tanida M., Sato Y. Over-expression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Mol. Breed. 2004;13:165–175. doi: 10.1023/B:MOLB.0000018764.30795.c1. [DOI] [Google Scholar]
  44. Murakami Y., Tsuyama M., Kobayashi Y., Kodama H., Iba K. Trienoic fatty acids and plant tolerance of high temperature. Science. 2000;287:476–479. doi: 10.1126/science.287.5452.476. [DOI] [PubMed] [Google Scholar]
  45. Murata N. Molecular species composition of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Cell Physiol. 1983;24:81–86. [Google Scholar]
  46. Murata N., Ishizaki-Nishizawa O., Higashi S., Hayashi H., Tasaka Y., Nishida I. Genetically engineered alteration in the chilling sensitivity of plants. Nature. 1992;356:710–713. doi: 10.1038/356710a0. [DOI] [Google Scholar]
  47. Neta-Sharir I., Isaacson T., Lurie S., Weiss D. Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell. 2005;17:1829–1838. doi: 10.1105/tpc.105.031914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Nieto-Sotelo J., Martinez L.M., Ponce G., Cassab G.I., Alagon A., Meeley R.B., Ribaut J.M., Yang R. Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell. 2002;14:1621–1633. doi: 10.1105/tpc.010487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Ou W., Park Y.-D., Zhou H.-M. Molecular mechanism for osmolyte protection of creatine kinase against guanidine denaturation. Euro J Biochem. 2001;268:5901–5911. doi: 10.1046/j.0014-2956.2001.02539.x. [DOI] [PubMed] [Google Scholar]
  50. Panchuk I.I., Volkov R.A., Schoffl F. Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 2002;129:838–853. doi: 10.1104/pp.001362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Papageorgiou G.C., Murata N. The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving Photosystem II complex. Photosynth Res. 1995;44:243–252. doi: 10.1007/BF00048597. [DOI] [PubMed] [Google Scholar]
  52. Park S.M., Hong C.B. Class I small heat shock protein gives thermotolerance in tobacco. J. Plant Physiol. 2002;159:25–30. doi: 10.1078/0176-1617-00660. [DOI] [Google Scholar]
  53. Pike C.S., Grieve J., Badger M.R., Price G.D. Thermoprotective properties of small heat shock proteins from rice, tomato and Synechocystis sp. PCC6803 overexpressed in, and isolated from, Escherichia coli. Aust. J. Plant Physiol. 2001;28:1219–1229. [Google Scholar]
  54. Prandl R., Hinderhofer K., Eggers-Schumacher G., Schoffl F. HSF3, a new heat shock factor from Arabidopsis thaliana, derepresses the heat shock response and confers thermotolerance when overexpressed in transgenic plants. Mol. Gen. Genet. 1998;258:269–278. doi: 10.1007/s004380050731. [DOI] [PubMed] [Google Scholar]
  55. Queitsch C., Hong S.W., Vierling E., Lindquist S. Hsp101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell. 2000;12:479–492. doi: 10.1105/tpc.12.4.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Raviol H., Sadlish H., Rodriguez F., Mayer M.P., Bukau B. Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J. 2006;25:2510–2518. doi: 10.1038/sj.emboj.7601139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ritossa F.M. A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia. 1962;18:571–573. doi: 10.1007/BF02172188. [DOI] [Google Scholar]
  58. Sage R.F., Kubien D.S. The temperature response of C3 and C4 photosynthesis. Plant Cell Environ. 2007;30:1086–1106. doi: 10.1111/j.1365-3040.2007.01682.x. [DOI] [PubMed] [Google Scholar]
  59. Sakuma Y., Maruyama K., Quin F., Osakabe Y., Shinozaki K., Yamaguchi-Shinozaki K. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl Acad Sci USA. 2006;103:18822–18827. doi: 10.1073/pnas.0605639103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Salvucci M.E., DeRidder B.P., Portis A.R., Jr. Effect of activase level and isoform on the thermotolerance of photosynthesis in Arabidopsis. J. Expt. Bot. 2006;57:3793–3799. doi: 10.1093/jxb/erl140. [DOI] [PubMed] [Google Scholar]
  61. Sanchez Y., Lindquist S. HSP104 required for induced thermotolerance. Science. 1990;248:1112–1114. doi: 10.1126/science.2188365. [DOI] [PubMed] [Google Scholar]
  62. Sanmiya K., Suzuki K., Egawa Y., Shono M. Mitochondrial small heat-shock protein enhances thermotolerance in tobacco plants. FEBS Lett. 2004;557:265–268. doi: 10.1016/S0014-5793(03)01494-7. [DOI] [PubMed] [Google Scholar]
  63. Scharf K.D., Siddique M., Vierling E. The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins) Cell Stress Chap. 2001;6:225–237. doi: 10.1379/1466-1268(2001)006<0225:TEFOAT>2.0.CO;2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Schramm, F., Larkindale, J., Kiehlmann, E., Ganguli, A., Englich, G., Vierling, E., and Koskull-Doring, P. (2007). A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. (In press). [DOI] [PubMed]
  65. Shabtai S., Salts Y., Kaluzky G., Barg R. Improved yielding and reduced puffiness under extreme temperatures induced by fruit-specific expression of rolB in processing tomatoes. Theor Appl Genet. 2007;114:1203–1209. doi: 10.1007/s00122-007-0511-7. [DOI] [PubMed] [Google Scholar]
  66. Shi W.M., Muramoto Y., Ueda A., Takabe T. Cloning of peroxisomal ascorbate peroxidase gene from barley and enhanced thermotolerance by overexpressing in Arabidopsis thaliana. Gene. 2001;273:23–27. doi: 10.1016/S0378-1119(01)00566-2. [DOI] [PubMed] [Google Scholar]
  67. Singla, S.L., Pareek, A. and Grover, A. (1997). High temperature stress. In: Physiological Ecology of Plants. (Ed M.N.V. Prasad), John Wiley and Sons, pp. 101–127.
  68. Sohn S.O., Back K. Transgenic rice tolerant to high temperature with elevated contents of dienoic fatty acids. Biol. Plant. 2007;51(2):340–342. doi: 10.1007/s10535-007-0067-z. [DOI] [Google Scholar]
  69. Suzuki N., Rizhsky L., Liang H., Shuman J., Shulaev V., Mittler R. Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol. 2005;139:1313–1322. doi: 10.1104/pp.105.070110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Tang L., Kwon S.Y., Kim S.H., Kim J.S., Choi J.S., Cho K.Y., Sung C.K., Kwak S.S., Lee H.S. Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep. 2006;25:1380–1386. doi: 10.1007/s00299-006-0199-1. [DOI] [PubMed] [Google Scholar]
  71. Thomas P.G., Dominy P.J., Vigh L., Mansourian A.R., Quinn P.J., Williams W.P. Increased thermal stability of pigment-protein complexes of pea thylakoids following catalytic hydrogenation of membrane lipids. Biochim Biophys Acta. 1986;849:131–140. doi: 10.1016/0005-2728(86)90104-0. [DOI] [Google Scholar]
  72. Tissieres A., Mitchell H. K., Tracey U. M. Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J. Mol. Biol. 1974;84:389–398. doi: 10.1016/0022-2836(74)90447-1. [DOI] [PubMed] [Google Scholar]
  73. Tognetti V.B., Palatnik J.F., Fillat M.F., Melzer M., Hajirezaei M.R., Valle E.M., Carrillo N. Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broad-range stress tolerance. Plant Cell. 2006;18:2035–2050. doi: 10.1105/tpc.106.042424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Vierling E. The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991;42:579–620. doi: 10.1146/annurev.pp.42.060191.003051. [DOI] [Google Scholar]
  75. Vigh L., Horvath I., Maresca B., Harwood J.L. Can the stress protein response be controlled by ‘membrane-lipid therapy’? Trends Biochem. Sci. 2007;32:357–363. doi: 10.1016/j.tibs.2007.06.009. [DOI] [PubMed] [Google Scholar]
  76. Vigh L., Maresca B., Harwood J.L. Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem. Sci. 1998;23:369–374. doi: 10.1016/S0968-0004(98)01279-1. [DOI] [PubMed] [Google Scholar]
  77. Wahid A., Gelani S., Ashraf M., Foolad M.R. Heat tolerance in plants: an overview. Environ. Expt. Bot. 2007;61:199–223. doi: 10.1016/j.envexpbot.2007.05.011. [DOI] [Google Scholar]
  78. Wang W., Vincour B., Shoseyov O., Altman A. Role of plant heat shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 2004;9:244–252. doi: 10.1016/j.tplants.2004.03.006. [DOI] [PubMed] [Google Scholar]
  79. Wang W., Vinocur B., Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 2003;218:1–14. doi: 10.1007/s00425-003-1105-5. [DOI] [PubMed] [Google Scholar]
  80. Wu C. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 1995;11:441–469. doi: 10.1146/annurev.cb.11.110195.002301. [DOI] [PubMed] [Google Scholar]
  81. Yang J.Y., Sun Y., Sun A.Q., Yi S.Y., Qin J., Li M.H., Liu J. The involvement of chloroplast HSP100/ClpB in the acquired thermotolerance in tomato. Plant Mol. Biol. 2006;62:385–395. doi: 10.1007/s11103-006-9027-9. [DOI] [PubMed] [Google Scholar]
  82. Yang X., Liang Z., Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. Plant Physiol. 2005;138:2299–2309. doi: 10.1104/pp.105.063164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Yeh C.H., Chang P.L., Yeh K.W., Lin W.C., Chen Y.M., Lin C.Y. Expression of a gene encoding a 16.9-kDa heat-shock protein, Oshsp16.9. Escherichia coli enhances thermotolerance. Proc. Natl. Acad. Sci. USA. 1997;94:10967–10972. doi: 10.1073/pnas.94.20.10967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Yeh C.H., Chen Y.M., Lin C. Y. Functional regions of rice heat shock protein, Oshsp16.9, required for conferring thermotolerance in Escherichia coli. Plant Physiol. 2002;128:661–668. doi: 10.1104/pp.128.2.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Yokotani, N., Ichikawa, T., Kondou, Y., Matsui, M., Hirochika, H., Iwabuchi, M. and Oda, K. (2007). Expression of rice heat stress transcription factor OshsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta (in press) DOI 10.1007/s00425-007-0670-4 [DOI] [PubMed]
  86. Young L.S., Yeh C. H., Chen Y.M., Lin C. Y. Molecular characterization of Oryza sativa 16.9 kDa heat shock protein. Biochem. J. 1999;344:31–38. doi: 10.1042/0264-6021:3440031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Zhang C., Guy C.L. Co-immunoprecipitation of Hsp101 with cytosolic Hsc70. Plant Physiol. Biochem. 2005;43:13–18. doi: 10.1016/j.plaphy.2004.10.006. [DOI] [PubMed] [Google Scholar]
  88. Zhang M., Barg R., Yin M., Gueta-Dahan Y., Leikin-Frenkel A., Salts Y., Shabtai S., Ben-Hayyim G. Modulated fatty acid desaturation via overexpression of two distinct omega-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J. 2005;44:361–371. doi: 10.1111/j.1365-313X.2005.02536.x. [DOI] [PubMed] [Google Scholar]

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