Identification and characterization of high temperature stress responsive genes in bread wheat (Triticum aestivum L.) and their regulation at various stages of development

Plant Molecular Biology

Volumn 75, Issue 1, 2011, Pages 35-51

  Chauhan, Harsh ^a   Khurana, Neetika ^a   Tyagi, Akhilesh K ^a,b   Khurana, Jitendra P ^a   Khurana, Paramjit ^a  

^a UNIVERSITY OF DELHI   (India)

^b NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

Author keywords

Heat stress; HSF; HSPs; Subtractive hybridization; Transcriptome; Wheat

Indexed keywords

ABSCISIC ACID; COMPLEMENTARY DNA; PHYTOHORMONE; SODIUM CHLORIDE;

ACCLIMATIZATION; ARTICLE; CHEMISTRY; DNA MICROARRAY; DNA SEQUENCE; DRUG EFFECT; EXPRESSED SEQUENCE TAG; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; HEAT; MOLECULAR GENETICS; NORTHERN BLOTTING; PHYSIOLOGICAL STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; WHEAT;

ABSCISIC ACID; ACCLIMATIZATION; BLOTTING, NORTHERN; DNA, COMPLEMENTARY; EXPRESSED SEQUENCE TAGS; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; HOT TEMPERATURE; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT GROWTH REGULATORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; TIME FACTORS; TRITICUM;

TRITICUM AESTIVUM;

EID: 78650517548     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-010-9702-8     Document Type: Article

References (91)

1. Abiko M, Akibayashi K, Sakata T, Kimura M, Kihara M, Itoh K, Asamizu E, Sato S, Takahashi H, Higashitani A (2005) High-temperature induction of male sterility during barley (Hordeum vulgare L.) anther development is mediated by transcriptional inhibition. Sexual Plant Rep 18: 91-100.
2. Altenbach SB, Kothari KM (2004) Transcript profiling of genes expressed in endosperm tissue are altered by high temperature during wheat grain development. J Cer Sci 40: 115-126.
3. Altenbach SB, Kothari KM, Lieu D (2002) Environmental conditions during wheat grain development alter temporal regulation of major gluten protein genes. Cereal Chem 79: 279-285.
4. Altenbach SB, DuPont FM, Kothari KM, Chan R (2003) Temperature, water and fertilizer influence the timing of key events during grain development in a US spring wheat. J Cer Sci 37: 9-20.
5. Altenbach SB, Kothari KM, Tanaka CK, Hurkman WJ (2007) Genes encoding the PR-4 protein wheatwin are developmentally regulated in wheat grains and respond to high temperature during grainfill. Plant Sci 173: 135-143.
6. Altenbach SB, Kothari KM, Tanaka CK, Hurkman WJ (2008) Expression of 9-kDa non-specific lipid transfer protein genes in developing wheat grain is enhanced by high temperatures but not by post-anthesis fertilizer. J Cer Sci 47: 201-213.
7. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
8. Barnabas B, Jager K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31: 11-38.
9. Bennett MD, Leitch IJ (2005) Nuclear DNA amounts in angiosperms: progress, problems and prospects. Ann Bot 95: 45-90.
10. Boominathan P, Shukla R, Kumar A, Manna D, Negi D, Verma PK, Chattopadhyay D (2004) Long term transcript accumulation during the development of dehydration adaptation in Cicer arietinum. Plant Physiol 135: 1608-1620.
11. Busch W, Wunderlich M, Schoffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41: 1-14.
12. Chae K, Kieslich CA, Morikis D, Kim SC, Lord EM (2009) A gain-of-function mutation of Arabidopsis Lipid Transfer Protein 5 disturbs pollen tube tip growth and fertilization. Plant Cell 21: 3902-3914.
13. Chen F, Li Q, Sun L, He Z (2006) The rice 14-3-3 gene family and its involvement in responses to biotic and abiotic stress. DNA Res 13: 53-63.
14. Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signalling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38: 432-447.
15. Dat JF, Foyer CH, Scott IM (1998) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118: 1455-1461.
16. DeRocher AE, Vierling E (1994) Developmental control of small heat shock protein expression during pea seed maturation. Plant J 5: 93-102.
17. Dhaubhadel S, Chaudhary S, Dobinson KF, Krishna P (1999) Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Mol Biol 40: 333-342.
18. Dhaubhadel S, Browning KS, Gallie DR, Krishna P (2002) Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. Plant J 29: 681-691.
19. DuPont FM, Hurkman WJ, Vensel WH, Tanaka CK, Kothari KM, Chung OK, Altenbach SB (2006) Protein accumulation and composition in wheat grains: effects of mineral nutrients and high temperature. Europian J Agronomy 25: 96-107.
20. Dwivedi RS, Breiman A, Herman EM (2003) Differential distribution of the cognate and heat-stress-induced isoforms of high Mr cis-trans prolyl peptidyl isomerase (FKBP) in the cytoplasm and nucleoplasm. J Exp Bot 54: 2679-2689.
21. Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149: 7-13.
22. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14: 1675-1690.
23. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 Is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488.
24. Geisler M, Bailly A (2007) Tete-a-tete: the function of FKBPs in plant development. Trends Plant Sci 12: 465-473.
25. Gill BS, Appels R, Botha-Oberholster AM, Buell CR, Bennetzen JL, Chalhoub B, Chumley F, Dvorak J, Iwanaga M, Keller B, Li W, McCombie WR, Ogihara Y, Quetier F, Sasaki T (2004) A workshop report on wheat genome sequencing: International Genome Research on Wheat Consortium. Genetics 168: 1087-1096.
26. Gong M, Li YJ, Dai X, Tian M, Li ZG (1997) Involvement of calcium and calmodulin in the acquisition of heat-shock induced thermotolerance in maize. J Plant Physiol 150: 615-621.
27. 2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116: 429-437.
28. Heil M, Bostock RM (2002) Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Ann Bot 89: 503-512.
29. Huang B, Xu C (2008) Identification and characterization of proteins associated with plant tolerance to heat stress. J Int Plant Biol 50: 1230-1237.
30. Hurkman WJ, McCue KF, Altenbach SB, Korn A, Tanaka CK, Kothari KM, Johnson EL, Bechtel DB, Wilson JD, Anderson OD, DuPont FM (2003) Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm. Plant Sci 164: 873-881.
31. Hurkman WJ, Vensel WH, Tanaka CK, Whiteland L, Altenbach SB (2009) Effect of high temperature on albumin and globulin accumulation in the endosperm proteome of developing wheat grain. J Cer Sci 49: 12-23.
32. Hussain SS, Mudasser M (2007) Prospects for wheat production under changing climate in mountain areas of Pakistan- an econometric analysis. Agriculture Systems 94: 494-501.
33. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7: 106-111.
34. Johnson JC, Clarke BC, Bhave M (2001) Isolation and characterisation of cDNAs encoding protein disulphide isomerases and cyclophilins in wheat. J Cer Sci 34: 159-171.
35. Joshi AK, Mishra B, Chatrath R, Ferrara GO, Singh RP (2007) Wheat improvement in India: present status, emerging challenges and future prospects. Euphytica 157: 431-446.
36. Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225: 353-364.
37. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136: 4159-4168.
38. Khripach V, Zhabinskii V, de Groot A (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century. Ann Bot 86: 441-447.
39. Klueva NY, Maestri E, Marmiroli N, Nguyen HT (2001) Mechanisms of thermotolerance in crops. Food Products Press, Binghamton.
40. Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16: 681-687.
41. Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf K-D (2007) Complexity of heat stress response in plants. Curr Opin Plant Biol 10: 310-316.
42. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141.
43. Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22: 289-297.
44. Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96: 4718-4723.
45. Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Zhu G (2007) Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19: 3230-3241.
46. Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1, 5-bisphosphate Carboxylase/Oxygenase. Plant Physiol 120: 173-182.
47. Lee GJ, Pokala N, Vierling E (1995) Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270: 10432-10438.
48. Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16: 659-671.
49. Liu HT, Li B, Shang ZL, Li XZ, Mu RL, Sun DY, Zhou RG (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol 132: 1186-1195.
50. Liu L, Zhou Y, Zhou G, Ye R, Zhao L, Li X, Lin Y (2008) Identification of early senescence-associated genes in rice flag leaves. Plant Mol Biol 67: 37-55.
51. Lobell DB, Field CB (2007) Global scale climate-crop yield relationships and the impacts of recent warming. Environment Res Lett 2: 014002 (7 pp).
52. Ma K, Xiao J, Li X, Zhang Q, Lian X (2009) Sequence and expression analysis of the C3HC4-type RING finger gene family in rice. Gene 444: 33-45.
53. Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48: 667-681.
54. Majee M, Maitra S, Dastidar KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL (2004) A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice: molecular cloning, bacterial overexpression, characterization, and functional introgression into tobacco-conferring salt tolerance phenotype. J Biol Chem 279: 28539-28552.
55. Majoul T, Bancel E, Triboi E, Ben Hamida J, Branlard G (2004) Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from non-prolamins fraction. Proteomics 4: 505-513.
56. McDonald GK, Suttan BG, Ellison FW (1983) The effect of time of sowing on the grain yield of irrigated wheat in the Namoi Valley, New South Wales. Australian J Agri Res 34: 229-240.
57. Mosser DD, Kotzbauer PT, Sarge KD, Morimoto RI (1990) In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation. Proc Natl Acad Sci USA 87: 3748-3752.
58. Nagarajan S (2005) Can India produce enough wheat even by 2020? Curr Sci 89: 1467-1471.
59. Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6: 177-189.
60. Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9: 432.
61. Ramalingam J, Pathan MS, Feril O, Ross K, Ma XF, Mahmoud AA, Layton J, Rodriguez-Milla MA, Chikmawati T, Valliyodan B, Skinner R, Matthews DE, Gustafson JP, Nguyen HT (2006) Structural and functional analyses of the wheat genomes based on expressed sequence tags (ESTs) related to abiotic stresses. Genome 49: 1324-1340.
62. Rane J, Chauhan H (2002) Rate of grain growth in advanced wheat (Triticum aestivum) accession under late-sown environment. Indian J Agric Sci 72: 581-585.
63. Ristic Z, Momcilovic I, Bukovnik U, Prasad PV, Fu J, Deridder BP, Elthon TE, Mladenov N (2009) Rubisco activase and wheat productivity under heat-stress conditions. J Exp Bot 60: 4003-4014.
64. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683-1696.
65. Rosegrant MW, Cline SA (2003) Global food security: challenges and policies. Science 302: 1917-1919.
66. Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJM, Goloubinoff P (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21: 2829-2843.
67. Saini HS, Aspinall D (1982) Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Ann Bot 49: 835-846.
68. Saini HS, Sedgley M, Aspinall D (1984) Developmental anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Aust J Plant Physiol 11: 243-253.
69. Salvucci ME (2008) Association of Rubisco activase with chaperonin-60beta: a possible mechanism for protecting photosynthesis during heat stress. J Exp Bot 59: 1923-1933.
70. Salvucci ME, Crafts-Brandner SJ (2004a) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120: 179-186.
71. Salvucci ME, Crafts-Brandner SJ (2004b) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiol 134: 1460-1470.
72. Salvucci ME, Ogren WL (1996) The mechanism of Rubisco activase: insights from studies of the properties and structure of the enzyme. Photosynth Res 47: 1-11.
73. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbour Press, New York.
74. Sayre KD, Rajaram S, Fischer RA (1997) Yield potential progress in short bread wheats in northwest Mexico. Crop Sci 37: 36-42.
75. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1, 300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13: 61-72.
76. Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression pattern of around 7, 000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2: 282-291.
77. Shinozaki K, Dennis ES (2003) Cell signalling and gene regulation: global analyses of signal transduction and gene expression profiles. Curr Opin Plant Biol 6: 405-409.
78. Sinclair TR, Jamieson PD (2006) Grain number, wheat yield and bottling beer: an analysis. Field Crops Res 98: 60-67.
79. Singh G, Kumar S, Singh P (2003) A quick method to isolate RNA from wheat and other carbohydrate-rich seeds. Plant Mol Biol Rep 21: 93a-93f.
80. Stone PJ (2001) The effect of heat stress on cereal yield and quality. Food Products Press, Binghamton.
81. Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137: 13-30.
82. Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8: 125.
83. Takeoka Y, Hirori K, Kitano H, Wada T (1991) Pistil hyperplasia in rice spikelets as affected by heat-stress. Sexual Plant Rep 4: 39-43.
84. Trevino MB, Ma OC (1998) Three drought-responsive members of the nonspecific lipid-transfer protein gene family in Lycopersicon pennellii show different developmental patterns of expression. Plant Physiol 116: 1461-1468.
85. Wardlaw IF, Blumenthal CS, Larroque O, Wrigley CW (2002) Contrasting effect of chronic heat stress and heat shock on kernel weight and flour quality in wheat. Funct Plant Biol 29: 25-34.
86. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57: 781-803.
87. Yamakawa H, Hirose T, Kuroda M, Yamaguchi T (2007) Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiol 144: 258-277.
88. Yan J, He C, Wang J, Mao Z, Holaday SA, Allen RD, Zhang H (2004) Overexpression of the Arabidopsis 14-3-3 protein GF14 lambda in cotton leads to a "stay-green" phenotype and improves stress tolerance under moderate drought conditions. Plant Cell Physiol 45: 1007-1014.
89. Zhang Y, Mian MA, Chekhovskiy K, So S, Kupfer D, Lai H, Roe BA (2005) Differential gene expression in Festuca under heat stress conditions. J Exp Bot 56: 897-907.
90. Zhang X, Wollenweber B, Jiang D, Liu F, Zhao J (2008) Water deficits and heat shock effects on photosynthesis of a transgenic Arabidopsis thaliana constitutively expressing ABP9, a bZIP transcription factor. J Exp Bot 59: 839-848.
91. Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4: 401-406.