Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Mittal, Dheeraj ^a   Madhyastha, Dinesh A ^b   Grover, Anil ^a  

^a UNIVERSITY OF DELHI   (India)

^b BIOBASE Databases India Private Limited   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CALCIUM; CARRIER PROTEIN; DESSICATION RESPONSE ELEMENT BINDING PROTEIN; HEAT SHOCK PROTEIN; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; SCAVENGER; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; MESSENGER RNA; MICRORNA; TRANSCRIPTOME;

ARTICLE; BINDING SITE; CALCIUM SIGNALING; COLD STRESS; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HEAT SHOCK TRANSCRIPTION FACTOR GENE; HEAT STRESS; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PLANT GENE; POLYMERASE CHAIN REACTION; PROMOTER REGION; REGULON; RICE; SEEDLING; SIGNAL TRANSDUCTION; TEMPERATURE STRESS; UPREGULATION; BIOLOGICAL MODEL; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; ORYZA; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENOME; TEMPERATURE;

CLUSTER ANALYSIS; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENES, PLANT; GENOME, PLANT; HEAT-SHOCK RESPONSE; MICRORNAS; MODELS, GENETIC; ORYZA; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; REGULON; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TEMPERATURE; TRANSCRIPTION FACTORS; TRANSCRIPTOME; UP-REGULATION;

EID: 84864015961     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040899     Document Type: Article

References (91)

1. Timperio AM, Egidi MG, Zolla L, (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71: 391-411.
2. Sanghera GS, Wani SH, Hussain W, Singh NB, (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12(1): 30-43.
3. Yoshida S, Satake T, Mackill DS, (1981) High temperature stress in rice. IRRI research paper series. No 67, International Rice Research Institute, Los Banos, Philippines pp. 1-15.
4. Slafer GA, Rawson HM, (1994) Sensitivity of wheat phasic development to major environmental factors: A re-examination of some assumptions by physiologists and modelers. Australian Journal of Plant Physiology 21: 393-426.
5. Satake T, Yoshida S, (1978) High temperature induced sterility in indica rices at flowering. Japanese Journal of Crop Sceince 47: 6-17.
6. Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, et al. (2004) Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci U S A 101: 9971-9975.
7. Yokoi S, Hogashi S, Kishtiani S, Murata N, Toriyama K, (1998) Identification of the cDNA for Arabidopsis glycerol-3-phosphate acyltransferase (GPAT) confers unsaturation of fatty acids and chilling tolerance of photosynthesis on rice. Molecular Breeding 4: 269-275.
8. Sakamoto A, Alia, Murata N, (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38: 1011-1019.
9. Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, et al. (2000) Enhanced tolerance to salt stress in transgenic rice that overexpress chloroplast glutamine synthetase. Plant Mol Biol 43: 103-111.
10. Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K, (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23: 319-327.
11. Katiyar-Agarwal S, Agarwal M, Grover A, (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51: 677-686.
12. Singh A, Grover A, (2008) Genetic engineering for heat tolerance in plants. Physiol Mol Biol Plants 14: 155-166.
13. Mittler R, (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11: 15-19.
14. Moller IM, (2001) Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561-591.
15. Mittler R, (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410.
16. Miller G, Shulaev V, Mittler R, (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133: 481-489.
17. Foyer CH, Noctor G, (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11: 861-905.
18. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F, (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498.
19. Davletova S, Schlauch K, Coutu J, Mittler R, (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139: 847-856.
20. Miller G, Mittler R, (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98: 279-288.
21. Volkov RA, Panchuk II, Mullineaux PM, Schoffl F, (2006) Heat stress-induced H(2)O(2) is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61: 733-746.
22. Wahid A, Gelani S, Ashraf M, Foolad MR, (2007) Heat tolerance in plants: An overview. Experimental and Experimental Botany 61: 199-223.
23. Suzuki N, Koussevitzky S, Mittler R, Miller G, (2011) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ DOI:10.1111/j.1365-3040.2011.02336.x.
24. Locato V, Gadaleta C, De Gara L De Pinto MC, (2008) Production of reactive species and modulation of antioxidant network in response to heat shock: a critical balance for cell fate. Plant Cell Environ 31: 1606-1619.
25. Chinnusamy V, Zhu J, Zhu JK, (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12: 444-451.
26. Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, et al. (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genomics 8: 175.
27. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, et al. (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9: 436-442.
28. Chinnusamy V, Schumaker K, Zhu JK, (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55: 225-236.
29. Sunkar R, Chinnusamy V, Zhu J, Zhu JK, (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12: 301-309.
30. Nakashima K, Ito Y, Yamaguchi-Shinozaki K, (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149: 88-95.
31. Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A, (2009) Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem 47: 785-795.
32. Kant P, Gordon M, Kant S, Zolla G, Davydov O, et al. (2008) Functional-genomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses. Plant Cell Environ 31: 697-714.
33. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, et al. (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133: 1755-1767.
34. Chao DY, Luo YH, Shi M, Luo D, Lin HX, (2005) Salt-responsive genes in rice revealed by cDNA microarray analysis. Cell Res 15: 796-810.
35. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, et al. (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139: 822-835.
36. Walia H, Wilson C, Zeng L, Ismail AM, Condamine P, et al. (2007) Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant Mol Biol 63: 609-623.
37. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, et al. (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8: 242.
38. Zhou J, Wang X, Jiao Y, Qin Y, Liu X, et al. (2007) Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol Biol 63: 591-608.
39. Wang D, Pan Y, Zhao X, Zhu L, Fu B, et al. (2011) Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics 12: 149.
40. Sabehat A, Lurie S, Weiss D, (1998) Expression of small heat shock proteins at low temperatures: a possible role in protecting against chilling injuries. Plant Physiol 117: 651-658.
41. Djanaguiraman M, Annie Sheeba J, Shnaker AK, Durga Devi D, Bangarusamy U, (2006) Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil 284: 363-373.
42. Goswami A, Banerjee R, Raha S, (2010) Mechanism of plant adaptation/memory in rice seedling under arsenic and heat stress: expression of heats-shock protein gene HSP70. AoB Plants DOI:10.1093/aobpl/plq023.
43. Ella ES, Dionisio-Sese ML, Ismail AM, (2011) Seed pretreatment in rice reduces damage, enhances carbohydrate mobilization and improves emergence and seedling establishment under flooded conditions. AoB Plants DOI:10.1093/aobpla/plr007.
44. Yoshida S, Forno DA, Cook JH Gomez KA, (1976) Laboratory Manual for Physiological Studies of Rice. 3rd ed. International Rice Research Institute, Los Banos, Philippines.
45. Quan LJ, Zhang B, Shi WW. Li HY, (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50: 2-18.
46. Kel AE, Gössling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, et al. (2003) MATCH™: a tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31: 3576-3579.
47. Kel A, Konovalova T, Waleev T, Cheremushkin E, Kel-Margoulis O, et al. (2006a) Composite Module Analyst: a fitness-based tool for identification of transcription factor binding site combinations. Bioinformatics 22: 1190-1197.
48. Kel A, Voss N, Jauregui R, Kel-Margoulis O, Wingender E, (2006b) Beyond microarrays: Find key transcription factors controlling signal transduction pathways. BMC Bioinformatics.
49. Waleev T, Shtokalo D, Konovalova T, Voss N, Cheremushkin E, et al. (2006) Composite Module Analyst: identification of transcription factor binding site combinations using genetic algorithm. Nucleic Acids Res 34: W541-545.
50. Paragh G, Schling P, Ugocsai P, Kel AE, Liebisch G, et al. (2008) Novel sphingolipid derivatives promote keratinocyte differentiation. Exp Dermatol 17: 1004-1016.
51. Archak S, Nagaraju J, (2007) Computational prediction of rice (Oryza sativa) miRNA targets. Genomics Proteomics Bioinformatics 5: 196-206.
52. Riano-Pachon DM, Ruzicic S, Dreyer I, Mueller-Roeber B, (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinformatics 8: 42.
53. Wojciak JM, Clubb RT, (2001) Finding the function buried in SAND. Nat Struct Biol 8: 568-570.
54. Singh A, Singh U, Mittal D, Grover A, (2010) Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC Genomics 11: 95.
55. 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.
56. Hu WH, Hu GC, Han B, (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176: 583-590.
57. Singh A, Mittal D, Lavania D, Agarwal M, Mishra RC, Grover A, (2011) OsHsfA2c and OsHsfB4b are involved in the transcriptional regulation of cytoplasmic OsClpB (Hsp100) gene in rice (Oryza sativa L.). Cell Stress and Chaperones DOI:10.1007/s12192-011-0303-5.
58. 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.
59. Lee BH, Won SH, Lee HS, Miyao M, Chung WI, et al. (2000) Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 245: 283-290.
60. Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N, (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27: 407-415.
61. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, et al. (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129: 661-677.
62. Liu D, Zhang X, Cheng Y, Takano T, Liu S, (2006) rHsp90 gene expression in response to several environmental stresses in rice (Oryza sativa L.). Plant Physiol Biochem 44: 380-386.
63. Singh A, Grover A, (2010) Plant Hsp100/ClpB-like proteins: poorly-analyzed cousins of yeast ClpB machine. Plant Mol Biol 74: 395-404.
64. Wang W, Vinocur B, Shoseyov O, Altman A, (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9: 244-252.
65. Banti V, Loreti E, Novi G, Santaniello A, Alpi A, et al. (2008) Heat acclimation and cross-tolerance against anoxia in Arabidopsis. Plant Cell Environ 31: 1029-1037.
66. Colinet H, Lee SF, Hoffmann A, (2010) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J 277: 174-185.
67. Neta-Sharir I, Isaacson T, Lurie S, Weiss D, (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17: 1829-1838.
68. Ye H, Du H, Tang N, Li X, Xiong L, (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71: 291-305.
69. Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, et al. (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci U S A 102: 10736-10741.
70. Mishra NS, Tuteja R. Tuteja N, (2006) Signaling through MAP kinase networks in plants. Arch Biochem Biophys 452: 55-68.
71. Xuan Y, Zhou S, Wang L, Cheng Y, Zhao L, (2010) Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiol 153: 1895-1906.
72. Zhang W, Zhou RG, Gao YJ, Zheng SZ, Xu P, et al. (2009) Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. Plant Physiol 149: 1773-1784.
73. Nishizawa A, Yabuta Y, Shigeoka S, (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147: 1251-1263.
74. 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.
75. Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schoffl F, (2004) Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 136: 3148-3158.
76. Marsoni M, Cantara C, De Pinto MC, Gadaleta C, De Gara L, et al. (2010) Exploring the soluble proteome of Tobacco Bright Yellow-2 cells at the switch towards different cell fates in response to heat shocks. Plant Cell Environ 33: 1161-1175.
77. Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, et al. (2010) Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci U S A 107: 8569-8574.
78. Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, et al. (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19: 408-413.
79. Carranco R, Espinosa JM, Prieto-Dapena P, Almoguera C, Jordano J, (2010) Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity. Proc Natl Acad Sci U S A 107: 21908-21913.
80. Hughes JD, Estep PW, Tavazoie S Church GM, (2000) Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J Mol Biol 296: 1205-1214.
81. Bussemaker HJ, Li H, Siggia ED, (2001) Regulatory element detection using correlation with expression. Nat Genet 27: 167-171.
82. Foat BC, Houshmandi SS, Olivas WM, Bussemaker HJ, (2005) Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. Proc Natl Acad Sci U S A 102: 17675-17680.
83. Elemento O, Slonim N, Tavazoie S, (2007) A universal framework for regulatory element discovery across all genomes and data types. Mol Cell 28: 337-350.
84. McGrath PT, Lee H, Zhang L, Iniesta AA, Hottes AK, et al. (2007) High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat Biotechnol 25: 584-592.
85. Haralampidis K, Milioni D, Rigas S, Hatzopoulos P, (2002) Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol 129: 1138-1149.
86. He L, Gao Z, Li R, (2009) Pretreatment of seed with H2O2 enhances drought tolerance of wheat (Triticum aestivum L.) seedlings. Af. J. Biotechnol 8(22): 6151-6157.
87. Wahid A, Sehar S, Perveen M, Gelani S, Basra SMA, Farooq M, (2008) Seed pretreatment with hydrogen peroxide improves heat tolerance in maize at germination and seedling growth stages. Seed Science and Technology 36(3): 633-645.
88. Pucciariello C, Banti V, Perata P, (2012) ROS signaling as common element in low oxygen and heat stresses. Plant Physiol Biochem DOI:10.1026/J.plaphy.2012.02.016.
89. Petrov VD, Breusegem FV, (2012) Hydrogen peroxide - a central hub for information in plant cells. AoB Plants DOI:10.1093/aobpla/pl5014.
90. Mahalingam R, Fedroff N, (2003) Stress response, cell death and signaling: the many facets of reactive oxygen species. Physiol Plant 119: 56-68.
91. Agarwal S, Sairam RK, Srivastava GC, Tyagi A, Meena RC, (2005) Role of ABA, salicylic acid, calcium and hydrogen peroxide on antioxidant enzyme induction in wheat seedlings. Plant Sci (169): 559-570.