Coexpression network analysis associated with call of rice seedlings for encountering heat stress

Plant Molecular Biology

Volumn 84, Issue 1-2, 2014, Pages 125-143

  Sarkar, Neelam K ^a   Kim, Yeon Ki ^b   Grover, Anil ^a  

^a UNIVERSITY OF DELHI   (India)

^b Myong Ji University   (South Korea)

Author keywords

Coexpression network; Early events; Heat stress; Microarray; Recovery; Rice

Indexed keywords

TRANSCRIPTOME; VEGETABLE PROTEIN;

ARTICLE; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; HEAT; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RICE; SIGNAL TRANSDUCTION;

CLUSTER ANALYSIS; GENE EXPRESSION REGULATION, PLANT; HOT TEMPERATURE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORYZA SATIVA; PLANT PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84888353325     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-013-0123-3     Document Type: Article

References (88)

1. Agarwal M, Sahi C, Katiyar-Agarwal S, Agarwal S, Young T, Gallie DR, Sharma VM, Ganesan K, Grover A (2003) Molecular characterization of rice hsp101: complementation of yeast hsp104 mutation by disaggregation of protein granules and differential expression in indica and japonica rice types. Plant Mol Biol 51: 543-553.
2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25: 25-29.
3. Aviezer-Hagai K, Skovorodnikova J, Galigniana M, Farchi-Pisanty O, Maayan E, Bocovza S, Efrat Y, von Koskull-Doring P, Ohad N, Breiman A (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol Biol 63: 237-255.
4. 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.
5. Charng YY, Liu HC, Liu NY, Hsu FC, Ko SS (2006) Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol 140: 1297-1305.
6. Chen H, Hwang JE, Lim CJ, Kim DY, Lee SY, Lim CO (2010) Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem Biophys Res Commun 401: 238-244.
7. Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genomics 8: 175.
8. Evrard A, Kumar M, Lecourieux D, Lucks J, von Koskull-Doring P, Hirt H (2013) Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1: e59.
9. Fernandes J, Morrow DJ, Casati P, Walbot V (2008) Distinctive transcriptome responses to adverse environmental conditions in Zea mays L. Plant Biotechnol J 6: 782-798.
10. Ficklin SP, Luo F, Feltus FA (2010) The association of multiple interacting genes with specific phenotypes in rice using gene coexpression networks. Plant Physiol 154: 13-24.
11. Gammulla CG, Pascovici D, Atwell BJ, Haynes PA (2010) Differential metabolic response of cultured rice (Oryza sativa) cells exposed to high- and low-temperature stress. Proteomics 10: 3001-3019.
12. Gao H, Brandizzi F, Benning C, Larkin RM (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA 105: 16398-16403.
13. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99: 15898-15903.
14. Guertin MJ, Lis JT (2010) Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6: e1001114.
15. Hahn JS, Hu Z, Thiele DJ, Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24: 5249-5256.
16. Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23: 741-755.
17. Hayashi S, Wakasa Y, Takahashi H, Kawakatsu T, Takaiwa F (2011) Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice. Plant J 69: 946-956.
18. Hu W, Hu G, 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.
19. Jung K-H, Ko H-J, Nguyen MX, Kim S-R, Ronald P, An G (2012) Genome-wide identification and analysis of early heat stress responsive genes in rice. J Plant Biol 55: 458-468.
20. 2+ dependent protein kinases and their substrate HsfB2a are differently involved in the heat response signaling pathway in Arabidopsis. Plant Biotechnol 27: 470-473.
21. Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51: 677-686.
22. Keunen E, Peshev D, Vangronsveld J, W VDE, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36: 1242-1255.
23. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19: 1065-1080.
24. Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147: 381-390.
25. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97: 2940-2945.
26. Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146: 748-761.
27. Lee TH, Kim YK, Pham TT, Song SI, Kim JK, Kang KY, An G, Jung KH, Galbraith DW, Kim M, Yoon UH, Nahm BH (2009) RiceArrayNet: a database for correlating gene expression from transcriptome profiling, and its application to the analysis of coexpressed genes in rice. Plant Physiol 151: 16-33.
28. Lee I, Seo YS, Coltrane D, Hwang S, Oh T, Marcotte EM, Ronald PC (2011) Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc Natl Acad Sci USA 108: 18548-18553.
29. Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2010) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnol J 9: 315-327.
30. Less H, Galili G (2008) Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol 147: 316-330.
31. 2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant Cell Physiol 45: 627-634.
32. Li S, Zhou X, Chen L, Huang W, Yu D (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol Cells 29: 475-483.
33. Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233: 1237-1252.
34. Li CR, Liang DD, Li J, Duan YB, Li H, Yang YC, Qin RY, Li L, Wei PC, Yang JB (2013) Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice alternative oxidase 1 genes. Plant, Cell Environ 36: 775-788.
35. Liu HT, Li GL, Chang H, Sun DY, Zhou RG, Li B (2007a) Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant, Cell Environ 30: 156-164.
36. Liu JX, Srivastava R, Che P, Howell SH (2007b) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19: 4111-4119.
37. Liu HT, Gao F, Li GL, Han JL, Liu DL, Sun DY, Zhou RG (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J 55: 760-773.
38. Liu J, Sun N, Liu M, Du B, Wang X, Qi X (2013) An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiol 162: 512-521.
39. Lu SJ, Yang ZT, Sun L, Song ZT, Liu JX (2012) Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Mol Plant 212: 504-514.
40. Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Genet Genomics 283: 185-196.
41. Matsuura H, Ishibashi Y, Shinmyo A, Kanaya S, Kato K (2010) Genome-wide analyses of early translational responses to elevated temperature and high salinity in Arabidopsis thaliana. Plant Cell Physiol 51: 448-462.
42. Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90. 1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59: 387-399.
43. Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98: 279-288.
44. Mishkind M, Vermeer JE, Darwish E, Munnik T (2009) Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J 60: 10-21.
45. Mittal D, Madhyastha DA, Grover A (2012) Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS ONE 7: e40899.
46. Morris RT, O'Connor TR, Wyrick JJ (2008) Osiris: an integrated promoter database for Oryza sativa L. Bioinformatics 24: 2915-2917.
47. Murakami Y, Toriyama K (2008) Enhanced high temperature tolerance in transgenic rice seedlings with elevated levels of alternative oxidase, OsAOX1a. Plant Biotechnol 25: 361-364.
48. Mutwil M, Klie S, Tohge T, Giorgi FM, Wilkins O, Campbell MM, Fernie AR, Usadel B, Nikoloski Z, Persson S (2011) PlaNet: combined sequence and expression comparisons across plant networks derived from seven species. Plant Cell 23: 895-910.
49. Ning J, Liu S, Hu H, Xiong L (2008) Systematic analysis of NPK1-like genes in rice reveals a stress-inducible gene cluster co-localized with a quantitative trait locus of drought resistance. Mol Genet Genomics 280: 535-546.
50. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138: 341-351.
51. Park SH, Chung PJ, Juntawong P, Bailey-Serres J, Kim YS, Jung H, Bang SW, Kim YK, Do Choi Y, Kim JK (2012) Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice. Plant Physiol 159: 1111-1124.
52. Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA 101: 9971-9975.
53. Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50: 54-69.
54. 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.
55. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (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.
56. Reddy AS, Shad Ali G (2011) Plant serine/arginine-rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses. Wiley Interdiscip Rev RNA 2: 875-889.
57. Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, 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.
58. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103: 18822-18827.
59. Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10: 393.
60. Sarkar NK, Kundnani P, Grover A (2013a) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18: 427-437.
61. Sarkar NK, Thapar U, Kundnani P, Panwar P, Grover A (2013b) Functional relevance of J-protein family of rice (Oryza sativa). Cell Stress Chaperones 18: 321-331.
62. Sato Y, Namiki N, Takehisa H, Kamatsuki K, Minami H, Ikawa H, Ohyanagi H, Sugimoto K, Itoh J, Antonio BA, Nagamura Y (2013) RiceFREND: a platform for retrieving coexpressed gene networks in rice. Nucleic Acids Res 41: D1214-D1221.
63. Schramm F, Larkindale J, Kiehlmann E, Ganguli A, Englich G, Vierling E, von Koskull-Doring P (2008) A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J 53: 264-274.
64. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
65. Shi W, Muthurajan R, Rahman H, Selvam J, Peng S, Zou Y, Jagadish KS (2013) Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytol 197: 825-837.
66. Shim D, Hwang JU, Lee J, Lee S, Choi Y, An G, Martinoia E, Lee Y (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21: 4031-4043.
67. Singh A, Singh U, Mittal D, Grover A (2010) Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC Genomics 11: 95.
68. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
69. Sugio A, Dreos R, Aparicio F, Maule AJ (2009) The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell 21: 642-654.
70. Suri SS, Dhindsa RS (2008) A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant, Cell Environ 31: 218-226.
71. Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R (2008) The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283: 9269-9275.
72. Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R (2011) Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 66: 844-851.
73. Takahashi H, Kawakatsu T, Wakasa Y, Hayashi S, Takaiwa F (2012) A rice transmembrane bZIP transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response. Plant Cell Physiol 53: 144-153.
74. Ueda K, Matsuura H, Yamaguchi M, Demura T, Kato K (2012) Genome-wide analyses of changes in translation state caused by elevated temperature in Oryza sativa. Plant Cell Physiol 53: 1481-1491.
75. 2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61: 733-746.
76. Wang D, Pan Y, Zhao X, Zhu L, Fu B, Li Z (2011) Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics 12: 149.
77. Wu WS, Li WH (2008) Identifying gene regulatory modules of heat shock response in yeast. BMC Genomics 9: 439.
78. Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28: 21-30.
79. Yamakawa H, Hakata M (2010) Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant Cell Physiol 51: 795-809.
80. Yan JJ, Zhang YB, Ding Y (2012) Binding mechanism between Hsp90 and Sgt1 explored by homology modeling and molecular dynamics simulations in rice. J Mol Model 18: 4665-4673.
81. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30: e15.
82. Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. J Plant Physiol 167: 959-966.
83. Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227: 957-967.
84. You J, Zong W, Li X, Ning J, Hu H, Xiao J, Xiong L (2013) The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64: 569-583.
85. Yun KY, Park MR, Mohanty B, Herath V, Xu F, Mauleon R, Wijaya E, Bajic VB, Bruskiewich R, de Los Reyes BG (2010) Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol 10: 16.
86. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4: R28.
87. Zhang X, Li J, Liu A, Zou J, Zhou X, Xiang J, Rerksiri W, Peng Y, Xiong X, Chen X (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS ONE 7: e49652.
88. Zou J, Liu C, Chen X (2011) Proteomics of rice in response to heat stress and advances in genetic engineering for heat tolerance in rice. Plant Cell Rep 30: 2155-2165.