Genome-wide transcriptome analysis during anthesis reveals new insights into the molecular basis of heat stress responses in tolerant and sensitive rice varieties

Plant and Cell Physiology

Volumn 57, Issue 1, 2016, Pages 57-68

  González Schain, Nahuel ^a,d   Dreni, Ludovico ^a,e   Lawas, Lovely M F ^b,f   Galbiati, Massimo ^a   Colombo, Lucia ^a   Heuer, Sigrid ^c   Jagadish, Krishna S V ^b,g   Kater, Martin M ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

^c Australian Centre for Plant Functional Genomics   (Australia)

^d UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^e SHANGHAI JIAO TONG UNIVERSITY   (China)

^f MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^g KANSAS STATE UNIVERSITY   (United States)

Author keywords

Anthesis; Heat stress; Pollen; Rice; RNA seq; Spikelet fertility

Indexed keywords

HEAT SHOCK PROTEIN; PLANT PROTEIN;

FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; HEAT SHOCK RESPONSE; METABOLISM; ORYZA; PHYSIOLOGY; SEQUENCE ANALYSIS;

FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE ONTOLOGY; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; ORYZA; PLANT PROTEINS; SEQUENCE ANALYSIS, RNA;

EID: 85032068842     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcv174     Document Type: Article

References (48)

1. Anderson, P.K., Cunningham, A.A., Patel, N.G., Morales, F.J., Epstein, P.R. and Daszak, P. (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19: 535-544.
2. Bahuguna, R.N., Jha, J., Pal, M., Shah, D., Lawas, L.M., Khetarpal, S., et al. (2014) Physiological and biochemical characterization of NERICA-L-44: a novel source of heat tolerance at the vegetative and reproductive stages in rice. Physiol. Plant. 154: 543-559.
3. Bakshi, M. and Oelmüller, R. (2014) WRKY transcription factors: Jack of many trades in plants. Plant Signal. Behav. 9: e27700.
4. Blatch, G.L. (2010) Networking of Chaperones by Co-chaperones. Springer Science & Business Media.
5. Chauhan, H., Khurana, N., Agarwal, P. and Khurana, P. (2011) Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Mol. Genet. Genomics 286: 171-187.
6. Cho, J. (1956) Double fertilization in Oryza sativa L. and development of the endosperm with special reference to the aleurone layer. Bull. Natl. Inst. Agric. Sci. 6: 61-101.
7. El-kereamy, A., Bi, Y.M., Ranathunge, K., Beatty, P.H., Good, A.G. and Rothstein, S.J. (2012) The Rice R2R3-MYB transcription factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism. PLoS One 7: e52030.
8. Endo, M., Tsuchiya, T., Hamada, K., Kawamura, S., Yano, K., Ohshima, M., et al. (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol. 50: 1911-1922.
9. Fu, Z.Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., et al. (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486: 228-232.
10. Fukuoka M., Yoshimoto, M. and Hasegawa, T. (2012) MINCER: a novel instrument for monitoring the micrometeorology of rice canopies. J. Agric. Meteorol. 68: 135-147.
11. Horváth, E., Szalai, G. and Janda, T. (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J. Plant Growth Regul. 26: 290-300.
12. Hu, W., Hu, G. and 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.
13. Itoh, J.I., Nonomura, K.I., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., et al. (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol. 46: 23-47.
14. Jagadish, K.S., Craufurd, P., Shi, W. and Oane, R. (2013) A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa L.). Funct. Plant Biol. 41: 48-55.
15. Jagadish, S.V.K., Craufurd, P.Q. and Wheeler, T.R. (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). J. Exp. Bot. 58: 1627-1635.
16. Jagadish, S.V.K., Craufurd, P.Q. and Wheeler, T.R. (2008) Phenotyping parents of mapping populations of rice for heat tolerance during anthesis. Crop Sci. 48: 1140-1146.
17. Jagadish, S.V.K., Murty, M.V.R. and Quick, W.P. (2014) Rice responses to rising temperatures - challenges, perspectives and future directions. Plant Cell Environ. 38: 1686-1698.
18. Jagadish, S.V.K., Muthurajan, R., Oane, R., Wheeler, T.R., Heuer, S., Bennett, J., et al. (2010) Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J. Exp. Bot. 61: 143-156.
19. Jin, G.H., Gho, H.J. and Jung, K.H. (2013) A systematic view of rice heat shock transcription factor family using phylogenomic analysis. J. Plant Physiol. 170: 321-329.
20. Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., et al. (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136: 4159-4168.
21. Khush, G.S. (2005) What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol. Biol. 59: 1-6.
22. Krishnaswamy, S., Verma, S., Rahman, M.H. and Kav, N.N. (2011). Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol. Biol. 75: 107-127.
23. Lawas, L.M.F., Oane, R. and Jagadish, S.V.K. (2013) Spikelet sterility and in vivo pollen germination and tube growth under hightemperature stress in rice. PrometheusWiki 19 May 2013 Web. 22 July 2015.
24. Li, X., Lawas, L.M., Malo, R., Glaubitz, U., Erban, A., Mauleon, R., et al. (2015) Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress. Plant Cell Environ. 38: 2171-2192.
25. Matsui, T., Namuco, O.S., Ziska, L.H. and Horie, T. (1997) Effects of high temperature and CO2 concentration on spikelet sterility in indica rice. Field Crops Res. 51: 213-219.
26. Matsui, T., Omasa, K. and Horie, T. (2001) The difference in sterility due to high temperatures during the flowering period among japonica-rice varieties. Plant Prod. Sci. 4: 90-93.
27. Mayer, R.R., Cherry, J.H. and Rhodes, D. (1990) Effects of heat shock on amino acid metabolism of cowpea cells. Plant Physiol. 94: 796-810.
28. Meiri, D. and 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.
29. Meiri, D., Tazat, K., Cohen-Peer, R., Farchi-Pisanty, O., Aviezer-Hagai, K., Avni, A., et al. (2010) Involvement of Arabidopsis ROF2 (FKBP65) in thermotolerance. Plant Mol. Biol. 72: 191-203.
30. Mittal, D., Madhyastha, D.A. and 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.
31. Prasad, P.V.V., Boote, K.J., Allen, L.H., Sheehy, J.E. and Thomas, J.M.G. (2006) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Res. 95: 398-411.
32. Qiu, Y.P. and Yu, D.Q. (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ. Exp. Bot. 65: 35-47.
33. Rang, Z.W., Jagadish, S.V.K., Zhou, Q.M., Craufurd, P.Q. and Heuer, S. (2011) Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environ. Exp. Bot. 70: 58-65.
34. Russell, S.D., Gou, X., Wong, C.E., Wang, X., Yuan, T., Wei, X., et al. (2012) Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage. New Phytol. 195: 560-573.
35. Shah, F., Huang, J., Cui, K., Nie, L., Shah, T., Chen, C., et al. (2011) Impact of high-temperature stress on rice plant and its traits related to tolerance. J. Agric. Sci. 149: 545-556.
36. Shimono, M., Sugano, S., Nakayama, A., Jiang, C.J., Ono, K., Toki, S., et al. (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19: 2064-2076.
37. Spurgeon, S.L., Jones, R.C. and Ramakrishnan, R. (2008) High throughput gene expression measurement with real time PCR in a microfluidic dynamic array. PLoS One 3: e1662.
38. Tao, Z., Kou, Y.J., Liu, H.B., Li, X.H., Xiao, J.H. and Wang, S.P. (2011) OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J. Exp. Bot. 62: 4863-4874.
39. The 3,000 rice genomes project (2014) The 3,000 rice genomes project. GigaScience 3: 7.
40. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37: 914-939.
41. Vikram, P., Swamy, B.M., Dixit, S., Ahmed, H.U., Cruz, M.T.S., Singh, A.K., et al. (2011) qDTY1.1, a major QTL for rice grain yield under reproductive- stage drought stress with a consistent effect in multiple elite genetic backgrounds. BMC Genet. 12: 89.
42. Wheeler, T. and von Braun, J. (2013) Climate change impacts on global food security. Science 341: 508-513.
43. Xiong, H., Li, J., Liu, P., Duan, J., Zhao, Y., Guo, X., et al. (2014) Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS One 9: e92913.
44. Yang, A., Dai, X.Y. and Zhang, W.H. (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J. Exp. Bot. 63: 2541-2556.
45. Ye, C., Argayoso, M.A., Redoña, E.D., Sierra, S.N., Laza, M.A., Dilla, C.J., et al. (2012) Mapping QTL for heat tolerance at flowering stage in rice using SNP markers. Plant Breed. 131: 33-41.
46. Yoshida, S., Satake, T. and Mackill, D.J. (1981) High temperature stress in rice. IRRI Research Paper Series Number 67. International Rice Research Institute, Manila.
47. Zhang, X.W., Li, J.P., Liu, A.L., Zou, J., Zhou, X.Y., Xiang, J.H., et al. (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS One 7: e49652.
48. Zinn, K.E., Tunc-Ozdemir, M. and Harper, J.F. (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J. Exp. Bot. 61: 1959-1968.