Comparative Transcriptome Analysis Reveals Differential Response of Phytohormone Biosynthesis Genes in Glumous Flowers of Cold-Tolerant and Cold-Sensitive Rice Varieties Upon Cold Stress at Booting Stage

  • Park, Myoung Ryoul (Institute of Agricultural Science & Technology, Chonbuk National University) ;
  • Kim, Ki-Young (Deapartment of Rice and Winter Cereal Crop, NICS, RDA) ;
  • Tyagi, Kuldeep (Institute of Agricultural Science & Technology, Chonbuk National University) ;
  • Baek, So-Hyeon (Deapartment of Rice and Winter Cereal Crop, NICS, RDA) ;
  • Yun, Song Joong (Institute of Agricultural Science & Technology, Chonbuk National University)
  • Received : 2010.03.08
  • Published : 2011.03.30

Abstract

Low temperature stress is one of the major negative factors affecting vegetative and reproductive growth of rice. To better understand responses of rice plants to low temperature we analyzed transcriptome expression patterns in glumous flower of cold-tolerant japonica rice variety, Stejaree45, and cold-susceptible variety, HR19621-AC6 at booting stage under cold water irrigation. A total of 2,411 probes were differentially expressed by low temperature in glumous flowers of the two varieties. Some important genes involved in hormone biosynthesis showed variety-specific regulation. Expression of GA20ox3 and GA2ox, among the genes involved in GA biosynthesis, was regulated differentially in the two varieties. Among the genes involved in IAA biosynthesis, YUCCA1 and TAA1:1 showed variety-specific regulation. Among the genes involved in cytokinin biosynthsis and signaling, expression of LOG, HK1 and HK3 was significantly down-regulated only in the cold-susceptible variety. Among the genes involved in ABA biosynthesis, NSY and AAO3 were down-regulated only in the cold-tolerant variety. In general, genes involved in GA, IAA and cytokinin biosynthesis responded to cold temperature in such a way that capacity of those bioactive hormones is maintained at relatively higher levels under cold temperature in the cold-tolerant variety, which can help minimize cold stress imposed to developing reproductive organs in the cold-tolerant variety.

Keywords

References

  1. Andaya VC, Tai TH. 2006. Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. 2006. Theor. Appl. Genet. 113:467-475. https://doi.org/10.1007/s00122-006-0311-5
  2. Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M. Cytokinin Oxidase Regulates Rice Grain Production. Science 309(29):741-745.
  3. Chu C, Lee T-M. 1989. The relationship between ethylene biosynthesis and chilling tolerance in seedlings of rice (Oryza sativa L_). Bot. Bull. Academia Sinica 30:263-273.
  4. Dall'Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R. 2007. Different roles of $\alpha$- and $\beta$-branch xanthophylls in photosystem assembly and photoprotection. Biol. Chem. 282:35056-35068. https://doi.org/10.1074/jbc.M704729200
  5. Garbero M, Pedranzani H, Zirulnik F, Molina A, Perez-Chaca MV, Vigliocco A, Abdala G. 2010. Shortterm cold stress in two cultivars of Digitaria eriantha: effects on stress-related hormones and antioxidant defense system. Acta Physiol. Plant. DOI 10.1007/s11738-010- 0573-z.
  6. Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguchi-Tanaka M, Matsuoka M. 2008. Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/ pollen and tapetum of rice. Plant Cell Physiol. 49:1429- 1450. https://doi.org/10.1093/pcp/pcn123
  7. Hunter DA, Ferrante A, Vernieri P, Reid MS. 2004. Role of abscisic acid in perianth senescence of daffodil. Physiol. Plant. 121:313-321. https://doi.org/10.1111/j.0031-9317.2004.0311.x
  8. Janowiak F, Maas B, Dörffling K. 2002. Importance of abscisic acid for chilling tolerance of maize seedlings. J. Plant Physiol. 159:635-643. https://doi.org/10.1078/0176-1617-0638
  9. Jeong EG, Ahn SN, Yea JD, Baek MK, Choi HC, Yi G, Nam M-H, Yoon KM. 2005. Evaluation of cold tolerancerelated traits of recombinant inbred lines in rice. Kor. J. Crop Sci. 50(3):205-211.
  10. Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G. 2005. Rice undeveloped tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705-2722. https://doi.org/10.1105/tpc.105.034090
  11. Kakimoto T. 2001. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ ADP isopentenyltransferases. Plant Cell Physiol. 42(7): 677-685. https://doi.org/10.1093/pcp/pce112
  12. Kakimoto T. 2003. Perception and signal transdiction of cytokines. Ann. Rev. Plant Biol. 54:605-627. https://doi.org/10.1146/annurev.arplant.54.031902.134802
  13. Kim K-Y, Kim B-K, Ko J-C, Ko J-K, Kim C-K, Yun SJ. 2006. Genetic analysis and combining ability on spikelet fertility related to cold tolerance in Japonica rice. Kor. J. Breed. 38(2):90-97.
  14. Kriechbaumer V, Glawischnig E. 2005. Auxin biosynthesis within the network of tryptophan metabolism. JNBT 2:53- 58.
  15. Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J. 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:652-655. https://doi.org/10.1038/nature05504
  16. Lang A, Reinhard E. 1961. Gibberellins and flower formation. Advances in Chemistry Series 28, Amer. Chem. Soc.:71-79.
  17. Lee MH. 2001. Low temperature tolerance in rice: the Korean experience. In: Increased lowland rice production in the Mekong region. Proceedings of an international workshop held in Vientiane, Laos, pp 109-117.
  18. Mamun EA, Alfred S, Cantrill LC. Overall RL. Sutton BG. 2006. Effects of chilling on male gametophyte development in rice. Cell Biol. International 30(7):583-591. https://doi.org/10.1016/j.cellbi.2006.03.004
  19. Murai M, Hirose S, Sato S, Takebe M. 1991. Effects of dwarfing genes from Dee-Geo-Woo-General and other varieties on cool temperature tolerance at booting stage in rice. Japn. J. of Breed. 41:241-254. https://doi.org/10.1270/jsbbs1951.41.241
  20. Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 56:165-185. https://doi.org/10.1146/annurev.arplant.56.032604.144046
  21. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y.1991. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677-684. https://doi.org/10.1105/tpc.3.7.677
  22. Oliver SN, Dennis ES, Dolferus R. 2007. ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol. 48(9):1319-1330. https://doi.org/10.1093/pcp/pcm100
  23. Panavas T, Walker EL, Rubinstein B.1988. Possible involvement of abscisic acid in senescence of daylily petals. J. Exp. Bot. 49:1987-1997.
  24. Pandey DM, Goswami CL, Kumar B. 2003. Physiological effects of plant hormones in cotton under drought. Biol. Plant. 47:535-540.
  25. Purty RS, Agrawal V, Gupta SC. 2005. Induction of a novel boiling stable protein in response to desiccation and ABA treatments in Sesbania sesban var. bicolour leaves. Biol. Plant. 49:137-140. https://doi.org/10.1007/s00000-005-7140-1
  26. Reinhardt D, Mandel T, Kuhlemeier C. 2000. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507-518. https://doi.org/10.1105/tpc.12.4.507
  27. Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi- Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K, Miyao A, Hirochika H, Kitano H, Ashikari M, Matsuoka M. 2004. An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol. 134(4):1642-1653. https://doi.org/10.1104/pp.103.033696
  28. Satake T. 1989. Male sterility caused by cooling treatment at the young microspore stage in rice stage plants. XXIX. The mechanism of enhancement in cool tolerance by raising water temperature before the critical stage. Japn. J. of Crop Sci. 58:240-245. https://doi.org/10.1626/jcs.58.240
  29. Seo M, Aoki H, Koiwai H, Kamiya Y, Nambara E, Koshiba T. 2004. Comparative studies on the Arabidopsis aldehyde oxidase (AAO) gene family revealed a major role of AAO3 in ABA biosynthesis in seeds. Plant Cell Physiol. 45(11):1694-703. https://doi.org/10.1093/pcp/pch198
  30. Shinomo H, Hasegawa T, Iwama K. 2002. Response of growth and grain yield in paddy rice to cool water at different growth stages. Field Crops Research 73:67-79. https://doi.org/10.1016/S0378-4290(01)00184-8
  31. Singh RP, Brennan JP, Farrell T, Williams R, Reinke R, Lewin L, Mullen J. 2005. Economic Analysis of Improving Cold Tolerance in Rice in Australia. Australasian Agribusiness Review 13:13.
  32. Tran LSP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K 2007. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl. Acad. Sci. USA 104: 20623-20628. https://doi.org/10.1073/pnas.0706547105
  33. Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K. 2010. Role of cytokinin responsive two-component system in ABA and osmotic stress signaling. Plant Signal Behav. 5(2):148-150. https://doi.org/10.4161/psb.5.2.10411
  34. Troncoso A, Garcia JL, Lavee S. 2010. Evaluation of the present information on the mechanisms leading to flower bud induction, evocation and differentiation. Acta Hortic. in press.
  35. Wang ZP, Chou WY, Wang CY. 2005. Roles of ammonium stress, cytokinin and phosphinothricin (PPT) in the induction of rice (Oryza sativa) microshoots. Plant Prot. Bull. 47:349-349.
  36. Xu SX, Liu GS, Chen RD. 2006. Characterization of an anther- and tapetum-specific gene and its highly specific promoter isolated from tomato. Plant Cell Rep. 25(3):231- 240. https://doi.org/10.1007/s00299-005-0056-7
  37. Yang J, Zhang J, Wang Z, Liu K, Wang P. 2006. Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. J. Exp. Bot. 57(1):149-160. https://doi.org/10.1093/jxb/erj018
  38. 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 andmultiple slide systematic variation. Nucl. Acids Res. 30:15. https://doi.org/10.1093/nar/30.4.e15
  39. Zeevaart JAD, Creelman RA. 1988. Metabolism and physiology of abscisic acid. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39:439-473. https://doi.org/10.1146/annurev.pp.39.060188.002255