Cloning of quantitative trait genes from rice reveals conservation and divergence of photoperiod flowering pathways in Arabidopsis and rice

Frontiers in Plant Science

Volumn 5, Issue MAY, 2014, Pages

  Matsubara, Kazuki ^a   Hori, Kiyosumi ^b   Ogiso Tanaka, Eri ^b   Yano, Masahiro ^a,b  

^a NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Breeding; Natural variation; Photoperiodic flowering; Quantitative trait gene; Rice

Indexed keywords

EID: 84901016815     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00193     Document Type: Review

References (62)

1. Abou-Elwafa, S. F., Büttner, B., Chia, T., Schulze-Buxloh, G., Hohmann, U., Mutasa-Göttgens, E., et al. (2011). Conservation and divergence of autonomous pathway genes in the flowering regulatory network of Beta vulgaris. J. Exp. Bot. 62, 3359-3374. doi: 10.1093/jxb/erq321
2. Andrés, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639. doi: 10.1038/nrg3291
3. Ballerini, E. S., and Kramer, E. M. (2011). In the light of evolution: a reevaluation of conservation in the CO-FT regulon and its role in photoperiodic regulation of flowering time. Front. Plant Sci. 2:81. doi: 10.3389/fpls.2011.00081
4. Benfey, P. N., and Mitchell-Olds, T. (2008). From genotype to phenotype: systems biology meets natural variation. Science 320, 495-497. doi: 10.1126/science.1153716
5. Bentley, A. R., Jensen, E. F., Mackay, I. J., Hönicka, H., Fladung, M., Hori, K., et al. (2013). "Flowering time, " in Genomics and Breeding for Climate-Resilient Crops: vol. 2 Target Traits, ed K. Chittaranjan (Berlin: Springer Berlin Heidelberg), 1-66.
6. Bian, X. F., Liu, X., Zhao, Z. G., Jiang, L., Gao, H., Zhang, Y. H., et al. (2011). Heading date gene, dth3 controlled late flowering in O. Glaberrima Steud. by down-regulating Ehd1. Plant Cell Rep. 30, 2243-2254. doi: 10.1007/s00299-011-1129-4
7. Brambilla, V., and Fornara, F. (2013). Molecular control of flowering in response to day length in rice. J. Integr. Plant Biol. 55, 410-418. doi: 10.1111/jipb.12033
8. Chen, J., Li, X., Cheng, C., Wang, Y., Qin, M., Zhu, H., et al. (2014). Characterization of epistatic interaction of QTLs LH8 and EH3 controlling heading date in rice. Sci. Rep. 4, 4263. doi: 10.1038/srep04263
9. Dai, C., and Xue, H. W. (2010). Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J. 29, 1916-1927. doi: 10.1038/emboj.2010.75
10. Dai, X., Ding, Y., Tan, L., Fu, Y., Liu, F., Zhu, Z., et al. (2012). LHD1, an allele of DTH8/Ghd8, controls late heading date in common wild rice (Oryza rufipogon). J. Intgr. Plant Biol. 54, 790-799. doi: 10.1111/j.1744-7909.2012.01166.x
11. Doi, K., Izawa, T., Fuse, T., Yamanouchi, U., Kubo, T., Shimatani, Z., et al. (2004). Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev. 18, 926-936. doi: 10.1101/gad.1189604
12. Ebana, K., Shibaya, T., Wu, J., Matsubara, K., Kanamori, H., Yamane, H., et al. (2011). Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars. Theor. Appl. Genet. 122, 1199-1210. doi: 10.1007/s00122-010-1524-1
13. Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., et al. (1999). GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18, 4679-4688. doi: 10.1093/emboj/18.17.4679
14. Fujino, K., Yamanouchi, U., and Yano, M. (2013). Roles of theHd5 gene controlling heading date for adaptation to the northern limits of rice cultivation. Theor. Appl. Genet. 126, 611-618. doi: 10.1007/s00122-012-2005-5
15. Greenup, A., Peacock, W. J., Dennis, E. S., and Trevaskis, B. (2009). The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann. Bot. 103, 1165-1172. doi: 10.1093/aob/mcp063
16. Gross, S. D., and Anderson, R. A. (1998). Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell. Signal. 10, 699-711. doi: 10.1016/S0898-6568(98)00042-4
17. Hayama, R., Yokoi, S., Tamaki, S., Masahiro Yano, M., and Shimamoto, K. (2003). Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422, 719-722. doi: 10.1038/nature01549
18. Hori, K., Kataoka, T., Miura, K., Yamaguchi, M., Saka, N., Nakahara, T., et al. (2012). Variation in heading date conceals quantitative trait loci for other traits of importance in breeding selection of rice. Breed. Sci. 62, 223-234. doi: 10.1270/jsbbs.62.223
19. Hori, K., Ogiso-Tanaka, E., Matsubara, K., Yamanouchi, U., Ebana, K., and Yano, M. (2013). Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response. Plant J. 76, 36-46. doi: 10.1111/tpj.12268
20. Ishikawa, R., Aoki, M., Kurotani, K., Yokoi, S., Shinomura, T., Takano, M., et al. (2011). Phytochrome B regulates Heading date 1 (Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice. Mol. Genet. Genomics 285, 461-470. doi: 10.1007/s00438-011-0621-4
21. Itoh, H., and Izawa, T. (2013). The coincidence of critical day length recognition for florigen gene expression and floral transition under long-day conditions in rice. Mol. Plant 6, 635-649. doi: 10.1093/mp/sst022
22. Izawa, T. (2007). Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J. Exp. Bot. 58, 3091-3097. doi: 10.1093/jxb/erm159
23. Jung, C., and Müller, A. E. (2009). Flowering time control and applications in plant breeding. Trends Plant Sci. 14, 563-573. doi: 10.1016/j.tplants.2009.07.005
24. Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T., et al. (2002). Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43, 1096-1105. doi: 10.1093/pcp/pcf156
25. Komiya, R., Ikegami, A., Tamaki, S., Yokoi, S., and Shimamoto, K. (2008). Hd3a and RFT1 are essential for flowering in rice. Development 135, 767-774. doi: 10.1242/dev.008631
26. Komiya, R., Yokoi, S., and Shimamoto, K. (2009). A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136, 3443-3450. doi: 10.1242/dev.040170
27. Koo, B. H., Yoo, S. C., Park, J. W., Kwon, C. T., Lee, B. D., An, G., et al. (2013). Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol. Plant 6, 1877-1888. doi: 10.1093/mp/sst088
28. Kwon, C. T., Yoo, S. C., Koo, B. H., Cho, S. H., Park, J. W., Zhang, Z., et al. (2014). Natural variation in Early flowering1 contributes to early flowering in japonica rice under long days. Plant Cell Environ. 37, 101-112. doi: 10.1111/pce.12134
29. Lee, S., Kim, J., Han, J. J., Han, M. J., and An, G. (2004). Functional analyses of the flowering time gene OsMADS50, the putative SUPPRESSOR OF OVEREXPRESSION OF CO 1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in rice. Plant J. 38, 754-764. doi: 10.1111/j.1365-313X.2004.02082.x
30. Lin, H., Ashikari, M., Yamanouchi, U., Sasaki, T., and Yano, M. (2002). Identification and characterization of a quantitative trait locus, Hd9, controlling heading date in rice. Breed. Sci. 52, 35-41. doi: 10.1270/jsbbs.52.35
31. Lin, H., Liang, Z. W., Sasaki, T., and Yano, M. (2003). Fine mapping and characterization of quantitative trait loci Hd4 and Hd5 controlling heading date in rice. Breed. Sci. 53, 51-59. doi: 10.1270/jsbbs.53.51
32. Liu, W., Xu, Z. H., Luo, D., and Xue, H. W. (2003). Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J. 36, 189-202. doi: 10.1046/j.1365-313X.2003.01866.x
33. Magallón, S. A., and Sanderson, M. J. (2005). Angiosperm divergence times: the effects of genes, codon positions, and time constraints. Evolution 59, 1653-1670. doi: 10.1554/04-565.1
34. Matsubara, K., Kono, I., Hori, K., Nonoue, Y., Ono, N., A. Shomura, A., et al. (2008). Novel QTLs for photoperiodic flowering revealed by using reciprocal backcross inbred lines from crosses between japonica rice cultivars. Theor. Appl. Genet. 117, 935-945. doi: 10.1007/s00122-008-0833-0
35. Matsubara, K., Ogiso-Tanaka, E., Hori, K., Ebana, K., Ando, T., and Yano, M. (2012). Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol. 53, 709-716. doi: 10.1093/pcp/pcs028
36. McClung, C. R. (2011). The genetics of plant clock. Adv. Genet. 74, 105-139. doi: 10.1016/B978-0-12-387690-4.00004-0
37. Murakami, M., Tago, Y., Yamashino, T., and Mizuno, T. (2007). Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol. 48, 110-121. doi: 10.1093/pcp/pcl043
38. Nagano, A. J., Sato, Y., Mihara, M., Antonio, B. A., Motoyama, R., Itoh, H., et al. (2012). Deciphering and prediction of transcriptome dynamics under Fluctuating Field Conditions. Cell 151, 1358-1369. doi: 10.1016/j.cell.2012.10.048
39. Ogiso, E., Takahashi, Y., Sasaki, T., Yano, M., and Izawa, T. (2010). The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol. 152, 808-820. doi: 10.1104/pp.109.148908
40. Ogiso-Tanaka, E., Matsubara, K., Yamamoto, S., Nonoue, Y., Wu, J., Fujisawa, H., et al. (2013). Natural variation of the RICE FLOWERING LOCUS T 1 contributes to flowering time divergence in rice. PLoS ONE 8:e75959. doi: 10.1371/journal.pone.0075959
41. Olsen, K. M., and Wendel, J. F. (2013). Crop plants as models for understanding plant adaptation and diversification. Front. Plant Sci. 4:290. doi: 10.3389/fpls.2013.00290
42. Park, D. H., Somers, D. E., Kim, Y. S., Choy, Y. H., Lim, H. K., Soh, M. S., et al. (1999). Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579-1582. doi: 10.1126/science.285.5433.1579
43. Pin, P. A., Benlloch, R., Bonnet, D., Wremerth-Weich, E., Kraft, T., Gielen, J. J. L., et al. (2010). An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330, 1397-1400. doi: 10.1126/science.1197004
44. Putterill, J., Robson, F., Lee, K., Simon, R., and Coupland, G. (1995). The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847-857. doi: 10.1016/0092-8674(95)90288-0
45. Ralph, M. R., and Menaker, M. (1988). A mutation of the circadian system in golden hamsters. Science 241, 1225-1227. doi: 10.1126/science.3413487
46. Rumpf, C., Cipak, L., Dudas, A., Benko, Z., Pozgajova, M., Riedel, C. G., et al. (2010). Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 9, 2655-2660. doi: 10.4161/cc.9.13.12146
47. Saito, H., Ogiso-Tanaka, E., Okumoto, Y., Yoshitake, Y., Izumi, H., Yokoo, T., et al. (2012). Ef7 encodes an ELF3-like protein and promotes rice flowering by negatively regulating the floral repressor gene Ghd7 under both short-and long-day conditions. Plant Cell Physiol. 53, 717-728. doi: 10.1093/pcp/pcs029
48. Saito, H., Yuan, Q., Okumoto, Y., Doi, K., Yoshimura, A., Inoue, H., et al. (2009). Multiple alleles at Early flowering 1 locus making variation in the basic vegetative growth period in rice (Oryza sativa L.). Theor. Appl. Genet. 119, 315-323. doi: 10.1007/s00122-009-1040-3
49. Takahashi, Y., Shomura, A., Sasaki, T., and Yano, M. (2001). Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the α subunit of protein kinase CK2. Proc. Natl. Acad. Sci. U.S.A. 98, 7922-7927. doi: 10.1073/pnas.111136798
50. Takahashi, Y., Teshima, K. M., Yokoi, S., Innan, H., and Shimamoto, K. (2009). Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc. Natl. Acad. Sci. U.S.A. 106, 4555-4560. doi: 10.1073/pnas.0812092106
51. Tamaki, S., Matsuo, S., Wong, H. L., Yokoi, S., and Shimamoto, K. (2007). Hd3a protein is a mobile flowering signal in rice. Science 316, 1033-1036. doi: 10.1126/science.1141753
52. Thomas, B., and Vince-Prue, D. (1997). Photoperiodism in Plants. 2nd Edn. San Diego, CA: Academic Press.
53. Tsuji, H., Taoka, K. I., and Shimamoto, K. (2011). Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Curr. Opin. Plant Biol. 14, 45-52. doi: 10.1016/j.pbi.2010.08.016
54. Tuazon, P., and Traugh, J. (1991). Casein kinase I and II-multipotential serine protein kinases: structure, function, and regulation. Adv. Second Messenger Phosphoprotein Res. 23, 123-164.
55. Wei, X., Xu, J., Guo, H., Jiang, L., Chen, S., Yu, C., et al. (2010). DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol. 153, 1747-1758. doi: 10.1104/pp.110.156943
56. Wu, W., Zheng, X. M., Lu, G., Zhong, Z., Gao, H., Chen, L., et al. (2013). Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc. Natl. Acad. Sci. U.S.A. 110, 2775-2780. doi: 10.1073/pnas.1213962110
57. Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., et al. (2008). Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761-767. doi: 10.1038/ng.143
58. Yan, W. H., Wang, P., Chen, H. X., Zhou, H. J., Li, Q. P., Wang, C. R., et al. (2011). A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol. Plant 4, 319-330. doi: 10.1093/mp/ssq070
59. Yang, Y., Peng, Q., Chen, G. X., Li, X. H., and Wu, C. Y. (2012). OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice. Mol. Plant 6, 202-215. doi: 10.1093/mp/sss062
60. Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., et al. (2000). Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12, 2473-2483. doi: 10.1105/tpc.12.12.2473
61. Zhao, D., Zhang, C., Feng, G., Yang, Q., Gu, M., and Liu, Q. (2013). Hd-q, a novel allele of Ef7 from a Chinese rice landrace, confers weak photoperiod sensitivity and improves local adaptability and yield potential. Mol. Breed. 32, 651-662. doi: 10.1007/s11032-013-9898-9
62. Zhao, J., Huang, X., Ouyang, X., Chen, W., Du, A., Zhu, L., et al. (2012). OsELF3-1, an ortholog of Arabidopsis EARLY FLOWERING 3, regulates rice circadian rhythm and photoperiodic flowering. PLoS ONE 7:e43705. doi: 10.1371/journal.pone.0043705