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Histone Deacetylase 701 (HDT701) Induces Flowering in Rice by Modulating Expression of OsIDS1

  • Cho, Lae-Hyeon (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Yoon, Jinmi (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Wai, Antt Htet (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • An, Gynheung (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University)
  • Received : 2018.03.28
  • Accepted : 2018.06.25
  • Published : 2018.07.31

Abstract

Rice is a facultative short-day (SD) plant in which flowering is induced under SD conditions or by other environmental factors and internal genetic programs. Overexpression of Histone Deacetylase 701 (HDT701) accelerates flowering in hybrid rice. In this study, mutants defective in HDT701 flowered late under both SD and long-day conditions. Expression levels of florigens Heading date 3a (Hd3a) and Rice Flowering Locus T1 (RFT1), and their immediate upstream floral activator Early heading date 1 (Ehd1), were significantly decreased in the hdt701 mutants, indicating that HDT701 functions upstream of Ehd1 in controlling flowering time. Transcript levels of OsINDETERMINATE SPIKELET 1 (OsIDS1), an upstream repressor of Ehd1, were significantly increased in the mutants while those of OsGI and Hd1 were reduced. Chromatin-immunoprecipitation assays revealed that HDT701 directly binds to the promoter region of OsIDS1. These results suggest that HDT701 induces flowering by suppressing OsIDS1.

Keywords

References

  1. An, G., Ebert, P.R., Mitra, A., and Ha, S.B. (1989). Binary vectors. In Plant Molecular Biology Manual. (Dordrecht: Kluwer Academic Publisher A3). pp.1-19.
  2. An, G., Jeong, D.H., Jung, K.H., and Lee, S. (2005a). Reverse genetic approaches for functional genomics of rice. Plant Mol. Biol. 59, 111-123. https://doi.org/10.1007/s11103-004-4037-y
  3. An, G., Lee, S., Kim, S.H., and Kim, S.R. (2005b). Molecular genetics using T-DNA in rice. Plant Cell Physiol. 46, 14-22. https://doi.org/10.1093/pcp/pci502
  4. Cho, L.H., Yoon, J., Pasriga, R., and An, G. (2016). Homodimerization of Ehd1 is required to induce flowering in rice. Plant Physiol. 170, 2159-2171. https://doi.org/10.1104/pp.15.01723
  5. Cho, L.H., Yoon, J., and An, G. (2017). The control of flowering time by environmental factors. Plant J. 90, 708-719. https://doi.org/10.1111/tpj.13461
  6. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C., and Coupland, G. (2007). FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033. https://doi.org/10.1126/science.1141752
  7. Dangl, M., Brosch, G., Haas, H., Loidl, P., and Lusser, A. (2001). Comparative analysis of HD2 type histone deacetylases in higher plants. Planta 213, 280-285. https://doi.org/10.1007/s004250000506
  8. Ding, B., Bellizzi Mdel, R., Ning, Y., Meyers, B.C., and Wang, G.L. (2012). HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24, 3783-3794. https://doi.org/10.1105/tpc.112.101972
  9. Doi, K., Izawa, T., Fuse, T., Yamanouchi, U., Kubo, T., Shimatani, Z., Yano, M., and Yoshimura, A. (2004). Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-Iike gene expression independently of Hd1. Genes Dev. 18, 926-936. https://doi.org/10.1101/gad.1189604
  10. Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Coupland, G., and Putterill, J. (1999). GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membranespanning domains. EMBO J. 18, 4679-4688. https://doi.org/10.1093/emboj/18.17.4679
  11. Fu, W., Wu, K., and Duan, J. (2007). Sequence and expression analysis of histone deacetylases in rice. Biochem. Biophys. Res. Commun. 356, 843-850. https://doi.org/10.1016/j.bbrc.2007.03.010
  12. Haring, M., Offermann, S., Danker, T., Horst, I., Peterhansel, C., and Stam, M. (2007). Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods 3, 1-16. https://doi.org/10.1186/1746-4811-3-1
  13. Hayama, R., Yokoi, S., Tamaki, S., Yano, M., and Shimamoto, K. (2003). Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422, 719-722. https://doi.org/10.1038/nature01549
  14. He, Y., Michaels, S.D., and Amasino, R.M. (2003). Regulation of flowering time by histone acetylation in Arabidopsis. Science 302, 1751-1754. https://doi.org/10.1126/science.1091109
  15. Hu, Y., Qin, F., Huang, L., Sun, Q., Li, C., Zhao, Y., and Zhou, D.X. (2009). Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem. Biophys. Res. Commun. 388, 266-271. https://doi.org/10.1016/j.bbrc.2009.07.162
  16. Ishikawa, R., Aoki, M., Kurotani, K., Yokoi, S., Shinomura, T., Takano, M., and Shimamoto, K. (2011). Phytochrome B regulates Heading date 1(Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice. Mol. Genet. Genom. 285, 461-470. https://doi.org/10.1007/s00438-011-0621-4
  17. Jeon, J.S., Lee, S., Jung, K.H., Jun, S.H., Jeong, D.H., Lee, J., Kim, C., Jang, S., Lee, S., Yang, K., et al. (2000). T-DNA insertional mutagenesis for functional genomics in rice. Plant J. 22, 561-570. https://doi.org/10.1046/j.1365-313x.2000.00767.x
  18. Jeong, D.H., An, S., Kang, H.G., Moon, S., Han, J.J., Park, S., Lee, H.S., An, K., and An, G. (2002). T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol. 130, 1636-1644. https://doi.org/10.1104/pp.014357
  19. Jeong, D.H., An, S., Park, S., Kang, H.G., Park, G.G., Kim, S.R., Sim, J., Kim, Y.O., Kim, M.K., Kim, S.R., et al. (2006). Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J. 45, 123-132. https://doi.org/10.1111/j.1365-313X.2005.02610.x
  20. Kim, S.R., Lee, D.Y., Yang, J.I., Moon, S., and An, G. (2009) Cloning vectors for rice. J. Plant Biol. 52, 73-78. https://doi.org/10.1007/s12374-008-9008-4
  21. Kim, S.L., Choi, M., Jung, K.H., and An, G. (2013). Analysis of the early-flowering mechanisms and generation of T-DNA tagging lines in Kitaake, a model rice cultivar, J. Exp. Bot. 64, 4169-4182. https://doi.org/10.1093/jxb/ert226
  22. 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. https://doi.org/10.1242/dev.008631
  23. Lee, Y.S., and An, G. (2015). OsGI controls flowering time by modulating rhythmic flowering time regulators preferentially under short day in rice. J. Plant Biol. 58, 137-145. https://doi.org/10.1007/s12374-015-0007-y
  24. Lee, Y.S., Jeong, D.H., Lee, D.Y., Yi, J., Ryu, C.H., Kim, S.L., Jeong, H.J., Choi, S.C., Jin, P., Yang, J., et al. (2010). OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J. 63, 18-30.
  25. Lee, Y.S., Lee, D.Y., Cho, L.H., and An, G. (2014). Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice. 7, 31. https://doi.org/10.1186/s12284-014-0031-4
  26. Lee, Y.S., Yi, J., Jung, K.H., and An, G. (2016) Comparison of rice flowering-time genes under paddy conditions. J. Plant Biol. 59, 238-246. https://doi.org/10.1007/s12374-016-0029-0
  27. Li, C., Huang, L., Xu, C., Zhao, Y., and Zhou, D.X. (2011). Altered levels of histone deacetylase OsHDT1 affect differential gene expression patterns in hybrid rice. PLoS One 6, e21789. https://doi.org/10.1371/journal.pone.0021789
  28. Luo, M., Wang, Y.Y., Liu, X., Yang, S., Lu, Q., Cui, Y., and Wu, K. (2012). HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J. Exp. Bot. 63, 3297-3306. https://doi.org/10.1093/jxb/ers059
  29. Luo, M., Tai, R., Yu, C.W., Yang, S., Chen, C.Y., Lin, W.D., Schmidt, W., and Wu, K. (2015). Regulation of flowering time by the histone deacetylase HDA5 in Arabidopsis. Plant J. 82, 925-936. https://doi.org/10.1111/tpj.12868
  30. Miao, J., Guo, D., Zhang, J., Huang, Q., Qin, G., Zhang, X., Wan, J., Gu, H., and Qu, L.J. (2013). Targeted mutagenesis in rice using the CRISPR-Cas system. Cell Res. 23, 1233-1236. https://doi.org/10.1038/cr.2013.123
  31. Morita, S., Wada, H., and Matsue, Y. (2017). Countermeasures for heat damage in rice grain quality under climate change. Plant Prod. Sci. 19, 1-11.
  32. Naito, Y., Hino, K., Bono, H., and Ui-Tei, K. (2015). CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics 31, 1120-1123. https://doi.org/10.1093/bioinformatics/btu743
  33. Nishida, H., Inoue, H., Okumoto, Y., and Tanisakao, T. (2002). A novel gene ef1-h conferring an extremely long basic vegetative growth period in rice. Crop Sci. 42, 348-354.
  34. Ouyang, S., Zhu, W., Hamilton, J., Lin, H., Campbell, M., Childs, K., Thibaud-Nissen, F., Malek, R.L., Lee, Y., Zheng, L., et al. (2007).The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 35, D883-D887. https://doi.org/10.1093/nar/gkl976
  35. Pandey, R., MuEller, A., Napoli, C.A., Selinger, D.A., Pikaard, C.S., Richards, E.J., Bender, J., Mount, D.W., and Jorgensen, R.A. (2002). Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 30, 5036-5055. https://doi.org/10.1093/nar/gkf660
  36. Park, D.H., Somers, D.E., Kim, Y.S., Choy, Y.H., Lim, H.K., Soh, M.S., Kim, H.J., Kay, S.A., and Nam, H.G. (1999). Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579-1582. https://doi.org/10.1126/science.285.5433.1579
  37. Peng, L.T., Shi, Z.Y., Li, L., Shen, G.Z., and Zhang, J.L. (2007). Ectopic expression of OsLFL1 in rice represses Ehd1 by binding on its promoter. Biochem. Biophys. Res. Commun. 360, 251-256. https://doi.org/10.1016/j.bbrc.2007.06.041
  38. Peng, L.T., Shi, Z.Y., Li, L., Shen, G.Z., and Zhang, J.L. (2008). Overexpression of transcription factor OsLFL1 delays flowering time in Oryza sativa. Plant Physiol. 165, 876-885. https://doi.org/10.1016/j.jplph.2007.07.010
  39. Ryu, C.H., Lee, S., Cho, L.H., Kim, S.L., Lee, Y.S., Choi, S.C., Jeong, H.J., Yi, J., Park, S.J., Han, C.D., et al. (2009). OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant Cell Environ. 32, 1412-1427. https://doi.org/10.1111/j.1365-3040.2009.02008.x
  40. Saito, H., Ogiso-Tanaka, E., Okumoto, Y., Yoshitake, Y., Izumi, H., Yokoo, T., Matsubara, K., Hori, K., Yano, M., Inoue, H., et al. (2012). Ef7 encodes an ELF3-likeprotein 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. https://doi.org/10.1093/pcp/pcs029
  41. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z.,Yanofsky, M.F., and Coupland, G. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616. https://doi.org/10.1126/science.288.5471.1613
  42. Sridha, S., and Wu, K. (2006). Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J. 46, 124-133. https://doi.org/10.1111/j.1365-313X.2006.02678.x
  43. Sun, C., Chen, D., Fang, J., Wang, P., Deng, X., and Chu, C. (2014). Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways. Protein Cell 5, 889-898. https://doi.org/10.1007/s13238-014-0068-6
  44. 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. https://doi.org/10.1126/science.1141753
  45. Tanaka, T., Antonio, B.A., Kikuchi, S., Matsumoto, T., Nagamura, Y., Numa, H., Sakai, H,. Wu, J., Itoh, T., Sasaki, T., et al. (2008). The rice annotation project database (RAP-DB): 2008 update. Nucleic Acids Res. 36, D1028-D1033.
  46. Ueno, Y., Ishikawa, T., Watanabe, K., Terakura, S., Iwakawa, H., Okada, K., Machida, C., and Machida, Y. (2007). Histone deacetylases and ASYMMETRIC LEAVES2 are involved in the establishment of polarity in leaves of Arabidopsis. Plant Cell 19, 445-457. https://doi.org/10.1105/tpc.106.042325
  47. Wei, J., Wu, Y., Cho, L.H., Yoon, J., Choi, H., Yoon, H., Jin, P., Yi, J., Lee, Y.S., Jeong, H.J., et al. (2017). Identification of root-preferential transcription factors in rice by analyzing GUS expression patterns of T-DNA tagging lines. J. Plant Biol. 60, 268-277. https://doi.org/10.1007/s12374-016-0597-z
  48. Wu, K., Tian, L., Malik, K., Brown, D., and Miki, B. (2000). Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana. Plant J. 22, 19-27. https://doi.org/10.1046/j.1365-313x.2000.00711.x
  49. Wu, K., Zhang, L., Zhou, C., Yu, C.W., and Chaikam, V. (2008). HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J. Exp. Bot. 59, 225-234. https://doi.org/10.1093/jxb/erm300
  50. Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C., Li, X., et al. (2008). Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice, Nat. Genet. 40, 761-767. https://doi.org/10.1038/ng.143
  51. Yanovsky, M.J., and Kay, S.A. (2002). Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308-312. https://doi.org/10.1038/nature00996
  52. Yoon, J., Cho, L.H., Kim, S.L., Choi, H., Koh, H.J., and An, G. (2014). The BEL1-type homeobox gene SH5 induces seed shattering by enhancing abscission-zone development and inhibiting lignin biosynthesis. Plant J. 79, 717-728. https://doi.org/10.1111/tpj.12581
  53. Yoon, J., Cho, L.H., Antt, H.W., Koh, H.J., and An, G. (2017). KNOX protein OSH15 induces grain shattering by repressing lignin biosynthesis genes. Plant Physiol. 174, 312-325. https://doi.org/10.1104/pp.17.00298
  54. Yi, J., and An, G. (2013). Utilization of T-DNA tagging lines in rice. J. Plant Biol. 56, 85-90. https://doi.org/10.1007/s12374-013-0905-9
  55. Zhang, J., Zhou, X., Yan, W., Zhang, Z., Lu, L., Han, Z., Zhao, H., Liu, H., Song, P., Hu, Y., et al. (2015). Combinations of the Ghd7, Ghd8 and Hd1 genes largely define the ecogeographical adaptation and yield potential of cultivated rice. New Phytol. 1056-1066.
  56. Zhang, Z., Hu, W., Shen, G., Liu, H., Hu, Y., Zhou, X., Liu, T., and Xing, Y. (2017). Alternative functions of Hd1 in repressing or promoting heading are determined by Ghd7 status under long-day conditions. Sci. Rep. 7, 5388. https://doi.org/10.1038/s41598-017-05873-1
  57. Zhao, X.L., Shi, Z.Y., Peng, L.T., Shen, G.Z., and Zhang, J.L. (2011). An atypical HLH protein OsLF in rice regulates flowering time and interacts with OsPIL13 and OsPIL15. N. Biotechnol. 28, 788-797. https://doi.org/10.1016/j.nbt.2011.04.006
  58. Zhao, J., Zhang, J., Zhang, W., Wu, K., Zheng, F., Tian, L., Liu, X., and Duan, J. (2015). Expression and functional analysis of the plant-specific histone deacetylase HDT701 in rice. Front. Plant Sci. 5, 764.
  59. Zhu, Q.H, and Helliwell, C.A. (2011). Regulation of flowering time and floral patterning by miR172. J. Exp. Bot. 62, 487-495. https://doi.org/10.1093/jxb/erq295

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