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Chromatin Interacting Factor OsVIL2 Is Required for Outgrowth of Axillary Buds in Rice

  • Yoon, Jinmi (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Cho, Lae-Hyeon (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Lee, Sichul (Center for Plant Aging Research, Institute for Basic Science) ;
  • Pasriga, Richa (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Tun, Win (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Yang, Jungil (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Yoon, Hyeryung (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Jeong, Hee Joong (Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University) ;
  • Jeon, Jong-Seong (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 : 2019.06.25
  • Accepted : 2019.10.29
  • Published : 2019.12.31

Abstract

Shoot branching is an essential agronomic trait that impacts on plant architecture and yield. Shoot branching is determined by two independent steps: axillary meristem formation and axillary bud outgrowth. Although several genes and regulatory mechanism have been studied with respect to shoot branching, the roles of chromatin-remodeling factors in the developmental process have not been reported in rice. We previously identified a chromatin-remodeling factor OsVIL2 that controls the trimethylation of histone H3 lysine 27 (H3K27me3) at target genes. In this study, we report that loss-of-function mutants in OsVIL2 showed a phenotype of reduced tiller number in rice. The reduction was due to a defect in axillary bud (tiller) outgrowth rather than axillary meristem initiation. Analysis of the expression patterns of the tiller-related genes revealed that expression of OsTB1, which is a negative regulator of bud outgrowth, was increased in osvil2 mutants. Chromatin immunoprecipitation assays showed that OsVIL2 binds to the promoter region of OsTB1 chromatin in wild-type rice, but the binding was not observed in osvil2 mutants. Tiller number of double mutant osvil2 ostb1 was similar to that of ostb1, suggesting that osvil2 is epistatic to ostb1. These observations indicate that OsVIL2 suppresses OsTB1 expression by chromatin modification, thereby inducing bud outgrowth.

Keywords

References

  1. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M., Sakakibara, H., and Kyozuka J. (2007). DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J. 51, 1019-1029. https://doi.org/10.1111/j.1365-313X.2007.03210.x
  2. Bemer, M. and Grossniklaus, U. (2012). Dynamic regulation of Polycomb groub activity during plant development. Curr. Opin. Plant Biol. 15, 523-529. https://doi.org/10.1016/j.pbi.2012.09.006
  3. Chen, Y., Fan, X., Song, W., Zhang, Y., and Xu, G. (2012). Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnol. J. 10, 139-149. https://doi.org/10.1111/j.1467-7652.2011.00637.x
  4. Cho, L.H., Pasriga, R., Yoon, J., Jeon, J.S., and An, G. (2018a). Roles of sugars in controlling flowering time. J. Plant Biol. 61, 121-113. https://doi.org/10.1007/s12374-018-0081-z
  5. 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
  6. Cho, L.H., Yoon, J., Wai, A.H., and An, G. (2018b). Histone deacetylase 701 (HDT701) induces flowering in rice by modulating expression of OsIDS1. Mol. Cells 41, 665-675. https://doi.org/10.14348/molcells.2018.0148
  7. Cohen, Y. and Cohen, J.Y. (2008). Analysis of variance. In Statistics and Data with R: An Applied Approach through Examples, Y. Cohen and J.Y. Cohen, eds. (Chichester: John Willey & Sons), pp. 417-461.
  8. Conrad, L.J., Khanday, I., Johnson, C., Guiderdoni, E., An, G., Vijayraghavan, U., and Sundaresan, V. (2014). The polycomb groub gene EMF2B is essential for maintenance of floral meristem determinacy in rice. Plant J. 80, 883-894. https://doi.org/10.1111/tpj.12688
  9. Deshpande, G.M., Ramakrishna, K., Chongloi, G.L., and Vijayraghavan, U. (2015). Functions for rice RFL in vegetative axillary meristem specification and outgrowth. J. Exp. Bot. 66, 2773-2784. https://doi.org/10.1093/jxb/erv092
  10. Greb, T., Mylne, J.S., Crevillen, P., Geraldo, N., An, H., Gendall, A.R., and Dean, C. (2007). The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr. Biol. 17, 73-78. https://doi.org/10.1016/j.cub.2006.11.052
  11. Guo, S., Xu, Y., Lie, H., Mao, Z., Zhang, C., Ma, Y., Zhang, Q., Meng, Z., and Chong, K. (2013). The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat. Commun. 4, 1566. https://doi.org/10.1038/ncomms2542
  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. Hussien, A., Tavakol, E., Horner, D.S., Munoz-Amatriain, M., Muehlbauer, G.J., and Rossini, L. (2014). Genetics of tillering in rice and barley. Plant Genome 7, 1-20.
  14. Ishikawa, S., Maekawa, M., Arite, T., Onishi, K., Takamure, I., and Junko, K. (2005). Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 46, 79-86. https://doi.org/10.1093/pcp/pci022
  15. Jeon, J.S., Lee, S., Jung, K.H., Jun, S.H., Jeong, D.H., Lee, J., King, 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
  16. Jeong, D.H., An, S., Kang, H.G., Moon, S., Han, J.J., Park, S., Lee, H., 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
  17. Jeong, H.J., Yang, J., Yi, J., and An, G. (2015). Controlling flowering time by histone methylation and acetylation in Arabidopsis and rice. J. Plant Biol. 58, 203-210. https://doi.org/10.1007/s12374-015-0219-1
  18. Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L., Meng, X., Liu, G., Yu, H., Yuan, Y., et al. (2013). DWARF53 acts as a repressor of strigolactone signaling in rice. Nature 504, 401-405. https://doi.org/10.1038/nature12870
  19. Lee, D.Y. and An, G. (2012). Two AP2 family genes, supernumerary bract (SNB) and Osindeterminate spikelet 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice. Plant J. 69, 445-461. https://doi.org/10.1111/j.1365-313X.2011.04804.x
  20. Lee, D.Y., Lee, J., Moon, S., Park, S.Y., and An, G. (2007). The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem. Plant J. 49, 64-78. https://doi.org/10.1111/j.1365-313X.2006.02941.x
  21. Li, X., Qian, Q., Fu, Z., Wang, Y., Xiong, G., Zeng, D., Wang, X., Liu, X., Teng, S., Hiroshi, F., et al. (2003). Control of tillering in rice. Nature 422, 618-621. https://doi.org/10.1038/nature01518
  22. Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J., et al. (2009). DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, requires rice tiller bud outgrowth. Plant Cell 21, 1512-1525. https://doi.org/10.1105/tpc.109.065987
  23. Minakuchi, K., Kameoka, H., Yasuno, N., Umehara, M., Luo, L., Kobayashi, K., Hanada, A., Ueno, K., Asami, T., Yamaguchi, S., et al. (2010). FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol. 51, 1127-1135. https://doi.org/10.1093/pcp/pcq083
  24. Mozgova, I. and Henning, L. (2015). The polycomb group protein regulatory network. Annu. Rev. Plant Biol. 66, 269-296. https://doi.org/10.1146/annurev-arplant-043014-115627
  25. Nakamura, H., Xue, Y.L., Miyakawa, T., Hou, F., Qin, H.M., Fukui, K., Shi, X., Ito, E., Ito, S., and Park, S.H. (2013). Molecular mechanism of strigolactone perception by DWARF14. Nat. Commun. 4, 2613. https://doi.org/10.1038/ncomms3613
  26. Oikawa, T. and Kyozuka, J. (2009). Two-step regulation of LAX PANICLE1 protein accumulation in axillary meristem formation in rice. Plant Cell 21, 1095-1108. https://doi.org/10.1105/tpc.108.065425
  27. Tabuchi, H., Zhang, Y., Hattori, S., Omae, M., Shimizu-Sato, S., Oikawa, T., Qian, Q., Nishimura, M., Kitano, H., Xie, H., et al. (2011). LAX PANICLE2 of rice encodes a novel nuclear protein and regulates the formation of axillary meristems. Plant Cell 23, 3276-3287. https://doi.org/10.1105/tpc.111.088765
  28. Takeda, T., Suwa, Y., Suzuki, M., Kitano, H., Ueguchi-Tanaka, M., Ashikari, M., Matsuoka, M., and Ueguchi, C. (2003). The OsTB1 gene negatively regulates lateral branching in rice. Plant J. 33, 513-520. https://doi.org/10.1046/j.1365-313X.2003.01648.x
  29. Tanaka, W., Ohmori, Y., Ushijima, T., Matsusaka, H., Matsushita, T., Kumamaru, T., Kawano, S., and Hirano, H.Y. (2015). Axillary meristem formation in rice requires the WUSCHEL ortholog TILLERS ABSENT1. Plant Cell 27, 1173-1184. https://doi.org/10.1105/tpc.15.00074
  30. Tian, C. and Jiao, Y. (2015). A systems approach to understand shoot branching. Curr. Opin. Plant Biol. 3-4, 13-19. https://doi.org/10.1016/S1369-5266(00)88572-6
  31. Wai, A.H. and An, G. (2017). Axillary meristem initiation and bud growth in rice. J. Plant Biol. 60, 440-451. https://doi.org/10.1007/s12374-017-0088-x
  32. Wang, Y. and Li, J. (2011). Branching in rice. Curr. Opin. Plant Biol. 14, 94-99. https://doi.org/10.1016/j.pbi.2010.11.002
  33. Wang, Y., Sun, S., Zhu, W., Jia, K., Yang, H., and Wang, X. (2013). Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev. Cell 27, 681-688. https://doi.org/10.1016/j.devcel.2013.11.010
  34. Xie, K., Minkenberg, B., and Yang, Y. (2015). Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc. Natl. Acad. Sci. U. S. A. 112, 3570-3575. https://doi.org/10.1073/pnas.1420294112
  35. Xu, M., Zhu, L., Shou, H., and Wu, P. (2005). A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46, 1674-1681. https://doi.org/10.1093/pcp/pci183
  36. Yang, J., Cho, L.H., Yoon, J., Yoon, H., Wai, A.H., Hong, W.J., Han, M.H., Sakakibara, H., Liang, W., Jung, K.H., et al. (2019). Chromatin interacting factor of OsVIL2 increases biomass and rice grain yield. Plant Biotechnol. J. 17, 178-187. https://doi.org/10.1111/pbi.12956
  37. Yang, J., Lee, S., Hang, R., Kim, S.R., Lee, Y.S., Cao, X., Amasino, R., and An, G. (2013). OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J. 73, 566-578. https://doi.org/10.1111/tpj.12057
  38. Yeh, S.Y., Chen, H.W., Ng, C.Y., Lin, C.Y., Tseng, T.H., Li, W.H., and Ku, M.S.B. (2015). Down-regulation of Cytokinin Oxidase 2 expression increases tiller number and improves rice yield. Rice 8, 36. https://doi.org/10.1186/s12284-014-0036-z
  39. Yoon, H., Yang, J., Liang, W., Zhang, D., and An, G. (2018). OsVIL2 regulates spikelet development by controlling regulatory genes in Oryza sativa. Front. Plant Sci. 9, 102. https://doi.org/10.3389/fpls.2018.00102
  40. 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
  41. 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
  42. Zhang, S., Li, G., Fang, J., Chen, W., Jiang, H., Zou, J., Liu, X., Zhao, X., Li, X., Chu, C., et al. (2010). The interaction among DWARF10, auxin and cytokinin underlie lateral bud outgrowth in rice. J. Integr. Plant Biol. 52, 626-638. https://doi.org/10.1111/j.1744-7909.2010.00960.x
  43. Zhao, J., Wang, T., Wang, M., Liu, Y., Yuan, S., Gao, Y., Yin, L., Sun, W., Peng, L., Zhang, W., et al. (2014). DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching. Plant Cell Physiol. 55, 1096-1109. https://doi.org/10.1093/pcp/pcu045
  44. Zou, J., Zhang, S., Zhang, W., Li, G., Chen, Z., Zhai, W., Zhao, X., Pan, X., Xie, Q., and Zhu, L. (2006). The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J. 48, 687-696. https://doi.org/10.1111/j.1365-313X.2006.02916.x

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