OsASHL1 and OsASHL2, two members of the COMPASS-like complex, control floral transition and plant development in rice

Guangxin Zhao; Jingying Wang; Xi Chen; Hanjing Sha; Xin Liu; Yunfei Han; Guankai Qiu; Fantao Zhang; Jun Fang

doi:10.1016/j.jgg.2022.02.026

Volume 49 Issue 9

Sep. 2022

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Article Navigation > Journal of Genetics and Genomics > 2022 > 49(9): 870-880

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OsASHL1 and OsASHL2, two members of the COMPASS-like complex, control floral transition and plant development in rice

doi: 10.1016/j.jgg.2022.02.026

a. Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, Heilongjiang 150081, China;
b. University of Chinese Academy of Sciences, Beijing 100049, China;
c. College of Agriculture, Northeast Agricultural University, Harbin, Heilongjiang 150030, China;
d. College of Life Sciences, Jiangxi Normal University, Nanchang, Jiangxi 330022, China

Funds:

We are grateful to Prof. Qingyun Bu for providing various strains, empty vectors, instruments and equipment, and Dr. Xiaojie Tian and Dr. Zhenyu Wang for kindly giving pointed suggestions on multiple experiments. We are grateful to our laboratory members for discussion and helpful suggestions. This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA24020301), the National Natural Science Foundation of China (31901524, U20A2025), and the Key R&D Program Project of Heilongjiang Province (GA21B014).

Received Date: 2022-01-23
Accepted Date: 2022-02-20
Rev Recd Date: 2022-02-14
Publish Date: 2022-03-16

Abstract

Abstract

COMPASS or COMPASS-like is a highly conserved polyprotein complex in eukaryotes that is often involved in methylation of histone H3 lysine 4 (H3K4). However, the biological function of this complex in rice (Oryza sativa) is unclear. Here, we report the identifiction of their functions in growth and development. The osashl1 osashl2 double mutant shows a dwarf and late-flowering phenotype. Lower expression of Ehd1, OsVIL4, and OsMADS51 in the osashl1 osashl2 double mutant background accompanies a delayed vegetative growth phase and photoperiod-sensitive phase compared with that in wild type. Notably, there is less H3K4 mono-, di- and tri-methylation genome-wide in the double mutant, in particular less H3K4 tri-methylation at OsVIL4. Consistent with this result, knockout of OsVIL4 gives rise to a late-flowering phenotype similar to that of the osashl1 osashl2 double mutant, suggesting that OsVIL4 is a target of the COMPASS-like complex. In addition, the expression of key genes in brassinosteroid and gibberellic acid metabolism is altered in the osashl1 osashl2 double mutant, suggesting that the COMPASS-like complex regulates plant growth and development by modulating the levels of these two phytohormones. In summary, we demonstrate that OsASHL1 and OsASHL2 are important for floral transition and plant development.
- Rice (Oryza sativa),
- OsASHL1,
- OsASHL2,
- Flowering,
- COMPASS-like,
- H3K4 methylation

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References

Amasino, R., 2010. Seasonal and developmental timing of flowering. Plant J. 61, 1001-1013.

Diaz-Granados, A., Petrescu, A.J., Goverse, A., Smant, G., 2016. SPRYSEC Effectors:A Versatile Protein-Binding Platform to Disrupt Plant Innate Immunity. Front. Plant Sci. 7, 1575.

Doi, K., Izawa, T., Fuse, T., Yamanouchi, U., Kubo, T., Shimatani, Z., Yano, M., Yoshimura, A., 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.

Dou, Y., Milne, T.A., Ruthenburg, A.J., Lee, S., Lee, J.W., Verdine, G.L., Allis, C.D., Roeder, R.G., 2006. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat. Struct. Mol. Biol. 13, 713-719.

Du, A., Tian, W., Wei, M., Yan, W., He, H., Zhou, D., Huang, X., Li, S., Ouyang, X., 2017. The DTH8-Hd1 Module Mediates Day-Length-Dependent Regulation of Rice Flowering. Mol. Plant 10, 948-961.

Fang, J., Zhang, F., Wang, H., Wang, W., Zhao, F., Li, Z., Sun, C., Chen, F., Xu, F., Chang, S., et al., 2019. Ef-cd locus shortens rice maturity duration without yield penalty. Proc. Natl. Acad. Sci. U. S. A. 116, 18717-18722.

Foroozani, M., Vandal, M.P., Smith, A.P., 2021. H3K4 trimethylation dynamics impact diverse developmental and environmental responses in plants. Planta 253, 4.

Hiei, Y., Ohta, S., Komari, T., Kumashiro, T., 1994. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282.

Hong, Z., Ueguchi-Tanaka, M., Umemura, K., Uozu, S., Fujioka, S., Takatsuto, S., Yoshida, S., Ashikari, M., Kitano, H., Matsuoka, M., 2003. A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15, 2900-2910.

Ishikawa, R., Aoki, M., Kurotani, K., Yokoi, S., Shinomura, T., Takano, M., Shimamoto, K., 2011. Phytochrome B regulates Heading date 1(Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice. Molecular Genetics&Genomics 285, 461-470.

Jiang, D., Kong, N.C., Gu, X., Li, Z., He, Y., 2011. Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet. 7, e1001330.

Jiang, P., Wang, S., Jiang, H., Cheng, B., Wu, K., Ding, Y., 2018. The COMPASS-Like Complex Promotes Flowering and Panicle Branching in Rice. Plant Physiol. 176, 2761-2771.

Jin, J., Shi, J., Liu, B., Liu, Y., Huang, Y., Yu, Y., Dong, A., 2015. MORF-RELATED GENE702, a Reader Protein of Trimethylated Histone H3 Lysine 4 and Histone H3 Lysine 36, Is Involved in Brassinosteroid-Regulated Growth and Flowering Time Control in Rice. Plant Physiol. 168, 1275-1285.

Karimi, M., De Meyer, B., Hilson, P., 2005. Modular cloning in plant cells. Trends Plant Sci. 10, 103-105.

Kobayashi, K., Yasuno, N., Sato, Y., Yoda, M., Yamazaki, R., Kimizu, M., Yoshida, H., Nagamura, Y., Kyozuka, J., 2012. Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 24, 1848-1859.

Komiya, R., Ikegami, A., Tamaki, S., Yokoi, S., Shimamoto, K., 2008. Hd3a and RFT1 are essential for flowering in rice. Development 135, 767-774.

Komiya, R., Yokoi, S., Shimamoto, K., 2009. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136, 3443-3450.

LaJeunesse, D., Shearn, A., 1995. Trans-regulation of thoracic homeotic selector genes of the Antennapedia and bithorax complexes by the trithorax group genes:absent, small, and homeotic discs 1 and 2. Mech Dev. 53, 123-139.

Lee, Y.S., Yi, J., An, G., 2016. OsPhyA modulates rice flowering time mainly through OsGI under short days and Ghd7 under long days in the absence of phytochrome B. Plant Mol. Biol. 91, 413-427.

Liu, C., Lu, F., Cui, X., Cao, X., 2010. Histone methylation in higher plants. Annu. Rev. Plant Biol. 61, 395-420.

Liu, K., Yu, Y., Dong, A., Shen, W.H., 2017. SET DOMAIN GROUP701 encodes a H3K4-methytransferase and regulates multiple key processes of rice plant development. New Phytol. 215, 609-623.

Liu, Y., Liu, K., Yin, L., Yu, Y., Qi, J., Shen, W.H., Zhu, J., Zhang, Y., Dong, A., 2019. H3K4me2 functions as a repressive epigenetic mark in plants. Epigenetics Chromatin 12, 40.

Local, A., Huang, H., Albuquerque, C.P., Singh, N., Lee, A.Y., Wang, W., Wang, C., Hsia, J.E., Shiau, A.K., Ge, K., et al., 2018. Identification of H3K4me1-associated proteins at mammalian enhancers. Nat. Genet. 50, 73-82.

Ma, X., Zhang, Q., Zhu, Q., Liu, W., Chen, Y., Qiu, R., Wang, B., Yang, Z., Li, H., Lin, Y., et al., 2015. A Robust CRISPR/Cas9 System for Convenient, High-Efficiency Multiplex Genome Editing in Monocot and Dicot Plants. Mol. Plant 8, 1274-1284.

Miller, T., Krogan, N.J., Dover, J., Erdjument-Bromage, H., Tempst, P., Johnston, M., Greenblatt, J.F., Shilatifard, A., 2001. COMPASS:a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. U. S. A. 98, 12902-12907.

Mohan, M., Herz, H.M., Smith, E.R., Zhang, Y., Jackson, J., Washburn, M.P., Florens, L., Eissenberg, J.C., Shilatifard, A., 2011. The COMPASS family of H3K4 methylases in Drosophila. Mol. Cell. Biol. 31, 4310-4318.

Moreno-Perez, A.J., Santos-Pereira, J.M., Martins-Noguerol, R., DeAndres-Gil, C., Troncoso-Ponce, M.A., Venegas-Caleron, M., Sanchez, R., Garces, R., Salas, J.J., Tena, J.J., et al., 2021. Genome-Wide Mapping of Histone H3 Lysine 4 Trimethylation (H3K4me3) and Its Involvement in Fatty Acid Biosynthesis in Sunflower Developing Seeds. Plants (Basel)10, 706.

Nemoto, Y., Nonoue, Y., Yano, M., Izawa, T., 2016. Hd1, a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. Plant J. 86, 221-233.

Nishida, H., Okumoto, Y., Nakagawa, H., Ichitani, K., Inoue, H., Tanisaka, T., 2001. Analysis of Tester Lines for Rice (Oryza sativa L.) Heading-time Genes Using Reciprocal Photoperiodic Transfer Treatments. Annals of Botany 88, 527-536.

Oikawa, T., Koshioka, M., Kojima, K., Yoshida, H., Kawata, M., 2004. A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice. Plant Mol. Biol. 55, 687-700.

Patel, A., Dharmarajan, V., Vought, V.E., Cosgrove, M.S., 2009. On the mechanism of multiple lysine methylation by the human mixed lineage leukemia protein-1(MLL1) core complex. J. Biol. Chem. 284, 24242-24256.

Rada-Iglesias, A., 2018. Is H3K4me1 at enhancers correlative or causative? Nat. Genet. 50, 4-5.

Ren, Y., Tian, X., Li, S., Mei, E., He, M., Tang, J., Xu, M., Li, X., Wang, Z., Li, C., et al., 2020. Oryza sativa mediator subunit OsMED25 interacts with OsBZR1 to regulate brassinosteroid signaling and plant architecture in rice. Journal of integrative plant biology 62, 793-811.

Sakamoto, T., Morinaka, Y., Ohnishi, T., Sunohara, H., Fujioka, S., Ueguchi-Tanaka, M., Mizutani, M., Sakata, K., Takatsuto, S., Yoshida, S., et al., 2006. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat. Biotechnol. 24, 105-109.

Shan, C., Mei, Z., Duan, J., Chen, H., Feng, H., Cai, W., 2014. OsGA2ox5, a gibberellin metabolism enzyme, is involved in plant growth, the root gravity response and salt stress. PLoS One 9, e87110.

Shang, J.Y., Lu, Y.J., Cai, X.W., Su, Y.N., Feng, C., Li, L., Chen, S., He, X.J., 2021. COMPASS functions as a module of the INO80 chromatin remodeling complex to mediate histone H3K4 methylation in Arabidopsis. Plant Cell 33, 3250-3271.

Shilatifard, A., 2012. The COMPASS family of histone H3K4 methylases:mechanisms of regulation in development and disease pathogenesis. Annu. Rev. Biochem. 81, 65-95.

Sun, C., Chen, D., Fang, J., Wang, P., Deng, X., Chu, C., 2014. Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways. Protein Cell 5, 889-898.

Sun, C., Fang, J., Zhao, T., Xu, B., Zhang, F., Liu, L., Tang, J., Zhang, G., Deng, X., Chen, F., et al., 2012. The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. Plant Cell 24, 3235-3247.

Sun, C., Zhang, K., Zhou, Y., Xiang, L., He, C., Zhong, C., Li, K., Wang, Q., Yang, C., Wang, Q., et al., 2021. Dual function of clock component OsLHY sets critical day length for photoperiodic flowering in rice. Plant Biotechnol. J. 19, 1644-1657.

Sze, C.C., Shilatifard, A., 2016. MLL3/MLL4/COMPASS Family on Epigenetic Regulation of Enhancer Function and Cancer. Cold Spring Harb. Perspect. Med. 6, a026427.

Takahashi, Y.H., Westfield, G.H., Oleskie, A.N., Trievel, R.C., Shilatifard, A., Skiniotis, G., 2011. Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proc. Natl. Acad. Sci. U. S. A. 108, 20526-20531.

Tamaki, S., Matsuo, S., Wong, H.L., Yokoi, S., Shimamoto, K., 2007. Hd3a Protein Is a Mobile Flowering Signal in Rice. Science 316, 1033-1036.

Tian, X., Li, X., Zhou, W., Ren, Y., Wang, Z., Liu, Z., Tang, J., Tong, H., Fang, J., Bu, Q., 2017. Transcription Factor OsWRKY53 Positively Regulates Brassinosteroid Signaling and Plant Architecture. Plant Physiol. 175, 1337-1349.

Wang, C.C., Chang, P.C., Ng, K.L., Chang, C.M., Sheu, P.C., Tsai, J.J., 2014. A model comparison study of the flowering time regulatory network in Arabidopsis. Bmc Systems Biology 8, 1-12.

Wang, Y., Ding, Z., Liu, X., Bao, Y., Huang, M., Wong, C.C.L., Hong, X., Cong, Y., 2018. Architecture and subunit arrangement of the complete Saccharomyces cerevisiae COMPASS complex. Sci. Rep. 8, 17405.

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.

Yang, J., Lee, S., Hang, R., Kim, S.R., Lee, Y.S., Cao, X., Amasino, R., An, G., 2013. OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J. 73, 566-578.

Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba, T., Yamamoto, K., Umehara, Y., Nagamura, Y., 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.

Yoshitake, Y., Yokoo, T., Saito, H., Tsukiyama, T., Quan, X., Zikihara, K., Katsura, H., Tokutomi, S., Aboshi, T., Mori, N., et al., 2015. The effects of phytochrome-mediated light signals on the developmental acquisition of photoperiod sensitivity in rice. Sci. Rep. 5, 7709.

Zhao, W., Neyt, P., Lijsebettens, M.V., Shen, W.H., Berr, A., 2019. Interactive and noninteractive roles of histone H2B monoubiquitination and H3K36 methylation in the regulation of active gene transcription and control of plant growth and development. New Phytol. 221, 1101-1116.

Zong, W., Ren, D., Huang, M., Sun, K., Feng, J., Zhao, J., Xiao, D., Xie, W., Liu, S., Zhang, H., et al., 2020. Strong photoperiod sensitivity is controlled by cooperation and competition among Hd1, Ghd7 and DTH8 in rice heading. New Phytol. 229, 1635-1649

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