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Volume 50 Issue 10
Oct.  2023
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Article Contents

The CCT transcriptional activator Ghd2 constantly delays the heading date by upregulating CO3 in rice

doi: 10.1016/j.jgg.2023.03.002
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This study was supported by the Natural Science Foundation of China (U20A2031) and the Earmarked Fund for China Agricultural Research System (CARS-01).

  • Received Date: 2023-02-27
  • Accepted Date: 2023-03-03
  • Rev Recd Date: 2023-03-03
  • Publish Date: 2023-03-10
  • CONSTANS, CO-like, and TOC1 (CCT) family genes play important roles in regulating heading date, which exerts a large impact on the regional and seasonal adaptation of rice. Previous studies have shown that Grain number, plant height, and heading date2 (Ghd2) exhibits a negative response to drought stress by directly upregulating Rubisco activase and exerting a negative effect on heading date. However, the target gene of Ghd2 regulating heading date is still unknown. In this study, CO3 is identified by analyzing Ghd2 ChIP-seq data. Ghd2 activates CO3 expression by binding to the CO3 promoter through its CCT domain. EMSA experiments show that the motif CCACTA in the CO3 promoter was recognized by Ghd2. A comparison of the heading dates among plants with CO3 knocked out or overexpressed and double-mutants with Ghd2 overexpressed and CO3 knocked out shows that CO3 negatively and constantly regulates flowering by repressing the transcription of Ehd1, Hd3a, and RFT1. In addition, the target genes of CO3 are explored via a comprehensive analysis of DAP-seq and RNA-seq data. Taken together, these results suggest that Ghd2 directly binds to the downstream gene CO3, and the Ghd2-CO3 module constantly delays heading date via the Ehd1-mediated pathway.
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  • Cai, Y., Chen, X., Xie, K., Xing, Q., Wu, Y., Li, J., Du, C., Sun, Z., Guo, Z.,Zhang, J.S., 2014. Dlf1, a wrky transcription factor, is involved in the control of flowering time and plant height in rice. PLoS One 9, e102529.
    Chai, J., Zhu, S., Li, C., Wang, C., Cai, M., Zheng, X., Zhou, L., Zhang, H., Sheng, P.,Wu, M., 2021. Osre1 interacts with osrip1 to regulate rice heading date by finely modulating ehd1 expression. Plant Biotechnol. J. 19, 300-310.
    Cho, L.-H., Yoon, J., Pasriga, R.,An, G., 2016. Homodimerization of ehd1 is required to induce flowering in rice. Plant Physiol. 170, 2159-2171.
    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.
    Dong, M.-Y., Lei, L., Fan, X.-W.,Li, Y.-Z., 2021. Analyses of open-access multi-omics data sets reveal genetic and expression characteristics of maize zmcct family genes. AoB Plants 13, plab048.
    Ecker, Joseph R., Galli, Mary, Huang, Shao-shan, Carol, Gallavotti,Andrea, 2017. Mapping genome-wide transcription-factor binding sites using dap-seq. Nat. Protoc. Erecipes for Researchers 12, 1659-1672.
    Engler, C., Gruetzner, R., Kandzia, R.,Marillonnet, S., 2009. Golden gate shuffling: a one-pot DNA shuffling method based on type iis restriction enzymes. PLoS One 4, e5553.
    Engler, C., Kandzia, R., Marillonnet, S.,El-Shemy, H.A., 2008. A one pot, one step, precision cloning method with high throughput capability. PLoS One 3, e3647.
    Fan, X., Liu, J., Zhang, Z., Xi, Y., Li, S., Xiong, L.,Xing, Y., 2022. A long transcript mutant of the rubisco activase gene rca upregulated by the transcription factor ghd2 enhances drought tolerance in rice. Plant J. 110, 673-687.
    Feng, C., Cai, X.W., Su, Y.N., Li, L., Chen, S.,He, X.J., 2021. Arabidopsis rpd3-like histone deacetylases form multiple complexes involved in stress response. J. Genet. Genomics 48, 369-383.
    Gao, X., Zhang, K., Zhou, H., Zellmer, L., Yuan, C., Huang, H.,Liao, D.J., 2021. At elevated temperatures, heat shock protein genes show altered ratios of different rnas and expression of new rnas, including several novel hspb1 mrnas encoding hsp27 protein isoforms. Exp. Ther. Med. 22, 1-11.
    Hendelman, A., Zebell, S., Rodriguez-Leal, D., Dukler, N., Robitaille, G., Wu, X., Kostyun, J., Tal, L., Wang, P.,Bartlett, M.E., 2021. Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection. Cell 184, 1724-1739. e1716.
    Hills, CB, Li,C, 2016. Genetic architecture of flowering phenology in cereals and opportunities for crop improvement. Front. Plant Sci. 7, 1906.
    Jang, S., Marchal, V., Panigrahi, K.C., Wenkel, S., Soppe, W., Deng, X.W., Valverde, F.,Coupland, G., 2008. Arabidopsis cop1 shapes the temporal pattern of co accumulation conferring a photoperiodic flowering response. EMBO J. 27, 1277-1288.
    Kim, S., K., Yun, C., H., Lee, J., H., Jang, Y., H., Park,H., Y., 2008. Osco3, a constans-like gene, controls flowering by negatively regulating the expression of ft-like genes under sd conditions in rice. PLANTA -BERLIN- 228, 355-365.
    Laubinger, S., Marchal, V., Gentilhomme, J., Wenkel, S., Adrian, J., Jang, S., Kulajta, C., Braun, H., Coupland, G.,Hoecker, U., 2006. Arabidopsis spa proteins regulate photoperiodic flowering and interact with the floral inducer constans to regulate its stability. Development 133, 3213-3222.
    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., 2010. Oscol4 is a constitutive flowering repressor upstream of ehd1 and downstream of osphyb. Plant J. 63, 18-30.
    Lei, Y., Lu, L., Liu, H.Y., Li, S., Xing, F.,Chen, L.L., 2014. Crispr-p: a web tool for synthetic single-guide rna design of crispr-system in plants. Mol. Plant 7, 1494-1496.
    Li, S., Hu, Y., An, C., Wen, Q., Fan, X., Zhang, Z., Sherif, A., Liu, H.,Xing, Y., 2022a. The amino acid residue e96 orf ghd8 is crucial for the formation of the flowering repression complex ghd7-ghd8-oshap5c in rice. J. Integr. Plant Biol. doi: 10.1111/jipb.13426.
    Li, Y.,Xu, M., 2017. CCT family genes in cereal crops: a current overview. Crop J.
    Li, Y., Yu, S., Zhang, Q., Wang, Z., Liu, M., Zhang, A., Dong, X., Fan, J., Zhu, Y.,Ruan, Y., 2022b. Genome-wide identification and characterization of the cct gene family in foxtail millet (setaria italica) response to diurnal rhythm and abiotic stress. Genes 13, 1829.
    Liang, L., Zhang, Z., Cheng, N., Liu, H., Song, S., Hu, Y., Zhou, X., Zhang, J.,Xing, Y., 2021. The transcriptional repressor osprr73 links circadian clock and photoperiod pathway to control heading date in rice. Plant Cell Environ. 44, 842-855.
    Lin, Y.J.,Zhang, Q., 2005. Optimising the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep. 23, 540-547.
    Liu, H., Dong, S., Sun, D., Liu, W., Gu, F., Liu, Y., Guo, T., Wang, H., Wang, J.,Chen, Z., 2016a. Constans-like 9 (oscol9) interacts with receptor for activated c-kinase 1 (osrack1) to regulate blast resistance through salicylic acid and ethylene signaling pathways. PLoS One 11, e0166249.
    Liu, H., Huang, X., Ma, B., Zhang, T., Sang, N., Zhuo, L.,Zhu, J., 2021. Components and functional diversification of florigen activation complexes in cotton. Plant Cell Physiol. 62, 1542-1555.
    Liu, H., Zhou, X., Li, Q., Wang, L.,Xing, Y., 2020. Cct domain-containing genes in cereal crops: flowering time and beyond. Theor. Appl. Genet. 133, 1385-1396.
    Liu, J., Shen, J., Xu, Y., Li, X., Xiao, J.,Xiong, L., 2016b. Ghd2, a constans-like gene, confers drought sensitivity through regulation of senescence in rice. J. Exp. Bot. 67, 5785-5798.
    Liu, L.-J., Zhang, Y.-C., Li, Q.-H., Sang, Y., Mao, J., Lian, H.-L., Wang, L.,Yang, H.-Q., 2008. Cop1-mediated ubiquitination of constans is implicated in cryptochrome regulation of flowering in arabidopsis. Plant Cell 20, 292-306.
    Ma, X., 2015. A robust crispr/cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274-1284.
    Mengarelli, D.A.,Zanor, M.I., 2021. Genome-wide characterization and analysis of the cct motif family genes in soybean (glycine max). Planta 253, 1-17.
    Min, J.H., Chung, J.S., Lee, K.H.,Kim, C.S., 2015. The constans-like 4 transcription factor, atcol4, positively regulates abiotic stress tolerance through an abscisic acid-dependent manner in arabidopsis. J. Integr. Plant Biol. 57, 313-324.
    Morita, R., Sugino, M., Hatanaka, T., Misoo, S.,Fukayama, H., 2015. Co2-responsive constans, constans-like, and time of chlorophyll a/b binding protein expression1 protein is a positive regulator of starch synthesis in vegetative organs of rice. Plant Physiol. 167, 1321-1331.
    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.
    Osella, A.V., Mengarelli, D.A., Mateos, J., Dong, S., Yanovsky, M.J., Balazadeh, S., Valle, E.M.,Zanor, M.I., 2018. Fitness, a cct domain-containing protein, deregulates reactive oxygen species levels and leads to fine-tuning trade-offs between reproductive success and defence responses in arabidopsis. Plant Cell Environ. 41, 2328-2341.
    Osugi, A., Itoh, H., Ikeda-Kawakatsu, K., Takano, M.,Izawa, T., 2011. Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol. 157, 1128-1137.
    Sawa, M., Nusinow, D.A., Kay, S.A.,Imaizumi, T., 2007. Fkf1 and gigantea complex formation is required for day-length measurement in arabidopsis. Science 318, 261-265.
    Shen, C., Liu, H., Guan, Z., Yan, J., Zheng, T., Yan, W., Wu, C., Zhang, Q., Yin, P.,Xing, Y., 2020. Structural insight into DNA recognition by cct/nf-yb/yc complexes in plant photoperiodic flowering. Plant Cell 32, 3469-3484.
    Shen, J., Liu, J., Xie, K., Xing, F., Xiong, F., Xiao, J., Li, X.,Xiong, L., 2017. Translational repression by a miniature inverted-repeat transposable element in the 3' untranslated region. Nat. Commun. 8, 1-10.
    Sheng, P., Wu, F., Tan, J., Zhang, H., Ma, W., Chen, L., Wang, J., Wang, J., Zhu, S.,Guo, X., 2016. A constans-like transcriptional activator, oscol13, functions as a negative regulator of flowering downstream of osphyb and upstream of ehd1 in rice. Plant Mol. Biol. 92, 209-222.
    Shim, J.S.,Jang, G., 2020. Environmental signal-dependent regulation of flowering time in rice. Int. J. Mol. Sci. 21, 6155.
    Shrestha, R., Gomez-Ariza, J., Brambilla, V.,Fornara, F., 2014. Molecular control of seasonal flowering in rice, arabidopsis and temperate cereals. Ann. Bot. 114, 1445-1458.
    Song, Y.H., Ito, S.,Imaizumi, T., 2013. Flowering time regulation: photoperiod-and temperature-sensing in leaves. Trends Plant Sci. 18, 575-583.
    Sun, K., Huang, M., Zong, W., Xiao, D., Lei, C., Luo, Y., Song, Y., Li, S., Hao, Y.,Luo, W., 2022. Hd1, ghd7, and dth8 synergistically determine the rice heading date and yield-related agronomic traits. J. Genet. Genomics 49, 437-447.
    Wang, G., Li, X., Ye, N., Huang, M., Feng, L., Li, H.,Zhang, J., 2021. Ostpp1 regulates seed germination through the crosstalk with abscisic acid in rice. New Phytol. 230, 1925-1939.
    Wang, P., Qi, F., Yao, H., Xu, X., Li, W., Meng, J., Zhang, Q., Xie, W.,Xing, Y., 2022. Fixation of hybrid sterility genes and favorable alleles of key yield-related genes with dominance contribute to the high yield of the Yongyou series of intersubspecific hybrid rice. J. Genet. Genomics 49, 448-457.
    Wang, L., Sun, S., Jin, J., Fu, D., Zhang, Q., 2015. Coordinated regulation of vegetative and reproductive branching in rice. Proc Natl Acad Sci USA 112, 15504–15509.
    Wei, H., Wang, X., He, Y., Xu, H.,Wang, L., 2020. Clock component osprr73 positively regulates rice salt tolerance by modulating oshkt2;1-ediated sodium homeostasis. EMBO J. 40.
    Wei, X., Xu, J., Guo, H., Jiang, L., Chen, S., Yu, C., Zhou, Z., Hu, P., Zhai, H.,Wan, J., 2010. Dth8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol. 153, 1747-1758.
    Wu, W., Zhang, Y., Zhang, M., Zhan, X., Shen, X., Yu, P., Chen, D., Liu, Q., Sinumporn, S.,Hussain, K., 2018. The rice constans-like protein oscol15 suppresses flowering by promoting ghd7 and repressing rid1. Biochem. Biophys. Res. Commun. 495, 1349-1355.
    Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C.,Li, X., 2008. Natural variation in ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761-767.
    Yan, W., Liu, H., Zhou, X., Li, Q., Zhang, J., Lu, L., Liu, T., Liu, H., Zhang, C.,Zhang, Z., 2013. Natural variation in ghd7. 1 plays an important role in grain yield and adaptation in rice. Cell Res. 23, 969-971.
    Yan, W.-H., Wang, P., Chen, H.-X., Zhou, H.-J., Li, Q.-P., Wang, C.-R., Ding, Z.-H., Zhang, Y.-S., Yu, S.-B.,Xing, Y.-Z., 2011. A major qtl, ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol. Plant 4, 319-330.
    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.
    Yoo, S.D., Cho, Y.H., Sheen, J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
    Zhang, B., Liu, H., Qi, F., Zhang, Z., Li, Q., Han, Z.,Xing, Y., 2019. Genetic interactions among ghd7, ghd8, osprr37 and hd1 contribute to large variation in heading date in rice. Rice 12, 1-13.
    Zhang, C., Liu, J., Zhao, T., Gomez, A., Li, C., Yu, C., Li, H., Lin, J., Yang, Y.,Liu, B., 2016. A drought-inducible transcription factor delays reproductive timing in rice. Plant Physiol., 334.
    Zhang, J., Fan, X.W., Hu, Y., Zhou, X.C., He, Q., Liang, L.W.,Xing, Y.Z., 2021. Global analysis of cct family knockout mutants identifies four genes involved in regulating heading date in rice. J. Integr. Plant Biol. 63, 913-923.
    Zhang, L., Li, Q., Dong, H., He, Q., Liang, L., Tan, C., Han, Z., Yao, W., Li, G.,Zhao, H., 2015. Three cct domain-containing genes were identified to regulate heading date by candidate gene-based association mapping and transformation in rice. Sci. Rep. 5, 1-11.
    Zhang, Z.Y., Hu, W., Shen, G.J., Liu, H.Y., Hu, Y., Zhou, X.C., Liu, T.M.,Xing, Y.Z., 2017. Alternative functions of hd1 in repressing or promoting heading are determined by ghd7 status under long-day conditions. Sci. Rep. 7.
    Zhou, S., Zhu, S., Cui, S., Hou, H., Wu, H., Hao, B., Cai, L., Xu, Z., Liu, L.,Jiang, L., 2021a. Transcriptional and post-transcriptional regulation of heading date in rice. New Phytol. 230, 943-956.
    Zhao, G., Wang, J., Chen, X., Sha, H., Liu, X., Han, Y., Qiu, G., Zhang, F., Fang, J., 2022. Osashl1 and osashl2,two members of the compass-like complex,control floral transition and plant development in rice. J. Genet. Genomics 49, 870–880.
    Zhou, X., He, J., Velanis, C.N., Zhu, Y., He, Y., Tang, K., Zhu, M., Graser, L., Leau, E.D.,Wang, X., 2021b. A domesticated harbinger transposase forms a complex with hda6 and promotes histone h3 deacetylation at genes but not tes in arabidopsis. J. Genet. Genomics 63, 13.
    Zong, W., Ren, D., Huang, M., Sun, K., Feng, J., Zhao, J., Xiao, D., Xie, W., Liu, S.,Zhang, H., 2021. Strong photoperiod sensitivity is controlled by cooperation and competition among hd1, ghd7 and dth8 in rice heading. New Phytol. 229, 1635-1649.
    Zong, W., Tang, N., Yang, J., Peng, L., Ma, S., Xu, Y., Li, G., Xiong, L. 2016. Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought-resistance-related genes. Plant Physiol. 171, 2810-2825.
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