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Volume 49 Issue 5
May  2022
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Article Contents

Hd1, Ghd7, and DTH8 synergistically determine the rice heading date and yield-related agronomic traits

doi: 10.1016/j.jgg.2022.02.018
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We thank Prof. Zhiqiang Chen for providing rice materials. This work was supported by grants from the National Natural Science Foundation of China (31921004 and 31871596), the Major Program of Guangdong Basic and Applied Research (2019B030302006), and the Laboratory of Lingnan Modern Agriculture Project (NT2021002).

  • Received Date: 2021-11-04
  • Accepted Date: 2022-02-16
  • Rev Recd Date: 2022-02-13
  • Publish Date: 2022-03-04
  • Heading date determines the seasonal and regional adaptation of rice (Oryza sativa L.) varieties and is mainly controlled by photoperiod sensitivity (PS). The core heading date genes Hd1, Ghd7, DTH8, and PRR37 act synergistically in regulating the PS. In this study, we systematically analyze the heading date, PS, and agronomic traits of eight homozygous lines with various combinations of Hd1, Ghd7, and DTH8 alleles in the prr37 background under long-day (LD) and short-day (SD) conditions, respectively. We find that Hd1 alone promotes heading, regardless of the day length. However, under LDs, Hd1 suppresses flowering, in coordination with functional Ghd7 or with Ghd7 and DTH8. These loci cooperate to negatively regulate the Ehd1-Hd3a/RFT1 pathway and delay heading. Under SDs, Hd1 competes with various heading suppressors to promote heading. Therefore, the dual function of Hd1 is vital for PS. The lines carrying Hd1 alone show reduced plant height with fewer primary and secondary branches in panicles. Lines carrying Ghd7 and DTH8 (with hd1) show delayed heading and improve agronomic traits. Overall, our results reveal the regulation of rice PS flowering by the core heading date genes and their effects on agronomic traits, providing valuable information for the selection of rice varieties for adaptation to different light and temperature conditions.
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  • Brambilla, V., Fornara, F., 2017. Y flowering? Regulation and activity of CONSTANS and CCT-domain proteins in Arabidopsis and crop species. Biochim. Biophys. Acta. Gene Regul. Mech. 1860, 655-660
    Cai, M., Chen, S., Wu, M., Zheng, T., Zhou, L., Li, C., Zhang, H., Wang, J., Xu, X., Chai, J., et al., 2019. Early heading 7 interacts with DTH8, and regulates flowering time in rice. Plant Cell Rep. 38, 521-532
    Chaves-Sanjuan, A., Gnesutta, N., Gobbini, A., Martignago, D., Bernardini, A., Fornara, F., Mantovani, R., Nardini, M., 2021. Structural determinants for NF-Y subunit organization and NF-Y/DNA association in plants. Plant J. 105, 49-61
    Chen, R., Deng, Y., Ding Y., Guo, J., Qiu, J., Wang, B., Wang, C., Xie, Y., Zhang, Z., Chen, J., et al., 2021. Rice functional genomics: decades' efforts and roads ahead. Sci. China Life Sci. 10.1007/s11427-021-2024-0
    Dai, X., Ding, Y., Tan, L., Fu, Y., Liu, F., Zhu, Z., Sun, X., Sun, X., Gu, P., Cai, H., et al., 2012. LHD1, an allele of DTH8/Ghd8, controls late heading date in common wild rice (Oryza rufipogon). J. Integr. Plant Biol. 54, 790-799
    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
    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
    Endo-Higashi, N., Izawa, T., 2011. Flowering time genes Heading date 1 and Early heading date 1 together control panicle development in rice. Plant Cell Physiol. 52, 1083-1094
    Fujino, K., Yamanouchi, U., Nonoue, Y., Obara, M., Yano, M., 2019. Switching genetic effects of the flowering time gene Hd1 in LD conditions by Ghd7 and OsPRR37 in rice. Breed Sci. 69, 127-132
    Gao, H., Jin, M., Zheng, X. M., Chen, J., Yuan, D., Xin, Y., Wang, M., Huang, D., Zhang, Z., Zhou, K., et al., 2014. Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc. Natl. Acad. Sci. U.S.A. 111, 16337-16342
    Gomez-Ariza, J., Galbiati, F., Goretti, D., Brambilla, V., Shrestha, R., Pappolla, A., Courtois, B., Fornara, F., 2015. Loss of floral repressor function adapts rice to higher latitudes in Europe. J. Exp. Bot. 66, 2027-2039
    Goretti, D., Martignago, D., Landini, M., Brambilla, V., Gomez-Ariza, J., Gnesutta, N., Galbiati, F., Collani, S., Takagi, H., Terauchi, R., et al., 2017. Transcriptional and post-transcriptional mechanisms limit Heading date 1 (Hd1) function to adapt rice to high latitudes. PLoS Genet. 13, e1006530
    Huang, X., Kurata, N., Wei, X., Wang, Z. X., Wang, A., Zhao, Q., Zhao, Y., Liu, K., Lu, H., Li, W., et al., 2012. A map of rice genome variation reveals the origin of cultivated rice. Nature 490 (7421), 497-501
    Immark, S., Mitchell, J. H., Jongdee, B., Boonwite, C., Somrith, B., Polvatana, A., Fukai, S., 1997. Determination of phenology development in rainfed lowland rice in Thailand and Lao PDR. Breed. Strat. Rain Fed. Lowl. Rice Drought-Prone Environ. 77, 89-97
    Ishikawa, R., Tamaki, S., Yokoi, S., Inagaki, N., Shinomura, T., Takano, M., Shimamoto, K., 2005. Suppression of the floral activator Hd3a is the principal cause of the night break effect in rice. Plant Cell 17, 3326-3336
    Izawa T, 2007. Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J. Exp. Bot. 58, 3091-3097
    Jin L., Lu Y., Xiao P., Sun M., Corke H., Bao J., 2010. Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor. Appl. Genet. 121, 475-487
    Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T., Yano, M., 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
    Komiya, R., Ikegami, A., Tamaki, S., Yokoi, S., Shimamoto, K., 2008. Hd3a and RFT1 are essential for flowering in rice. Development. 135, 767-774
    Koo, B. H., Yoo, S. C., Park, J. W., Kwon, C. T., Lee, B. D., An, G., Zhang, Z., Li, J., Li, Z., Paek, N. C., 2013. Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol. Plant 6, 1877-1888
    Leng, Y., Gao, Y., Chen, L., Yang, Y., Huang, L., Dai, L., Ren, D., Xu, Q., Zhang, Y., Ponce, K., et al., 2020. Using Heading date 1 preponderant alleles from indica cultivars to breed high-yield, high-quality japonica rice varieties for cultivation in south China. Plant Biotechnol. J. 18, 119-128
    Li, X., Liu, H., Wang, M., Liu, H., Tian, X., Zhou, W., Lu, T., Wang, Z., Chu, C., Fang, J., et al., 2015. Combinations of Hd2 and Hd4 genes determine rice adaptability to Heilongjiang Province, northern limit of China. J. Integr. Plant Biol. 57, 698-707
    Liu, T., Liu, H., Zhang, H., Xing, Y., 2013. Validation and characterization of Ghd7.1, a major quantitative trait locus with pleiotropic effects on spikelets per panicle, plant height, and heading date in rice (Oryza sativa L.). J. Integr. Plant Biol. 55, 917-927
    Liu, Y., Wang, H., Liang, K., Zhang, J., Guo, T., Xiao, M., Chen, Z., 2014. Breeding and utilization of indica CMS line Ning A with good grain quality and blast resistance in rice. Hybrid. Rice 29, 10-11
    Liu, C., Song, G., Zhou, Y., Qu, X., Guo, Z., Liu, Z., Jiang, D., Yang, D., 2015. OsPRR37 and Ghd7 are the major genes for general combining ability of DTH, PH and SPP in rice. Sci. Rep. 5, 12803
    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, S., Song, M., 2021. Analysis on the contribution rate of variety improvement to corn yield. J. Henan Agric. Univ. 55, 364-371
    Matsubara, K., Ogiso-Tanaka, E., Hori, K., Ebana, K., Ando, T., 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
    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
    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
    Song, Y. H., Shim, J. S., Kinmonth-Schultz, H. A., Imaizumi, T., 2015. Photoperiodic flowering: time measurement mechanisms in leaves. Annu. Rev. Plant Biol. 66, 441-464
    Su, L., Shan, J. X., Gao, J. P., Lin, H. X., 2016. OsHAL3, a blue light-responsive protein, interacts with the floral regulator Hd1 to activate flowering in rice. Mol. Plant 9, 233-244
    Takahashi, Y., Teshima, K. M., Yokoi, S., Innan, H., 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
    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
    Tiwari, S. B., Shen, Y., Chang, H. C., Hou, Y., Harris, A., Ma, S. F., McPartland, M., Hymus, G. J., Adam, L., Marion, C., et al., 2010. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187, 57-66
    Wang, P., Gong, R., Yang, Y., Yu, S., 2019. Ghd8 controls rice photoperiod sensitivity by forming a complex that interacts with Ghd7. BMC Plant Biol. 19, 462
    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
    Weng, X., Wang, L., Wang, J., Hu, Y., Du, H., Xu, C., Xing, Y., Li, X., Xiao, J., Zhang, Q., 2014. Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response. Plant Physiol. 164, 735-747
    Wu, W., Zheng, X., Lu, G., Zhong, Z., Gao, H., Chen, L., Wu, C., Wang, H., Wang, Q., Zhou, K., 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
    Xiao, W., Luo, L., Wang, H., Liu, Y., Guo, T., Liang, K., Huang, M., Wang, J., Wang, W., Yang, Q., et al., 2017. Breeding and utilization of restorer line Hanghui 1179 with good blast resistance in rice. Hybrid. Rice 32, 18-22
    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
    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., 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
    Yan, W., Liu, H., Zhou, X., Li, Q., Zhang, J., Lu, L., Liu, T., Liu, H., Zhang, C., Zhang, Z., et al. 2013. Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice. Cell Res. 23, 969-971
    Yang, Y., Fu, D., Zhu, C., He, Y., Zhang, H., Liu, T., Li, X., Wu, C., 2015. The RING-Finger ubiquitin ligase HAF1 mediates Heading date 1 degradation during photoperiodic flowering in rice. Plant Cell 27, 2455-2468
    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, 2473-2484
    Ye, J., Niu, X., Yang, Y., Wang, S., Xu, Q., Yuan, X., Yu, H., Wang, Y., Wang, S., Feng, Y., et al., 2018. Divergent Hd1, Ghd7, and DTH7 alleles control heading date and yield potential of japonica rice in Northeast China. Front. Plant Sci. 9, 35
    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. 208, 1056-1066
    Zhang, Z., Cao, L., Chen, J., Zhang, Y., Zhuang, J., Cheng, S., 2016. Effects of Hd2 in the presence of the photoperiod-insensitive functional allele of Hd1 in rice. Biol. Open. 5, 1719-1726
    Zhang, Z., Hu, W., Shen, G., Liu, H., Hu, Y., Zhou, X., Liu, T., Xing, Y., 2017a. Alternative functions of Hd1 in repressing or promoting heading are determined by Ghd7 status under long-day conditions. Sci. Rep. 7, 5388
    Zhang, J., Hu, Y., Xu, L., He, Q., Fan, X., Xing, Y., 2017b. The CCT domain-containing gene family has large impacts on heading date, regional adaptation, and grain yield in rice. J. Integr. Agric. 16, 2686-2697
    Zhang, B., Liu, H., Qi, F., Zhang, Z., Li, Q., Han, Z., Xing, Y., 2019a. Genetic interactions among Ghd7, Ghd8, OsPRR37 and Hd1 aontribute to large variation in heading date in rice. Rice 12, 48
    Zhang, Z., Zhang, B., Qi, F., Wu, H., Li, Z., Xing, Y., 2019b. Hd1 function conversion in regulating heading is dependent on gene combinations of Ghd7, Ghd8, and Ghd7.1 under long-day conditions in rice. Mol. Breed. 39, 92
    Zhang, W., Liang, W., Zhang, Z., Hao, T., 2021. Aerobic granular sludge (AGS) scouring to mitigate membrane fouling: performance, hydrodynamic mechanism and contribution quantification model. Water Res. 188, 116518
    Zhao, J., Chen, H., Ren, D., Tang, H., Qiu, R., Feng, J., Long, Y., Niu, B., Chen, D., Zhong, T., 2015. Genetic interactions between diverged alleles of Early heading date 1 (Ehd1) and Heading date 3a (Hd3a)/RICE FLOWERING LOCUS T1 (RFT1) control differential heading and contribute to regional adaptation in rice (Oryza sativa). New Phytol. 208, 936-948
    Zhou, S., Zhu, S., Cui, S., Hou, H., Wu, H., Hao, B., Cai, L., Xu, Z., Liu, L., Jiang, L., 2021. Transcriptional and post-transcriptional regulation of heading date in rice. New Phytol. 230, 943-956
    Zong, W., Ren, D., Huang, M., Sun, K., Feng, J., Zhao, J., Xiao, D., Xie, W., Liu, S., Zhang, H., et al., 2021. 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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