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Transcription factor bZIP65 delays flowering via suppressing Ehd1 expression in rice

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Abstract

Flowering time is one of the most fundamental factors that determine the distribution and final yield of rice. Ehd1 (Early heading date 1) is a B-type response regulator which functions as a flowering time activator. Although diverse flowering time genes have been reported as regulatory factors of Ehd1 expression, the potential regulators of Ehd1 largely remain to be identified. Here, we identified a basic leucine zipper transcription factor bZIP65, a homolog of bZIP71, as a new negative regulator of Ehd1. The overexpression of bZIP65 delays flowering, while bzip65 mutants have similar flowering time to SJ2 (Songjing2) in both long-day and short-day conditions. Biochemically, bZIP65 associates with Ehd1 promoter and transcriptionally represses the expression of Ehd1. Moreover, we found that bZIP65 enhances H3K27me3 level of Ehd1. Taken together, we cloned a new gene, bZIP65, regulating rice heading date, and uncovered the mechanism of bZIP65 delaying flowering time, where bZIP65 increases the H3K27me3 level of Ehd1 and transcriptionally represses the expression of Ehd1, similar to its homolog bZIP71.

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Fig. 1

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Abbreviations

SD :

short-day

LD :

long-day

Hd1 :

Heading date1

Ehd1 :

Early heading date1

Hd3a :

Heading date 3a

RFT1 :

RICE FLOWERING LOCUS T1

Hd2 :

Heading date 2

Hd4 :

Heading date 4

Hd5 :

Heading date 5

COL4 :

CONSTANS-like 4

DTH3 :

Days to Heading 3

Ehd2 :

Early heading date 2

Ehd4 :

Early heading date 4

Hd17 :

Heading date 17

SDG :

SET domain group protein

OsTrx1 :

Trithorax-like protein

PRC2 :

Polycomb-Repressive Complex 2

DHD4 :

delayed heading date 4

bZIP :

basic leucine zipper

FAC :

florigen activation complex

HBF1 :

Hd3a BINDING REPRESSOR FACTOR 1

OsABF1 :

ABA-responsive element binding factor 1

LUC :

Firefly luciferase

REN :

Renilla luciferase

References

  • Brambilla V, Martignago D, Goretti D, Cerise M, Somssich M, de Rosa M, Galbiati F, Shrestha R, Lazzaro F, Simon R, Fornara F (2017) Antagonistic transcription factor complexes modulate the floral transition in rice. Plant Cell 29(11):2801–2816

    Article  CAS  Google Scholar 

  • Cai MH, Zhu SS, Wu MM, Zheng XM, Wang JC, Zhou L, Zheng TH, Cui S, Zhou SR, Li CN, Zhang H, Chai JT, Zhang XY, Jin X, Cheng ZJ, Zhang X, Lei CL, Ren YL, Lin QB, Guo XP, Zhao L, Wang J, Zhao ZC, Jiang L, Wang HY, Wan JM (2021) DHD4, a CONSTANS-like family transcription factor, delays heading date by affecting the formation of the FAC complex in rice. Mol Plant 14(2):330–343

    Article  CAS  Google Scholar 

  • Chai J, Zhu S, Li C, Wang C, Cai M, Zheng X, Zhou L, Zhang H, Sheng P, Wu M, Jin X, Cheng Z, Zhang X, Lei C, Ren Y, Lin Q, Zhou S, Guo X, Wang J, Zhao Z, Wan J (2021) OsRE1 interacts with OsRIP1 to regulate rice heading date by finely modulating Ehd1 expression. Plant Biotechnol J 19(2):300–310

    Article  CAS  Google Scholar 

  • Choi SC, Lee S, Kim SR, Lee YS, Liu C, Cao X, An G (2014) Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3. Plant Physiol 164(3):1326–1337

    Article  CAS  Google Scholar 

  • 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 Development 18(8):926–936

    Article  CAS  Google Scholar 

  • Gao H, Zheng XM, Fei GL, Chen J, Jin MN, Ren YL, Wu WX, Zhou KN, Sheng PK, Zhou F, Jiang L, Wang J, Zhang X, Guo XP, Wang JL, Cheng ZJ, Wu CY, Wang HY, Wan JM (2013) Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLoS Genet 9(2):e1003281

    Article  CAS  Google Scholar 

  • Gao H, Jin M, Zheng XM, Chen J, Yuan D, Xin Y, Wang M, Huang D, Zhang Z, Zhou K, Sheng P, Ma J, Ma W, Deng H, Jiang L, Liu S, Wang H, Wu C, Yuan L, Wan J (2014) Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc Natl Acad Sci 111(46):16337–16342

    Article  CAS  Google Scholar 

  • Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422(6933):719–722

    Article  CAS  Google Scholar 

  • Hori K, Matsubara K, Yano M (2016) Genetic control of flowering time in rice: integration of Mendelian genetics and genomics. Theor Appl Genet 129(12):2241–2252

    Article  Google Scholar 

  • Jiang PF, Wang SL, Jiang HY, Cheng BJ, Wu KQ, Ding Y (2018) The COMPASS-like complex promotes flowering and panicle branching in rice. Plant Physiol 176(4):2761–2771

    Article  CAS  Google Scholar 

  • 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(20):3443–3450

    Article  CAS  Google Scholar 

  • Lee YS, Jeong DH, Lee DY, Yi J, Ryu CH, Kim SL, Jeong HJ, Choi SC, Jin P, Yang J, Cho LH, Choi H, An G (2010) OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J 63(1):18–30

    CAS  PubMed  Google Scholar 

  • Leng YJ, Gao Y, Chen LH, Yang YL, Huang LC, Dai LP, Ren DY, Xu QK, Zhang Y, Ponce K, Hu J, Shen L, Zhang GH, Chen G, Dong GJ, Gao ZY, Guo LB, Ye GY, Qian Q, Zhu L, Zeng DL (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(1):119–128

    Article  CAS  Google Scholar 

  • Li XF, Tian XJ, He ML, Liu XX, Li ZY, Tang JQ, Mei EY, Xu M, Liu YX, Wang ZY, Guan QJ, Meng W, Fang J, Zhang J, Bu QY (2022) bZIP71 delays flowering by suppressing Ehd1 expression in rice. J Integr Plant Biol 64(7):1352–1363

    Article  CAS  Google Scholar 

  • Liu XY, Zhou C, Zhao Y, Zhou SL, Wang WT, Zhou DX (2014) The rice enhancer of zeste [E(z)] genes SDG711 and SDG718 are respectively involved in long day and short day signaling to mediate the accurate photoperiod control of flowering time. Front Plant Sci 5:591

    Article  Google Scholar 

  • Liu B, Wei G, Shi JL, Jin J, Shen T, Ni T, Shen WH, Yu Y, Dong AW (2016) SET DOMAIN GROUP 708, a histone H3 lysine 36-specific methyltransferase, controls flowering time in rice (Oryza sativa). New Phytol 210(2):577–588

    Article  CAS  Google Scholar 

  • Liu KP, Yu Y, Dong AW, Shen WH (2017) SET DOMAIN GROUP701 encodes a H3K4-methytransferase and regulates multiple key processes of rice plant development. New Phytol 215(2):609–623

    Article  CAS  Google Scholar 

  • Matsubara K, Yamanouchi U, Wang ZX, Minobe Y, Izawa T, Yano M (2008) Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol 148(3):1425–1435

    Article  CAS  Google Scholar 

  • 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(4):709–716

    Article  CAS  Google Scholar 

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146(2):333–350

    Article  CAS  Google Scholar 

  • Peng Q, Zhu CM, Liu T, Zhang S, Feng SJ, Wu CY (2021) Phosphorylation of OsFD1 by OsCIPK3 promotes the formation of RFT1-containing florigen activation complex for long-day flowering in rice. Mol Plant 14(7):1135–1148

    Article  CAS  Google Scholar 

  • Qin FJ, Sun QW, Huang LM, Chen XS, Zhou DX (2010) Rice SUVH histone methyltransferase genes display specific functions in chromatin modification and retrotransposon repression. Mol Plant 3(4):773–782

    Article  CAS  Google Scholar 

  • Ryu C-H, Lee S, Cho L-H, Kim SL, Lee Y-S, Choi SC, Jeong HJ, Yi J, Park SJ, Han C-D, An G (2009) OsMADS50 and OsMADS56 function antagonistically in regulating long day (LD)-dependent flowering in rice. Plant, Cell Environ 32(10):1412–1427

    Article  CAS  Google Scholar 

  • Song S, Chen Y, Liu L, Wang Y, Bao S, Zhou X, Teo ZW, Mao C, Gan Y, Yu H (2017) OsFTIP1-mediated regulation of florigen transport in rice is negatively regulated by the ubiquitin-like domain kinase OsUbDKγ4. Plant Cell 29(3):491–507

    Article  CAS  Google Scholar 

  • Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F (2012) The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. Plant Cell 24(8):3235–3247

    Article  CAS  Google Scholar 

  • 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(4):1747–1758

    Article  CAS  Google Scholar 

  • Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40(6):761–767

    Article  CAS  Google Scholar 

  • Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12(12):2473–2483

    Article  CAS  Google Scholar 

  • Zhang CY, Liu J, Zhao T, Gomez A, Li C, Yu CS, Li HY, Lin JZ, Yang YZ, Liu B, Lin CT (2016) A drought-inducible transcription factor delays reproductive timing in rice. Plant Physiol 171(1):334–343

    Article  CAS  Google Scholar 

  • Zhang ZY, Hu W, Shen GJ, Liu HY, Hu Y, Zhou XC, Liu TM, Xing YZ (2017) Alternative functions of Hd1 in repressing or promoting heading are determined by Ghd7 status under long-day conditions. Sci Rep 7(1):5388

    Article  Google Scholar 

  • Zhang B, Liu HY, Qi FX, Zhang ZY, Li QP, Han ZM, Xing YZ (2019) Genetic interactions among Ghd7, Ghd8, OsPRR37 and Hd1 contribute to large variation in heading date in rice. Rice 12(1):48

    Article  Google Scholar 

  • Zong WB, Ren D, Huang MH, Sun KL, Feng JL, Zhao J, Xiao DD, Xie WH, Liu SQ, Zhang H, Qiu R, Tang WJ, Yang RQ, Chen HY, Xie XR, Chen LT, Liu YG, Guo JX (2021) Strong photoperiod sensitivity is controlled by cooperation and competition among Hd1, Ghd7 and DTH8 in rice heading. New Phytol 229(3):1635–1649

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. Yaoguang Liu for providing the vector pYLCRISPR/Cas9Pubi-H.

Funding

This study was supported by the Youth Innovation Promotion Association CAS (Grant No. 2022231), the National Natural Science Foundation of China (Grant No. 31801327), and the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA28100301).

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Authors and Affiliations

  1. College of Agriculture, Heilongjiang Bayi Agricultural University, Daqing, 163319, China

    Tingting Pan & Xingfen Miao

  2. Northeast Institute of Geography and Agroecology, Key Laboratory of Soybean Molecular Design Breeding, Chinese Academy of Sciences, Harbin, 150081, China

    Mingliang He, Xiaojie Tian, Zhenyu Wang & Xiufeng Li

  3. Graduate University of Chinese Academy of Sciences, Beijing, 100049, China

    Mingliang He

  4. College of Agriculture, Rice Research Institute, Northeast Agricultural University, Harbin, 150030, China

    Hualong Liu

  5. Beidahuang Group Erdaohe Farm Co., Ltd, Harbin, China

    Xinglong Yu

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  1. Tingting Pan
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Contributions

XFL and XFM designed and supervised the research. TTP, MLH, and HLL performed the experiments. XJT, ZYW, and XLY analyzed the data. TTP and XFL wrote the paper. The author(s) read and approved the final manuscript.

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Correspondence to Xingfen Miao or Xiufeng Li.

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Pan, T., He, M., Liu, H. et al. Transcription factor bZIP65 delays flowering via suppressing Ehd1 expression in rice. Mol Breeding 42, 63 (2022). https://doi.org/10.1007/s11032-022-01334-4

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