OsELF3.1-OsCATA-Ghd7 Pathway Regulates Rice Heading
Received date: 2025-01-27
Accepted date: 2025-06-20
Online published: 2025-06-24
Rice, a critical global staple crop, relies heavily on heading date, a key agronomic trait marking the transition from vegetative to reproductive growth. Understanding the genetic regulation of heading date is vital for enhancing the adaptability of high-quality rice varieties across diverse geographical regions and for bolstering local food security. In this study, we uncovered a novel role for OsCATA, a catalase gene, in the regulation of photoperiodic flowering in rice. We identified a novel allele of OsELF3.1, whose mutation resulted in delayed heading. Further analyses revealed that OsELF3.1 physically interacted with OsCATA. Notably, OsCATA exhibited rhythmic expression patterns similar to OsELF3.1 and, when mutated, also delayed flowering. Expression analyses showed that the delayed heading phenotype could be attributed to elevated Ghd7 expression under both long-day and short-day conditions, with OsCATA expression positively regulated by OsELF3.1. Double mutants of OsELF3.1 and OsCATA displayed a heading delay similar to that of oself3.1 single mutants. Additionally, OsELF3.1 could interact with Ghd7 in vivo, alleviating its suppression of Ehd1. Luciferase assays confirmed that Ghd7 repressed Ehd1 expression, while OsELF3.1 mitigated this repression. Collectively, our findings reveal that OsCATA is critical in suppressing Ghd7 expression through the OsELF3.1-OsCATA-Ghd7 transcriptional pathway, thereby regulating rice heading.
Key words： rice; heading date; OsELF3.1; Ghd7; OsCATA
Wu Zhaozhong, Zhong Zhengzheng, Xu Peng, Liu Ling, Wang Beifang, Yang Qinqin, Wen Xiaoxia, Ma Guifang, Luo Mili, Zhang Yingxin, Liu Qun’en, Peng Zequn, Zhan Xiaodeng, Cao Liyong, Cheng Shihua, Wu Weixun . OsELF3.1-OsCATA-Ghd7 Pathway Regulates Rice Heading[J]. Rice Science, 2025 , 32(5) : 658 -672 . DOI: 10.1016/j.rsci.2025.06.001
| [1] | Abe A, Kosugi S, Yoshida K, et al. 2012. Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol, 30(2): 174-178. |
| [2] | Cai Z Z, Zhang Y D, Tang W Q, et al. 2022. LUX ARRHYTHMO interacts with ELF3a and ELF4a to coordinate vegetative growth and photoperiodic flowering in rice. Front Plant Sci, 13: 853042. |
| [3] | Cheng Q, Gan Z R, Wang Y P, et al. 2020. The soybean gene J contributes to salt stress tolerance by up-regulating salt-responsive genes. Front Plant Sci, 11: 272. |
| [4] | Doi K, Izawa T, Fuse T, et al. 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(8): 926-936. |
| [5] | Du Y Y, Wang P C, Chen J, et al. 2008. Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J Integr Plant Biol, 50(10): 1318-1326. |
| [6] | Fang X L, Han Y P, Liu M S, et al. 2021. Modulation of evening complex activity enables north-to-south adaptation of soybean. Sci China Life Sci, 64(2): 179-195. |
| [7] | Fu C, Yang X O, Chen X, et al. 2009. OsEF3, a homologous gene of Arabidopsis ELF3, has pleiotropic effects in rice. Plant Biol, 11(5), 751-757. |
| [8] | Fujiwara S, Oda A, Yoshida R, et al. 2008. Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell, 20(11): 2960-2971. |
| [9] | Gao M J, He Y, Yin X, et al. 2021. Ca2+ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector. Cell, 184(21): 5391-5404. |
| [10] | Guo T, Chen K, Dong N Q, et al. 2018. GRAIN SIZE AND NUMBER1 negatively regulates the OsMKKK10-OsMKK4-OsMPK6 cascade to coordinate the trade-off between grain number per panicle and grain size in rice. Plant Cell, 30(4): 871-888. |
| [11] | Hu B, Jiang Z M, Wang W, et al. 2019. Nitrate-NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat Plants, 5(4): 401-413. |
| [12] | Hu Y, Song S, Weng X Y, et al. 2021. The heading-date gene Ghd7 inhibits seed germination by modulating the balance between abscisic acid and gibberellins. Crop J, 9(2): 297-304. |
| [13] | Izawa T. 2007. Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. J Exp Bot, 58(12): 3091-3097. |
| [14] | Joo J, Lee Y H, Song S I. 2014. Rice CatA, CatB, and CatC are involved in environmental stress response, root growth, and photorespiration, respectively. J Plant Biol, 57( 6): 375-382. |
| [15] | Jung J H, Barbosa A D, Hutin S, et al. 2020. A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature, 585: 256-260. |
| [16] | 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. |
| [17] | Lai A G, Doherty C J, Mueller-Roeber B, et al. 2012. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc Natl Acad Sci USA, 109(42): 17129-17134. |
| [18] | Liu X L, Covington M F, Fankhauser C, et al. 2001. ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell, 13(6): 1293-1304. |
| [19] | Liu Z, Cao M A, Kuča K, et al. 2024. Cloning of CAT genes in Satsuma mandarin and their expression characteristics in response to environmental stress and arbuscular mycorrhizal fungi. Plant Cell Rep, 43(5): 123. |
| [20] | Luan W J, Chen H Z, Fu Y P, et al. 2009. The effect of the crosstalk between photoperiod and temperature on the heading-date in rice. PLoS One, 4(6): e5891. |
| [21] | Matsubara K, Ogiso-Tanaka E, Hori K, et al. 2012. Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. Plant Cell Physiol, 53(4): 709-716. |
| [22] | McClung C R. 1997. Regulation of catalases in Arabidopsis. Free Radic Biol Med, 23(3): 489-496. |
| [23] | Mhamdi A, Queval G, Chaouch S, et al. 2010. Catalase function in plants: A focus on Arabidopsis mutants as stress-mimic models. J Exp Bot, 61(15): 4197-4220. |
| [24] | Mhamdi A, Noctor G, Baker A. 2012. Plant catalases: Peroxisomal redox guardians. Arch Biochem Biophys, 525(2): 181-194. |
| [25] | Michael T P, McClung C R. 2002. Phase-specific circadian clock regulatory elements in Arabidopsis. Plant Physiol, 130(2): 627-638. |
| [26] | Mouradov A, Cremer F, Coupland G. 2002. Control of flowering time: Interacting pathways as a basis for diversity. Plant Cell, 14: S111-S130. |
| [27] | 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(3): 221-233. |
| [28] | Ning Y S, Shi X T, Wang R Y, et al. 2015. OsELF3-2, an ortholog of Arabidopsis ELF3, interacts with the E3 ligase APIP6 and negatively regulates immunity against Magnaporthe oryzae in rice. Mol Plant, 8(11): 1679-1682. |
| [29] | Nusinow D A, Helfer A, Hamilton E E, et al. 2011. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature, 475(7356): 398-402. |
| [30] | Riseh R S, Fathi F, Vatankhah M, et al. 2024. Catalase-associated immune responses in plant-microbe interactions: A review. Int J Biol Macromol, 280: 135859. |
| [31] | Ronald J, Su C, Wang L, et al. 2022. Cellular localization of Arabidopsis EARLY FLOWERING3 is responsive to light quality. Plant Physiol, 190(2): 1024-1036. |
| [32] | Sakuraba Y, Jeong J, Kang M Y, et al. 2014. Phytochrome-interacting transcription factors PIF4 and PIF5 induce leaf senescence in Arabidopsis. Nat Commun, 5: 4636. |
| [33] | Sakuraba Y, Han S H, Yang H J, et al. 2016. Mutation of Rice Early Flowering3.1 (OsELF3.1) delays leaf senescence in rice. Plant Mol Biol, 92(1/2): 223-234. |
| [34] | Su T, Wang P P, Li H J, et al. 2018. The Arabidopsis catalase triple mutant reveals important roles of catalases and peroxisome-derived signaling in plant development. J Integr Plant Biol, 60(7): 591-607. |
| [35] | Sun K L, Huang M H, Zong W B, et al. 2022. Hd1, Ghd7, and DTH8 synergistically determine the rice heading date and yield-related agronomic traits. J Genet Genomics, 49(5): 437-447. |
| [36] | Sun K L, Zong W B, Xiao D D, et al. 2023. Effects of the core heading date genes Hd1, Ghd7, DTH8 and PRR37 on yield-related traits in rice. Theor Appl Genet, 136(11): 227. |
| [37] | Takahashi Y, Shimamoto K. 2011. Hd1), an ortholog of Arabidopsis CONSTANS, is a possible target of human selection during domestication to diversify flowering times of cultivated rice. Genes Genet Syst, 86(3): 175-182. |
| [38] | Tamaki S, Tsuji H, Matsumoto A, et al. 2015. FT-like proteins induce transposon silencing in the shoot apex during floral induction in rice. Proc Natl Acad Sci USA, 112(8): E901-E910. |
| [39] | Wang B F, Xue P, Zhang Y X, et al. 2024. OsCPK12 phosphorylates OsCATA and OsCATC to regulate H2O2 homeostasis and improve oxidative stress tolerance in rice. Plant Commun, 5(3): 100780. |
| [40] | Wang C, Shen L, Fu Y P, et al. 2015. A simple CRISPR/Cas9 system for multiplex genome editing in rice. J Genet Genomics, 42(12): 703-706. |
| [41] | Wang Q, Su Q M, Nian J Q, et al. 2021. The Ghd7 transcription factor represses ARE1 expression to enhance nitrogen utilization and grain yield in rice. Mol Plant, 14(6): 1012-1023. |
| [42] | Wang X L, He Y Q, Wei H, et al. 2021. A clock regulatory module is required for salt tolerance and control of heading date in rice. Plant Cell Environ, 44(10): 3283-3301. |
| [43] | Weng X Y, Wang L, Wang J, et al. 2014. Grain number, plant height, and heading date7 is a central regulator of growth, development, and stress response. Plant Physiol, 164( 2): 735-747. |
| [44] | Xia A A, Zheng L M, Wang Z, et al. 2023. The RHW1-ZCN4 regulatory pathway confers natural variation of husk leaf width in maize. New Phytol, 239(6): 2367-2381. |
| [45] | Xu P, Zhang Y X, Wen X X, et al. 2023. The clock component OsLUX regulates rice heading through recruiting OsELF3-1 and OsELF4s to repress Hd1 and Ghd7. J Adv Res, 48: 17-31. |
| [46] | Xu X, Shi X T, You X M, et al. 2024. A pair of E3 ubiquitin ligases control immunity and flowering by targeting different ELF3 proteins in rice. Dev Cell, 59(20): 2731-2744.e4. |
| [47] | Xue W Y, Xing Y Z, Weng X Y, et al. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet, 40(6): 761-767. |
| [48] | Yang Y, Peng Q, Chen G X, et al. 2013. OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice. Mol Plant, 6(1): 202-215. |
| [49] | Yi H, Shi H, Mao W, et al. 2024. E3 ubiquitin ligase IPI1 controls rice immunity and flowering via both E3 ligase-dependent and -independent pathways. Dev Cell, 59(20): 2719-2730. |
| [50] | You X M, Zhang F, Liu Z, et al. 2022. Rice catalase OsCATC is degraded by E3 ligase APIP6 to negatively regulate immunity. Plant Physiol, 190(2): 1095-1099. |
| [51] | Yu J W, Rubio V, Lee N Y, et al. 2008. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell, 32(5): 617-630. |
| [52] | Zagotta M T, Hicks K A, Jacobs C I, et al. 1996. The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J, 10(4): 691-702. |
| [53] | Zhang Z S, Xu Y Y, Xie Z W, et al. 2016. Association-dissociation of glycolate oxidase with catalase in rice: A potential switch to modulate intracellular H2O2 levels. Mol Plant, 9(5): 737-748. |
| [54] | Zhang Z Y, Hu W, Shen G J, et al. 2017. Alternative functions of Hd1 in repressing or promoting heading are determined by Ghd7 status under long-day conditions. Sci Rep, 7(1): 5388. |
| [55] | Zhao J M, Huang X, Ouyang X H, et al. 2012. OsELF3-1, an ortholog of Arabidopsis EARLY FLOWERING 3, regulates rice circadian rhythm and photoperiodic flowering. PLoS One, 7(8): e43705. |
| [56] | Zhao Y P, Zhao B B, Xie Y R, et al. 2023. The evening complex promotes maize flowering and adaptation to temperate regions. Plant Cell, 35(1): 369-389. |
| [57] | Zhong H H, McClung C R. 1996. The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol Gen Genet, 251(2): 196-203. |
| [58] | Zhou S R, Zhu S S, Cui S, et al. 2021. Transcriptional and post-transcriptional regulation of heading date in rice. New Phytol, 230(3): 943-956. |
| [59] | Zhou Y B, Liu C, Tang D Y, et al. 2018. The receptor-like cytoplasmic kinase STRK1 phosphorylates and activates CatC, thereby regulating H2O2 homeostasis and improving salt tolerance in rice. Plant Cell, 30(5): 1100-1118. |
| [60] | Zhu C M, Peng Q, Fu D B, et al. 2018. The E3 ubiquitin ligase HAF1 modulates circadian accumulation of EARLY FLOWERING3 to control heading date in rice under long-day conditions. Plant Cell, 30(10): 2352-2367. |
| [61] | Zong W B, Ren D, Huang M H, et al. 2021. Strong photoperiod sensitivity is controlled by cooperation and competition among Hd1, Ghd7 and DTH8 in rice heading. New Phytol, 229(3): 1635-1649. |
| [62] | Zou J J, Li X D, Ratnasekera D, et al. 2015. Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell, 27(5): 1445-1460. |
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