OsNCED3 and OsPYL1 promote the closure of rice florets by regulating sugar transporters through endogenous abscisic acid

doi:10.1016/j.jia.2023.11.004

Journal of Integrative Agriculture

2025, Vol. 24

Issue (2): 441-452 DOI: 10.1016/j.jia.2023.11.004

Crop Science

Advanced Online Publication | Current Issue | Archive | Adv Search

OsNCED3 and OsPYL1 promote the closure of rice florets by regulating sugar transporters through endogenous abscisic acid

Xiawan Zhai^{1, 2}, Wenbin Kai^{1, 2}, Youming Huang³, Jinyin Chen²^#, Xiaochun Zeng^{1, 3}^#

¹Jiangxi Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Jiangxi Agricultural University, Nanchang 330045, China

²College of Agronomy, Jiangxi Agricultural University, Nanchang 330045, China

³ College of Life Science and Resources and Environment, Yichun University, Yichun 336000, China

Highlights
● OsNCED3 plays a crucial role in abscisic acid (ABA) synthesis in rice florets, and the receptor OsPYL1 modulates floret sensitivity to ABA.
● Increased endogenous ABA content or sensitivity promotes rice floret closure.
● Differential expression of ABA-regulated sugar transporters causes floret closure.

Abstract
References

Download: PDF in ScienceDirect
Export: BibTeX | EndNote (RIS)

摘要

水稻作为世界第一大粮食作物，在杂交制种中常遇到父母本花时不遇的问题，且母本的颖花关闭慢会导致种子发霉，影响品质。植物激素脱落酸（ABA）在植物响应非生物胁迫中起着至关重要的作用。前人研究表明，外源ABA能够促进颖花关闭，然而其分子机制以及内源脱落酸对颖花关闭的作用尚不清楚。本研究通过改变水稻OsNCED3和OsPYL1的表达水平，探究内源ABA水平的改变对颖花关闭时间的影响，以及ABA通过糖转运蛋白对颖花关闭的作用机理。结果表明，过表达OsNCED3能够提高颖花内源脱落酸水平，从而使颖花关闭比野生型提前5.91分钟，OsNCED3下调则使颖花关闭推迟5.08分钟；进一步发现OsPYL1能够调控内源脱落酸水平同时改变对ABA敏感性，从而使过表达和敲除该基因的颖花关闭时间分别提前9.84分钟和延迟12.78分钟，且导致敲除株系种子裂颖率提高至15.4%。通过qRT-PCR检测发现，ABA对颖花关闭的促进作用可能是通过信号通路下游糖转运蛋白的响应来完成的，且OsPYL1与OsSWEET4能够在细胞膜上发生相互作用。以上结果表明，脱落酸能够促进水稻颖花关闭，增强植物对ABA的敏感性会促进该效果，其分子机制主要与下游响应ABA信号通路的糖转运蛋白相关，特别是OsSWEET4。

Abstract

Rice is the world’s largest food crop, but it often encounters flowering asynchronization problems during hybrid rice seed production. In addition, the slow closure of female florets leads to seed mildew and affects the quality. The hormone abscisic acid (ABA) plays a crucial role in plant responses to abiotic stresses. Previous studies showed that exogenous ABA promotes floret closure, although the molecular mechanisms and effects of endogenous ABA on floret closure remain unknown. In this study, the effect of endogenous ABA on floret closure and the molecular mechanism by which ABA promotes floret closure through sugar transporters were investigated by changing the expression levels of OsNCED3 and OsPYL1 in rice. The results showed that overexpression (OE)-OsNCED3 increased the endogenous ABA level of florets. Florets closed 5.91 min earlier and OsNCED3 gene knockout line delayed the closure of florets by 5.08 min compared with the wild type. In addition, OsPYL1 regulated the endogenous ABA content and changed the sensitivity to ABA such that the floret closure times for OE and CRISPR-Cas9 (CR) were 9.84 min earlier and 12.78 min later, respectively, resulting in an increase in the split husk rate to 15.4%. The gene expression levels of some sugar transporters (STs) changed. The OsPYL1 and OsSWEET4 proteins could interact on the cell membrane. These results indicate that ABA promotes the closure of rice florets and the enhanced sensitivity to ABA promotes this effect even more. The molecular mechanism is mainly related to downstream sugar transporters that respond to the ABA signaling pathway, especially OsSWEET4.

Keywords: rice floret closure sugar transporter abscisic acid seed quality

Received: 09 June 2023 Accepted: 28 September 2023

Fund:

This study was supported by the National Natural Science Foundation of China (32260780 and 31360297), the China Postdoctoral Science Foundation (2021M701513), the Jiangxi 2011 Collaborative Innovation Centre of Postharvest Key Technology and Quality Safety of Fruits and Vegetables, China (JXGS-05), and the Gan Po 555 Engineering Excellence Talents Project in Jiangxi Province, China.

About author: Xiawan Zhai, E-mail: zhaixiawan@163.com; #Correspondence Jinyin Chen, Tel: +86-791-83813185, E-mail: jinyinchen@163.com; Xiaochun Zeng, Tel: +86-795-3200698, E-mail xchzeng2013@163.com

	Service
	E-mail this article
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors

Cite this article:

Xiawan Zhai, Wenbin Kai, Youming Huang, Jinyin Chen, Xiaochun Zeng. 2025. OsNCED3 and OsPYL1 promote the closure of rice florets by regulating sugar transporters through endogenous abscisic acid. Journal of Integrative Agriculture, 24(2): 441-452.

Boursiac Y, Leran S, Corratge-Faillie C, Gojon A, Krouk G, Lacombe B. 2013. ABA transport and transporters. Trends Plant Science, 18, 325–333.

Chen K, Li G J, Bressan R A, Song C P, Zhu J K, Zhao Y. 2020. Abscisic acid dynamics, signaling, and functions in plants. Journal of Integrative Plant Biology, 62, 25–54.

Cutler S R, Rodriguez P L, Finkelstein R R, Abrams S R. 2010. Abscisic acid: Emergence of a core signaling network. Annual Review of Plant Biology, 61, 651–679.

Deng X, An B, Zhong H, Yang J, Kong W, Li Y. 2019. A novel insight into functional divergence of the MST gene family in rice based on comprehensive expression patterns. Gene, 10, 239.

Fang Z, Ji Y, Hu J, Guo R, Wang X. 2019. Strigolactones and brassinosteroids antagonistically regulate the stability of D53-OsBZR1 complex to determine FC1 expression in rice tillering. Molecular Plant, 13, 586–597.

Fei H, Yang Z, Lu Q, Wen X, Lu C. 2021. OsSWEET14 cooperates with OsSWEET11 to contribute to grain filling in rice. Plant Science, 306, 110851.

He Y, Zhao J, Yang B, Sun S, Peng L, Wang Z. 2020. Indole-3-acetate beta-glucosyltransferase OsIAGLU regulates seed vigour through mediating crosstalk between auxin and abscisic acid in rice. Plant Biotechnology Journal, 18, 1933–1945.

Hibara K I, Isono M, Mimura M, Sentoku N, Kojima M, Sakakibara H, Kitomi Y, Yoshikawa T, Itoh J I, Nagato Y. 2016. Jasmonate regulates juvenile-adult phase transition in rice. Development, 143, 3407–3416.

Hu Z, Tang Z, Zhang Y, Niu L, Yang F, Zhang D, Hu Y. 2021. Rice SUT and SWEET transporters. International Journal of Molecular Sciences, 22, 11198.

Huang Y, Zeng X, Cao H. 2018. Hormonal regulation of floret closure of rice (Oryza sativa). PLoS ONE, 13, e0198828.

Hwang S G, Lee C Y, Tseng C S. 2018. Heterologous expression of rice 9-cis-epoxycarotenoid dioxygenase 4 (OsNCED4) in Arabidopsis confers sugar oversensitivity and drought tolerance. Botanical Studies, 59, 2.

Jung C, Nguyen N H, Cheong J J. 2020. Transcriptional regulation of protein phosphatase 2C genes to modulate abscisic acid signaling. International Journal of Molecular Sciences, 21, 9517.

Liu L, Zou Z, Qian K, Xia C, He Y, Zeng H, Zhou X, Riemann M, Yin C. 2017. Jasmonic acid deficiency leads to scattered floret opening time in cytoplasmic male sterile rice Zhenshan 97A. Journal of Experimental Botany, 68, 4613–4625.

Ma L, Zhang D, Miao Q, Yang J, Xuan Y, Hu Y. 2017. Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiology, 58, 863–873.

Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324, 1064–1068.

Misra V A, Wafula E K, Wang Y, Depamphilis C W, Timko M P. 2019. Genome-wide identification of MST, SUT and SWEET family sugar transporters in root parasitic angiosperms and analysis of their expression during host parasitism. BMC Plant Biology, 19, 196.

Park S Y, Fung P, Nishimura N, Jensen D R, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T F F, et al. 2009. Abscisic acid inhibits Type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, 1068–1071.

Rodriguez P L, Lozano-Juste J, Albert A. 2019. PYR/PYL/RCAR ABA receptors. Advances in Botanical Research, 92, 51–82.

Seo M, Marion-Poll A. 2019. Abscisic acid metabolism and transport. Advances in Botanical Research, 92, 1–49.

Sosso D, Luo D, Li Q B, Sasse J, Yang J, Gendrot G, Suzuki M, Koch K E, McCarty D R, Chourey P S, Rogowsky P M, Ibarra J R, Yang B, Frommer W B. 2015. Seed filling in domesticated maise and rice depends on SWEET-mediated hexose transport. Nature Genetics, 47, 1489–1493.

Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K. 2009. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 106, 17588–17593.

Wang C, Zhao Y, Han P, Yu J, Hao Y, Xu Q, You C, Hu D. 2022. Auxin response factor gene MdARF2 is involved in ABA signaling and salt stress response in apple. Journal of Integrative Agriculture, 21, 2264–2274.

Weiner J J, Peterson F C, Volkman B F, Cutler S R. 2010. Structural and functional insights into core ABA signaling. Current Opinion in Plant Biology, 13, 495–502.

Wilson R N, Heckman J W, Somerville C R. 1992. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiology, 100, 403–408.

Xiao Y, Chen Y, Charnikhova T, Mulder P P J, Ouwerkerk P B F. 2014. OsJAR1 is required for JA-regulated floret opening and anther dehiscence in rice. Plant Molecular Biology, 86, 19–33.

Yadav S K, Santosh Kumar V V, Verma R K, Yadav P, Saroha A, Wankhede D P, Chaudhary B, Chinnusamy V. 2020. Genome-wide identification and characterisation of ABA receptor PYL gene family in rice. BMC Genomics, 21, 676.

Yolande H H, Heslop-Harrison J S. 1996. Lodicule function and filament extension in the grasses: Potassium ion movement and tissue specialisation. Annals of Botany, 77, 573–582.

Yoshida H, Nagato Y. 2011. Flower development in rice. Journal of Experimental Botany, 62, 4719–4730.

Zeng X, Zhou X, Zhang W, Murofushi N, Kitahara T, Kamuro Y. 1999. Opening of rice floret in rapid response to methyl jasmonate. Journal of Plant Growth Regulation, 18, 153–158.

Zeng Z, Lyu T, Lyu Y. 2022. LoSWEET14, a sugar transporter in lily, is regulated by transcription factor LoABF2 to participate in the ABA signaling pathway and enhance tolerance to multiple abiotic stresses in tobacco. International Journal of Molecular Sciences, 23, 15093.

Zhai X, Lan D, Jia M, Gan Z, Chen C, Zeng X, Chen J, Kai W. 2023. Characterisation and expression analysis of key abscisic acid signal transduction genes during kiwifruit development. Scientia Horticulturae, 309, 111672.

Zhang B, Fan W M, Zhu Z Z, Wang Y, Zhao Z Y. 2023. Functional analysis of MdSUT2.1, a plasma membrane sucrose transporter from apple. Journal of Integrative Agriculture, 22, 762–775.

Zhao Q, Zhou L J, Liu J C, Cao Z Z, Du X X, Huang F D, Pan G, Cheng F M. 2018. Involvement of CAT in the detoxification of HT-induced ROS burst in rice anther and its relation to pollen fertility. Plant Cell Reports, 37, 741–757.

Zhao Z, Wang C, Yu X, Tian Y, Wang W, Zhang Y, Bai W, Yang N, Zhang T, Zheng H, et al. 2022. Auxin regulates source-sink carbohydrate partitioning and reproductive organ development in rice. Proceedings of the National Academy of Sciences of the United States of America, 119, e2121671119.

Zhu G, Ye N, Zhang J. 2009. Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiology, 50, 644–651.

[1]	Shan Sun, Wenjun Li, Yanfen Fang, Qianqian Huang, Zhibo Huang, Chengjing Wang, Jia Zhao, Yongqi He, Zhoufei Wang. *Small auxin-up RNA gene OsSAUR33* promotes seed aging tolerance in rice**[J]. >Journal of Integrative Agriculture, 2025, 24(1): 61-71.
[2]	Chengwei Huang, Zhijuan Ji, Qianqian Huang, Liling Peng, Wenwen Li, Dandan Wang, Zepeng Wu, Jia Zhao, Yongqi He, Zhoufei Wang. *Natural variation in the cytochrome c oxidase subunit 5B OsCOX5B* regulates seed vigor by altering energy production in rice**[J]. >Journal of Integrative Agriculture, 2024, 23(9): 2898-2910.
[3]	Gaozhao Wu, Xingyu Chen, Yuguang Zang, Ying Ye, Xiaoqing Qian, Weiyang Zhang, Hao Zhang, Lijun Liu, Zujian Zhang, Zhiqin Wang, Junfei Gu, Jianchang Yang. An optimized strategy of nitrogen-split application based on the leaf positional differences in chlorophyll meter readings[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2605-2617.
[4]	Xiaogang He, Zirong Li, Sicheng Guo, Xingfei Zheng, Chunhai Liu, Zijie Liu, Yongxin Li, Zheming Yuan, Lanzhi Li. Epistasis-aware genome-wide association studies provide insights into the efficient breeding of high-yield and high-quality rice[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2541-2556.
[5]	Bingli Jiang, Wei Gao, Yating Jiang, Shengnan Yan, Jiajia Cao, Litian Zhang, Yue Zhang, Jie Lu, Chuanxi Ma, Cheng Chang, Haiping Zhang. *Identification of P-type plasma membrane H⁺-ATPases in common wheat and characterization of TaHA7* associated with seed dormancy and germination**[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2164-2177.
[6]	Shuang Cheng, Zhipeng Xing, Chao Tian, Mengzhu Liu, Yuan Feng, Hongcheng Zhang. Optimized tillage methods increase mechanically transplanted rice yield and reduce the greenhouse gas emissions [J]. >Journal of Integrative Agriculture, 2024, 23(4): 1150-1163.
[7]	Yunping Chen, Jie Hu, Zhiwen Cai, Jingya Yang, Wei Zhou, Qiong Hu, Cong Wang, Liangzhi You, Baodong Xu. A phenology-based vegetation index for improving ratoon rice mapping using harmonized Landsat and Sentinel-2 data [J]. >Journal of Integrative Agriculture, 2024, 23(4): 1164-1178.
[8]	Jingnan Zou, Ziqin Pang, Zhou Li, Chunlin Guo, Hongmei Lin, Zheng Li, Hongfei Chen, Jinwen Huang, Ting Chen, Hailong Xu, Bin Qin, Puleng Letuma, Weiwei Lin, Wenxiong Lin. The underlying mechanism of variety–water–nitrogen–stubble damage interactions on yield formation in ratoon rice with low stubble height under mechanized harvesting [J]. >Journal of Integrative Agriculture, 2024, 23(3): 806-823.
[9]	Shuliang Jiao, Qinyan Li, Fan Zhang, Yonghong Tao, Yingzhen Yu, Fan Yao, Qingmao Li, Fengyi Hu, Liyu Huang. *Artificial selection of the Green Revolution gene Semidwarf 1* is implicated in upland rice breeding** [J]. >Journal of Integrative Agriculture, 2024, 23(3): 769-780.
[10]	Min Jiang, Zhang Chen, Yuan Li , Xiaomin Huang, Lifen Huang, Zhongyang Huo. Rice canopy temperature is affected by nitrogen fertilizer [J]. >Journal of Integrative Agriculture, 2024, 23(3): 824-835.
[11]	Tingting Zhou, Qian Zhao, Chengzhou Li, Lu Ye, Yanfang Li, Nemat O. Keyhani, Zhen Huang. Synergistic effects of the entomopathogenic fungus Isaria javanica and low doses of dinotefuran on the efficient control of the rice pest Sogatella furcifera[J]. >Journal of Integrative Agriculture, 2024, 23(2): 621-638.
[12]	Yongjian Chen, Lan Dai, Siren Cheng, Yong Ren, Huizi Deng, Xinyi Wang, Yuzhan Li, Xiangru Tang, Zaiman Wang, Zhaowen Mo. *Regulation of 2-acetyl-1-pyrroline and grain quality in early-season indica* fragrant rice by nitrogen and silicon fertilization under different plantation methods** [J]. >Journal of Integrative Agriculture, 2024, 23(2): 511-535.
[13]	Tingcheng Zhao, Aibin He, Mohammad Nauman Khan, Qi Yin, Shaokun Song, Lixiao Nie. Coupling of reduced inorganic fertilizer with plant-based organic fertilizer as a promising fertilizer management strategy for colored rice in tropical regions [J]. >Journal of Integrative Agriculture, 2024, 23(1): 93-107.
[14]	SHI Shi-jie, ZHANG Gao-yu, CAO Cou-gui, JIANG Yang . Untargeted UHPLC–Q-Exactive-MS-based metabolomics reveals associations between pre- and post-cooked metabolites and the taste quality of geographical indication rice and regular rice[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2271-2281.
[15]	HE Wen-jun, HE Bin, WU Bo-yang, WANG Yu-hui, YAN Fei-yu, DING Yan-feng, LI Gang-hua. Growth of tandem long-mat rice seedlings using controlled release fertilizers: Mechanical transplantation can be more economical and high yielding[J]. >Journal of Integrative Agriculture, 2023, 22(12): 3652-3666.

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Shared

Discussed

Cite this article:

About JIA

Editorial board

For authors