ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3

Low-temperature (LT) stress is a significant abiotic stress in rice growth, especially under direct seeding cultivation, where low temperatures can significantly affect seed germination and seedling growth of direct-seeded rice, thereby impacting the final yield of rice. In this study, we have ident...

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Main Authors: Zhonge Qin, Jiahan Lyu, Zhenning Teng, Shuang Meng, Yan Peng, Dingyang Yuan, Meijuan Duan, Jianhua Zhang, Nenghui Ye
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2025-06-01
Series:Crop Journal
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Online Access:http://www.sciencedirect.com/science/article/pii/S2214514125000960
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author Zhonge Qin
Jiahan Lyu
Zhenning Teng
Shuang Meng
Yan Peng
Dingyang Yuan
Meijuan Duan
Jianhua Zhang
Nenghui Ye
author_facet Zhonge Qin
Jiahan Lyu
Zhenning Teng
Shuang Meng
Yan Peng
Dingyang Yuan
Meijuan Duan
Jianhua Zhang
Nenghui Ye
author_sort Zhonge Qin
collection DOAJ
description Low-temperature (LT) stress is a significant abiotic stress in rice growth, especially under direct seeding cultivation, where low temperatures can significantly affect seed germination and seedling growth of direct-seeded rice, thereby impacting the final yield of rice. In this study, we have identified a trehalose synthesis pathway gene, trehalose-6-phosphate phosphatase 3 (OsTPP3), involved in the regulation of low-temperature (LT) germination in rice, as well as its upstream regulatory factor, the ABA signaling pathway gene OsbZIP23. LT stress induced the accumulation of ABA by upregulating the expression of OsNCED3. Consistently, the overexpression of OsNCED3 significantly inhibited seed germination under LT. RT-qPCR experiments found that the expression of OsbZIP23 was also significantly induced under LT stress and ABA treatment. Overexpression of OsbZIP23 has increased the sensitivity to LT stress of rice seed, resembling the phenotype of OsNCED3 overexpressing seeds. Furthermore, both LT stress and exogenous ABA treatment increased the trehalose content in WT seeds by upregulating the expression of OsTPP3. Enhancing the expression of OsTPP3 or application of exogenous trehalose have significantly increased the sensitivity to LT stress during seed germination. Transcriptional activation and yeast one-hybrid assays demonstrated that OsbZIP23 bound to the promoter of OsTPP3 and activated its expression, which was intensified by LT stress or the application of ABA. Our study discovered an ABA-dependent OsbZIP23–OsTPP3 module that responds to LT stress, inhibiting seed germination under LT conditions by increasing trehalose accumulation, thus might balance the growth and stress resistance and provide a new insight into the genetic improvement of rice cultivars with better LT germination performance.
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publishDate 2025-06-01
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spelling doaj-art-91a1bf9ac6f44441b11f4f9f3f5c59c02025-08-20T03:47:13ZengKeAi Communications Co., Ltd.Crop Journal2214-51412025-06-0113375276310.1016/j.cj.2025.03.014ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3Zhonge Qin0Jiahan Lyu1Zhenning Teng2Shuang Meng3Yan Peng4Dingyang Yuan5Meijuan Duan6Jianhua Zhang7Nenghui Ye8Hunan Provincial Key Laboratory of Stress Biology, College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; Yuelushan Laboratory, Hunan Agricultural University, Changsha 410128, Hunan, ChinaHunan Provincial Key Laboratory of Stress Biology, College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; Yuelushan Laboratory, Hunan Agricultural University, Changsha 410128, Hunan, ChinaHunan Provincial Key Laboratory of Stress Biology, College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; Yuelushan Laboratory, Hunan Agricultural University, Changsha 410128, Hunan, China; School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin 999077, Hong Kong, ChinaHunan Provincial Key Laboratory of Stress Biology, College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; Yuelushan Laboratory, Hunan Agricultural University, Changsha 410128, Hunan, ChinaHunan Provincial Key Laboratory of Stress Biology, College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; Yuelushan Laboratory, Hunan Agricultural University, Changsha 410128, Hunan, ChinaState Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Hunan Academy of Agricultural Sciences, Changsha 410128, Hunan, ChinaHunan Provincial Key Laboratory of Stress Biology, College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; Hunan Women’s University, Changsha 410128, Hunan, China; Key Laboratory of Crop Physiology and Molecular Biology, Ministry of Education, Hunan Agricultural University, Changsha 410128, Hunan, China; Corresponding authors.Department of Biology, Hong Kong Baptist University, Kowloon 999077, Hong Kong, China; School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin 999077, Hong Kong, China; Corresponding authors.Hunan Provincial Key Laboratory of Stress Biology, College of Agronomy, Hunan Agricultural University, Changsha 410128, Hunan, China; Yuelushan Laboratory, Hunan Agricultural University, Changsha 410128, Hunan, China; School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin 999077, Hong Kong, China; Key Laboratory of Crop Physiology and Molecular Biology, Ministry of Education, Hunan Agricultural University, Changsha 410128, Hunan, China; Corresponding authors.Low-temperature (LT) stress is a significant abiotic stress in rice growth, especially under direct seeding cultivation, where low temperatures can significantly affect seed germination and seedling growth of direct-seeded rice, thereby impacting the final yield of rice. In this study, we have identified a trehalose synthesis pathway gene, trehalose-6-phosphate phosphatase 3 (OsTPP3), involved in the regulation of low-temperature (LT) germination in rice, as well as its upstream regulatory factor, the ABA signaling pathway gene OsbZIP23. LT stress induced the accumulation of ABA by upregulating the expression of OsNCED3. Consistently, the overexpression of OsNCED3 significantly inhibited seed germination under LT. RT-qPCR experiments found that the expression of OsbZIP23 was also significantly induced under LT stress and ABA treatment. Overexpression of OsbZIP23 has increased the sensitivity to LT stress of rice seed, resembling the phenotype of OsNCED3 overexpressing seeds. Furthermore, both LT stress and exogenous ABA treatment increased the trehalose content in WT seeds by upregulating the expression of OsTPP3. Enhancing the expression of OsTPP3 or application of exogenous trehalose have significantly increased the sensitivity to LT stress during seed germination. Transcriptional activation and yeast one-hybrid assays demonstrated that OsbZIP23 bound to the promoter of OsTPP3 and activated its expression, which was intensified by LT stress or the application of ABA. Our study discovered an ABA-dependent OsbZIP23–OsTPP3 module that responds to LT stress, inhibiting seed germination under LT conditions by increasing trehalose accumulation, thus might balance the growth and stress resistance and provide a new insight into the genetic improvement of rice cultivars with better LT germination performance.http://www.sciencedirect.com/science/article/pii/S2214514125000960Seed germinationAbscisic acidTrehaloseOsbzip23Low-temperature stressOstpp3
spellingShingle Zhonge Qin
Jiahan Lyu
Zhenning Teng
Shuang Meng
Yan Peng
Dingyang Yuan
Meijuan Duan
Jianhua Zhang
Nenghui Ye
ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3
Crop Journal
Seed germination
Abscisic acid
Trehalose
Osbzip23
Low-temperature stress
Ostpp3
title ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3
title_full ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3
title_fullStr ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3
title_full_unstemmed ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3
title_short ABA biosynthesis rather than ABA catabolism is induced by low temperature and inhibits seed germination by activating OsTPP3
title_sort aba biosynthesis rather than aba catabolism is induced by low temperature and inhibits seed germination by activating ostpp3
topic Seed germination
Abscisic acid
Trehalose
Osbzip23
Low-temperature stress
Ostpp3
url http://www.sciencedirect.com/science/article/pii/S2214514125000960
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