DNA去甲基化参与了一氧化氮诱导的番茄开花

doi:10.1016/j.jia.2024.09.037

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (5): 1769-1785.DOI: 10.1016/j.jia.2024.09.037

DNA去甲基化参与了一氧化氮诱导的番茄开花

收稿日期:2023-12-28 修回日期:2024-09-30 接受日期:2024-05-07 出版日期:2025-05-20 发布日期:2025-04-14

DNA demethylation is involved in nitric oxide-induced flowering in tomato

Xuemei Hou¹, Meimei Shi¹, Zhuohui Zhang¹, Yandong Yao¹, Yihua Li², Changxia Li³, Wenjin Yu³, Chunlei Wang¹, Weibiao Liao^1#

¹ College of Horticulture, Gansu Agricultural University, Lanzhou 730070, China
²College of Agriculture and Ecological Engineering, Hexi University, Zhangye 734000, China
³Department of Horticulture, College of Agriculture, Guangxi University, Nanning 530004, China

Received:2023-12-28 Revised:2024-09-30 Accepted:2024-05-07 Online:2025-05-20 Published:2025-04-14
About author:#Corresponence Weibiao Liao, Tel: +86-931-7632399, Fax: +86-931-7631145, E-mail: liaowb@gsau.edu.cn
Supported by:
This work was supported by the National Natural Science Foundation of China (32360743, 32072559, and 31860568); the National Key Research and Development Program, China (2018YFD1000800); and the Fostering Foundation for the Excellent Ph D Dissertation of Gansu Agricultural University, China (YB2022004).

摘要/Abstract

摘要：

开花期是决定果实成熟和种子传播时机的最重要物候期之一。迄今为止，已有研究表明一氧化氮(NO)和DNA去甲基化对植物开花具有调节作用。然而，没有直接的实验证据表明NO与DNA去甲基化在植物开花调控中相互作用促进开花。本研究采用NO供体和DNA甲基化抑制剂来探讨DNA去甲基化对NO介导的番茄开花的影响。结果表明，NO对番茄开花的促进作用呈剂量依赖效应，其中10 μmol L^-1S-亚硝基谷胱甘肽(GSNO,NO供体)的促进作用最为显著。用50μmol L^-1DNA甲基化抑制剂5-氮杂胞苷(5-AzaC)处理也显著促进番茄开花。此外，GSNO和5-AzaC提高了过氧化物酶(POD)和过氧化氢酶(CAT)活性，增加了细胞分裂素(CTK)和脯氨酸含量，降低了赤霉素(GA3)和吲哚-3-乙酸(IAA)含量。GSNO与5-AzaC共处理增强了GSNO或5-AzaC对番茄开花的积极作用。同时，与GSNO或5-AzaC单独处理相比，GSNO+5-AzaC共处理显著提高了番茄各组织中整体DNA去甲基化水平。结果还表明，DNA去甲基化可能参与了NO诱导的开花过程。GSNO+5-AzaC处理显著改变了花诱导基因和花抑制基因的表达。其中，ARGONAUTE 4 (AGO4A)、SlSP3D/SINGLE FLOWER TRUSS (SFT)、MutS HOMOLOG 1 (MSH1)、锌指蛋白2 (ZFP2)和开花位点D (FLD) 5个花诱导基因被作为候选基因进一步研究。McrBC-PCR分析表明，顶端SFT基因和茎部FLD基因的DNA去甲基化可能参与了NO诱导的开花过程。因此，我们的研究表明，NO可能通过介导开花诱导基因的DNA去甲基化来促进番茄开花。本研究揭示了NO和DNA去甲基化在促进番茄开花中的协同作用。

Abstract:

Flowering is one of the most important phenological periods, as it determines the timing of fruit maturation and seed dispersal. To date, both nitric oxide (NO) and DNA demethylation have been reported to regulate flowering in plants. However, there is no compelling experimental evidence for a relationship between NO and DNA demethylation during plant flowering. In this study, an NO donor and a DNA methylation inhibitor were used to investigate the involvement of DNA demethylation in NO-mediated tomato (Solanum lycopersicum cv. Micro-Tom) flowering. The results showed that the promoting effect of NO on tomato flowering was dose-dependent, with the greatest positive effect observed at 10 μmol L^–1 of the NO donor S-nitrosoglutathione (GSNO). Treatment with 50 μmol L^–1 of the DNA methylation inhibitor 5-azacitidine (5-AzaC) also significantly promoted tomato flowering. Moreover, GSNO and 5-AzaC increased the peroxidase (POD) and catalase (CAT) activities and cytokinin (CTK) and proline contents, while they reduced the gibberellic acid (GA3) and indole-3-acetic acid (IAA) contents. Co-treatment with GSNO and 5-AzaC accelerated the positive effects of GSNO and 5-AzaC in promoting tomato flowering. Meanwhile, compared with a GSNO or 5-AzaC treatment alone, co-treatment with GSNO+5-AzaC significantly increased the global DNA demethylation levels in different tissues of tomato. The results also indicate that DNA demethylation may be involved in NO-induced flowering. The expression of flowering genes was significantly altered by the GSNO+5-AzaC treatment. Five of these flowering induction genes, ARGONAUTE 4 (AGO4A), SlSP3D/SINGLE FLOWER TRUSS (SFT), MutS HOMOLOG 1 (MSH1), ZINC FINGER PROTEIN 2 (ZFP2), and FLOWERING LOCUS D (FLD), were selected as candidate genes for further study. An McrBC-PCR analysis showed that DNA demethylation of the SFT gene in the apex and the FLD gene in the stem might be involved in NO-induced flowering. Therefore, this study shows that NO might promote tomato flowering by mediating the DNA demethylation of flowering induction genes, and it provides direct evidence for a synergistic effect of NO and DNA demethylation in promoting tomato flowering.

Key words: S-nitrosoglutathione , 5-azacitidine , flowering induction genes , tomato flowering

Xuemei Hou, Meimei Shi, Zhuohui Zhang, Yandong Yao, Yihua Li, Changxia Li, Wenjin Yu, Chunlei Wang, Weibiao Liao. DNA去甲基化参与了一氧化氮诱导的番茄开花[J]. Journal of Integrative Agriculture, 2025, 24(5): 1769-1785.

Xuemei Hou, Meimei Shi, Zhuohui Zhang, Yandong Yao, Yihua Li, Changxia Li, Wenjin Yu, Chunlei Wang, Weibiao Liao. DNA demethylation is involved in nitric oxide-induced flowering in tomato[J]. Journal of Integrative Agriculture, 2025, 24(5): 1769-1785.

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DNA去甲基化参与了一氧化氮诱导的番茄开花

DNA demethylation is involved in nitric oxide-induced flowering in tomato

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