Cold-Induced Promoter Methylation Attenuates ScMYB7-Mediated Repression of the CBF Pathway: A Proposed Mechanism for Sugarcane Cold Adaptation.

IF 6.3 1区 生物学 Q1 PLANT SCIENCES
Weiwei Liu, Qiuyue Ou, Meichang Feng, Yue Li, Linghan Huang, Xuan Peng, Xiaoqiang Zhong, Guoqiang Huang, Hengbo Wang, Jinlong Guo
{"title":"Cold-Induced Promoter Methylation Attenuates ScMYB7-Mediated Repression of the CBF Pathway: A Proposed Mechanism for Sugarcane Cold Adaptation.","authors":"Weiwei Liu, Qiuyue Ou, Meichang Feng, Yue Li, Linghan Huang, Xuan Peng, Xiaoqiang Zhong, Guoqiang Huang, Hengbo Wang, Jinlong Guo","doi":"10.1111/pce.70180","DOIUrl":null,"url":null,"abstract":"<p><p>Cold stress is a critical environmental factor adversely affecting plant growth and development. As a tropical-origin crop constituting the primary global source of sucrose, sugarcane (Saccharum spp. hybrid) exhibits particular vulnerability to suboptimal temperature conditions, with chilling injury substantially compromising its yield potential. Despite its agricultural significance, the molecular mechanisms underlying cold acclimation in sugarcane remain poorly characterized. Here, we report a cold-repressed 1R-MYB gene, ScMYB7, from sugarcane, whose promoter (pro-ScMYB7) contains multiple cis-acting elements, including two cytosine-phosphate diester-guanine (CpG) islands. Bisulfite sequencing PCR (BSP) and qPCR results showed that low-temperature treatment increased the methylation level of the CpG islands in the promoter to reduce the transcription of the ScMYB7 gene. The outcomes of GUS enzyme activity measurement of the promoter also indicated that low-temperature treatment inhibits the promoter's transcriptional activity, and methylation inhibitors could alleviate this inhibition. By generating transgenic Arabidopsis lines overexpressing ScMYB7, ScMYB7's roles in regulating cold tolerance were investigated. We observed that the transgenic plants reduced cold tolerance, featured by a decreased survival rate after recovery, fluctuated physiological traits, and significantly lower expression levels of the C-repeat binding factor (CBF)-dependent pathway genes (AtCBFs, AtCOR15, and AtRD29A). Yeast one-hybrid assays demonstrated direct binding of ScMYB7 to the AtCBF1 promoter, while repression of sugarcane ScDREB1A occurred indirectly. Furthermore, the dual-luciferase reporter assay indicated that ScMYB7 was able to inhibit the expression of the AtCBF1 or ScDREB1A. Taken together, we propose a model in which ScMYB7 acts as a repressor of cold tolerance via the CBF-dependent pathway. Under low-temperature stress, increased methylation of the pro-ScMYB7 promoter reduces ScMYB7 expression, thereby alleviating its repression of sugarcane DREB/CBF-type transcription factors and enhancing cold adaptation.</p>","PeriodicalId":222,"journal":{"name":"Plant, Cell & Environment","volume":" ","pages":""},"PeriodicalIF":6.3000,"publicationDate":"2025-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant, Cell & Environment","FirstCategoryId":"2","ListUrlMain":"https://doi.org/10.1111/pce.70180","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Cold stress is a critical environmental factor adversely affecting plant growth and development. As a tropical-origin crop constituting the primary global source of sucrose, sugarcane (Saccharum spp. hybrid) exhibits particular vulnerability to suboptimal temperature conditions, with chilling injury substantially compromising its yield potential. Despite its agricultural significance, the molecular mechanisms underlying cold acclimation in sugarcane remain poorly characterized. Here, we report a cold-repressed 1R-MYB gene, ScMYB7, from sugarcane, whose promoter (pro-ScMYB7) contains multiple cis-acting elements, including two cytosine-phosphate diester-guanine (CpG) islands. Bisulfite sequencing PCR (BSP) and qPCR results showed that low-temperature treatment increased the methylation level of the CpG islands in the promoter to reduce the transcription of the ScMYB7 gene. The outcomes of GUS enzyme activity measurement of the promoter also indicated that low-temperature treatment inhibits the promoter's transcriptional activity, and methylation inhibitors could alleviate this inhibition. By generating transgenic Arabidopsis lines overexpressing ScMYB7, ScMYB7's roles in regulating cold tolerance were investigated. We observed that the transgenic plants reduced cold tolerance, featured by a decreased survival rate after recovery, fluctuated physiological traits, and significantly lower expression levels of the C-repeat binding factor (CBF)-dependent pathway genes (AtCBFs, AtCOR15, and AtRD29A). Yeast one-hybrid assays demonstrated direct binding of ScMYB7 to the AtCBF1 promoter, while repression of sugarcane ScDREB1A occurred indirectly. Furthermore, the dual-luciferase reporter assay indicated that ScMYB7 was able to inhibit the expression of the AtCBF1 or ScDREB1A. Taken together, we propose a model in which ScMYB7 acts as a repressor of cold tolerance via the CBF-dependent pathway. Under low-temperature stress, increased methylation of the pro-ScMYB7 promoter reduces ScMYB7 expression, thereby alleviating its repression of sugarcane DREB/CBF-type transcription factors and enhancing cold adaptation.

冷诱导启动子甲基化减弱scmyb7介导的CBF通路抑制:甘蔗冷适应的一种可能机制
冷胁迫是影响植物生长发育的重要环境因子。作为全球蔗糖主要来源的热带作物,甘蔗(Saccharum spp.杂种)特别容易受到次优温度条件的影响,冷害严重影响其产量潜力。尽管具有重要的农业意义,但甘蔗冷驯化的分子机制仍不清楚。在这里,我们报道了甘蔗冷抑制1R-MYB基因ScMYB7,其启动子(前ScMYB7)包含多个顺式作用元件,包括两个胞嘧啶-磷酸二酯-鸟嘌呤(CpG)岛。亚硫酸盐测序PCR (BSP)和qPCR结果显示,低温处理增加了启动子中CpG岛的甲基化水平,从而降低了ScMYB7基因的转录。启动子GUS酶活性测定结果也表明,低温处理抑制了启动子的转录活性,甲基化抑制剂可以减轻这种抑制作用。通过构建过表达ScMYB7的转基因拟南芥株系,研究了ScMYB7在调节耐寒性中的作用。我们观察到,转基因植株的耐寒性降低,表现为恢复后存活率下降,生理性状波动,c -重复结合因子(CBF)依赖通路基因(AtCBFs、AtCOR15和AtRD29A)的表达水平显著降低。酵母单杂交实验表明ScMYB7与AtCBF1启动子直接结合,而甘蔗ScDREB1A的抑制是间接发生的。此外,双荧光素酶报告基因实验表明,ScMYB7能够抑制AtCBF1或ScDREB1A的表达。综上所述,我们提出了一个模型,其中ScMYB7通过cbf依赖途径作为耐寒性的抑制因子。低温胁迫下,促ScMYB7启动子甲基化增加,可降低ScMYB7的表达,从而减轻其对甘蔗DREB/ cbf型转录因子的抑制,增强冷适应能力。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Plant, Cell & Environment
Plant, Cell & Environment 生物-植物科学
CiteScore
13.30
自引率
4.10%
发文量
253
审稿时长
1.8 months
期刊介绍: Plant, Cell & Environment is a premier plant science journal, offering valuable insights into plant responses to their environment. Committed to publishing high-quality theoretical and experimental research, the journal covers a broad spectrum of factors, spanning from molecular to community levels. Researchers exploring various aspects of plant biology, physiology, and ecology contribute to the journal's comprehensive understanding of plant-environment interactions.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信