Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress

DNA methylation plays an important role against adverse environment by reshaping transcriptional profile in plants. To better understand the molecular mechanisms of watermelon response to osmotic stress, the suspension cultured watermelon cells were treated with 100mM mannitol, and then a methylated...

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Autores principales:	Fangming Zhu, Mingyan Li, Manwen Yan, Fei Qiao, Xuefei Jiang
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	Citrullus lanatus osmotic stress transcriptome analysis whole genome bisulfite sequencing DNA methylation Plant culture SB1-1110
Acceso en línea:	https://doaj.org/article/ca92a2d9ef17477c8726e465620df96c
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spelling	oai:doaj.org-article:ca92a2d9ef17477c8726e465620df96c2021-12-01T14:24:42ZIntegrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress1664-462X10.3389/fpls.2021.769712https://doaj.org/article/ca92a2d9ef17477c8726e465620df96c2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fpls.2021.769712/fullhttps://doaj.org/toc/1664-462XDNA methylation plays an important role against adverse environment by reshaping transcriptional profile in plants. To better understand the molecular mechanisms of watermelon response to osmotic stress, the suspension cultured watermelon cells were treated with 100mM mannitol, and then a methylated cytosines map was generated by whole genome bisulfite sequencing (WGBS). Combined with transcriptome sequencing, the effects of osmotic stress on differentially methylated expressed genes (DMEGs) were assessed. It was found that genes related to plant hormone synthesis, signal transduction, osmoregulatory substance-related and reactive oxygen species scavenging-related enzyme could rapidly respond to osmotic stress. The overall methylation level of watermelon decreased after osmotic stress treatment, and demethylation occurred in CG, CHG, and CHH contexts. Moreover, differentially methylated expressed genes (DMEGs) were significantly enriched in RNA transport, starch and sucrose metabolism, plant hormone signal transduction and biosynthesis of secondary metabolites, especially in biosynthesis of osmolytes synthase genes. Interestingly, demethylation of a key enzyme gene Cla014489 in biosynthesis of inositol upregulated its expression and promoted accumulation of inositol, which could alleviate the inhibition of cell growth caused by osmotic stress. Meanwhile, a recombinant plasmid pET28a-Cla014489 was constructed and transferred into Escherichia coli BL21 for prokaryotic expression and the expression of ClMIPS protein could improve the tolerance of E. coli to osmotic stress. The effect of methylation level on the expression properties of inositol and its related genes was further confirmed by application of DNA methylation inhibitor 5-azacytidine. These results provide a preliminary insight into the altered methylation levels of watermelon cells in response to osmotic stress and suggest a new mechanism that how watermelon cells adapt to osmotic stress.Fangming ZhuFangming ZhuMingyan LiMingyan LiManwen YanFei QiaoFei QiaoXuefei JiangXuefei JiangFrontiers Media S.A.articleCitrullus lanatusosmotic stresstranscriptome analysiswhole genome bisulfite sequencingDNA methylationPlant cultureSB1-1110ENFrontiers in Plant Science, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Citrullus lanatus osmotic stress transcriptome analysis whole genome bisulfite sequencing DNA methylation Plant culture SB1-1110
spellingShingle	Citrullus lanatus osmotic stress transcriptome analysis whole genome bisulfite sequencing DNA methylation Plant culture SB1-1110 Fangming Zhu Fangming Zhu Mingyan Li Mingyan Li Manwen Yan Fei Qiao Fei Qiao Xuefei Jiang Xuefei Jiang Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress
description	DNA methylation plays an important role against adverse environment by reshaping transcriptional profile in plants. To better understand the molecular mechanisms of watermelon response to osmotic stress, the suspension cultured watermelon cells were treated with 100mM mannitol, and then a methylated cytosines map was generated by whole genome bisulfite sequencing (WGBS). Combined with transcriptome sequencing, the effects of osmotic stress on differentially methylated expressed genes (DMEGs) were assessed. It was found that genes related to plant hormone synthesis, signal transduction, osmoregulatory substance-related and reactive oxygen species scavenging-related enzyme could rapidly respond to osmotic stress. The overall methylation level of watermelon decreased after osmotic stress treatment, and demethylation occurred in CG, CHG, and CHH contexts. Moreover, differentially methylated expressed genes (DMEGs) were significantly enriched in RNA transport, starch and sucrose metabolism, plant hormone signal transduction and biosynthesis of secondary metabolites, especially in biosynthesis of osmolytes synthase genes. Interestingly, demethylation of a key enzyme gene Cla014489 in biosynthesis of inositol upregulated its expression and promoted accumulation of inositol, which could alleviate the inhibition of cell growth caused by osmotic stress. Meanwhile, a recombinant plasmid pET28a-Cla014489 was constructed and transferred into Escherichia coli BL21 for prokaryotic expression and the expression of ClMIPS protein could improve the tolerance of E. coli to osmotic stress. The effect of methylation level on the expression properties of inositol and its related genes was further confirmed by application of DNA methylation inhibitor 5-azacytidine. These results provide a preliminary insight into the altered methylation levels of watermelon cells in response to osmotic stress and suggest a new mechanism that how watermelon cells adapt to osmotic stress.
format	article
author	Fangming Zhu Fangming Zhu Mingyan Li Mingyan Li Manwen Yan Fei Qiao Fei Qiao Xuefei Jiang Xuefei Jiang
author_facet	Fangming Zhu Fangming Zhu Mingyan Li Mingyan Li Manwen Yan Fei Qiao Fei Qiao Xuefei Jiang Xuefei Jiang
author_sort	Fangming Zhu
title	Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress
title_short	Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress
title_full	Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress
title_fullStr	Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress
title_full_unstemmed	Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress
title_sort	integrated transcriptome analysis and single-base resolution methylomes of watermelon (citrullus lanatus) reveal epigenome modifications in response to osmotic stress
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/ca92a2d9ef17477c8726e465620df96c
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Integrated Transcriptome Analysis and Single-Base Resolution Methylomes of Watermelon (Citrullus lanatus) Reveal Epigenome Modifications in Response to Osmotic Stress

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