Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thaliana

Methyl-CPG-Binding Domain (MBD) proteins play important roles in plant growth, development, and stress responses. The present study characterized the MBD families in watermelon and other cucurbit plants regarding the gene numbers and structures, phylogenetic and syntenic relationships, evolution eve...

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Main Authors: Jiayu Liang, Xiaodan Li, Ya Wen, Xinyi Wu, Hui Wang, Dayong Li, Fengming Song
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.886965/full
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author Jiayu Liang
Xiaodan Li
Ya Wen
Xinyi Wu
Hui Wang
Dayong Li
Fengming Song
author_facet Jiayu Liang
Xiaodan Li
Ya Wen
Xinyi Wu
Hui Wang
Dayong Li
Fengming Song
author_sort Jiayu Liang
collection DOAJ
description Methyl-CPG-Binding Domain (MBD) proteins play important roles in plant growth, development, and stress responses. The present study characterized the MBD families in watermelon and other cucurbit plants regarding the gene numbers and structures, phylogenetic and syntenic relationships, evolution events, and conserved domain organization of the MBD proteins. The watermelon ClMBD proteins were found to be localized in nucleus, and ClMBD2 and ClMBD3 interacted with ClIDM2 and ClIDM3. ClMBD2 bound to DNA harboring methylated CG sites but not to DNA with methylated CHG and CHH sites in vitro. The ClMBD genes exhibited distinct expression patterns in watermelon plants after SA and MeJA treatment and after infection by fungal pathogens Fusarium oxysporum f.sp. niveum and Didymella bryoniae. Overexpression of ClMBD2, ClMBD3, or ClMBD5 in Arabidopsis resulted in attenuated resistance against Botrytis cinerea, accompanied by down-regulated expression of AtPDF1.2 and increased accumulation of H2O2 upon B. cinerea infection. Overexpression of ClMBD1 and ClMBD2 led to down-regulated expression of AtPR1 and decreased resistance while overexpression of ClMBD5 resulted in up-regulated expression of AtPR1 and increased resistance against Pseudomonas syringae pv. tomato DC3000. Transcriptome analysis revealed that overexpression of ClMBD2 in Arabidopsis up-regulated the expression of a small set of genes that negatively regulate Arabidopsis immunity. These data suggest the importance of some ClMBD genes in plant immunity and provide the possibility to improve plant immunity through modification of specific ClMBD genes.
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spelling doaj.art-5dc58eb8dae048139d18735884ebf5022022-12-22T02:23:58ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-05-011310.3389/fpls.2022.886965886965Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thalianaJiayu LiangXiaodan LiYa WenXinyi WuHui WangDayong LiFengming SongMethyl-CPG-Binding Domain (MBD) proteins play important roles in plant growth, development, and stress responses. The present study characterized the MBD families in watermelon and other cucurbit plants regarding the gene numbers and structures, phylogenetic and syntenic relationships, evolution events, and conserved domain organization of the MBD proteins. The watermelon ClMBD proteins were found to be localized in nucleus, and ClMBD2 and ClMBD3 interacted with ClIDM2 and ClIDM3. ClMBD2 bound to DNA harboring methylated CG sites but not to DNA with methylated CHG and CHH sites in vitro. The ClMBD genes exhibited distinct expression patterns in watermelon plants after SA and MeJA treatment and after infection by fungal pathogens Fusarium oxysporum f.sp. niveum and Didymella bryoniae. Overexpression of ClMBD2, ClMBD3, or ClMBD5 in Arabidopsis resulted in attenuated resistance against Botrytis cinerea, accompanied by down-regulated expression of AtPDF1.2 and increased accumulation of H2O2 upon B. cinerea infection. Overexpression of ClMBD1 and ClMBD2 led to down-regulated expression of AtPR1 and decreased resistance while overexpression of ClMBD5 resulted in up-regulated expression of AtPR1 and increased resistance against Pseudomonas syringae pv. tomato DC3000. Transcriptome analysis revealed that overexpression of ClMBD2 in Arabidopsis up-regulated the expression of a small set of genes that negatively regulate Arabidopsis immunity. These data suggest the importance of some ClMBD genes in plant immunity and provide the possibility to improve plant immunity through modification of specific ClMBD genes.https://www.frontiersin.org/articles/10.3389/fpls.2022.886965/fullwatermelon (Citrullus lanatus L.)methyl-CPG-binding domain (MBD) proteinClMBD2disease resistanceDNA methylationArabidopsis
spellingShingle Jiayu Liang
Xiaodan Li
Ya Wen
Xinyi Wu
Hui Wang
Dayong Li
Fengming Song
Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thaliana
Frontiers in Plant Science
watermelon (Citrullus lanatus L.)
methyl-CPG-binding domain (MBD) protein
ClMBD2
disease resistance
DNA methylation
Arabidopsis
title Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thaliana
title_full Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thaliana
title_fullStr Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thaliana
title_full_unstemmed Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thaliana
title_short Genome-Wide Characterization of the Methyl CpG Binding Domain-Containing Proteins in Watermelon and Functional Analysis of Their Roles in Disease Resistance Through Ectopic Overexpression in Arabidopsis thaliana
title_sort genome wide characterization of the methyl cpg binding domain containing proteins in watermelon and functional analysis of their roles in disease resistance through ectopic overexpression in arabidopsis thaliana
topic watermelon (Citrullus lanatus L.)
methyl-CPG-binding domain (MBD) protein
ClMBD2
disease resistance
DNA methylation
Arabidopsis
url https://www.frontiersin.org/articles/10.3389/fpls.2022.886965/full
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