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Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)

INTRODUCTION: The wild allotetraploid peanut Arachis monticola contains a higher oil content than the cultivated allotetraploid Arachis hypogaea. Besides the fact that increasing oil content is the most important peanut breeding objective, a proper understanding of its molecular mechanism controllin...

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Autores principales: Liu, Nian, Wu, Bei, Pandey, Manish K., Huang, Li, Luo, Huaiyong, Chen, Yuning, Zhou, Xiaojing, Chen, Weigang, Huai, Dongxin, Yu, Bolun, Chen, Hao, Guo, Jianbin, Lei, Yong, Liao, Boshou, Varshney, Rajeev K., Jiang, Huifang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9802669/
https://www.ncbi.nlm.nih.gov/pubmed/36589096
http://dx.doi.org/10.3389/fpls.2022.1065267
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author Liu, Nian
Wu, Bei
Pandey, Manish K.
Huang, Li
Luo, Huaiyong
Chen, Yuning
Zhou, Xiaojing
Chen, Weigang
Huai, Dongxin
Yu, Bolun
Chen, Hao
Guo, Jianbin
Lei, Yong
Liao, Boshou
Varshney, Rajeev K.
Jiang, Huifang
author_facet Liu, Nian
Wu, Bei
Pandey, Manish K.
Huang, Li
Luo, Huaiyong
Chen, Yuning
Zhou, Xiaojing
Chen, Weigang
Huai, Dongxin
Yu, Bolun
Chen, Hao
Guo, Jianbin
Lei, Yong
Liao, Boshou
Varshney, Rajeev K.
Jiang, Huifang
author_sort Liu, Nian
collection PubMed
description INTRODUCTION: The wild allotetraploid peanut Arachis monticola contains a higher oil content than the cultivated allotetraploid Arachis hypogaea. Besides the fact that increasing oil content is the most important peanut breeding objective, a proper understanding of its molecular mechanism controlling oil accumulation is still lacking. METHODS: We investigated this aspect by performing comparative transcriptomics from developing seeds between three wild and five cultivated peanut varieties. RESULTS: The analyses not only showed species-specific grouping transcriptional profiles but also detected two gene clusters with divergent expression patterns between two species enriched in lipid metabolism. Further analysis revealed that expression alteration of lipid metabolic genes with co-expressed transcription factors in wild peanut led to enhanced activity of oil biogenesis and retarded the rate of lipid degradation. In addition, bisulfite sequencing was conducted to characterize the variation of DNA methylation between wild allotetraploid (245, WH 10025) and cultivated allotetraploid (Z16, Zhh 7720) genotypes. CG and CHG context methylation was found to antagonistically correlate with gene expression during seed development. Differentially methylated region analysis and transgenic assay further illustrated that variations of DNA methylation between wild and cultivated peanuts could affect the oil content via altering the expression of peroxisomal acyl transporter protein (Araip.H6S1B). DISCUSSION: From the results, we deduced that DNA methylation may negatively regulate lipid metabolic genes and transcription factors to subtly affect oil accumulation divergence between wild and cultivated peanuts. Our work provided the first glimpse on the regulatory mechanism of gene expression altering for oil accumulation in wild peanut and gene resources for future breeding applications.
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spelling pubmed-98026692022-12-31 Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola) Liu, Nian Wu, Bei Pandey, Manish K. Huang, Li Luo, Huaiyong Chen, Yuning Zhou, Xiaojing Chen, Weigang Huai, Dongxin Yu, Bolun Chen, Hao Guo, Jianbin Lei, Yong Liao, Boshou Varshney, Rajeev K. Jiang, Huifang Front Plant Sci Plant Science INTRODUCTION: The wild allotetraploid peanut Arachis monticola contains a higher oil content than the cultivated allotetraploid Arachis hypogaea. Besides the fact that increasing oil content is the most important peanut breeding objective, a proper understanding of its molecular mechanism controlling oil accumulation is still lacking. METHODS: We investigated this aspect by performing comparative transcriptomics from developing seeds between three wild and five cultivated peanut varieties. RESULTS: The analyses not only showed species-specific grouping transcriptional profiles but also detected two gene clusters with divergent expression patterns between two species enriched in lipid metabolism. Further analysis revealed that expression alteration of lipid metabolic genes with co-expressed transcription factors in wild peanut led to enhanced activity of oil biogenesis and retarded the rate of lipid degradation. In addition, bisulfite sequencing was conducted to characterize the variation of DNA methylation between wild allotetraploid (245, WH 10025) and cultivated allotetraploid (Z16, Zhh 7720) genotypes. CG and CHG context methylation was found to antagonistically correlate with gene expression during seed development. Differentially methylated region analysis and transgenic assay further illustrated that variations of DNA methylation between wild and cultivated peanuts could affect the oil content via altering the expression of peroxisomal acyl transporter protein (Araip.H6S1B). DISCUSSION: From the results, we deduced that DNA methylation may negatively regulate lipid metabolic genes and transcription factors to subtly affect oil accumulation divergence between wild and cultivated peanuts. Our work provided the first glimpse on the regulatory mechanism of gene expression altering for oil accumulation in wild peanut and gene resources for future breeding applications. Frontiers Media S.A. 2022-12-16 /pmc/articles/PMC9802669/ /pubmed/36589096 http://dx.doi.org/10.3389/fpls.2022.1065267 Text en Copyright © 2022 Liu, Wu, Pandey, Huang, Luo, Chen, Zhou, Chen, Huai, Yu, Chen, Guo, Lei, Liao, Varshney and Jiang https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Liu, Nian
Wu, Bei
Pandey, Manish K.
Huang, Li
Luo, Huaiyong
Chen, Yuning
Zhou, Xiaojing
Chen, Weigang
Huai, Dongxin
Yu, Bolun
Chen, Hao
Guo, Jianbin
Lei, Yong
Liao, Boshou
Varshney, Rajeev K.
Jiang, Huifang
Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)
title Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)
title_full Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)
title_fullStr Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)
title_full_unstemmed Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)
title_short Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)
title_sort gene expression and dna methylation altering lead to the high oil content in wild allotetraploid peanut (a. monticola)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9802669/
https://www.ncbi.nlm.nih.gov/pubmed/36589096
http://dx.doi.org/10.3389/fpls.2022.1065267
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