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DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis

BACKGROUND: The aleurone layer is a part of many plant seeds, and during seed germination, aleurone cells undergo PCD, which is promoted by GA from the embryo. However, the numerous components of the GA signaling pathway that mediate PCD of the aleurone layers remain to be identified. Few genes and...

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Autores principales: Wu, Yequn, Hou, Jiaqi, Ren, Ruifei, Chen, Zhenfei, Yue, Mengxia, Li, Le, Hou, Haoli, Zheng, Xueke, Li, Lijia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10664605/
https://www.ncbi.nlm.nih.gov/pubmed/37993774
http://dx.doi.org/10.1186/s12870-023-04565-5
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author Wu, Yequn
Hou, Jiaqi
Ren, Ruifei
Chen, Zhenfei
Yue, Mengxia
Li, Le
Hou, Haoli
Zheng, Xueke
Li, Lijia
author_facet Wu, Yequn
Hou, Jiaqi
Ren, Ruifei
Chen, Zhenfei
Yue, Mengxia
Li, Le
Hou, Haoli
Zheng, Xueke
Li, Lijia
author_sort Wu, Yequn
collection PubMed
description BACKGROUND: The aleurone layer is a part of many plant seeds, and during seed germination, aleurone cells undergo PCD, which is promoted by GA from the embryo. However, the numerous components of the GA signaling pathway that mediate PCD of the aleurone layers remain to be identified. Few genes and transcriptomes have been studied thus far in aleurone layers to improve our understanding of how PCD occurs and how the regulatory mechanism functions during PCD. Our previous studies have shown that histone deacetylases (HDACs) are required in GA-induced PCD of aleurone layer. To further explore the molecular mechanisms by which epigenetic modifications regulate aleurone PCD, we performed a global comparative transcriptome analysis of embryoless aleurones treated with GA or histone acetylase (HAT) inhibitors. RESULTS: In this study, a total of 7,919 differentially expressed genes (DEGs) were analyzed, 2,554 DEGs of which were found to be common under two treatments. These identified DEGs were involved in various biological processes, including DNA methylation, lipid metabolism and ROS signaling. Further investigations revealed that inhibition of DNA methyltransferases prevented aleurone PCD, suggesting that active DNA methylation plays a role in regulating aleurone PCD. GA or HAT inhibitor induced lipoxygenase gene expression, leading to lipid degradation, but this process was not affected by DNA methylation. However, DNA methylation inhibitor could regulate ROS-related gene expression and inhibit GA-induced production of hydrogen peroxide (H(2)O(2)). CONCLUSION: Overall, linking of lipoxygenase, DNA methylation, and H(2)O(2) may indicate that GA-induced higher HDAC activity in aleurones causes breakdown of lipids via regulating lipoxygenase gene expression, and increased DNA methylation positively mediates H(2)O(2) production; thus, DNA methylation and lipid metabolism pathways may represent an important and complex signaling network in maize aleurone PCD. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04565-5.
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spelling pubmed-106646052023-11-22 DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis Wu, Yequn Hou, Jiaqi Ren, Ruifei Chen, Zhenfei Yue, Mengxia Li, Le Hou, Haoli Zheng, Xueke Li, Lijia BMC Plant Biol Research BACKGROUND: The aleurone layer is a part of many plant seeds, and during seed germination, aleurone cells undergo PCD, which is promoted by GA from the embryo. However, the numerous components of the GA signaling pathway that mediate PCD of the aleurone layers remain to be identified. Few genes and transcriptomes have been studied thus far in aleurone layers to improve our understanding of how PCD occurs and how the regulatory mechanism functions during PCD. Our previous studies have shown that histone deacetylases (HDACs) are required in GA-induced PCD of aleurone layer. To further explore the molecular mechanisms by which epigenetic modifications regulate aleurone PCD, we performed a global comparative transcriptome analysis of embryoless aleurones treated with GA or histone acetylase (HAT) inhibitors. RESULTS: In this study, a total of 7,919 differentially expressed genes (DEGs) were analyzed, 2,554 DEGs of which were found to be common under two treatments. These identified DEGs were involved in various biological processes, including DNA methylation, lipid metabolism and ROS signaling. Further investigations revealed that inhibition of DNA methyltransferases prevented aleurone PCD, suggesting that active DNA methylation plays a role in regulating aleurone PCD. GA or HAT inhibitor induced lipoxygenase gene expression, leading to lipid degradation, but this process was not affected by DNA methylation. However, DNA methylation inhibitor could regulate ROS-related gene expression and inhibit GA-induced production of hydrogen peroxide (H(2)O(2)). CONCLUSION: Overall, linking of lipoxygenase, DNA methylation, and H(2)O(2) may indicate that GA-induced higher HDAC activity in aleurones causes breakdown of lipids via regulating lipoxygenase gene expression, and increased DNA methylation positively mediates H(2)O(2) production; thus, DNA methylation and lipid metabolism pathways may represent an important and complex signaling network in maize aleurone PCD. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04565-5. BioMed Central 2023-11-22 /pmc/articles/PMC10664605/ /pubmed/37993774 http://dx.doi.org/10.1186/s12870-023-04565-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Wu, Yequn
Hou, Jiaqi
Ren, Ruifei
Chen, Zhenfei
Yue, Mengxia
Li, Le
Hou, Haoli
Zheng, Xueke
Li, Lijia
DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis
title DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis
title_full DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis
title_fullStr DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis
title_full_unstemmed DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis
title_short DNA methylation and lipid metabolism are involved in GA-induced maize aleurone layers PCD as revealed by transcriptome analysis
title_sort dna methylation and lipid metabolism are involved in ga-induced maize aleurone layers pcd as revealed by transcriptome analysis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10664605/
https://www.ncbi.nlm.nih.gov/pubmed/37993774
http://dx.doi.org/10.1186/s12870-023-04565-5
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