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Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency

Peanut embryo development is easily affected by a variety of nutrient elements in the soil, especially the calcium level. Peanut produces abortive embryos in calcium-deficient soil, but underlying mechanism remains unclear. Thus, identifying key transcriptional regulators and their associated regula...

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Autores principales: Chen, Hua, Yang, Qiang, Fu, Huiwen, Chen, Kun, Zhao, Shanshan, Zhang, Chong, Cai, Tiecheng, Wang, Lihui, Lu, Wenzhi, Dang, Hao, Gao, Meijia, Li, Huaqi, Yuan, Xinyi, Varshney, Rajeev K., Zhuang, Weijian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8978587/
https://www.ncbi.nlm.nih.gov/pubmed/35386666
http://dx.doi.org/10.3389/fpls.2022.814015
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author Chen, Hua
Yang, Qiang
Fu, Huiwen
Chen, Kun
Zhao, Shanshan
Zhang, Chong
Cai, Tiecheng
Wang, Lihui
Lu, Wenzhi
Dang, Hao
Gao, Meijia
Li, Huaqi
Yuan, Xinyi
Varshney, Rajeev K.
Zhuang, Weijian
author_facet Chen, Hua
Yang, Qiang
Fu, Huiwen
Chen, Kun
Zhao, Shanshan
Zhang, Chong
Cai, Tiecheng
Wang, Lihui
Lu, Wenzhi
Dang, Hao
Gao, Meijia
Li, Huaqi
Yuan, Xinyi
Varshney, Rajeev K.
Zhuang, Weijian
author_sort Chen, Hua
collection PubMed
description Peanut embryo development is easily affected by a variety of nutrient elements in the soil, especially the calcium level. Peanut produces abortive embryos in calcium-deficient soil, but underlying mechanism remains unclear. Thus, identifying key transcriptional regulators and their associated regulatory networks promises to contribute to a better understanding of this process. In this study, cellular biology and gene expression analyses were performed to investigate peanut embryo development with the aim to discern the global architecture of gene regulatory networks underlying peanut embryo abortion under calcium deficiency conditions. The endomembrane systems tended to disintegrate, impairing cell growth and starch, protein and lipid body accumulation, resulting in aborted seeds. RNA-seq analysis showed that the gene expression profile in peanut embryos was significantly changed under calcium deficiency. Further analysis indicated that multiple signal pathways were involved in the peanut embryo abortion. Differential expressed genes (DEGs) related to cytoplasmic free Ca(2+) were significantly altered. DEGs in plant hormone signaling pathways tended to be associated with increased IAA and ethylene but with decreased ABA, gibberellin, cytokinin, and brassinosteroid levels. Certain vital genes, including apoptosis-inducing factor, WRKYs and ethylene-responsive transcription factors, were up-regulated, while key regulators of embryo development, such as TCP4, WRI1, FUS3, ABI3, and GLK1 were down-regulated. Weighted gene co-expression network analysis (WGCNA) identified 16 significant modules associated with the plant hormone signaling, MAPK signaling, ubiquitin mediated proteolysis, reserve substance biosynthesis and metabolism pathways to decipher regulatory network. The most significant module was darkolivegreen2 and FUS3 (AH06G23930) had the highest connectivity among this module. Importantly, key transcription factors involved in embryogenesis or ovule development including TCP4, GLK1, ABI3, bHLH115, MYC2, etc., were also present in this module and down regulated under calcium deficiency. This study presents the first global view of the gene regulatory network involved in peanut embryo abortion under calcium deficiency conditions and lays foundation for improving peanut tolerances to calcium deficiency by a targeted manipulation of molecular breeding.
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spelling pubmed-89785872022-04-05 Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency Chen, Hua Yang, Qiang Fu, Huiwen Chen, Kun Zhao, Shanshan Zhang, Chong Cai, Tiecheng Wang, Lihui Lu, Wenzhi Dang, Hao Gao, Meijia Li, Huaqi Yuan, Xinyi Varshney, Rajeev K. Zhuang, Weijian Front Plant Sci Plant Science Peanut embryo development is easily affected by a variety of nutrient elements in the soil, especially the calcium level. Peanut produces abortive embryos in calcium-deficient soil, but underlying mechanism remains unclear. Thus, identifying key transcriptional regulators and their associated regulatory networks promises to contribute to a better understanding of this process. In this study, cellular biology and gene expression analyses were performed to investigate peanut embryo development with the aim to discern the global architecture of gene regulatory networks underlying peanut embryo abortion under calcium deficiency conditions. The endomembrane systems tended to disintegrate, impairing cell growth and starch, protein and lipid body accumulation, resulting in aborted seeds. RNA-seq analysis showed that the gene expression profile in peanut embryos was significantly changed under calcium deficiency. Further analysis indicated that multiple signal pathways were involved in the peanut embryo abortion. Differential expressed genes (DEGs) related to cytoplasmic free Ca(2+) were significantly altered. DEGs in plant hormone signaling pathways tended to be associated with increased IAA and ethylene but with decreased ABA, gibberellin, cytokinin, and brassinosteroid levels. Certain vital genes, including apoptosis-inducing factor, WRKYs and ethylene-responsive transcription factors, were up-regulated, while key regulators of embryo development, such as TCP4, WRI1, FUS3, ABI3, and GLK1 were down-regulated. Weighted gene co-expression network analysis (WGCNA) identified 16 significant modules associated with the plant hormone signaling, MAPK signaling, ubiquitin mediated proteolysis, reserve substance biosynthesis and metabolism pathways to decipher regulatory network. The most significant module was darkolivegreen2 and FUS3 (AH06G23930) had the highest connectivity among this module. Importantly, key transcription factors involved in embryogenesis or ovule development including TCP4, GLK1, ABI3, bHLH115, MYC2, etc., were also present in this module and down regulated under calcium deficiency. This study presents the first global view of the gene regulatory network involved in peanut embryo abortion under calcium deficiency conditions and lays foundation for improving peanut tolerances to calcium deficiency by a targeted manipulation of molecular breeding. Frontiers Media S.A. 2022-03-21 /pmc/articles/PMC8978587/ /pubmed/35386666 http://dx.doi.org/10.3389/fpls.2022.814015 Text en Copyright © 2022 Chen, Yang, Fu, Chen, Zhao, Zhang, Cai, Wang, Lu, Dang, Gao, Li, Yuan, Varshney and Zhuang. 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
Chen, Hua
Yang, Qiang
Fu, Huiwen
Chen, Kun
Zhao, Shanshan
Zhang, Chong
Cai, Tiecheng
Wang, Lihui
Lu, Wenzhi
Dang, Hao
Gao, Meijia
Li, Huaqi
Yuan, Xinyi
Varshney, Rajeev K.
Zhuang, Weijian
Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency
title Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency
title_full Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency
title_fullStr Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency
title_full_unstemmed Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency
title_short Identification of Key Gene Networks and Deciphering Transcriptional Regulators Associated With Peanut Embryo Abortion Mediated by Calcium Deficiency
title_sort identification of key gene networks and deciphering transcriptional regulators associated with peanut embryo abortion mediated by calcium deficiency
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8978587/
https://www.ncbi.nlm.nih.gov/pubmed/35386666
http://dx.doi.org/10.3389/fpls.2022.814015
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