Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot

Gibberella stalk rot (GSR) caused by Fusarium graminearum is one of the most devastating diseases causing significant yield loss of maize, and GSR resistance is a quantitative trait controlled by multiple genes. Although a few quantitative trait loci/resistance genes have been identified, the molecu...

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Main Authors: Yali Sun, Xinsen Ruan, Qing Wang, Yu Zhou, Fang Wang, Liang Ma, Zhenhua Wang, Xiquan Gao
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.664733/full
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author Yali Sun
Yali Sun
Yali Sun
Xinsen Ruan
Xinsen Ruan
Xinsen Ruan
Qing Wang
Qing Wang
Qing Wang
Yu Zhou
Fang Wang
Fang Wang
Fang Wang
Liang Ma
Liang Ma
Liang Ma
Zhenhua Wang
Xiquan Gao
Xiquan Gao
Xiquan Gao
author_facet Yali Sun
Yali Sun
Yali Sun
Xinsen Ruan
Xinsen Ruan
Xinsen Ruan
Qing Wang
Qing Wang
Qing Wang
Yu Zhou
Fang Wang
Fang Wang
Fang Wang
Liang Ma
Liang Ma
Liang Ma
Zhenhua Wang
Xiquan Gao
Xiquan Gao
Xiquan Gao
author_sort Yali Sun
collection DOAJ
description Gibberella stalk rot (GSR) caused by Fusarium graminearum is one of the most devastating diseases causing significant yield loss of maize, and GSR resistance is a quantitative trait controlled by multiple genes. Although a few quantitative trait loci/resistance genes have been identified, the molecular mechanisms underlying GSR resistance remain largely unexplored. To identify potential resistance genes and to better understand the molecular mechanism of GSR resistance, a joint analysis using a comparative transcriptomic and metabolomic approaches was conducted using two inbred lines with contrasting GSR resistance, K09 (resistant) and A08 (susceptible), upon infection with F. graminearum. While a substantial number of differentially expressed genes associated with various defense-related signaling pathways were identified between two lines, multiple hub genes likely associated with GSR resistance were pinpointed using Weighted Gene Correlation Network Analysis and K-means clustering. Moreover, a core set of metabolites, including anthocyanins, associated with the hub genes was determined. Among the complex co-expression networks, ZmHIR3 showed strong correlation with multiple key genes, and genetic and histological studies showed that zmhir3 mutant is more susceptible to GSR, accompanied by enhanced cell death in the stem in response to infection with F. graminearum. Taken together, our study identified differentially expressed key genes and metabolites, as well as co-expression networks associated with distinct infection stages of F. graminearum. Moreover, ZmHIR3 likely plays a positive role in disease resistance to GSR, probably through the transcriptional regulation of key genes, functional metabolites, and the control of cell death.
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spelling doaj.art-8507127cf7f040868805419c92b042c52022-12-21T19:06:15ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-05-011210.3389/fpls.2021.664733664733Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk RotYali Sun0Yali Sun1Yali Sun2Xinsen Ruan3Xinsen Ruan4Xinsen Ruan5Qing Wang6Qing Wang7Qing Wang8Yu Zhou9Fang Wang10Fang Wang11Fang Wang12Liang Ma13Liang Ma14Liang Ma15Zhenhua Wang16Xiquan Gao17Xiquan Gao18Xiquan Gao19State Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, ChinaJiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, ChinaJiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, ChinaJiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Northeast Agricultural University, Harbin, ChinaState Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, ChinaJiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, ChinaJiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Northeast Agricultural University, Harbin, ChinaState Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, ChinaJiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, ChinaCollege of Agriculture, Nanjing Agricultural University, Nanjing, ChinaGibberella stalk rot (GSR) caused by Fusarium graminearum is one of the most devastating diseases causing significant yield loss of maize, and GSR resistance is a quantitative trait controlled by multiple genes. Although a few quantitative trait loci/resistance genes have been identified, the molecular mechanisms underlying GSR resistance remain largely unexplored. To identify potential resistance genes and to better understand the molecular mechanism of GSR resistance, a joint analysis using a comparative transcriptomic and metabolomic approaches was conducted using two inbred lines with contrasting GSR resistance, K09 (resistant) and A08 (susceptible), upon infection with F. graminearum. While a substantial number of differentially expressed genes associated with various defense-related signaling pathways were identified between two lines, multiple hub genes likely associated with GSR resistance were pinpointed using Weighted Gene Correlation Network Analysis and K-means clustering. Moreover, a core set of metabolites, including anthocyanins, associated with the hub genes was determined. Among the complex co-expression networks, ZmHIR3 showed strong correlation with multiple key genes, and genetic and histological studies showed that zmhir3 mutant is more susceptible to GSR, accompanied by enhanced cell death in the stem in response to infection with F. graminearum. Taken together, our study identified differentially expressed key genes and metabolites, as well as co-expression networks associated with distinct infection stages of F. graminearum. Moreover, ZmHIR3 likely plays a positive role in disease resistance to GSR, probably through the transcriptional regulation of key genes, functional metabolites, and the control of cell death.https://www.frontiersin.org/articles/10.3389/fpls.2021.664733/fullanthocyaninco-expression networkcell deathGibberella stalk rothypersensitive induced reaction 3maize
spellingShingle Yali Sun
Yali Sun
Yali Sun
Xinsen Ruan
Xinsen Ruan
Xinsen Ruan
Qing Wang
Qing Wang
Qing Wang
Yu Zhou
Fang Wang
Fang Wang
Fang Wang
Liang Ma
Liang Ma
Liang Ma
Zhenhua Wang
Xiquan Gao
Xiquan Gao
Xiquan Gao
Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot
Frontiers in Plant Science
anthocyanin
co-expression network
cell death
Gibberella stalk rot
hypersensitive induced reaction 3
maize
title Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot
title_full Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot
title_fullStr Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot
title_full_unstemmed Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot
title_short Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot
title_sort integrated gene co expression analysis and metabolites profiling highlight the important role of zmhir3 in maize resistance to gibberella stalk rot
topic anthocyanin
co-expression network
cell death
Gibberella stalk rot
hypersensitive induced reaction 3
maize
url https://www.frontiersin.org/articles/10.3389/fpls.2021.664733/full
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