Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot

Gibberella stalk rot caused by Fusarium graminearum is one of the devastating diseases of maize that causes significant yield losses worldwide. The molecular mechanisms regulating defense against this pathogen remain poorly understood. According to recent studies, a major oxylipin hormone produced b...

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Main Authors: Qing Wang, Yali Sun, Fang Wang, Pei-Cheng Huang, Yinying Wang, Xinsen Ruan, Liang Ma, Xin Li, Michael V. Kolomiets, Xiquan Gao
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.699146/full
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author Qing Wang
Qing Wang
Qing Wang
Yali Sun
Yali Sun
Yali Sun
Fang Wang
Fang Wang
Fang Wang
Pei-Cheng Huang
Yinying Wang
Yinying Wang
Yinying Wang
Xinsen Ruan
Xinsen Ruan
Xinsen Ruan
Liang Ma
Liang Ma
Liang Ma
Xin Li
Xin Li
Xin Li
Michael V. Kolomiets
Xiquan Gao
Xiquan Gao
Xiquan Gao
author_facet Qing Wang
Qing Wang
Qing Wang
Yali Sun
Yali Sun
Yali Sun
Fang Wang
Fang Wang
Fang Wang
Pei-Cheng Huang
Yinying Wang
Yinying Wang
Yinying Wang
Xinsen Ruan
Xinsen Ruan
Xinsen Ruan
Liang Ma
Liang Ma
Liang Ma
Xin Li
Xin Li
Xin Li
Michael V. Kolomiets
Xiquan Gao
Xiquan Gao
Xiquan Gao
author_sort Qing Wang
collection DOAJ
description Gibberella stalk rot caused by Fusarium graminearum is one of the devastating diseases of maize that causes significant yield losses worldwide. The molecular mechanisms regulating defense against this pathogen remain poorly understood. According to recent studies, a major oxylipin hormone produced by 13-lipoxygenases (LOX) namely jasmonic acid (JA) has been associated with maize susceptibility to GSR. However, the specific roles of numerous 9-LOX-derived oxylipins in defense against Gibberella stalk rot (GSR) remain unexplained. In this study, we have shown that disruption of a 9-LOX gene, ZmLOX5, resulted in increased susceptibility to GSR, indicating its role in defense. To understand how ZmLOX5 regulates GSR resistance, we conducted transcriptome and oxylipin profiling using a zmlox5-3 mutant and near-isogenic wild type B73, upon infection with F. graminearum. The results showed that JA biosynthetic pathway genes were highly up-regulated, whereas multiple 9-LOX pathway genes were down-regulated in the infected zmlox5-3 mutant. Furthermore, oxylipin profiling of the mutant revealed significantly higher contents of several jasmonates but relatively lower levels of 9-oxylipins in zmlox5-3 upon infection. In contrast, B73 and W438, a more resistant inbred line, displayed relatively lower levels of JAs, but a considerable increase of 9-oxylipins. These results suggest antagonistic interaction between 9-oxylipins and JAs, wherein 9-oxylipins contribute to resistance while JAs facilitate susceptibility to F. graminearum.
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spelling doaj.art-13bbca765006495a9b9bfecae4c1d0ee2022-12-21T17:15:51ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-09-011210.3389/fpls.2021.699146699146Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk RotQing Wang0Qing Wang1Qing Wang2Yali Sun3Yali Sun4Yali Sun5Fang Wang6Fang Wang7Fang Wang8Pei-Cheng Huang9Yinying Wang10Yinying Wang11Yinying Wang12Xinsen Ruan13Xinsen Ruan14Xinsen Ruan15Liang Ma16Liang Ma17Liang Ma18Xin Li19Xin Li20Xin Li21Michael V. Kolomiets22Xiquan Gao23Xiquan Gao24Xiquan Gao25State 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, ChinaDepartment of Plant Pathology and Microbiology, Texas A&M University, College Station, TX, United StatesState 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, 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, ChinaDepartment of Plant Pathology and Microbiology, Texas A&M University, College Station, TX, United StatesState 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 caused by Fusarium graminearum is one of the devastating diseases of maize that causes significant yield losses worldwide. The molecular mechanisms regulating defense against this pathogen remain poorly understood. According to recent studies, a major oxylipin hormone produced by 13-lipoxygenases (LOX) namely jasmonic acid (JA) has been associated with maize susceptibility to GSR. However, the specific roles of numerous 9-LOX-derived oxylipins in defense against Gibberella stalk rot (GSR) remain unexplained. In this study, we have shown that disruption of a 9-LOX gene, ZmLOX5, resulted in increased susceptibility to GSR, indicating its role in defense. To understand how ZmLOX5 regulates GSR resistance, we conducted transcriptome and oxylipin profiling using a zmlox5-3 mutant and near-isogenic wild type B73, upon infection with F. graminearum. The results showed that JA biosynthetic pathway genes were highly up-regulated, whereas multiple 9-LOX pathway genes were down-regulated in the infected zmlox5-3 mutant. Furthermore, oxylipin profiling of the mutant revealed significantly higher contents of several jasmonates but relatively lower levels of 9-oxylipins in zmlox5-3 upon infection. In contrast, B73 and W438, a more resistant inbred line, displayed relatively lower levels of JAs, but a considerable increase of 9-oxylipins. These results suggest antagonistic interaction between 9-oxylipins and JAs, wherein 9-oxylipins contribute to resistance while JAs facilitate susceptibility to F. graminearum.https://www.frontiersin.org/articles/10.3389/fpls.2021.699146/full9-oxylipinslipoxygenaseketolstranscriptomeFusarium graminearum
spellingShingle Qing Wang
Qing Wang
Qing Wang
Yali Sun
Yali Sun
Yali Sun
Fang Wang
Fang Wang
Fang Wang
Pei-Cheng Huang
Yinying Wang
Yinying Wang
Yinying Wang
Xinsen Ruan
Xinsen Ruan
Xinsen Ruan
Liang Ma
Liang Ma
Liang Ma
Xin Li
Xin Li
Xin Li
Michael V. Kolomiets
Xiquan Gao
Xiquan Gao
Xiquan Gao
Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot
Frontiers in Plant Science
9-oxylipins
lipoxygenase
ketols
transcriptome
Fusarium graminearum
title Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot
title_full Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot
title_fullStr Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot
title_full_unstemmed Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot
title_short Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot
title_sort transcriptome and oxylipin profiling joint analysis reveals opposite roles of 9 oxylipins and jasmonic acid in maize resistance to gibberella stalk rot
topic 9-oxylipins
lipoxygenase
ketols
transcriptome
Fusarium graminearum
url https://www.frontiersin.org/articles/10.3389/fpls.2021.699146/full
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