Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response

Maize is one of the major crops in the world; however, diseases caused by various pathogens seriously affect its yield and quality. The maize Rp1-D21 mutant (mt) caused by the intragenic recombination between two nucleotide-binding, leucine-rich repeat (NLR) proteins, exhibits autoactive hypersensit...

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Main Authors: Chunxia Ge, Yi-Ge Wang, Shouping Lu, Xiang Yu Zhao, Bing-Kai Hou, Peter J. Balint-Kurti, Guan-Feng Wang
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.2021.738261/full
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author Chunxia Ge
Chunxia Ge
Yi-Ge Wang
Shouping Lu
Xiang Yu Zhao
Bing-Kai Hou
Peter J. Balint-Kurti
Peter J. Balint-Kurti
Guan-Feng Wang
author_facet Chunxia Ge
Chunxia Ge
Yi-Ge Wang
Shouping Lu
Xiang Yu Zhao
Bing-Kai Hou
Peter J. Balint-Kurti
Peter J. Balint-Kurti
Guan-Feng Wang
author_sort Chunxia Ge
collection DOAJ
description Maize is one of the major crops in the world; however, diseases caused by various pathogens seriously affect its yield and quality. The maize Rp1-D21 mutant (mt) caused by the intragenic recombination between two nucleotide-binding, leucine-rich repeat (NLR) proteins, exhibits autoactive hypersensitive response (HR). In this study, we integrated transcriptomic and metabolomic analyses to identify differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) in Rp1-D21 mt compared to the wild type (WT). Genes involved in pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) were enriched among the DEGs. The salicylic acid (SA) pathway and the phenylpropanoid biosynthesis pathway were induced at both the transcriptional and metabolic levels. The DAMs identified included lipids, flavones, and phenolic acids, including 2,5-DHBA O-hexoside, the production of which is catalyzed by uridinediphosphate (UDP)-dependent glycosyltransferase (UGT). Four maize UGTs (ZmUGTs) homologous genes were among the DEGs. Functional analysis by transient co-expression in Nicotiana benthamiana showed that ZmUGT9250 and ZmUGT5174, but not ZmUGT9256 and ZmUGT8707, partially suppressed the HR triggered by Rp1-D21 or its N-terminal coiled-coil signaling domain (CCD21). None of the four ZmUGTs interacted physically with CCD21 in yeast two-hybrid or co-immunoprecipitation assays. We discuss the possibility that ZmUGTs might be involved in defense response by regulating SA homeostasis.
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spelling doaj.art-e2f203264ce24b0b89d2ea9ae60785e62022-12-21T22:16:56ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-09-011210.3389/fpls.2021.738261738261Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense ResponseChunxia Ge0Chunxia Ge1Yi-Ge Wang2Shouping Lu3Xiang Yu Zhao4Bing-Kai Hou5Peter J. Balint-Kurti6Peter J. Balint-Kurti7Guan-Feng Wang8The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, ChinaSchool of Public Health and Management, Binzhou Medical University, Yantai, ChinaThe Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, ChinaMaize Research Institute, Shandong Academy of Agricultural Sciences, Jinan, ChinaState Key Laboratory of Crop Biology, Shandong Agricultural University, Tai'an, ChinaThe Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, ChinaDepartment of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United StatesUS Department of Agriculture-Agricultural Research Service, Plant Science Research Unit, Raleigh, NC, United StatesThe Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, ChinaMaize is one of the major crops in the world; however, diseases caused by various pathogens seriously affect its yield and quality. The maize Rp1-D21 mutant (mt) caused by the intragenic recombination between two nucleotide-binding, leucine-rich repeat (NLR) proteins, exhibits autoactive hypersensitive response (HR). In this study, we integrated transcriptomic and metabolomic analyses to identify differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) in Rp1-D21 mt compared to the wild type (WT). Genes involved in pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) were enriched among the DEGs. The salicylic acid (SA) pathway and the phenylpropanoid biosynthesis pathway were induced at both the transcriptional and metabolic levels. The DAMs identified included lipids, flavones, and phenolic acids, including 2,5-DHBA O-hexoside, the production of which is catalyzed by uridinediphosphate (UDP)-dependent glycosyltransferase (UGT). Four maize UGTs (ZmUGTs) homologous genes were among the DEGs. Functional analysis by transient co-expression in Nicotiana benthamiana showed that ZmUGT9250 and ZmUGT5174, but not ZmUGT9256 and ZmUGT8707, partially suppressed the HR triggered by Rp1-D21 or its N-terminal coiled-coil signaling domain (CCD21). None of the four ZmUGTs interacted physically with CCD21 in yeast two-hybrid or co-immunoprecipitation assays. We discuss the possibility that ZmUGTs might be involved in defense response by regulating SA homeostasis.https://www.frontiersin.org/articles/10.3389/fpls.2021.738261/fulldisease resistanceETIhypersensitive responsemaizeNLRsalicylic acid
spellingShingle Chunxia Ge
Chunxia Ge
Yi-Ge Wang
Shouping Lu
Xiang Yu Zhao
Bing-Kai Hou
Peter J. Balint-Kurti
Peter J. Balint-Kurti
Guan-Feng Wang
Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response
Frontiers in Plant Science
disease resistance
ETI
hypersensitive response
maize
NLR
salicylic acid
title Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response
title_full Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response
title_fullStr Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response
title_full_unstemmed Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response
title_short Multi-Omics Analyses Reveal the Regulatory Network and the Function of ZmUGTs in Maize Defense Response
title_sort multi omics analyses reveal the regulatory network and the function of zmugts in maize defense response
topic disease resistance
ETI
hypersensitive response
maize
NLR
salicylic acid
url https://www.frontiersin.org/articles/10.3389/fpls.2021.738261/full
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