Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize

Abstract Background Gray leaf spot (GLS), which is caused by the necrotrophic fungi Cercospora zeae-maydis and Cercospora zeina, is one of the most impactful diseases in maize worldwide. The aim of the present study is to identify the resistance genes and understand the molecular mechanisms for GLS...

Full description

Bibliographic Details
Main Authors: Yang Yu, Jianyang Shi, Xiyang Li, Jian Liu, Qi Geng, Haichun Shi, Yongpei Ke, Qun Sun
Format: Article
Language:English
Published: BMC 2018-10-01
Series:BMC Genomics
Subjects:
MRM
Online Access:http://link.springer.com/article/10.1186/s12864-018-5072-4
id doaj-59d43e97699649f6a38885a5856a6d63
record_format Article
spelling doaj-59d43e97699649f6a38885a5856a6d632020-11-25T01:25:39ZengBMCBMC Genomics1471-21642018-10-0119111710.1186/s12864-018-5072-4Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maizeYang Yu0Jianyang Shi1Xiyang Li2Jian Liu3Qi Geng4Haichun Shi5Yongpei Ke6Qun Sun7Key Laboratory of Bio-resources and Eco-environment of the Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-resources and Eco-environment of the Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-resources and Eco-environment of the Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-resources and Eco-environment of the Ministry of Education, College of Life Sciences, Sichuan UniversityKey Laboratory of Bio-resources and Eco-environment of the Ministry of Education, College of Life Sciences, Sichuan UniversityAgronomy College, Sichuan Agriculture UniversityAgronomy College, Sichuan Agriculture UniversityKey Laboratory of Bio-resources and Eco-environment of the Ministry of Education, College of Life Sciences, Sichuan UniversityAbstract Background Gray leaf spot (GLS), which is caused by the necrotrophic fungi Cercospora zeae-maydis and Cercospora zeina, is one of the most impactful diseases in maize worldwide. The aim of the present study is to identify the resistance genes and understand the molecular mechanisms for GLS resistance. Results Two cultivars, ‘Yayu889’ and ‘Zhenghong532,’ which are distinguished as resistant and susceptible cultivars, respectively, were challenged with the GLS disease and a RNA-seq experiment was conducted on infected plants at 81, 89, 91, and 93 days post planting (dap). Compared with the beginning stage at 81 dap, 4666, 1733, and 1166 differentially expressed genes (DEGs) were identified at 89, 91, and 93 dap, respectively, in ‘Yayu889,’ while relatively fewer, i.e., 4713, 881, and 722 DEGs, were identified in ‘Zhenghong532.’ Multiple pathways involved in the response of maize to GLS, including ‘response to salicylic acid,’ ‘protein phosphorylation,’ ‘oxidation-reduction process,’ and ‘carotenoid biosynthetic process,’ were enriched by combining differential expression analysis and Weighted Gene Co-expression Network Analysis (WGCNA). The expression of 12 candidate resistance proteins in these pathways were quantified by the multiple reaction monitoring (MRM) method. This approach identified two candidate resistance proteins, a calmodulin-like protein and a leucine-rich repeat receptor-like protein kinase with SNPs that were located in QTL regions for GLS resistance. Metabolic analysis showed that, compared with ‘Zhenghong532,’ the amount of salicylic acid (SA) and total carotenoids in ‘Yayu889’ increased, while peroxidase activity decreased during the early infection stages, suggesting that increased levels of SA, carotenoids, and reactive oxygen species (ROS) may enhance the defense response of ‘Yayu889’ to GLS. Conclusion By combining transcriptome and proteome analyses with comparisons of resistance QTL regions, calmodulin-like protein and leucine-rich repeat receptor-like protein kinase were identified as candidate GLS resistance proteins. Moreover, we found that the metabolic pathways for ROS, SA, and carotenoids are especially active in the resistant cultivar. These findings could lead to a better understanding of the GLS resistance mechanisms and facilitate the breeding of GLS-resistant maize cultivars.http://link.springer.com/article/10.1186/s12864-018-5072-4Gray leaf spot (GLS)RNA-seqWGCNADisease resistanceMaizeMRM
collection DOAJ
language English
format Article
sources DOAJ
author Yang Yu
Jianyang Shi
Xiyang Li
Jian Liu
Qi Geng
Haichun Shi
Yongpei Ke
Qun Sun
spellingShingle Yang Yu
Jianyang Shi
Xiyang Li
Jian Liu
Qi Geng
Haichun Shi
Yongpei Ke
Qun Sun
Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize
BMC Genomics
Gray leaf spot (GLS)
RNA-seq
WGCNA
Disease resistance
Maize
MRM
author_facet Yang Yu
Jianyang Shi
Xiyang Li
Jian Liu
Qi Geng
Haichun Shi
Yongpei Ke
Qun Sun
author_sort Yang Yu
title Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize
title_short Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize
title_full Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize
title_fullStr Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize
title_full_unstemmed Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize
title_sort transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2018-10-01
description Abstract Background Gray leaf spot (GLS), which is caused by the necrotrophic fungi Cercospora zeae-maydis and Cercospora zeina, is one of the most impactful diseases in maize worldwide. The aim of the present study is to identify the resistance genes and understand the molecular mechanisms for GLS resistance. Results Two cultivars, ‘Yayu889’ and ‘Zhenghong532,’ which are distinguished as resistant and susceptible cultivars, respectively, were challenged with the GLS disease and a RNA-seq experiment was conducted on infected plants at 81, 89, 91, and 93 days post planting (dap). Compared with the beginning stage at 81 dap, 4666, 1733, and 1166 differentially expressed genes (DEGs) were identified at 89, 91, and 93 dap, respectively, in ‘Yayu889,’ while relatively fewer, i.e., 4713, 881, and 722 DEGs, were identified in ‘Zhenghong532.’ Multiple pathways involved in the response of maize to GLS, including ‘response to salicylic acid,’ ‘protein phosphorylation,’ ‘oxidation-reduction process,’ and ‘carotenoid biosynthetic process,’ were enriched by combining differential expression analysis and Weighted Gene Co-expression Network Analysis (WGCNA). The expression of 12 candidate resistance proteins in these pathways were quantified by the multiple reaction monitoring (MRM) method. This approach identified two candidate resistance proteins, a calmodulin-like protein and a leucine-rich repeat receptor-like protein kinase with SNPs that were located in QTL regions for GLS resistance. Metabolic analysis showed that, compared with ‘Zhenghong532,’ the amount of salicylic acid (SA) and total carotenoids in ‘Yayu889’ increased, while peroxidase activity decreased during the early infection stages, suggesting that increased levels of SA, carotenoids, and reactive oxygen species (ROS) may enhance the defense response of ‘Yayu889’ to GLS. Conclusion By combining transcriptome and proteome analyses with comparisons of resistance QTL regions, calmodulin-like protein and leucine-rich repeat receptor-like protein kinase were identified as candidate GLS resistance proteins. Moreover, we found that the metabolic pathways for ROS, SA, and carotenoids are especially active in the resistant cultivar. These findings could lead to a better understanding of the GLS resistance mechanisms and facilitate the breeding of GLS-resistant maize cultivars.
topic Gray leaf spot (GLS)
RNA-seq
WGCNA
Disease resistance
Maize
MRM
url http://link.springer.com/article/10.1186/s12864-018-5072-4
work_keys_str_mv AT yangyu transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
AT jianyangshi transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
AT xiyangli transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
AT jianliu transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
AT qigeng transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
AT haichunshi transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
AT yongpeike transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
AT qunsun transcriptomeanalysisrevealsthemolecularmechanismsofthedefenseresponsetograyleafspotdiseaseinmaize
_version_ 1725112803243589632