Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infection

Abstract Background Diseases are the major factor affecting the quality and yield of sugarcane during its growth and development. However, our knowledge about the factors regulating disease responses remain limited. The present study focuses on identifying genes regulating transcriptional mechanisms...

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Main Authors: Yaying Ma, Hongying Yu, Yijing Lu, Sanji Gao, Mahpara Fatima, Ray Ming, Jingjing Yue
Format: Article
Language:English
Published: BMC 2023-01-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04073-6
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author Yaying Ma
Hongying Yu
Yijing Lu
Sanji Gao
Mahpara Fatima
Ray Ming
Jingjing Yue
author_facet Yaying Ma
Hongying Yu
Yijing Lu
Sanji Gao
Mahpara Fatima
Ray Ming
Jingjing Yue
author_sort Yaying Ma
collection DOAJ
description Abstract Background Diseases are the major factor affecting the quality and yield of sugarcane during its growth and development. However, our knowledge about the factors regulating disease responses remain limited. The present study focuses on identifying genes regulating transcriptional mechanisms responsible for resistance to leaf scald caused by Xanthomonas albilineans in S. spontaneum and S. officinarum. Results After inoculation of the two sugarcane varieties SES208 (S. spontaneum) and LA Purple (S. officinarum) with Xanthomonas albilineans, SES208 exhibited significantly greater resistance to leaf scald caused by X. albilineans than did LA Purple. Using transcriptome analysis, we identified a total of 4323 and 1755 differentially expressed genes (DEGs) in inoculated samples of SES208 and LA Purple, respectively. Significantly, 262 DEGs were specifically identified in SES208 that were enriched for KEGG pathway terms such as plant-pathogen interaction, MAPK signaling pathway, and plant hormone signal transduction. Furthermore, we built a transcriptional regulatory co-expression network that specifically identified 16 and 25 hub genes in SES208 that were enriched for putative functions in plant-pathogen interactions, MAPK signaling, and plant hormone signal transduction. All of these essential genes might be significantly involved in resistance-regulating responses in SES208 after X. albilineans inoculation. In addition, we found allele-specific expression in SES208 that was associated with the resistance phenotype of SES208 when infected by X. albilineans. After infection with X. albilineans, a great number of DEGs associated with the KEGG pathways ‘phenylpropanoid biosynthesis’ and ‘flavonoid biosynthesis’ exhibited significant expression changes in SES208 compared to LA Purple that might contribute to superior leaf scald resistance in SES208. Conclusions We provided the first systematical transcriptome map that the higher resistance of SES208 is associated with and elicited by the rapid activation of multiple clusters of defense response genes after infection by X. albilineans and not merely due to changes in the expression of genes generically associated with stress resistance. These results will serve as the foundation for further understanding of the molecular mechanisms of resistance against X. albilineans in S. spontaneum.
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spelling doaj.art-d088c8ea12be42b4b77809e1dfbb525e2023-01-29T12:08:11ZengBMCBMC Plant Biology1471-22292023-01-0123111910.1186/s12870-023-04073-6Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infectionYaying Ma0Hongying Yu1Yijing Lu2Sanji Gao3Mahpara Fatima4Ray Ming5Jingjing Yue6Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry UniversityShenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesCenter for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry UniversityNational Engineering Research Center for Sugarcane, Fujian Agriculture and Forestry UniversityCollege of Agriculture, Fujian Agriculture and Forestry UniversityCollege of Agriculture, Fujian Agriculture and Forestry UniversityCollege of Agriculture, Fujian Agriculture and Forestry UniversityAbstract Background Diseases are the major factor affecting the quality and yield of sugarcane during its growth and development. However, our knowledge about the factors regulating disease responses remain limited. The present study focuses on identifying genes regulating transcriptional mechanisms responsible for resistance to leaf scald caused by Xanthomonas albilineans in S. spontaneum and S. officinarum. Results After inoculation of the two sugarcane varieties SES208 (S. spontaneum) and LA Purple (S. officinarum) with Xanthomonas albilineans, SES208 exhibited significantly greater resistance to leaf scald caused by X. albilineans than did LA Purple. Using transcriptome analysis, we identified a total of 4323 and 1755 differentially expressed genes (DEGs) in inoculated samples of SES208 and LA Purple, respectively. Significantly, 262 DEGs were specifically identified in SES208 that were enriched for KEGG pathway terms such as plant-pathogen interaction, MAPK signaling pathway, and plant hormone signal transduction. Furthermore, we built a transcriptional regulatory co-expression network that specifically identified 16 and 25 hub genes in SES208 that were enriched for putative functions in plant-pathogen interactions, MAPK signaling, and plant hormone signal transduction. All of these essential genes might be significantly involved in resistance-regulating responses in SES208 after X. albilineans inoculation. In addition, we found allele-specific expression in SES208 that was associated with the resistance phenotype of SES208 when infected by X. albilineans. After infection with X. albilineans, a great number of DEGs associated with the KEGG pathways ‘phenylpropanoid biosynthesis’ and ‘flavonoid biosynthesis’ exhibited significant expression changes in SES208 compared to LA Purple that might contribute to superior leaf scald resistance in SES208. Conclusions We provided the first systematical transcriptome map that the higher resistance of SES208 is associated with and elicited by the rapid activation of multiple clusters of defense response genes after infection by X. albilineans and not merely due to changes in the expression of genes generically associated with stress resistance. These results will serve as the foundation for further understanding of the molecular mechanisms of resistance against X. albilineans in S. spontaneum.https://doi.org/10.1186/s12870-023-04073-6Saccharum spp.Xanthomonas albilineansLeaf scaldRNA-SeqDisease resistance
spellingShingle Yaying Ma
Hongying Yu
Yijing Lu
Sanji Gao
Mahpara Fatima
Ray Ming
Jingjing Yue
Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infection
BMC Plant Biology
Saccharum spp.
Xanthomonas albilineans
Leaf scald
RNA-Seq
Disease resistance
title Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infection
title_full Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infection
title_fullStr Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infection
title_full_unstemmed Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infection
title_short Transcriptome analysis of sugarcane reveals rapid defense response of SES208 to Xanthomonas albilineans in early infection
title_sort transcriptome analysis of sugarcane reveals rapid defense response of ses208 to xanthomonas albilineans in early infection
topic Saccharum spp.
Xanthomonas albilineans
Leaf scald
RNA-Seq
Disease resistance
url https://doi.org/10.1186/s12870-023-04073-6
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