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Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance
BACKGROUND: Sorghum grain mold is the most important disease of the crop. The disease results from simultaneous infection of the grain by multiple fungal species. Host responses to these fungi and the underlying molecular and cellular processes are poorly understood. To understand the genetic, molec...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8063297/ https://www.ncbi.nlm.nih.gov/pubmed/33888060 http://dx.doi.org/10.1186/s12864-021-07609-y |
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author | Nida, Habte Lee, Sanghun Li, Ying Mengiste, Tesfaye |
author_facet | Nida, Habte Lee, Sanghun Li, Ying Mengiste, Tesfaye |
author_sort | Nida, Habte |
collection | PubMed |
description | BACKGROUND: Sorghum grain mold is the most important disease of the crop. The disease results from simultaneous infection of the grain by multiple fungal species. Host responses to these fungi and the underlying molecular and cellular processes are poorly understood. To understand the genetic, molecular and biochemical components of grain mold resistance, transcriptome profiles of the developing grain of resistant and susceptible sorghum genotypes were studied. RESULTS: The developing kernels of grain mold resistant RTx2911 and susceptible RTx430 sorghum genotypes were inoculated with a mixture of fungal pathogens mimicking the species complexity of the disease under natural infestation. Global transcriptome changes corresponding to multiple molecular and cellular processes, and biological functions including defense, secondary metabolism, and flavonoid biosynthesis were observed with differential regulation in the two genotypes. Genes encoding pattern recognition receptors (PRRs), regulators of growth and defense homeostasis, antimicrobial peptides, pathogenesis-related proteins, zein seed storage proteins, and phytoalexins showed increased expression correlating with resistance. Notably, SbLYK5 gene encoding an orthologue of chitin PRR, defensin genes SbDFN7.1 and SbDFN7.2 exhibited higher expression in the resistant genotype. The SbDFN7.1 and SbDFN7.2 genes are tightly linked and transcribed in opposite orientation with a likely common bidirectional promoter. Interestingly, increased expression of JAZ and other transcriptional repressors were observed that suggested the tight regulation of plant defense and growth. The data suggest a pathogen inducible defense system in the developing grain of sorghum that involves the chitin PRR, MAPKs, key transcription factors, downstream components regulating immune gene expression and accumulation of defense molecules. We propose a model through which the biosynthesis of 3-deoxyanthocynidin phytoalexins, defensins, PR proteins, other antimicrobial peptides, and defense suppressing proteins are regulated by a pathogen inducible defense system in the developing grain. CONCLUSIONS: The transcriptome data from a rarely studied tissue shed light into genetic, molecular, and biochemical components of disease resistance and suggested that the developing grain shares conserved immune response mechanisms but also components uniquely enriched in the grain. Resistance was associated with increased expression of genes encoding regulatory factors, novel grain specific antimicrobial peptides including defensins and storage proteins that are potential targets for crop improvement. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07609-y. |
format | Online Article Text |
id | pubmed-8063297 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-80632972021-04-23 Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance Nida, Habte Lee, Sanghun Li, Ying Mengiste, Tesfaye BMC Genomics Research BACKGROUND: Sorghum grain mold is the most important disease of the crop. The disease results from simultaneous infection of the grain by multiple fungal species. Host responses to these fungi and the underlying molecular and cellular processes are poorly understood. To understand the genetic, molecular and biochemical components of grain mold resistance, transcriptome profiles of the developing grain of resistant and susceptible sorghum genotypes were studied. RESULTS: The developing kernels of grain mold resistant RTx2911 and susceptible RTx430 sorghum genotypes were inoculated with a mixture of fungal pathogens mimicking the species complexity of the disease under natural infestation. Global transcriptome changes corresponding to multiple molecular and cellular processes, and biological functions including defense, secondary metabolism, and flavonoid biosynthesis were observed with differential regulation in the two genotypes. Genes encoding pattern recognition receptors (PRRs), regulators of growth and defense homeostasis, antimicrobial peptides, pathogenesis-related proteins, zein seed storage proteins, and phytoalexins showed increased expression correlating with resistance. Notably, SbLYK5 gene encoding an orthologue of chitin PRR, defensin genes SbDFN7.1 and SbDFN7.2 exhibited higher expression in the resistant genotype. The SbDFN7.1 and SbDFN7.2 genes are tightly linked and transcribed in opposite orientation with a likely common bidirectional promoter. Interestingly, increased expression of JAZ and other transcriptional repressors were observed that suggested the tight regulation of plant defense and growth. The data suggest a pathogen inducible defense system in the developing grain of sorghum that involves the chitin PRR, MAPKs, key transcription factors, downstream components regulating immune gene expression and accumulation of defense molecules. We propose a model through which the biosynthesis of 3-deoxyanthocynidin phytoalexins, defensins, PR proteins, other antimicrobial peptides, and defense suppressing proteins are regulated by a pathogen inducible defense system in the developing grain. CONCLUSIONS: The transcriptome data from a rarely studied tissue shed light into genetic, molecular, and biochemical components of disease resistance and suggested that the developing grain shares conserved immune response mechanisms but also components uniquely enriched in the grain. Resistance was associated with increased expression of genes encoding regulatory factors, novel grain specific antimicrobial peptides including defensins and storage proteins that are potential targets for crop improvement. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07609-y. BioMed Central 2021-04-22 /pmc/articles/PMC8063297/ /pubmed/33888060 http://dx.doi.org/10.1186/s12864-021-07609-y Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Nida, Habte Lee, Sanghun Li, Ying Mengiste, Tesfaye Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance |
title | Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance |
title_full | Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance |
title_fullStr | Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance |
title_full_unstemmed | Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance |
title_short | Transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance |
title_sort | transcriptome analysis of early stages of sorghum grain mold disease reveals defense regulators and metabolic pathways associated with resistance |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8063297/ https://www.ncbi.nlm.nih.gov/pubmed/33888060 http://dx.doi.org/10.1186/s12864-021-07609-y |
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