Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>

ABSTRACT Botrytis cinerea is a plant-pathogenic fungus producing apothecia as sexual fruiting bodies. To study the function of mating type (MAT) genes, single-gene deletion mutants were generated in both genes of the MAT1-1 locus and both genes of the MAT1-2 locus. Deletion mutants in two MAT genes...

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Autores principales:	Sander Y. A. Rodenburg, Razak B. Terhem, Javier Veloso, Joost H. M. Stassen, Jan A. L. van Kan
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	ascospore epigenetic regulation plant disease sexual reproduction transcriptome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9fcf2c0295ef40cda994e27864a9d707
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spelling	oai:doaj.org-article:9fcf2c0295ef40cda994e27864a9d7072021-11-15T15:53:26ZFunctional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>10.1128/mBio.01939-172150-7511https://doaj.org/article/9fcf2c0295ef40cda994e27864a9d7072018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01939-17https://doaj.org/toc/2150-7511ABSTRACT Botrytis cinerea is a plant-pathogenic fungus producing apothecia as sexual fruiting bodies. To study the function of mating type (MAT) genes, single-gene deletion mutants were generated in both genes of the MAT1-1 locus and both genes of the MAT1-2 locus. Deletion mutants in two MAT genes were entirely sterile, while mutants in the other two MAT genes were able to develop stipes but never formed an apothecial disk. Little was known about the reprogramming of gene expression during apothecium development. We analyzed transcriptomes of sclerotia, three stages of apothecium development (primordia, stipes, and apothecial disks), and ascospores by RNA sequencing. Ten secondary metabolite gene clusters were upregulated at the onset of sexual development and downregulated in ascospores released from apothecia. Notably, more than 3,900 genes were differentially expressed in ascospores compared to mature apothecial disks. Among the genes that were upregulated in ascospores were numerous genes encoding virulence factors, which reveals that ascospores are transcriptionally primed for infection prior to their arrival on a host plant. Strikingly, the massive transcriptional changes at the initiation and completion of the sexual cycle often affected clusters of genes, rather than randomly dispersed genes. Thirty-five clusters of genes were jointly upregulated during the onset of sexual reproduction, while 99 clusters of genes (comprising >900 genes) were jointly downregulated in ascospores. These transcriptional changes coincided with changes in expression of genes encoding enzymes participating in chromatin organization, hinting at the occurrence of massive epigenetic regulation of gene expression during sexual reproduction. IMPORTANCE Fungal fruiting bodies are formed by sexual reproduction. We studied the development of fruiting bodies (“apothecia”) of the ubiquitous plant-pathogenic ascomycete Botrytis cinerea. The role of mating type genes in apothecium development was investigated by targeted mutation. Two genes are essential for the initiation of sexual development; mutants in these genes are sterile. Two other genes were not essential for development of stipes; however, they were essential for stipes to develop a disk and produce sexual ascospores. We examined gene expression profiles during apothecium development, as well as in ascospores sampled from apothecia. We provide the first study ever of the transcriptome of pure ascospores in a filamentous fungus. The expression of numerous genes involved in plant infection was induced in the ascospores, implying that ascospores are developmentally primed for infection before their release from apothecia.Sander Y. A. RodenburgRazak B. TerhemJavier VelosoJoost H. M. StassenJan A. L. van KanAmerican Society for Microbiologyarticleascosporeepigenetic regulationplant diseasesexual reproductiontranscriptomeMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	ascospore epigenetic regulation plant disease sexual reproduction transcriptome Microbiology QR1-502
spellingShingle	ascospore epigenetic regulation plant disease sexual reproduction transcriptome Microbiology QR1-502 Sander Y. A. Rodenburg Razak B. Terhem Javier Veloso Joost H. M. Stassen Jan A. L. van Kan Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>
description	ABSTRACT Botrytis cinerea is a plant-pathogenic fungus producing apothecia as sexual fruiting bodies. To study the function of mating type (MAT) genes, single-gene deletion mutants were generated in both genes of the MAT1-1 locus and both genes of the MAT1-2 locus. Deletion mutants in two MAT genes were entirely sterile, while mutants in the other two MAT genes were able to develop stipes but never formed an apothecial disk. Little was known about the reprogramming of gene expression during apothecium development. We analyzed transcriptomes of sclerotia, three stages of apothecium development (primordia, stipes, and apothecial disks), and ascospores by RNA sequencing. Ten secondary metabolite gene clusters were upregulated at the onset of sexual development and downregulated in ascospores released from apothecia. Notably, more than 3,900 genes were differentially expressed in ascospores compared to mature apothecial disks. Among the genes that were upregulated in ascospores were numerous genes encoding virulence factors, which reveals that ascospores are transcriptionally primed for infection prior to their arrival on a host plant. Strikingly, the massive transcriptional changes at the initiation and completion of the sexual cycle often affected clusters of genes, rather than randomly dispersed genes. Thirty-five clusters of genes were jointly upregulated during the onset of sexual reproduction, while 99 clusters of genes (comprising >900 genes) were jointly downregulated in ascospores. These transcriptional changes coincided with changes in expression of genes encoding enzymes participating in chromatin organization, hinting at the occurrence of massive epigenetic regulation of gene expression during sexual reproduction. IMPORTANCE Fungal fruiting bodies are formed by sexual reproduction. We studied the development of fruiting bodies (“apothecia”) of the ubiquitous plant-pathogenic ascomycete Botrytis cinerea. The role of mating type genes in apothecium development was investigated by targeted mutation. Two genes are essential for the initiation of sexual development; mutants in these genes are sterile. Two other genes were not essential for development of stipes; however, they were essential for stipes to develop a disk and produce sexual ascospores. We examined gene expression profiles during apothecium development, as well as in ascospores sampled from apothecia. We provide the first study ever of the transcriptome of pure ascospores in a filamentous fungus. The expression of numerous genes involved in plant infection was induced in the ascospores, implying that ascospores are developmentally primed for infection before their release from apothecia.
format	article
author	Sander Y. A. Rodenburg Razak B. Terhem Javier Veloso Joost H. M. Stassen Jan A. L. van Kan
author_facet	Sander Y. A. Rodenburg Razak B. Terhem Javier Veloso Joost H. M. Stassen Jan A. L. van Kan
author_sort	Sander Y. A. Rodenburg
title	Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>
title_short	Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>
title_full	Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>
title_fullStr	Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>
title_full_unstemmed	Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>
title_sort	functional analysis of mating type genes and transcriptome analysis during fruiting body development of <italic toggle="yes">botrytis cinerea</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/9fcf2c0295ef40cda994e27864a9d707
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Functional Analysis of Mating Type Genes and Transcriptome Analysis during Fruiting Body Development of <italic toggle="yes">Botrytis cinerea</italic>

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