Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates

ABSTRACT Most fungal genomes are poorly annotated, and many fungal traits of industrial and biomedical relevance are not well suited to classical genetic screens. Assigning genes to phenotypes on a genomic scale thus remains an urgent need in the field. We developed an approach to infer gene functio...

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Autores principales:	Christopher E. Ellison, David Kowbel, N. Louise Glass, John W. Taylor, Rachel B. Brem
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/41257da3b1c34ed4ae037eb2adfe43e9
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spelling	oai:doaj.org-article:41257da3b1c34ed4ae037eb2adfe43e92021-11-15T15:45:12ZDiscovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates10.1128/mBio.01046-132150-7511https://doaj.org/article/41257da3b1c34ed4ae037eb2adfe43e92014-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01046-13https://doaj.org/toc/2150-7511ABSTRACT Most fungal genomes are poorly annotated, and many fungal traits of industrial and biomedical relevance are not well suited to classical genetic screens. Assigning genes to phenotypes on a genomic scale thus remains an urgent need in the field. We developed an approach to infer gene function from expression profiles of wild fungal isolates, and we applied our strategy to the filamentous fungus Neurospora crassa. Using transcriptome measurements in 70 strains from two well-defined clades of this microbe, we first identified 2,247 cases in which the expression of an unannotated gene rose and fell across N. crassa strains in parallel with the expression of well-characterized genes. We then used image analysis of hyphal morphologies, quantitative growth assays, and expression profiling to test the functions of four genes predicted from our population analyses. The results revealed two factors that influenced regulation of metabolism of nonpreferred carbon and nitrogen sources, a gene that governed hyphal architecture, and a gene that mediated amino acid starvation resistance. These findings validate the power of our population-transcriptomic approach for inference of novel gene function, and we suggest that this strategy will be of broad utility for genome-scale annotation in many fungal systems. IMPORTANCE Some fungal species cause deadly infections in humans or crop plants, and other fungi are workhorses of industrial chemistry, including the production of biofuels. Advances in medical and industrial mycology require an understanding of the genes that control fungal traits. We developed a method to infer functions of uncharacterized genes by observing correlated expression of their mRNAs with those of known genes across wild fungal isolates. We applied this strategy to a filamentous fungus and predicted functions for thousands of unknown genes. In four cases, we experimentally validated the predictions from our method, discovering novel genes involved in the metabolism of nutrient sources relevant for biofuel production, as well as colony morphology and starvation resistance. Our strategy is straightforward, inexpensive, and applicable for predicting gene function in many fungal species.Christopher E. EllisonDavid KowbelN. Louise GlassJohn W. TaylorRachel B. BremAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 2 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Christopher E. Ellison David Kowbel N. Louise Glass John W. Taylor Rachel B. Brem Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates
description	ABSTRACT Most fungal genomes are poorly annotated, and many fungal traits of industrial and biomedical relevance are not well suited to classical genetic screens. Assigning genes to phenotypes on a genomic scale thus remains an urgent need in the field. We developed an approach to infer gene function from expression profiles of wild fungal isolates, and we applied our strategy to the filamentous fungus Neurospora crassa. Using transcriptome measurements in 70 strains from two well-defined clades of this microbe, we first identified 2,247 cases in which the expression of an unannotated gene rose and fell across N. crassa strains in parallel with the expression of well-characterized genes. We then used image analysis of hyphal morphologies, quantitative growth assays, and expression profiling to test the functions of four genes predicted from our population analyses. The results revealed two factors that influenced regulation of metabolism of nonpreferred carbon and nitrogen sources, a gene that governed hyphal architecture, and a gene that mediated amino acid starvation resistance. These findings validate the power of our population-transcriptomic approach for inference of novel gene function, and we suggest that this strategy will be of broad utility for genome-scale annotation in many fungal systems. IMPORTANCE Some fungal species cause deadly infections in humans or crop plants, and other fungi are workhorses of industrial chemistry, including the production of biofuels. Advances in medical and industrial mycology require an understanding of the genes that control fungal traits. We developed a method to infer functions of uncharacterized genes by observing correlated expression of their mRNAs with those of known genes across wild fungal isolates. We applied this strategy to a filamentous fungus and predicted functions for thousands of unknown genes. In four cases, we experimentally validated the predictions from our method, discovering novel genes involved in the metabolism of nutrient sources relevant for biofuel production, as well as colony morphology and starvation resistance. Our strategy is straightforward, inexpensive, and applicable for predicting gene function in many fungal species.
format	article
author	Christopher E. Ellison David Kowbel N. Louise Glass John W. Taylor Rachel B. Brem
author_facet	Christopher E. Ellison David Kowbel N. Louise Glass John W. Taylor Rachel B. Brem
author_sort	Christopher E. Ellison
title	Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates
title_short	Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates
title_full	Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates
title_fullStr	Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates
title_full_unstemmed	Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates
title_sort	discovering functions of unannotated genes from a transcriptome survey of wild fungal isolates
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/41257da3b1c34ed4ae037eb2adfe43e9
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Discovering Functions of Unannotated Genes from a Transcriptome Survey of Wild Fungal Isolates

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