Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>

ABSTRACT Long noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. In filamentous fungi, however, little is known about the expression and roles of lncRNAs during fruiting body formation. By profiling developmental transcriptomes during the life cycle of the plant-pathog...

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Autores principales:	Wonyong Kim, Cristina Miguel-Rojas, Jie Wang, Jeffrey P. Townsend, Frances Trail
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Fusarium graminearum Xrn1 exonuclease fruiting body long noncoding RNAs perithecia sexual development Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6315c7c0635b48429ddad4a245cfa37c
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spelling	oai:doaj.org-article:6315c7c0635b48429ddad4a245cfa37c2021-11-15T16:00:14ZDevelopmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>10.1128/mBio.01292-182150-7511https://doaj.org/article/6315c7c0635b48429ddad4a245cfa37c2018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01292-18https://doaj.org/toc/2150-7511ABSTRACT Long noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. In filamentous fungi, however, little is known about the expression and roles of lncRNAs during fruiting body formation. By profiling developmental transcriptomes during the life cycle of the plant-pathogenic fungus Fusarium graminearum, we identified 547 lncRNAs whose expression was highly dynamic, with about 40% peaking at the meiotic stage. Many lncRNAs were found to be antisense to mRNAs, forming 300 sense-antisense pairs. Although small RNAs were produced from these overlapping loci, antisense lncRNAs appeared not to be involved in gene silencing pathways. Genome-wide analysis of small RNA clusters identified many silenced loci at the meiotic stage. However, we found transcriptionally active small RNA clusters, many of which were associated with lncRNAs. Also, we observed that many antisense lncRNAs and their respective sense transcripts were induced in parallel as the fruiting bodies matured. The nonsense-mediated decay (NMD) pathway is known to determine the fates of lncRNAs as well as mRNAs. Thus, we analyzed mutants defective in NMD and identified a subset of lncRNAs that were induced during sexual development but suppressed by NMD during vegetative growth. These results highlight the developmental stage-specific nature and functional potential of lncRNA expression in shaping the fungal fruiting bodies and provide fundamental resources for studying sexual stage-induced lncRNAs. IMPORTANCE Fusarium graminearum is the causal agent of the head blight on our major staple crops, wheat and corn. The fruiting body formation on the host plants is indispensable for the disease cycle and epidemics. Long noncoding RNA (lncRNA) molecules are emerging as key regulatory components for sexual development in animals and plants. To date, however, there is a paucity of information on the roles of lncRNAs in fungal fruiting body formation. Here we characterized hundreds of lncRNAs that exhibited developmental stage-specific expression patterns during fruiting body formation. Also, we discovered that many lncRNAs were induced in parallel with their overlapping transcripts on the opposite DNA strand during sexual development. Finally, we found a subset of lncRNAs that were regulated by an RNA surveillance system during vegetative growth. This research provides fundamental genomic resources that will spur further investigations on lncRNAs that may play important roles in shaping fungal fruiting bodies.Wonyong KimCristina Miguel-RojasJie WangJeffrey P. TownsendFrances TrailAmerican Society for MicrobiologyarticleFusarium graminearumXrn1 exonucleasefruiting bodylong noncoding RNAsperitheciasexual developmentMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Fusarium graminearum Xrn1 exonuclease fruiting body long noncoding RNAs perithecia sexual development Microbiology QR1-502
spellingShingle	Fusarium graminearum Xrn1 exonuclease fruiting body long noncoding RNAs perithecia sexual development Microbiology QR1-502 Wonyong Kim Cristina Miguel-Rojas Jie Wang Jeffrey P. Townsend Frances Trail Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>
description	ABSTRACT Long noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. In filamentous fungi, however, little is known about the expression and roles of lncRNAs during fruiting body formation. By profiling developmental transcriptomes during the life cycle of the plant-pathogenic fungus Fusarium graminearum, we identified 547 lncRNAs whose expression was highly dynamic, with about 40% peaking at the meiotic stage. Many lncRNAs were found to be antisense to mRNAs, forming 300 sense-antisense pairs. Although small RNAs were produced from these overlapping loci, antisense lncRNAs appeared not to be involved in gene silencing pathways. Genome-wide analysis of small RNA clusters identified many silenced loci at the meiotic stage. However, we found transcriptionally active small RNA clusters, many of which were associated with lncRNAs. Also, we observed that many antisense lncRNAs and their respective sense transcripts were induced in parallel as the fruiting bodies matured. The nonsense-mediated decay (NMD) pathway is known to determine the fates of lncRNAs as well as mRNAs. Thus, we analyzed mutants defective in NMD and identified a subset of lncRNAs that were induced during sexual development but suppressed by NMD during vegetative growth. These results highlight the developmental stage-specific nature and functional potential of lncRNA expression in shaping the fungal fruiting bodies and provide fundamental resources for studying sexual stage-induced lncRNAs. IMPORTANCE Fusarium graminearum is the causal agent of the head blight on our major staple crops, wheat and corn. The fruiting body formation on the host plants is indispensable for the disease cycle and epidemics. Long noncoding RNA (lncRNA) molecules are emerging as key regulatory components for sexual development in animals and plants. To date, however, there is a paucity of information on the roles of lncRNAs in fungal fruiting body formation. Here we characterized hundreds of lncRNAs that exhibited developmental stage-specific expression patterns during fruiting body formation. Also, we discovered that many lncRNAs were induced in parallel with their overlapping transcripts on the opposite DNA strand during sexual development. Finally, we found a subset of lncRNAs that were regulated by an RNA surveillance system during vegetative growth. This research provides fundamental genomic resources that will spur further investigations on lncRNAs that may play important roles in shaping fungal fruiting bodies.
format	article
author	Wonyong Kim Cristina Miguel-Rojas Jie Wang Jeffrey P. Townsend Frances Trail
author_facet	Wonyong Kim Cristina Miguel-Rojas Jie Wang Jeffrey P. Townsend Frances Trail
author_sort	Wonyong Kim
title	Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>
title_short	Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>
title_full	Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>
title_fullStr	Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>
title_full_unstemmed	Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>
title_sort	developmental dynamics of long noncoding rna expression during sexual fruiting body formation in <named-content content-type="genus-species">fusarium graminearum</named-content>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/6315c7c0635b48429ddad4a245cfa37c
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Developmental Dynamics of Long Noncoding RNA Expression during Sexual Fruiting Body Formation in <named-content content-type="genus-species">Fusarium graminearum</named-content>

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