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Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes

Gene expression divergence through evolutionary processes is thought to be important for achieving programmed development in multicellular organisms. To test this premise in filamentous fungi, we investigated transcriptional profiles of 3,942 single-copy orthologous genes (SCOGs) in five related sor...

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Autores principales: Kim, Wonyong, Wang, Zheng, Kim, Hyeonjae, Pham, Kasey, Tu, Yujia, Townsend, Jeffrey P., Trail, Frances
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239162/
https://www.ncbi.nlm.nih.gov/pubmed/35638737
http://dx.doi.org/10.1128/mbio.01100-22
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author Kim, Wonyong
Wang, Zheng
Kim, Hyeonjae
Pham, Kasey
Tu, Yujia
Townsend, Jeffrey P.
Trail, Frances
author_facet Kim, Wonyong
Wang, Zheng
Kim, Hyeonjae
Pham, Kasey
Tu, Yujia
Townsend, Jeffrey P.
Trail, Frances
author_sort Kim, Wonyong
collection PubMed
description Gene expression divergence through evolutionary processes is thought to be important for achieving programmed development in multicellular organisms. To test this premise in filamentous fungi, we investigated transcriptional profiles of 3,942 single-copy orthologous genes (SCOGs) in five related sordariomycete species that have morphologically diverged in the formation of their flask-shaped perithecia. We compared expression of the SCOGs to inferred gene expression levels of the most recent common ancestor of the five species, ranking genes from their largest increases to smallest increases in expression during perithecial development in each of the five species. We found that a large proportion of the genes that exhibited evolved increases in gene expression were important for normal perithecial development in Fusarium graminearum. Many of these genes were previously uncharacterized, encoding hypothetical proteins without any known functional protein domains. Interestingly, the developmental stages during which aberrant knockout phenotypes appeared largely coincided with the elevated expression of the deleted genes. In addition, we identified novel genes that affected normal perithecial development in Magnaporthe oryzae and Neurospora crassa, which were functionally and transcriptionally diverged from the orthologous counterparts in F. graminearum. Furthermore, comparative analysis of developmental transcriptomes and phylostratigraphic analysis suggested that genes encoding hypothetical proteins are generally young and transcriptionally divergent between related species. This study provides tangible evidence of shifts in gene expression that led to acquisition of novel function of orthologous genes in each lineage and demonstrates that several genes with hypothetical function are crucial for shaping multicellular fruiting bodies.
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spelling pubmed-92391622022-06-29 Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes Kim, Wonyong Wang, Zheng Kim, Hyeonjae Pham, Kasey Tu, Yujia Townsend, Jeffrey P. Trail, Frances mBio Research Article Gene expression divergence through evolutionary processes is thought to be important for achieving programmed development in multicellular organisms. To test this premise in filamentous fungi, we investigated transcriptional profiles of 3,942 single-copy orthologous genes (SCOGs) in five related sordariomycete species that have morphologically diverged in the formation of their flask-shaped perithecia. We compared expression of the SCOGs to inferred gene expression levels of the most recent common ancestor of the five species, ranking genes from their largest increases to smallest increases in expression during perithecial development in each of the five species. We found that a large proportion of the genes that exhibited evolved increases in gene expression were important for normal perithecial development in Fusarium graminearum. Many of these genes were previously uncharacterized, encoding hypothetical proteins without any known functional protein domains. Interestingly, the developmental stages during which aberrant knockout phenotypes appeared largely coincided with the elevated expression of the deleted genes. In addition, we identified novel genes that affected normal perithecial development in Magnaporthe oryzae and Neurospora crassa, which were functionally and transcriptionally diverged from the orthologous counterparts in F. graminearum. Furthermore, comparative analysis of developmental transcriptomes and phylostratigraphic analysis suggested that genes encoding hypothetical proteins are generally young and transcriptionally divergent between related species. This study provides tangible evidence of shifts in gene expression that led to acquisition of novel function of orthologous genes in each lineage and demonstrates that several genes with hypothetical function are crucial for shaping multicellular fruiting bodies. American Society for Microbiology 2022-05-31 /pmc/articles/PMC9239162/ /pubmed/35638737 http://dx.doi.org/10.1128/mbio.01100-22 Text en Copyright © 2022 Kim et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Kim, Wonyong
Wang, Zheng
Kim, Hyeonjae
Pham, Kasey
Tu, Yujia
Townsend, Jeffrey P.
Trail, Frances
Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes
title Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes
title_full Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes
title_fullStr Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes
title_full_unstemmed Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes
title_short Transcriptional Divergence Underpinning Sexual Development in the Fungal Class Sordariomycetes
title_sort transcriptional divergence underpinning sexual development in the fungal class sordariomycetes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239162/
https://www.ncbi.nlm.nih.gov/pubmed/35638737
http://dx.doi.org/10.1128/mbio.01100-22
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