Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.

Mushroom-forming fungi are complex multicellular organisms that form the basis of a large industry, yet, our understanding of the mechanisms of mushroom development and its responses to various stresses remains limited. The winter mushroom (Flammulina filiformis) is cultivated at a large commercial...

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Main Authors: Xiao-Bin Liu, En-Hua Xia, Meng Li, Yang-Yang Cui, Pan-Meng Wang, Jin-Xia Zhang, Bao-Gui Xie, Jian-Ping Xu, Jun-Jie Yan, Jing Li, László G Nagy, Zhu L Yang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0239890
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spelling doaj-bab29400b01e4f7eac3073e356e89fcd2021-03-03T22:18:27ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-011510e023989010.1371/journal.pone.0239890Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.Xiao-Bin LiuEn-Hua XiaMeng LiYang-Yang CuiPan-Meng WangJin-Xia ZhangBao-Gui XieJian-Ping XuJun-Jie YanJing LiLászló G NagyZhu L YangMushroom-forming fungi are complex multicellular organisms that form the basis of a large industry, yet, our understanding of the mechanisms of mushroom development and its responses to various stresses remains limited. The winter mushroom (Flammulina filiformis) is cultivated at a large commercial scale in East Asia and is a species with a preference for low temperatures. This study investigated fruiting body development in F. filiformis by comparing transcriptomes of 4 developmental stages, and compared the developmental genes to a 200-genome dataset to identify conserved genes involved in fruiting body development, and examined the response of heat sensitive and -resistant strains to heat stress. Our data revealed widely conserved genes involved in primordium development of F. filiformis, many of which originated before the emergence of the Agaricomycetes, indicating co-option for complex multicellularity during evolution. We also revealed several notable fruiting-specific genes, including the genes with conserved stipe-specific expression patterns and the others which related to sexual development, water absorption, basidium formation and sporulation, among others. Comparative analysis revealed that heat stress induced more genes in the heat resistant strain (M1) than in the heat sensitive one (XR). Of particular importance are the hsp70, hsp90 and fes1 genes, which may facilitate the adjustment to heat stress in the early stages of fruiting body development. These data highlighted novel genes involved in complex multicellular development in fungi and aid further studies on gene function and efforts to improve the productivity and heat tolerance in mushroom-forming fungi.https://doi.org/10.1371/journal.pone.0239890
collection DOAJ
language English
format Article
sources DOAJ
author Xiao-Bin Liu
En-Hua Xia
Meng Li
Yang-Yang Cui
Pan-Meng Wang
Jin-Xia Zhang
Bao-Gui Xie
Jian-Ping Xu
Jun-Jie Yan
Jing Li
László G Nagy
Zhu L Yang
spellingShingle Xiao-Bin Liu
En-Hua Xia
Meng Li
Yang-Yang Cui
Pan-Meng Wang
Jin-Xia Zhang
Bao-Gui Xie
Jian-Ping Xu
Jun-Jie Yan
Jing Li
László G Nagy
Zhu L Yang
Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.
PLoS ONE
author_facet Xiao-Bin Liu
En-Hua Xia
Meng Li
Yang-Yang Cui
Pan-Meng Wang
Jin-Xia Zhang
Bao-Gui Xie
Jian-Ping Xu
Jun-Jie Yan
Jing Li
László G Nagy
Zhu L Yang
author_sort Xiao-Bin Liu
title Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.
title_short Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.
title_full Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.
title_fullStr Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.
title_full_unstemmed Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis.
title_sort transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus flammulina filiformis.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description Mushroom-forming fungi are complex multicellular organisms that form the basis of a large industry, yet, our understanding of the mechanisms of mushroom development and its responses to various stresses remains limited. The winter mushroom (Flammulina filiformis) is cultivated at a large commercial scale in East Asia and is a species with a preference for low temperatures. This study investigated fruiting body development in F. filiformis by comparing transcriptomes of 4 developmental stages, and compared the developmental genes to a 200-genome dataset to identify conserved genes involved in fruiting body development, and examined the response of heat sensitive and -resistant strains to heat stress. Our data revealed widely conserved genes involved in primordium development of F. filiformis, many of which originated before the emergence of the Agaricomycetes, indicating co-option for complex multicellularity during evolution. We also revealed several notable fruiting-specific genes, including the genes with conserved stipe-specific expression patterns and the others which related to sexual development, water absorption, basidium formation and sporulation, among others. Comparative analysis revealed that heat stress induced more genes in the heat resistant strain (M1) than in the heat sensitive one (XR). Of particular importance are the hsp70, hsp90 and fes1 genes, which may facilitate the adjustment to heat stress in the early stages of fruiting body development. These data highlighted novel genes involved in complex multicellular development in fungi and aid further studies on gene function and efforts to improve the productivity and heat tolerance in mushroom-forming fungi.
url https://doi.org/10.1371/journal.pone.0239890
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