Cargando…

Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis

Flammulina filiformis, a typical agaric fungus, is a widely cultivated and consumed edible mushroom. Elongation of its stipe (as the main edible part) is closely related to its yield and commercial traits; however, the endogenous hormones during stipe elongation and their regulatory mechanisms are n...

Descripción completa

Detalles Bibliográficos
Autores principales: Li, Hui, Yao, Sen, Xia, Weiwei, Ma, Xinbin, Shi, Lei, Ju, Huimin, Li, Ziyan, Zhong, Yingli, Xie, Baogui, Tao, Yongxin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548271/
https://www.ncbi.nlm.nih.gov/pubmed/37799602
http://dx.doi.org/10.3389/fmicb.2023.1195709
_version_ 1785115241327099904
author Li, Hui
Yao, Sen
Xia, Weiwei
Ma, Xinbin
Shi, Lei
Ju, Huimin
Li, Ziyan
Zhong, Yingli
Xie, Baogui
Tao, Yongxin
author_facet Li, Hui
Yao, Sen
Xia, Weiwei
Ma, Xinbin
Shi, Lei
Ju, Huimin
Li, Ziyan
Zhong, Yingli
Xie, Baogui
Tao, Yongxin
author_sort Li, Hui
collection PubMed
description Flammulina filiformis, a typical agaric fungus, is a widely cultivated and consumed edible mushroom. Elongation of its stipe (as the main edible part) is closely related to its yield and commercial traits; however, the endogenous hormones during stipe elongation and their regulatory mechanisms are not well understood. Gibberellin (GA) plays an important role in the regulation of plant growth, but little has been reported in macro fungi. In this study, we first treated F. filiformis stipes in the young stage with PBZ (an inhibitor of GA) and found that PBZ significantly inhibited elongation of the stipe. Then, we performed GA-targeted metabolome and transcriptome analyses of the stipe at both the young and elongation stages. A total of 13 types of GAs were detected in F. filiformis; the contents of ten of them, namely, GA3, GA4, GA8, GA14, GA19, GA20, GA24, GA34, GA44, and GA53, were significantly decreased, and the contents of three (GA5, GA9, and GA29) were significantly increased during stipe elongation. Transcriptome analysis showed that the genes in the terpenoid backbone biosynthesis pathway showed varying expression patterns: HMGS, HMGR, GPS, and FPPS were significantly upregulated, while CPS/KS had no significant difference in transcript level during stipe elongation. In total, 37 P450 genes were annotated to be involved in GA biosynthesis; eight of them were upregulated, twelve were downregulated, and the rest were not differentially expressed. In addition, four types of differentially expressed genes involved in stipe elongation were identified, including six signal transduction genes, five cell cycle-controlling genes, twelve cell wall-related enzymes and six transcription factors. The results identified the types and content of GAs and the expression patterns of their synthesis pathways during elongation in F. filiformis and revealed the molecular mechanisms by which GAs may affect the synthesis of cell wall components and the cell cycle of the stipe through the downstream action of cell wall-related enzymes, transcription factors, signal transduction and cell cycle control, thus regulating stipe elongation. This study is helpful for understanding the roles of GAs in stipe development in mushrooms and lays the foundation for the rational regulation of stipe length in agaric mushrooms during production.
format Online
Article
Text
id pubmed-10548271
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-105482712023-10-05 Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis Li, Hui Yao, Sen Xia, Weiwei Ma, Xinbin Shi, Lei Ju, Huimin Li, Ziyan Zhong, Yingli Xie, Baogui Tao, Yongxin Front Microbiol Microbiology Flammulina filiformis, a typical agaric fungus, is a widely cultivated and consumed edible mushroom. Elongation of its stipe (as the main edible part) is closely related to its yield and commercial traits; however, the endogenous hormones during stipe elongation and their regulatory mechanisms are not well understood. Gibberellin (GA) plays an important role in the regulation of plant growth, but little has been reported in macro fungi. In this study, we first treated F. filiformis stipes in the young stage with PBZ (an inhibitor of GA) and found that PBZ significantly inhibited elongation of the stipe. Then, we performed GA-targeted metabolome and transcriptome analyses of the stipe at both the young and elongation stages. A total of 13 types of GAs were detected in F. filiformis; the contents of ten of them, namely, GA3, GA4, GA8, GA14, GA19, GA20, GA24, GA34, GA44, and GA53, were significantly decreased, and the contents of three (GA5, GA9, and GA29) were significantly increased during stipe elongation. Transcriptome analysis showed that the genes in the terpenoid backbone biosynthesis pathway showed varying expression patterns: HMGS, HMGR, GPS, and FPPS were significantly upregulated, while CPS/KS had no significant difference in transcript level during stipe elongation. In total, 37 P450 genes were annotated to be involved in GA biosynthesis; eight of them were upregulated, twelve were downregulated, and the rest were not differentially expressed. In addition, four types of differentially expressed genes involved in stipe elongation were identified, including six signal transduction genes, five cell cycle-controlling genes, twelve cell wall-related enzymes and six transcription factors. The results identified the types and content of GAs and the expression patterns of their synthesis pathways during elongation in F. filiformis and revealed the molecular mechanisms by which GAs may affect the synthesis of cell wall components and the cell cycle of the stipe through the downstream action of cell wall-related enzymes, transcription factors, signal transduction and cell cycle control, thus regulating stipe elongation. This study is helpful for understanding the roles of GAs in stipe development in mushrooms and lays the foundation for the rational regulation of stipe length in agaric mushrooms during production. Frontiers Media S.A. 2023-09-20 /pmc/articles/PMC10548271/ /pubmed/37799602 http://dx.doi.org/10.3389/fmicb.2023.1195709 Text en Copyright © 2023 Li, Yao, Xia, Ma, Shi, Ju, Li, Zhong, Xie and Tao. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Li, Hui
Yao, Sen
Xia, Weiwei
Ma, Xinbin
Shi, Lei
Ju, Huimin
Li, Ziyan
Zhong, Yingli
Xie, Baogui
Tao, Yongxin
Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis
title Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis
title_full Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis
title_fullStr Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis
title_full_unstemmed Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis
title_short Targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in Flammulina filiformis
title_sort targeted metabolome and transcriptome analyses reveal changes in gibberellin and related cell wall-acting enzyme-encoding genes during stipe elongation in flammulina filiformis
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548271/
https://www.ncbi.nlm.nih.gov/pubmed/37799602
http://dx.doi.org/10.3389/fmicb.2023.1195709
work_keys_str_mv AT lihui targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT yaosen targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT xiaweiwei targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT maxinbin targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT shilei targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT juhuimin targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT liziyan targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT zhongyingli targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT xiebaogui targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis
AT taoyongxin targetedmetabolomeandtranscriptomeanalysesrevealchangesingibberellinandrelatedcellwallactingenzymeencodinggenesduringstipeelongationinflammulinafiliformis