GPCR-mediated glucose sensing system regulates light-dependent fungal development and mycotoxin production

Thaila Fernanda dos Reis; Laura Mellado; Jessica M. Lohmar; Lilian Pereira Silva; Jing Jiang Zhou; Ana M. Calvo; Gustavo H. Goldman; Neil A. Brown

doi:10.1371/journal.pgen.1008419

GPCR-mediated glucose sensing system regulates light-dependent fungal development and mycotoxin production

Thaila Fernanda dos Reis, Laura Mellado, Jessica M. Lohmar, Lilian Pereira Silva, Jing Jiang Zhou, Ana M. Calvo, Gustavo H. Goldman, Neil A. Brown

Department of Life Sciences

Research output: Contribution to journal › Article › peer-review

23 Citations (SciVal)

Abstract

Microorganisms sense environmental fluctuations in nutrients and light, coordinating their growth and development accordingly. Despite their critical roles in fungi, only a few G-protein coupled receptors (GPCRs) have been characterized. The Aspergillus nidulans genome encodes 86 putative GPCRs. Here, we characterise a carbon starvation-induced GPCR-mediated glucose sensing mechanism in A. nidulans. This includes two class V (gprH and gprI) and one class VII (gprM) GPCRs, which in response to glucose promote cAMP signalling, germination and hyphal growth, while negatively regulating sexual development in a light-dependent manner. We demonstrate that GprH regulates sexual development via influencing VeA activity, a key light-dependent regulator of fungal morphogenesis and secondary metabolism. We show that GprH and GprM are light-independent negative regulators of sterigmatocystin biosynthesis. Additionally, we reveal the epistatic interactions between the three GPCRs in regulating sexual development and sterigmatocystin production. In conclusion, GprH, GprM and GprI constitute a novel carbon starvation-induced glucose sensing mechanism that functions upstream of cAMP-PKA signalling to regulate fungal development and mycotoxin production.

Original language	English
Article number	e1008419
Pages (from-to)	1-27
Number of pages	27
Journal	Plos Genetics
Volume	15
Issue number	10
DOIs	https://doi.org/10.1371/journal.pgen.1008419
Publication status	Published - 14 Oct 2019

Funding

This work was supported by the Funda??o de Amparo ? Pesquisa do Estado de S?o Paulo (FAPESP). This collaboration was founded by the BBSRC GCRF Accelerator Award [BB/GCRF-IAA/18]. The continued collaboration between Neil Brown and Gustavo Goldman was supported by a Research England QR 2018.19 funding and a University of Bath-FAPESP Sprint Award [VBBB3FNB and FAPESP 2018/22040-8]. Laura Mellado was supported by FAPESP 2015/12415-6 fellowship and a BEPE 2017/02464-5 to spend six months performing experiments in Dr Brown and Dr Zhou?s labs. Neil Brown was also supported by the BBSRC Future Leader Fellowship [BB/ N011686/1]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Dr Jae-Hyuk Yu (UW-Madison) for providing the original A. nidulans GPCR knockout strains.

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Molecular Biology
Genetics
Genetics(clinical)
Cancer Research

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1371/journal.pgen.1008419Licence: CC BY

Cite this

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title = "GPCR-mediated glucose sensing system regulates light-dependent fungal development and mycotoxin production",

abstract = "Microorganisms sense environmental fluctuations in nutrients and light, coordinating their growth and development accordingly. Despite their critical roles in fungi, only a few G-protein coupled receptors (GPCRs) have been characterized. The Aspergillus nidulans genome encodes 86 putative GPCRs. Here, we characterise a carbon starvation-induced GPCR-mediated glucose sensing mechanism in A. nidulans. This includes two class V (gprH and gprI) and one class VII (gprM) GPCRs, which in response to glucose promote cAMP signalling, germination and hyphal growth, while negatively regulating sexual development in a light-dependent manner. We demonstrate that GprH regulates sexual development via influencing VeA activity, a key light-dependent regulator of fungal morphogenesis and secondary metabolism. We show that GprH and GprM are light-independent negative regulators of sterigmatocystin biosynthesis. Additionally, we reveal the epistatic interactions between the three GPCRs in regulating sexual development and sterigmatocystin production. In conclusion, GprH, GprM and GprI constitute a novel carbon starvation-induced glucose sensing mechanism that functions upstream of cAMP-PKA signalling to regulate fungal development and mycotoxin production.",

author = "{dos Reis}, {Thaila Fernanda} and Laura Mellado and Lohmar, {Jessica M.} and Silva, {Lilian Pereira} and Zhou, {Jing Jiang} and Calvo, {Ana M.} and Goldman, {Gustavo H.} and Brown, {Neil A.}",

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AU - Goldman, Gustavo H.

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GPCR-mediated glucose sensing system regulates light-dependent fungal development and mycotoxin production

Abstract

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ASJC Scopus subject areas

UN SDGs

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Fellowship - Do G-protein coupled receptors regulate pathogenesis any mycotoxin biosynthesis in filamentous phytopathogenic fungi?

Neil Brown

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GPCR-mediated glucose sensing system regulates light-dependent fungal development and mycotoxin production

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Funding

ASJC Scopus subject areas

UN SDGs

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Fellowship - Do G-protein coupled receptors regulate pathogenesis any mycotoxin biosynthesis in filamentous phytopathogenic fungi?

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Neil Brown

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