The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling

ABSTRACT Fungal pathogens require the unfolded protein response (UPR) to maintain protein homeostasis of the endoplasmic reticulum (ER) during pathogenic development. In the corn smut fungus Ustilago maydis, pathogenic development is controlled by the a and b mating-type loci. The UPR is specificall...

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Autores principales:	Lara Schmitz, Melina Ayaka Schwier, Kai Heimel
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	MAP kinase phosphatases Ustilago mating type mitogen-activated protein kinases pathogenic development plant pathogens Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/63906f77c0d6401dbb46cb7c018caad8
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spelling	oai:doaj.org-article:63906f77c0d6401dbb46cb7c018caad82021-11-15T15:54:46ZThe Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling10.1128/mBio.02756-192150-7511https://doaj.org/article/63906f77c0d6401dbb46cb7c018caad82019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02756-19https://doaj.org/toc/2150-7511ABSTRACT Fungal pathogens require the unfolded protein response (UPR) to maintain protein homeostasis of the endoplasmic reticulum (ER) during pathogenic development. In the corn smut fungus Ustilago maydis, pathogenic development is controlled by the a and b mating-type loci. The UPR is specifically activated after plant penetration and required for efficient secretion of effectors and suppression of the plant defense response. The interaction between the UPR regulator Cib1 and the central developmental regulator Clp1 modulates the pathogenic program and triggers fungal colonization of the host plant. By contrast, when activated before plant penetration, the UPR interferes with fungal virulence by reducing expression of bE and bW, the central regulators of pathogenic development encoded by the b mating-type locus. Here, we show that this inhibitory effect results from UPR-mediated suppression of the pheromone response pathway upstream of the b regulatory network. UPR activity prompts dephosphorylation of the pheromone-responsive mitogen-activated protein kinase (MAPK) Kpp2, reducing activity of the pheromone response factor Prf1 that regulates expression of bE and bW. Deletion of the dual specificity phosphatase rok1 fully suppressed UPR-dependent inhibition of Kpp2 phosphorylation, formation of infectious filaments, and fungal virulence. Rok1 determines the activity of mating-type signaling pathways and thus the degree of fungal virulence. We propose that UPR-dependent regulation of Rok1 aligns ER physiology with fungal aggressiveness and effector gene expression during biotrophic growth of U. maydis in the host plant. IMPORTANCE The unfolded protein response (UPR) is crucial for endoplasmic reticulum (ER) homeostasis and disease development in fungal pathogens. In the plant-pathogenic fungus Ustilago maydis, the UPR supports fungal proliferation in planta and effector secretion for plant defense suppression. In this study, we uncovered that UPR activity, which is normally restricted to the biotrophic stage in planta, inhibits mating and the formation of infectious filaments by Rok1-dependent dephosphorylation of the pheromone responsive mitogen-activated protein kinase (MAPK) Kpp2. This observation is relevant for understanding how the fungal virulence program is regulated by cellular physiology. UPR-mediated control of mating-type signaling pathways predicts that effector gene expression and the virulence potential are controlled by ER stress levels.Lara SchmitzMelina Ayaka SchwierKai HeimelAmerican Society for MicrobiologyarticleMAP kinase phosphatasesUstilagomating typemitogen-activated protein kinasespathogenic developmentplant pathogensMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	MAP kinase phosphatases Ustilago mating type mitogen-activated protein kinases pathogenic development plant pathogens Microbiology QR1-502
spellingShingle	MAP kinase phosphatases Ustilago mating type mitogen-activated protein kinases pathogenic development plant pathogens Microbiology QR1-502 Lara Schmitz Melina Ayaka Schwier Kai Heimel The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling
description	ABSTRACT Fungal pathogens require the unfolded protein response (UPR) to maintain protein homeostasis of the endoplasmic reticulum (ER) during pathogenic development. In the corn smut fungus Ustilago maydis, pathogenic development is controlled by the a and b mating-type loci. The UPR is specifically activated after plant penetration and required for efficient secretion of effectors and suppression of the plant defense response. The interaction between the UPR regulator Cib1 and the central developmental regulator Clp1 modulates the pathogenic program and triggers fungal colonization of the host plant. By contrast, when activated before plant penetration, the UPR interferes with fungal virulence by reducing expression of bE and bW, the central regulators of pathogenic development encoded by the b mating-type locus. Here, we show that this inhibitory effect results from UPR-mediated suppression of the pheromone response pathway upstream of the b regulatory network. UPR activity prompts dephosphorylation of the pheromone-responsive mitogen-activated protein kinase (MAPK) Kpp2, reducing activity of the pheromone response factor Prf1 that regulates expression of bE and bW. Deletion of the dual specificity phosphatase rok1 fully suppressed UPR-dependent inhibition of Kpp2 phosphorylation, formation of infectious filaments, and fungal virulence. Rok1 determines the activity of mating-type signaling pathways and thus the degree of fungal virulence. We propose that UPR-dependent regulation of Rok1 aligns ER physiology with fungal aggressiveness and effector gene expression during biotrophic growth of U. maydis in the host plant. IMPORTANCE The unfolded protein response (UPR) is crucial for endoplasmic reticulum (ER) homeostasis and disease development in fungal pathogens. In the plant-pathogenic fungus Ustilago maydis, the UPR supports fungal proliferation in planta and effector secretion for plant defense suppression. In this study, we uncovered that UPR activity, which is normally restricted to the biotrophic stage in planta, inhibits mating and the formation of infectious filaments by Rok1-dependent dephosphorylation of the pheromone responsive mitogen-activated protein kinase (MAPK) Kpp2. This observation is relevant for understanding how the fungal virulence program is regulated by cellular physiology. UPR-mediated control of mating-type signaling pathways predicts that effector gene expression and the virulence potential are controlled by ER stress levels.
format	article
author	Lara Schmitz Melina Ayaka Schwier Kai Heimel
author_facet	Lara Schmitz Melina Ayaka Schwier Kai Heimel
author_sort	Lara Schmitz
title	The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling
title_short	The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling
title_full	The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling
title_fullStr	The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling
title_full_unstemmed	The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling
title_sort	unfolded protein response regulates pathogenic development of <named-content content-type="genus-species">ustilago maydis</named-content> by rok1-dependent inhibition of mating-type signaling
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/63906f77c0d6401dbb46cb7c018caad8
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The Unfolded Protein Response Regulates Pathogenic Development of <named-content content-type="genus-species">Ustilago maydis</named-content> by Rok1-Dependent Inhibition of Mating-Type Signaling

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