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A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum

Sclerotinia sclerotiorum is a plant pathogenic fungus that causes white mold or stem rot diseases. It affects mostly dicotyledonous crops, resulting in significant economic losses worldwide. Sclerotia formation is a special feature of S. sclerotiorum, allowing its survival in soil for extended perio...

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Autores principales: Xu, Yan, Qiu, Yilan, Zhang, Yuelin, Li, Xin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264682/
https://www.ncbi.nlm.nih.gov/pubmed/37324679
http://dx.doi.org/10.3389/fpls.2023.1175552
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author Xu, Yan
Qiu, Yilan
Zhang, Yuelin
Li, Xin
author_facet Xu, Yan
Qiu, Yilan
Zhang, Yuelin
Li, Xin
author_sort Xu, Yan
collection PubMed
description Sclerotinia sclerotiorum is a plant pathogenic fungus that causes white mold or stem rot diseases. It affects mostly dicotyledonous crops, resulting in significant economic losses worldwide. Sclerotia formation is a special feature of S. sclerotiorum, allowing its survival in soil for extended periods and facilitates the spread of the pathogen. However, the detailed molecular mechanisms of how sclerotia are formed and how virulence is achieved in S. sclerotiorum are not fully understood. Here, we report the identification of a mutant that cannot form sclerotia using a forward genetics approach. Next-generation sequencing of the mutant’s whole genome revealed candidate genes. Through knockout experiments, the causal gene was found to encode a cAMP phosphodiesterase (SsPDE2). From mutant phenotypic examinations, we found that SsPDE2 plays essential roles not only in sclerotia formation, but also in the regulation of oxalic acid accumulation, infection cushion functionality and virulence. Downregulation of SsSMK1 transcripts in Sspde2 mutants revealed that these morphological defects are likely caused by cAMP-dependent inhibition of MAPK signaling. Moreover, when we introduced HIGS construct targeting SsPDE2 in Nicotiana benthamiana, largely compromised virulence was observed against S. sclerotiorum. Taken together, SsPDE2 is indispensable for key biological processes of S. sclerotiorum and can potentially serve as a HIGS target to control stem rot in the field.
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spelling pubmed-102646822023-06-15 A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum Xu, Yan Qiu, Yilan Zhang, Yuelin Li, Xin Front Plant Sci Plant Science Sclerotinia sclerotiorum is a plant pathogenic fungus that causes white mold or stem rot diseases. It affects mostly dicotyledonous crops, resulting in significant economic losses worldwide. Sclerotia formation is a special feature of S. sclerotiorum, allowing its survival in soil for extended periods and facilitates the spread of the pathogen. However, the detailed molecular mechanisms of how sclerotia are formed and how virulence is achieved in S. sclerotiorum are not fully understood. Here, we report the identification of a mutant that cannot form sclerotia using a forward genetics approach. Next-generation sequencing of the mutant’s whole genome revealed candidate genes. Through knockout experiments, the causal gene was found to encode a cAMP phosphodiesterase (SsPDE2). From mutant phenotypic examinations, we found that SsPDE2 plays essential roles not only in sclerotia formation, but also in the regulation of oxalic acid accumulation, infection cushion functionality and virulence. Downregulation of SsSMK1 transcripts in Sspde2 mutants revealed that these morphological defects are likely caused by cAMP-dependent inhibition of MAPK signaling. Moreover, when we introduced HIGS construct targeting SsPDE2 in Nicotiana benthamiana, largely compromised virulence was observed against S. sclerotiorum. Taken together, SsPDE2 is indispensable for key biological processes of S. sclerotiorum and can potentially serve as a HIGS target to control stem rot in the field. Frontiers Media S.A. 2023-05-31 /pmc/articles/PMC10264682/ /pubmed/37324679 http://dx.doi.org/10.3389/fpls.2023.1175552 Text en Copyright © 2023 Xu, Qiu, Zhang and Li 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 Plant Science
Xu, Yan
Qiu, Yilan
Zhang, Yuelin
Li, Xin
A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum
title A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum
title_full A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum
title_fullStr A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum
title_full_unstemmed A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum
title_short A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum
title_sort camp phosphodiesterase is essential for sclerotia formation and virulence in sclerotinia sclerotiorum
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10264682/
https://www.ncbi.nlm.nih.gov/pubmed/37324679
http://dx.doi.org/10.3389/fpls.2023.1175552
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