Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression

ABSTRACT The oomycete Phytophthora infestans, the causal agent of potato and tomato blight, expresses two extracellular invertases. Unlike typical fungal invertases, the P. infestans genes are not sucrose induced or glucose repressed but instead appear to be under developmental control. Transcript l...

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Autores principales:	Meenakshi S. Kagda, Domingo Martínez-Soto, Audrey M. V. Ah-Fong, Howard S. Judelson
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	metabolism nutrition oomycetes plant pathogens transcriptional regulation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/424554d64e7742fdae041c20818113bf
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spelling	oai:doaj.org-article:424554d64e7742fdae041c20818113bf2021-11-15T16:19:09ZInvertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression10.1128/mBio.01251-202150-7511https://doaj.org/article/424554d64e7742fdae041c20818113bf2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01251-20https://doaj.org/toc/2150-7511ABSTRACT The oomycete Phytophthora infestans, the causal agent of potato and tomato blight, expresses two extracellular invertases. Unlike typical fungal invertases, the P. infestans genes are not sucrose induced or glucose repressed but instead appear to be under developmental control. Transcript levels of both genes were very low in mycelia harvested from artificial medium but high in preinfection stages (sporangia, zoospores, and germinated cysts), high during biotrophic growth in leaves and tubers, and low during necrotrophy. Genome-wide analyses of metabolic enzymes and effectors indicated that this expression profile was fairly unusual, matched only by a few other enzymes, such as carbonic anhydrases and a few RXLR effectors. Genes for other metabolic enzymes were typically downregulated in the preinfection stages. Overall metabolic gene expression during the necrotrophic stage of infection clustered with artificial medium, while the biotrophic phase formed a separate cluster. Confocal microscopy of transformants expressing green fluorescent protein (GFP) fusions indicated that invertase protein resided primarily in haustoria during infection. This localization was not attributable to haustorium-specific promoter activity. Instead, the N-terminal regions of proteins containing signal peptides were sufficient to deliver proteins to haustoria. Invertase expression during leaf infection was linked to a decline in apoplastic sucrose, consistent with a role of the enzymes in plant pathogenesis. This was also suggested by the discovery that invertase genes occur across multiple orders of oomycetes but not in most animal pathogens or a mycoparasite. IMPORTANCE Oomycetes cause hundreds of diseases in economically and environmentally significant plants. How these microbes acquire host nutrients is not well understood. Many oomycetes insert specialized hyphae called haustoria into plant cells, but unlike their fungal counterparts, a role in nutrition has remained unproven. The discovery that Phytophthora invertases localize to haustoria provides the first strong evidence that these structures participate in feeding. Since regions of proteins containing signal peptides targeted proteins to the haustorium-plant interface, haustoria appear to be the primary machinery for secreting proteins during biotrophic pathogenesis. Although oomycete invertases were acquired laterally from fungi, their expression patterns have adapted to the Phytophthora lifestyle by abandoning substrate-level regulation in favor of developmental control, allowing the enzymes to be produced in anticipation of plant colonization. This study highlights how a widely distributed hydrolytic enzyme has evolved new behaviors in oomycetes.Meenakshi S. KagdaDomingo Martínez-SotoAudrey M. V. Ah-FongHoward S. JudelsonAmerican Society for Microbiologyarticlemetabolismnutritionoomycetesplant pathogenstranscriptional regulationMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	metabolism nutrition oomycetes plant pathogens transcriptional regulation Microbiology QR1-502
spellingShingle	metabolism nutrition oomycetes plant pathogens transcriptional regulation Microbiology QR1-502 Meenakshi S. Kagda Domingo Martínez-Soto Audrey M. V. Ah-Fong Howard S. Judelson Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression
description	ABSTRACT The oomycete Phytophthora infestans, the causal agent of potato and tomato blight, expresses two extracellular invertases. Unlike typical fungal invertases, the P. infestans genes are not sucrose induced or glucose repressed but instead appear to be under developmental control. Transcript levels of both genes were very low in mycelia harvested from artificial medium but high in preinfection stages (sporangia, zoospores, and germinated cysts), high during biotrophic growth in leaves and tubers, and low during necrotrophy. Genome-wide analyses of metabolic enzymes and effectors indicated that this expression profile was fairly unusual, matched only by a few other enzymes, such as carbonic anhydrases and a few RXLR effectors. Genes for other metabolic enzymes were typically downregulated in the preinfection stages. Overall metabolic gene expression during the necrotrophic stage of infection clustered with artificial medium, while the biotrophic phase formed a separate cluster. Confocal microscopy of transformants expressing green fluorescent protein (GFP) fusions indicated that invertase protein resided primarily in haustoria during infection. This localization was not attributable to haustorium-specific promoter activity. Instead, the N-terminal regions of proteins containing signal peptides were sufficient to deliver proteins to haustoria. Invertase expression during leaf infection was linked to a decline in apoplastic sucrose, consistent with a role of the enzymes in plant pathogenesis. This was also suggested by the discovery that invertase genes occur across multiple orders of oomycetes but not in most animal pathogens or a mycoparasite. IMPORTANCE Oomycetes cause hundreds of diseases in economically and environmentally significant plants. How these microbes acquire host nutrients is not well understood. Many oomycetes insert specialized hyphae called haustoria into plant cells, but unlike their fungal counterparts, a role in nutrition has remained unproven. The discovery that Phytophthora invertases localize to haustoria provides the first strong evidence that these structures participate in feeding. Since regions of proteins containing signal peptides targeted proteins to the haustorium-plant interface, haustoria appear to be the primary machinery for secreting proteins during biotrophic pathogenesis. Although oomycete invertases were acquired laterally from fungi, their expression patterns have adapted to the Phytophthora lifestyle by abandoning substrate-level regulation in favor of developmental control, allowing the enzymes to be produced in anticipation of plant colonization. This study highlights how a widely distributed hydrolytic enzyme has evolved new behaviors in oomycetes.
format	article
author	Meenakshi S. Kagda Domingo Martínez-Soto Audrey M. V. Ah-Fong Howard S. Judelson
author_facet	Meenakshi S. Kagda Domingo Martínez-Soto Audrey M. V. Ah-Fong Howard S. Judelson
author_sort	Meenakshi S. Kagda
title	Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression
title_short	Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression
title_full	Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression
title_fullStr	Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression
title_full_unstemmed	Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression
title_sort	invertases in <named-content content-type="genus-species">phytophthora infestans</named-content> localize to haustoria and are programmed for infection-specific expression
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/424554d64e7742fdae041c20818113bf
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Invertases in <named-content content-type="genus-species">Phytophthora infestans</named-content> Localize to Haustoria and Are Programmed for Infection-Specific Expression

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