Vacuolar proteases and autophagy in phytopathogenic fungi: A review

Autophagy (macroautophagy) is a survival and virulence mechanism of different eukaryotic pathogens. Autophagosomes sequester cytosolic material and organelles, then fuse with or enter into the vacuole or lysosome (the lytic compartment of most fungal/plant cells and many animal cells, respectively)....

Full description

Bibliographic Details
Main Authors: Margarita Juárez-Montiel, Daniel Clark-Flores, Pedro Tesillo-Moreno, Esaú de la Vega-Camarillo, Dulce Andrade-Pavón, Juan Alfredo Hernández-García, César Hernández-Rodríguez, Lourdes Villa-Tanaca
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Fungal Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/ffunb.2022.948477/full
_version_ 1811234473250914304
author Margarita Juárez-Montiel
Daniel Clark-Flores
Pedro Tesillo-Moreno
Esaú de la Vega-Camarillo
Dulce Andrade-Pavón
Juan Alfredo Hernández-García
César Hernández-Rodríguez
Lourdes Villa-Tanaca
author_facet Margarita Juárez-Montiel
Daniel Clark-Flores
Pedro Tesillo-Moreno
Esaú de la Vega-Camarillo
Dulce Andrade-Pavón
Juan Alfredo Hernández-García
César Hernández-Rodríguez
Lourdes Villa-Tanaca
author_sort Margarita Juárez-Montiel
collection DOAJ
description Autophagy (macroautophagy) is a survival and virulence mechanism of different eukaryotic pathogens. Autophagosomes sequester cytosolic material and organelles, then fuse with or enter into the vacuole or lysosome (the lytic compartment of most fungal/plant cells and many animal cells, respectively). Subsequent degradation of cargoes delivered to the vacuole via autophagy and endocytosis maintains cellular homeostasis and survival in conditions of stress, cellular differentiation, and development. PrA and PrB are vacuolar aspartyl and serine endoproteases, respectively, that participate in the autophagy of fungi and contribute to the pathogenicity of phytopathogens. Whereas the levels of vacuolar proteases are regulated by the expression of the genes encoding them (e.g., PEP4 for PrA and PRB1 for PrB), their activity is governed by endogenous inhibitors. The aim of the current contribution is to review the main characteristics, regulation, and role of vacuolar soluble endoproteases and Atg proteins in the process of autophagy and the pathogenesis of three fungal phytopathogens: Ustilago maydis, Magnaporthe oryzae, and Alternaria alternata. Aspartyl and serine proteases are known to participate in autophagy in these fungi by degrading autophagic bodies. However, the gene responsible for encoding the vacuolar serine protease of U. maydis has yet to be identified. Based on in silico analysis, this U. maydis gene is proposed to be orthologous to the Saccharomyces cerevisiae genes PRB1 and PBI2, known to encode the principal protease involved in the degradation of autophagic bodies and its inhibitor, respectively. In fungi that interact with plants, whether phytopathogenic or mycorrhizal, autophagy is a conserved cellular degradation process regulated through the TOR, PKA, and SNF1 pathways by ATG proteins and vacuolar proteases. Autophagy plays a preponderant role in the recycling of cell components as well as in the fungus-plant interaction.
first_indexed 2024-04-12T11:36:53Z
format Article
id doaj.art-ce43d956de974696be631287d32c8462
institution Directory Open Access Journal
issn 2673-6128
language English
last_indexed 2024-04-12T11:36:53Z
publishDate 2022-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Fungal Biology
spelling doaj.art-ce43d956de974696be631287d32c84622022-12-22T03:34:49ZengFrontiers Media S.A.Frontiers in Fungal Biology2673-61282022-10-01310.3389/ffunb.2022.948477948477Vacuolar proteases and autophagy in phytopathogenic fungi: A reviewMargarita Juárez-MontielDaniel Clark-FloresPedro Tesillo-MorenoEsaú de la Vega-CamarilloDulce Andrade-PavónJuan Alfredo Hernández-GarcíaCésar Hernández-RodríguezLourdes Villa-TanacaAutophagy (macroautophagy) is a survival and virulence mechanism of different eukaryotic pathogens. Autophagosomes sequester cytosolic material and organelles, then fuse with or enter into the vacuole or lysosome (the lytic compartment of most fungal/plant cells and many animal cells, respectively). Subsequent degradation of cargoes delivered to the vacuole via autophagy and endocytosis maintains cellular homeostasis and survival in conditions of stress, cellular differentiation, and development. PrA and PrB are vacuolar aspartyl and serine endoproteases, respectively, that participate in the autophagy of fungi and contribute to the pathogenicity of phytopathogens. Whereas the levels of vacuolar proteases are regulated by the expression of the genes encoding them (e.g., PEP4 for PrA and PRB1 for PrB), their activity is governed by endogenous inhibitors. The aim of the current contribution is to review the main characteristics, regulation, and role of vacuolar soluble endoproteases and Atg proteins in the process of autophagy and the pathogenesis of three fungal phytopathogens: Ustilago maydis, Magnaporthe oryzae, and Alternaria alternata. Aspartyl and serine proteases are known to participate in autophagy in these fungi by degrading autophagic bodies. However, the gene responsible for encoding the vacuolar serine protease of U. maydis has yet to be identified. Based on in silico analysis, this U. maydis gene is proposed to be orthologous to the Saccharomyces cerevisiae genes PRB1 and PBI2, known to encode the principal protease involved in the degradation of autophagic bodies and its inhibitor, respectively. In fungi that interact with plants, whether phytopathogenic or mycorrhizal, autophagy is a conserved cellular degradation process regulated through the TOR, PKA, and SNF1 pathways by ATG proteins and vacuolar proteases. Autophagy plays a preponderant role in the recycling of cell components as well as in the fungus-plant interaction.https://www.frontiersin.org/articles/10.3389/ffunb.2022.948477/fullphytopathogenic fungusautophagyATG8 and TORvacuolar proteases PrA and PrBautophagic body degradation
spellingShingle Margarita Juárez-Montiel
Daniel Clark-Flores
Pedro Tesillo-Moreno
Esaú de la Vega-Camarillo
Dulce Andrade-Pavón
Juan Alfredo Hernández-García
César Hernández-Rodríguez
Lourdes Villa-Tanaca
Vacuolar proteases and autophagy in phytopathogenic fungi: A review
Frontiers in Fungal Biology
phytopathogenic fungus
autophagy
ATG8 and TOR
vacuolar proteases PrA and PrB
autophagic body degradation
title Vacuolar proteases and autophagy in phytopathogenic fungi: A review
title_full Vacuolar proteases and autophagy in phytopathogenic fungi: A review
title_fullStr Vacuolar proteases and autophagy in phytopathogenic fungi: A review
title_full_unstemmed Vacuolar proteases and autophagy in phytopathogenic fungi: A review
title_short Vacuolar proteases and autophagy in phytopathogenic fungi: A review
title_sort vacuolar proteases and autophagy in phytopathogenic fungi a review
topic phytopathogenic fungus
autophagy
ATG8 and TOR
vacuolar proteases PrA and PrB
autophagic body degradation
url https://www.frontiersin.org/articles/10.3389/ffunb.2022.948477/full
work_keys_str_mv AT margaritajuarezmontiel vacuolarproteasesandautophagyinphytopathogenicfungiareview
AT danielclarkflores vacuolarproteasesandautophagyinphytopathogenicfungiareview
AT pedrotesillomoreno vacuolarproteasesandautophagyinphytopathogenicfungiareview
AT esaudelavegacamarillo vacuolarproteasesandautophagyinphytopathogenicfungiareview
AT dulceandradepavon vacuolarproteasesandautophagyinphytopathogenicfungiareview
AT juanalfredohernandezgarcia vacuolarproteasesandautophagyinphytopathogenicfungiareview
AT cesarhernandezrodriguez vacuolarproteasesandautophagyinphytopathogenicfungiareview
AT lourdesvillatanaca vacuolarproteasesandautophagyinphytopathogenicfungiareview