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Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum

Phytopathogens secrete effector proteins to manipulate their hosts for effective colonization. Hemibiotrophic fungi must maintain host viability during initial biotrophic growth and elicit host death for subsequent necrotrophic growth. To identify effectors mediating these opposing processes, we dee...

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Autores principales: Kleemann, Jochen, Rincon-Rivera, Linda J., Takahara, Hiroyuki, Neumann, Ulla, van Themaat, Emiel Ver Loren, van der Does, H. Charlotte, Hacquard, Stéphane, Stüber, Kurt, Will, Isa, Schmalenbach, Wolfgang, Schmelzer, Elmon, O'Connell, Richard J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3320591/
https://www.ncbi.nlm.nih.gov/pubmed/22496661
http://dx.doi.org/10.1371/journal.ppat.1002643
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author Kleemann, Jochen
Rincon-Rivera, Linda J.
Takahara, Hiroyuki
Neumann, Ulla
van Themaat, Emiel Ver Loren
van der Does, H. Charlotte
Hacquard, Stéphane
Stüber, Kurt
Will, Isa
Schmalenbach, Wolfgang
Schmelzer, Elmon
O'Connell, Richard J.
author_facet Kleemann, Jochen
Rincon-Rivera, Linda J.
Takahara, Hiroyuki
Neumann, Ulla
van Themaat, Emiel Ver Loren
van der Does, H. Charlotte
Hacquard, Stéphane
Stüber, Kurt
Will, Isa
Schmalenbach, Wolfgang
Schmelzer, Elmon
O'Connell, Richard J.
author_sort Kleemann, Jochen
collection PubMed
description Phytopathogens secrete effector proteins to manipulate their hosts for effective colonization. Hemibiotrophic fungi must maintain host viability during initial biotrophic growth and elicit host death for subsequent necrotrophic growth. To identify effectors mediating these opposing processes, we deeply sequenced the transcriptome of Colletotrichum higginsianum infecting Arabidopsis. Most effector genes are host-induced and expressed in consecutive waves associated with pathogenic transitions, indicating distinct effector suites are deployed at each stage. Using fluorescent protein tagging and transmission electron microscopy-immunogold labelling, we found effectors localised to stage-specific compartments at the host-pathogen interface. In particular, we show effectors are focally secreted from appressorial penetration pores before host invasion, revealing new levels of functional complexity for this fungal organ. Furthermore, we demonstrate that antagonistic effectors either induce or suppress plant cell death. Based on these results we conclude that hemibiotrophy in Colletotrichum is orchestrated through the coordinated expression of antagonistic effectors supporting either cell viability or cell death.
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spelling pubmed-33205912012-04-11 Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum Kleemann, Jochen Rincon-Rivera, Linda J. Takahara, Hiroyuki Neumann, Ulla van Themaat, Emiel Ver Loren van der Does, H. Charlotte Hacquard, Stéphane Stüber, Kurt Will, Isa Schmalenbach, Wolfgang Schmelzer, Elmon O'Connell, Richard J. PLoS Pathog Research Article Phytopathogens secrete effector proteins to manipulate their hosts for effective colonization. Hemibiotrophic fungi must maintain host viability during initial biotrophic growth and elicit host death for subsequent necrotrophic growth. To identify effectors mediating these opposing processes, we deeply sequenced the transcriptome of Colletotrichum higginsianum infecting Arabidopsis. Most effector genes are host-induced and expressed in consecutive waves associated with pathogenic transitions, indicating distinct effector suites are deployed at each stage. Using fluorescent protein tagging and transmission electron microscopy-immunogold labelling, we found effectors localised to stage-specific compartments at the host-pathogen interface. In particular, we show effectors are focally secreted from appressorial penetration pores before host invasion, revealing new levels of functional complexity for this fungal organ. Furthermore, we demonstrate that antagonistic effectors either induce or suppress plant cell death. Based on these results we conclude that hemibiotrophy in Colletotrichum is orchestrated through the coordinated expression of antagonistic effectors supporting either cell viability or cell death. Public Library of Science 2012-04-05 /pmc/articles/PMC3320591/ /pubmed/22496661 http://dx.doi.org/10.1371/journal.ppat.1002643 Text en Kleemann et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kleemann, Jochen
Rincon-Rivera, Linda J.
Takahara, Hiroyuki
Neumann, Ulla
van Themaat, Emiel Ver Loren
van der Does, H. Charlotte
Hacquard, Stéphane
Stüber, Kurt
Will, Isa
Schmalenbach, Wolfgang
Schmelzer, Elmon
O'Connell, Richard J.
Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
title Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
title_full Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
title_fullStr Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
title_full_unstemmed Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
title_short Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
title_sort sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen colletotrichum higginsianum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3320591/
https://www.ncbi.nlm.nih.gov/pubmed/22496661
http://dx.doi.org/10.1371/journal.ppat.1002643
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