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Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif

Pathogens that infect plants and animals use a diverse arsenal of effector proteins to suppress the host immune system and promote infection. Identification of effectors in pathogen genomes is foundational to understanding mechanisms of pathogenesis, for monitoring field pathogen populations, and fo...

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Autores principales: Wood, Kelsey J., Nur, Munir, Gil, Juliana, Fletcher, Kyle, Lakeman, Kim, Gann, Dasan, Gothberg, Ayumi, Khuu, Tina, Kopetzky, Jennifer, Naqvi, Sanye, Pandya, Archana, Zhang, Chi, Maisonneuve, Brigitte, Pel, Mathieu, Michelmore, Richard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7644090/
https://www.ncbi.nlm.nih.gov/pubmed/33104763
http://dx.doi.org/10.1371/journal.ppat.1009012
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author Wood, Kelsey J.
Nur, Munir
Gil, Juliana
Fletcher, Kyle
Lakeman, Kim
Gann, Dasan
Gothberg, Ayumi
Khuu, Tina
Kopetzky, Jennifer
Naqvi, Sanye
Pandya, Archana
Zhang, Chi
Maisonneuve, Brigitte
Pel, Mathieu
Michelmore, Richard
author_facet Wood, Kelsey J.
Nur, Munir
Gil, Juliana
Fletcher, Kyle
Lakeman, Kim
Gann, Dasan
Gothberg, Ayumi
Khuu, Tina
Kopetzky, Jennifer
Naqvi, Sanye
Pandya, Archana
Zhang, Chi
Maisonneuve, Brigitte
Pel, Mathieu
Michelmore, Richard
author_sort Wood, Kelsey J.
collection PubMed
description Pathogens that infect plants and animals use a diverse arsenal of effector proteins to suppress the host immune system and promote infection. Identification of effectors in pathogen genomes is foundational to understanding mechanisms of pathogenesis, for monitoring field pathogen populations, and for breeding disease resistance. We identified candidate effectors from the lettuce downy mildew pathogen Bremia lactucae by searching the predicted proteome for the WY domain, a structural fold found in effectors that has been implicated in immune suppression as well as effector recognition by host resistance proteins. We predicted 55 WY domain containing proteins in the genome of B. lactucae and found substantial variation in both sequence and domain architecture. These candidate effectors exhibit several characteristics of pathogen effectors, including an N-terminal signal peptide, lineage specificity, and expression during infection. Unexpectedly, only a minority of B. lactucae WY effectors contain the canonical N-terminal RXLR motif, which is a conserved feature in the majority of cytoplasmic effectors reported in Phytophthora spp. Functional analysis of 21 effectors containing WY domains revealed 11 that elicited cell death on wild accessions and domesticated lettuce lines containing resistance genes, indicative of recognition of these effectors by the host immune system. Only two of the 11 recognized effectors contained the canonical RXLR motif, suggesting that there has been an evolutionary divergence in sequence motifs between genera; this has major consequences for robust effector prediction in oomycete pathogens.
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spelling pubmed-76440902020-11-16 Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif Wood, Kelsey J. Nur, Munir Gil, Juliana Fletcher, Kyle Lakeman, Kim Gann, Dasan Gothberg, Ayumi Khuu, Tina Kopetzky, Jennifer Naqvi, Sanye Pandya, Archana Zhang, Chi Maisonneuve, Brigitte Pel, Mathieu Michelmore, Richard PLoS Pathog Research Article Pathogens that infect plants and animals use a diverse arsenal of effector proteins to suppress the host immune system and promote infection. Identification of effectors in pathogen genomes is foundational to understanding mechanisms of pathogenesis, for monitoring field pathogen populations, and for breeding disease resistance. We identified candidate effectors from the lettuce downy mildew pathogen Bremia lactucae by searching the predicted proteome for the WY domain, a structural fold found in effectors that has been implicated in immune suppression as well as effector recognition by host resistance proteins. We predicted 55 WY domain containing proteins in the genome of B. lactucae and found substantial variation in both sequence and domain architecture. These candidate effectors exhibit several characteristics of pathogen effectors, including an N-terminal signal peptide, lineage specificity, and expression during infection. Unexpectedly, only a minority of B. lactucae WY effectors contain the canonical N-terminal RXLR motif, which is a conserved feature in the majority of cytoplasmic effectors reported in Phytophthora spp. Functional analysis of 21 effectors containing WY domains revealed 11 that elicited cell death on wild accessions and domesticated lettuce lines containing resistance genes, indicative of recognition of these effectors by the host immune system. Only two of the 11 recognized effectors contained the canonical RXLR motif, suggesting that there has been an evolutionary divergence in sequence motifs between genera; this has major consequences for robust effector prediction in oomycete pathogens. Public Library of Science 2020-10-26 /pmc/articles/PMC7644090/ /pubmed/33104763 http://dx.doi.org/10.1371/journal.ppat.1009012 Text en © 2020 Wood 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 (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wood, Kelsey J.
Nur, Munir
Gil, Juliana
Fletcher, Kyle
Lakeman, Kim
Gann, Dasan
Gothberg, Ayumi
Khuu, Tina
Kopetzky, Jennifer
Naqvi, Sanye
Pandya, Archana
Zhang, Chi
Maisonneuve, Brigitte
Pel, Mathieu
Michelmore, Richard
Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif
title Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif
title_full Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif
title_fullStr Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif
title_full_unstemmed Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif
title_short Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif
title_sort effector prediction and characterization in the oomycete pathogen bremia lactucae reveal host-recognized wy domain proteins that lack the canonical rxlr motif
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7644090/
https://www.ncbi.nlm.nih.gov/pubmed/33104763
http://dx.doi.org/10.1371/journal.ppat.1009012
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