Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles

[EN] Phytophthora cinnamomi is a hemibiotrophic oomycete causing Phytophthora root rot in over 5,000 plant species, threatening natural ecosystems, forestry, and agriculture. Genomic studies of P. cinnamomi are limited compared to other Phytophthora spp. despite the importance of this destructive an...

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Authors: Shands, Aidan C.; Xu, Guangyuan; Belisle, Rodger J.; Seifbarghi, Shirin; Jackson, Natasha; Cano, Liliana M.; Manosalva, Patricia M.; Bombarely A
Format: Article
Publication date:2024
Country:España
Institution:Universitat Politècnica de València (UPV)
Repository:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
Language:English
OAI Identifier:oai:riunet.upv.es:10251/208042
Online Access:https://riunet.upv.es/handle/10251/208042
Access Level:Open access
Keyword:Phytophthora
Oomycete
Phytophthora root rot
Two-speed genome
Effectors
Cell wall-degrading enzymes
RXLRs
Transcriptome analyses
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author Shands, Aidan C.
author2 Xu, Guangyuan
Belisle, Rodger J.
Seifbarghi, Shirin
Jackson, Natasha
Cano, Liliana M.
Manosalva, Patricia M.
Bombarely A
author2_role author
author
author
author
author
author
author
author_browse Belisle, Rodger J.
Bombarely A
Cano, Liliana M.
Jackson, Natasha
Manosalva, Patricia M.
Seifbarghi, Shirin
Shands, Aidan C.
Xu, Guangyuan
author_facet Shands, Aidan C.
Xu, Guangyuan
Belisle, Rodger J.
Seifbarghi, Shirin
Jackson, Natasha
Cano, Liliana M.
Manosalva, Patricia M.
Bombarely A
author_role author
collection RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
description [EN] Phytophthora cinnamomi is a hemibiotrophic oomycete causing Phytophthora root rot in over 5,000 plant species, threatening natural ecosystems, forestry, and agriculture. Genomic studies of P. cinnamomi are limited compared to other Phytophthora spp. despite the importance of this destructive and highly invasive pathogen. The genome of two genetically and phenotypically distinct P. cinnamomi isolates collected from avocado orchards in California were sequenced using PacBio and Illumina sequencing. Genome sizes were estimated by flow cytometry and assembled de novo to 140-141 Mb genomes with 21,111-21,402 gene models. Genome analyses revealed that both isolates exhibited complex heterozygous genomes fitting the two-speed genome model. The more virulent isolate encodes a larger secretome and more RXLR effectors when compared to the less virulent isolate. Transcriptome analysis after P. cinnamomi infection in Arabidopsis thaliana, Nicotiana benthamiana, and Persea americana de Mill (avocado) showed that this pathogen deploys common gene repertoires in all hosts and host-specific subsets, especially among effectors. Overall, our results suggested that clonal P. cinnamomi isolates employ similar strategies as other Phytophthora spp. to increase phenotypic diversity (e.g., polyploidization, gene duplications, and a bipartite genome architecture) to cope with environmental changes. Our study also provides insights into common and host-specific P. cinnamomi infection strategies and may serve as a method for narrowing and selecting key candidate effectors for functional studies to determine their contributions to plant resistance or susceptibility.
eu_rights_str_mv openAccess
format article
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institution Universitat Politècnica de València (UPV)
instname_str Universitat Politècnica de València (UPV)
language eng
network_acronym_str ES
network_name_str España
oai_identifier_str oai:riunet.upv.es:10251/208042
publishDate 2024
publishDateSort 2024
publisher Frontiers Media SA
publisherStr Frontiers Media SA
reponame_str RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
spelling Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles Shands, Aidan C. Xu, Guangyuan Belisle, Rodger J. Seifbarghi, Shirin Jackson, Natasha Cano, Liliana M. Manosalva, Patricia M. Bombarely A Phytophthora Oomycete Phytophthora root rot Two-speed genome Effectors Cell wall-degrading enzymes RXLRs Transcriptome analyses [EN] Phytophthora cinnamomi is a hemibiotrophic oomycete causing Phytophthora root rot in over 5,000 plant species, threatening natural ecosystems, forestry, and agriculture. Genomic studies of P. cinnamomi are limited compared to other Phytophthora spp. despite the importance of this destructive and highly invasive pathogen. The genome of two genetically and phenotypically distinct P. cinnamomi isolates collected from avocado orchards in California were sequenced using PacBio and Illumina sequencing. Genome sizes were estimated by flow cytometry and assembled de novo to 140-141 Mb genomes with 21,111-21,402 gene models. Genome analyses revealed that both isolates exhibited complex heterozygous genomes fitting the two-speed genome model. The more virulent isolate encodes a larger secretome and more RXLR effectors when compared to the less virulent isolate. Transcriptome analysis after P. cinnamomi infection in Arabidopsis thaliana, Nicotiana benthamiana, and Persea americana de Mill (avocado) showed that this pathogen deploys common gene repertoires in all hosts and host-specific subsets, especially among effectors. Overall, our results suggested that clonal P. cinnamomi isolates employ similar strategies as other Phytophthora spp. to increase phenotypic diversity (e.g., polyploidization, gene duplications, and a bipartite genome architecture) to cope with environmental changes. Our study also provides insights into common and host-specific P. cinnamomi infection strategies and may serve as a method for narrowing and selecting key candidate effectors for functional studies to determine their contributions to plant resistance or susceptibility. The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was funded by the UC MEXUS-CONACYT Collaborative Grants (grant number CN-19-112), the USDA/NIFA-AFRI, Pests and Beneficial Species in Agricultural Production Systems (grant number 2020-67014-31859), the USDA-NIFA, Specialty Crop Research Initiative (grant number 2020-51181-32198), and the California Avocado Commission (grant number 65211). Frontiers Media SA https://riunet.upv.es/handle/10251/208042
spellingShingle Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles
Shands, Aidan C.
Phytophthora
Oomycete
Phytophthora root rot
Two-speed genome
Effectors
Cell wall-degrading enzymes
RXLRs
Transcriptome analyses
title Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles
title_full Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles
title_fullStr Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles
title_full_unstemmed Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles
title_short Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles
title_sort Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles
topic Phytophthora
Oomycete
Phytophthora root rot
Two-speed genome
Effectors
Cell wall-degrading enzymes
RXLRs
Transcriptome analyses
topic_facet Phytophthora
Oomycete
Phytophthora root rot
Two-speed genome
Effectors
Cell wall-degrading enzymes
RXLRs
Transcriptome analyses
url https://riunet.upv.es/handle/10251/208042