Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.

Biotrophic eukaryotic plant pathogens require a living host for their growth and form an intimate haustorial interface with parasitized cells. Evolution to biotrophy occurred independently in fungal rusts and powdery mildews, and in oomycete white rusts and downy mildews. Biotroph evolution and mole...

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Autores principales: Eric Kemen, Anastasia Gardiner, Torsten Schultz-Larsen, Ariane C Kemen, Alexi L Balmuth, Alexandre Robert-Seilaniantz, Kate Bailey, Eric Holub, David J Studholme, Dan Maclean, Jonathan D G Jones
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Publicado: Public Library of Science (PLoS) 2011
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spelling oai:doaj.org-article:5ac1ce2d1f134a2f83365bcad4be6e312021-11-18T05:36:07ZGene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.1544-91731545-788510.1371/journal.pbio.1001094https://doaj.org/article/5ac1ce2d1f134a2f83365bcad4be6e312011-07-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21750662/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Biotrophic eukaryotic plant pathogens require a living host for their growth and form an intimate haustorial interface with parasitized cells. Evolution to biotrophy occurred independently in fungal rusts and powdery mildews, and in oomycete white rusts and downy mildews. Biotroph evolution and molecular mechanisms of biotrophy are poorly understood. It has been proposed, but not shown, that obligate biotrophy results from (i) reduced selection for maintenance of biosynthetic pathways and (ii) gain of mechanisms to evade host recognition or suppress host defence. Here we use Illumina sequencing to define the genome, transcriptome, and gene models for the obligate biotroph oomycete and Arabidopsis parasite, Albugo laibachii. A. laibachii is a member of the Chromalveolata, which incorporates Heterokonts (containing the oomycetes), Apicomplexa (which includes human parasites like Plasmodium falciparum and Toxoplasma gondii), and four other taxa. From comparisons with other oomycete plant pathogens and other chromalveolates, we reveal independent loss of molybdenum-cofactor-requiring enzymes in downy mildews, white rusts, and the malaria parasite P. falciparum. Biotrophy also requires "effectors" to suppress host defence; we reveal RXLR and Crinkler effectors shared with other oomycetes, and also discover and verify a novel class of effectors, the "CHXCs", by showing effector delivery and effector functionality. Our findings suggest that evolution to progressively more intimate association between host and parasite results in reduced selection for retention of certain biosynthetic pathways, and particularly reduced selection for retention of molybdopterin-requiring biosynthetic pathways. These mechanisms are not only relevant to plant pathogenic oomycetes but also to human pathogens within the Chromalveolata.Eric KemenAnastasia GardinerTorsten Schultz-LarsenAriane C KemenAlexi L BalmuthAlexandre Robert-SeilaniantzKate BaileyEric HolubDavid J StudholmeDan MacleanJonathan D G JonesPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 9, Iss 7, p e1001094 (2011)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Eric Kemen
Anastasia Gardiner
Torsten Schultz-Larsen
Ariane C Kemen
Alexi L Balmuth
Alexandre Robert-Seilaniantz
Kate Bailey
Eric Holub
David J Studholme
Dan Maclean
Jonathan D G Jones
Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.
description Biotrophic eukaryotic plant pathogens require a living host for their growth and form an intimate haustorial interface with parasitized cells. Evolution to biotrophy occurred independently in fungal rusts and powdery mildews, and in oomycete white rusts and downy mildews. Biotroph evolution and molecular mechanisms of biotrophy are poorly understood. It has been proposed, but not shown, that obligate biotrophy results from (i) reduced selection for maintenance of biosynthetic pathways and (ii) gain of mechanisms to evade host recognition or suppress host defence. Here we use Illumina sequencing to define the genome, transcriptome, and gene models for the obligate biotroph oomycete and Arabidopsis parasite, Albugo laibachii. A. laibachii is a member of the Chromalveolata, which incorporates Heterokonts (containing the oomycetes), Apicomplexa (which includes human parasites like Plasmodium falciparum and Toxoplasma gondii), and four other taxa. From comparisons with other oomycete plant pathogens and other chromalveolates, we reveal independent loss of molybdenum-cofactor-requiring enzymes in downy mildews, white rusts, and the malaria parasite P. falciparum. Biotrophy also requires "effectors" to suppress host defence; we reveal RXLR and Crinkler effectors shared with other oomycetes, and also discover and verify a novel class of effectors, the "CHXCs", by showing effector delivery and effector functionality. Our findings suggest that evolution to progressively more intimate association between host and parasite results in reduced selection for retention of certain biosynthetic pathways, and particularly reduced selection for retention of molybdopterin-requiring biosynthetic pathways. These mechanisms are not only relevant to plant pathogenic oomycetes but also to human pathogens within the Chromalveolata.
format article
author Eric Kemen
Anastasia Gardiner
Torsten Schultz-Larsen
Ariane C Kemen
Alexi L Balmuth
Alexandre Robert-Seilaniantz
Kate Bailey
Eric Holub
David J Studholme
Dan Maclean
Jonathan D G Jones
author_facet Eric Kemen
Anastasia Gardiner
Torsten Schultz-Larsen
Ariane C Kemen
Alexi L Balmuth
Alexandre Robert-Seilaniantz
Kate Bailey
Eric Holub
David J Studholme
Dan Maclean
Jonathan D G Jones
author_sort Eric Kemen
title Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.
title_short Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.
title_full Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.
title_fullStr Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.
title_full_unstemmed Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.
title_sort gene gain and loss during evolution of obligate parasitism in the white rust pathogen of arabidopsis thaliana.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/5ac1ce2d1f134a2f83365bcad4be6e31
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