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

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Kemen, Eric, Gardiner, Anastasia, Schultz-Larsen, Torsten, Kemen, Ariane C., Balmuth, Alexi L., Robert-Seilaniantz, Alexandre, Bailey, Kate, Holub, E. B., Studholme, David J., MacLean, Daniel and Jones, Jonathan D.. (2011) Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biology, Vol.9 (No.7). Article No. e1001094 . ISSN 1545-7885

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Official URL: http://dx.doi.org/10.1371/journal.pbio.1001094

Abstract

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 molybdopterinrequiring biosynthetic pathways. These mechanisms are not only relevant to plant pathogenic oomycetes but also to human pathogens within the Chromalveolata.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Albuginaceae -- Genetics, Albuginaceae -- Evolution, Arabidopsis thaliana, Host-parasite relationships
Journal or Publication Title:	PLoS Biology
Publisher:	Public Library of Science
ISSN:	1545-7885
Date:	5 July 2011
Volume:	Vol.9
Number:	No.7
Page Range:	Article No. e1001094
Identification Number:	10.1371/journal.pbio.1001094
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Open Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), European Research Council (ERC), Gatsby Charitable Foundation (GCF), Deutsche Forschungsgemeinschaft (DFG), Danish Agency for Science, Technology and Innovation (DASTI)
Grant number:	233376 (ERC), KE 1509/1-1 (DFG)
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URI:	http://wrap.warwick.ac.uk/id/eprint/36783