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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Public Library of Science (PLoS)
2011-07-01
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| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001094&type=printable |
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| 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 |
| collection | DOAJ |
| 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 |
| id | doaj-art-5ac1ce2d1f134a2f83365bcad4be6e31 |
| institution | Kabale University |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2011-07-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-5ac1ce2d1f134a2f83365bcad4be6e312025-08-20T03:46:42ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852011-07-0197e100109410.1371/journal.pbio.1001094Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana.Eric KemenAnastasia GardinerTorsten Schultz-LarsenAriane C KemenAlexi L BalmuthAlexandre Robert-SeilaniantzKate BaileyEric HolubDavid J StudholmeDan MacleanJonathan D G JonesBiotrophic 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.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001094&type=printable |
| spellingShingle | 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. PLoS Biology |
| title | 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_short | 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 |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001094&type=printable |
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