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 molybdopterin-requiring biosynthetic pathways. These mechanisms are not only relevant to plant pathogenic oomycetes but also to human pathogens within the Chromalveolata.
Highlights
For more than 150 years, attempts to culture downy mildews, powdery mildews, and rusts on artificial nutrient media have been unsuccessful
We found that A. laibachii, like Hyaloperonospora arabidopsidis and Plasmodium falciparum, lacks molybdopterin-requiring biosynthetic pathways, suggesting relaxed selection for retention of, or even selection against, this pathway
While the highly repetitive tRNAs are not resolved within the A. laibachii mitochondrial genome, regions of high synteny between the Py. ultimum and the P. infestans mitochondrial genome are found in ribosomal proteins and subunits of the NADH dehydrogenase as well as cytochrome C oxidase
Summary
For more than 150 years, attempts to culture downy mildews, powdery mildews, and rusts on artificial nutrient media have been unsuccessful. Recent research on the obligate biotroph powdery mildew fungus Blumeria graminis or downy mildew oomycete Hyaloperonospora arabidopsidis reveals a close correlation between the biotrophic life style and massive gene losses in primary and secondary metabolism [3,4]. Obligate biotrophs form an intimate haustorial interface with parasitized cells. Haustoria are differentiated intercellular hyphae, but little is known about their functionality and evolution beyond their involvement in nutrient uptake [5,6]. The obligate biotroph oomycete Albugo laibachii is a member of the Chromalveolata, which incorporates Dinophyta, Ciliophora, Heterokonts (containing the oomycetes), Haptophyta, Cryptophyta, and Apicomplexa (which includes human parasites like Plasmodium falciparum and Toxoplasma gondii [7,8])
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