Gene Gain and Loss during Evolution of Obligate Parasitism in the White Rust Pathogen of Arabidopsis thaliana

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.

Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics

“…Molybdoprotein biosynthesis and nutrient uptake pathways, such as thiamine biosynthesis play vital roles in lifestyle of pathogenic fungi 38 . The genes involved in these biosynthesis pathways were compared among U. virens and some obligate biotrophs, hemibiotrophs and necrotrophs to better understand evolution to biotrophy (Supplementary Note 8).…”

The wheat powdery mildew genome shows the unique evolution of an obligate biotroph

“…Most of the gene space was covered, as 96% of the eukaryotic core genes were full length, and 98% were partially present (CEGMA evaluation; Supplementary Note). In comparison to non-obligate biotrophs, many gene families involved in primary and secondary metabolism were reduced or absent as in other obligate biotrophs 7,[14][15][16] ( Supplementary Figs. 1-3 and Supplementary Note).…”

Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi

“…Given that most metabolic pathways are represented, the obligate biotrophy of AMF cannot be ascribed to massive gene loss. This view is also emerging from the study of obligate biotrophic pathogens such as the fungus Blumeria graminis [ 39] and the oomycetes Albugo laibachii and Hyaloperonospora arabodopsis [ 40]. The loss of certain pathways (i.e.…”

“…The loss of certain pathways (i.e. thiamine biosynthesis, which is also, curiously, missing in Glomus transcriptome) has been interpreted as a secondary phase, while the evolution of ways to circumvent host defences and to develop a sophisticated exchange interface with the host is considered the primary step towards obligate biotrophy [ 40]. Indeed, recurrent themes in biotrophs (and Glomus fits perfectly) include a decrease of the enzymatic arsenal against plant cell wall polymers and the presence of SSPs mainly expressed in planta, all changes that are presumably aimed to elude plant immunity.…”