Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome

Abstract

Many oomycete and fungal plant pathogens are obligate biotrophs, which extract nutrients only from living plant tissue and cannot grow apart from their hosts. Although these pathogens cause substantial crop losses, little is known about the molecular basis or evolution of obligate biotrophy. Here, we report the genome sequence of the oomycete Hyaloperonospora arabidopsidis (Hpa), an obligate biotroph and natural pathogen of Arabidopsis thaliana. In comparison with genomes of related, hemibiotrophic Phytophthora species, the Hpa genome exhibits dramatic reductions in genes encoding (i) RXLR effectors and other secreted pathogenicity proteins, (ii) enzymes for assimilation of inorganic nitrogen and sulfur, and (iii) proteins associated with zoospore formation and motility. These attributes comprise a genomic signature of evolution toward obligate biotrophy.

Fig. 1

Diversity, evolutionary history, and functional analysis of oomycete necrosis and ethylene-inducing (Nep1)-like proteins (NLPs). (A) Phylogeny of oomycete NLPs. A consensus tree from the Bayesian Inference is shown. Thick lines indicate high support in Minimum Evolution (> 90), Maximum Likelihood (> 90) and Bayesian inference (> 0.95). Hollow lines indicate branches highly supported in at least two analyses. Branches with high support in less than two analyses are represented by thin lines. (B) An Hpa NLP ortholog does not induce necrosis in plant leaves. NLP genes were transiently expressed in Nicotiana tabacum by agroinfiltration.

Fig. 2

Synteny of conserved RXLR effectors. (A) Region around HaRxL23, spanning scaffold_9:467737- 739923 (v6) and supercontig16:325445- 40488 (v8.3.2) (B) Region around HaRxL13 and HaRxL136, spanning scaffold_150: 3503-183330 (v6) and supercontig35:456072-268293 (v8.3.2). Colored boxes show order of gene models. Non-coding DNA is not represented. Dark green, orthologs; light green, orthologs found only in Phytophthora; dark brown, syntenic paralogs; light brown, syntenic orthologs found only in Phytophthora; white, syntenic gene families; dark blue, syntenic conserved RXLR effectors; cyan, syntenic RXLR effectors conserved only in Phytophthora; yellow, RXLR effectors not syntenic or conserved; blue-gray, other genes not conserved or syntenic. Black lines join syntenic genes with the same orientation; red lines join genes with reversed orientations. Staggered black lines in (A) show scaffold joins predicted from the synteny analysis. HaRxL23, HaRxL13 and HaRxL136 have 47%, 38% and 40% amino acid identity, respectively, with their most similar Phytophthora ortholog, within the normally hypervariable C terminus.