Comparative genome analysis reveals an absence of leucine-rich repeat pattern-recognition receptor proteins in the kingdom Fungi

Abstract

Background: In plants and animals innate immunity is the first line of defence against attack by microbial pathogens. Specific molecular features of bacteria and fungi are recognised by pattern recognition receptors that have extracellular domains containing leucine rich repeats. Recognition of microbes by these receptors induces defence responses that protect hosts against potential microbial attack.

Methodology/principal findings: A survey of genome sequences from 101 species, representing a broad cross-section of the eukaryotic phylogenetic tree, reveals an absence of leucine rich repeat-domain containing receptors in the fungal kingdom. Uniquely, however, fungi possess adenylate cyclases that contain distinct leucine rich repeat-domains, which have been demonstrated to act as an alternative means of perceiving the presence of bacteria by at least one fungal species. Interestingly, the morphologically similar osmotrophic oomycetes, which are taxonomically distant members of the stramenopiles, possess pattern recognition receptors with similar domain structures to those found in plants.

Conclusions: The absence of pattern recognition receptors suggests that fungi may possess novel classes of pattern-recognition receptor, such as the modified adenylate cyclase, or instead rely on secretion of anti-microbial secondary metabolites for protection from microbial attack. The absence of pattern recognition receptors in fungi, coupled with their abundance in oomycetes, suggests this may be a unique characteristic of the fungal kingdom rather than a consequence of the osmotrophic growth form.

Figure 1. Phylogenetic distribution of LRR domain containing proteins.

Species tree showing the numbers of LRR-domain (L) and LRR-receptor (LR) encoding genes in the genomes of representative species from each of the taxonomic groups studied. Broad phylogenetic groups are indicated by coloured bars (A =  Amoebozoa, R = Rhodphyta, H = Haptophyte). The tree is schematic and is based on Burki et al., .

Figure 2. Domain structure and phylogeny of fungal adenylate cyclases.

A Phylogenetic tree (100 bootstraps) constructed using the adenylate cyclase domain from fungal LRR-domain containing adenylate cyclases and other closely related sequences. These sequences had been identified in a full phylogenetic tree made from adenylate cyclase domains from species in each of the taxonomic groups used in this study (Table S6). Bootstrap scores of 50 or above shown for each branch. Protein IDs (from database sources listed in Table S1) are shown for each taxon. B Domain structure of a typical fungal adenylate cyclase. Order of domains shown from N-terminus on left to C-terminus on right. The size of the boxes is not intended to indicate the size of the domains.

Figure 3. A comparison of LRR-receptors in stramenopiles.

A Species tree of stramenopiles showing the number of LRR-receptor (LR) and LRR-receptor kinase (LRK) encoding genes in each genome. Broad phylogenetic groups are indicated by coloured bars (BA  =  Brown algae). The tree is schematic and based on Burki et al., . B Phylogenetic tree showing LRR-receptor kinases in oomycetes. Bootstrap support scores of 50 or above shown for each branch. Protein IDs (from database sources listed in Table S1) are shown for each taxon.