Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea

Abstract

BackgroundHydrophobins are proteins containing eight conserved cysteine residues that occur uniquely in mycelial fungi. Their main function is to confer hydrophobicity to fungal surfaces in contact with air or during attachment of hyphae to hydrophobic surfaces of hosts, symbiotic partners or themselves resulting in morphogenetic signals. Based on their hydropathy patterns and solubility characteristics, hydrophobins are divided into two classes (I and II), the latter being found only in ascomycetes.ResultsWe have investigated the mechanisms driving the evolution of the class II hydrophobins in nine species of the mycoparasitic ascomycetous genus Trichoderma/Hypocrea, using three draft sequenced genomes (H. jecorina = T. reesei, H. atroviridis = T. atroviride; H. virens = T. virens) an additional 14,000 ESTs from six other Trichoderma spp. (T. asperellum, H. lixii = T. harzianum, T. aggressivum var. europeae, T. longibrachiatum, T. cf. viride). The former three contained six, ten and nine members, respectively. Ten is the highest number found in any ascomycete so far. All the hydrophobins we examined had the conserved four beta-strands/one helix structure, which is stabilized by four disulfide bonds. In addition, a small number of these hydrophobins (HFBs)contained an extended N-terminus rich in either proline and aspartate, or glycine-asparagine. Phylogenetic analysis reveals a mosaic of terminal clades containing duplicated genes and shows only three reasonably supported clades. Calculation of the ratio of differences in synonymous vs. non-synonymous nucleotide substitutions provides evidence for strong purifying selection (KS/Ka >> 1). A genome database search for class II HFBs from other ascomycetes retrieved a much smaller number of hydrophobins (2–4) from each species, and most were from Sordariomycetes. A combined phylogeny of these sequences with those of Trichoderma showed that the Trichoderma HFBs mostly formed their own clades, whereas those of other Sordariomycetes occurred in shared clades.ConclusionOur study shows that the genus Trichoderma/Hypocrea has a proliferated arsenal of class II hydrophobins which arose by birth-and-death evolution followed by purifying selection.

Genome-wide analysis of cell wall-related genes in Tuber melanosporum

“…Interestingly, the three corresponding genes, TmelHYD1, TmelHYD2 and TmelHYD3, are all located on the same scaffold (scaffold_3). Class II hydrophobins seems to be absent in T. melanosporum, unlike other Ascomycetes (Kubicek et al 2008). All the putative T. melanosporum hydrophobin sequences had a predicted signal peptide, and a hydrophobin/HYDRO domain was recognized by means of InterProScan (not shown).…”

Variations and evolution of polyubiquitin genes from ciliates

“…Concerted evolution and birth-and-death evolution can be easily distinguished by analysis of genes from many pairs of closely related species (Nei et al 2000). The high level of the proportion of synonymous nucleotide differences per synonymous site (p S ) relative to the proportion of non-synonymous differences per non-synonymous site (p N ) between the individual members is diagnostic for birthand-death evolution (Kubicek et al 2008;Nei et al 2000;Piontkivska et al 2002). We then calculated the mean p S and p N values from intraspecific monomers using the DnaSP (Librado and Rozas 2009).…”

Interspecific variability of class II hydrophobin GEO1 in the genus Geosmithia

“…On the other hand the N-terminal regions, corresponding to the putative signal peptides, were highly hydrophobic as expected. Structure models were also obtained with Swiss Model using the HFBII protein from Trichoderma reesei (PDB ID 1R2M) as template, and showed that all the GEO1 proteins analysed had an a-helix, four antiparallel b-sheets and four loops (data not shown), coherently with the general structure of hydrophobins determined so far (de Vocht et al 1998;Hakanp€ a€ a et al 2004;Kubicek et al 2008).…”

“…This process generates groups of functionally similar paralogous proteins, offered to natural selection (Nei et al 2000;Nei & Rooney 2005;Jiang et al 2006). Such a mechanism is prominent in the evolution of fungal hydrophobins, as was found in Trichoderma (Kubicek et al 2008), Paxillus (Rajashekar et al 2007) and Phlebiopsis (Mgbeahuruike et al 2012). As we showed, the GEO1 sequences from unrelated Geosmithia species can be very similar, a finding that can be ascribed to strong purifying selection.…”