Evolution of the cutinase gene family: Evidence for lateral gene transfer of a candidate Phytophthora virulence factor

Abstract

Lateral gene transfer (LGT) can facilitate the acquisition of new functions in recipient lineages, which may enable them to colonize new environments. Several recent publications have shown that gene transfer between prokaryotes and eukaryotes occurs with appreciable frequency. Here we present a study of interdomain gene transfer of cutinases -well documented virulence factors in fungi -between eukaryotic plant pathogens Phytophthora species and prokaryotic bacterial lineages. Two putative cutinase genes were cloned from Phytophthora brassicae and Northern blotting experiments showed that these genes are expressed early during the infection of the host Arabidopsis thaliana and induced during cyst germination of the pathogen. Analysis of the gene organisation of this gene family in Phytophthora ramorum and P. sojae showed three and ten copies in tight succession within a region of 5 and 25 kb, respectively, probably indicating a recent expansion in Phytophthora lineages by gene duplications. Bioinformatic analyses identified orthologues only in three genera of Actinobacteria, and in two distantly related eukaryotic groups: oomycetes and fungi. Together with phylogenetic analyses this limited distribution of the gene in the tree of life strongly support a scenario where cutinase genes originated after the origin of land plants in a microbial lineage living in proximity of plants and subsequently were transferred between distantly related plant-degrading microbes. More precisely, a cutinase gene was likely acquired by an ancestor of P. brassicae, P. sojae, P. infestans and P. ramorum, possibly from an actinobacterial source, suggesting that gene transfer might be an important mechanism in the evolution of their virulence. These findings could indeed provide an interesting model system to study acquisition of virulence factors in these important plant pathogens.

Phylogenomic Analysis Demonstrates a Pattern of Rare and Ancient Horizontal Gene Transfer between Plants and Fungi

“…Several studies of phagotrophic eukaryotes appear to be consistent with the principle of the "you are what you eat hypothesis" because several phagotrophic single-celled protozoa possess genes of recent prokaryotic ancestry Archibald et al, 2003;Eichinger et al, 2005;Loftus et al, 2005). There is, however, also some evidence for HGT involving nonphagotrophic fungi and oomycetes (Garcia-Vallve et al, 2000;Friesen et al, 2006;Richards et al, 2006a;Belbahri et al, 2008).…”

Horizontal gene transfer in osmotrophs: playing with public goods

“…A review of published reports of HGT can didates demonstrates that genes encoding secreted enzymes (28 HGT events or genes), transporters (24 HGT events or genes) and toxin biosynthesis systems (28 HGT events transferring a total of 69 genes) have all been subjected to HGT into osmotrophic eukaryotic microorganisms, such as fungi and oomycetes (see Supplementary informa tion S1-S3 (tables) and REFS 87,88). This group of 121 HGT candidates predicted to function in osmotrophic and public goods phenotypes represents more than 32% of the 370 collated HGTs into fungi 76,87,88 and oomycetes 89,96 . We therefore propose that HGT has played a part in the generation, protection and acquisition of public goods by osmotrophic eukaryotes.…”

“…Next, we collated all published examples of fungal 76,87 and oomycete 89,96 genes that were acquired by HGT and encode secreted depolymerizing enzymes (Supplementary information S1 (table)) and transporter proteins (Supplementary information S2 (table)). These lists are derived from a larger collated list of previously published and revalidated HGT studies in fungi (a total of 323 genes 76,87 ), recent studies focusing on HGT of fructose transporter genes 88 and ammonium transporter genes 87 into fungi (ten and two transfers, respectively), and individual studies of HGT into oomycetes (a further 35 genes 89,96 ), giving 370 genes in total.…”

Evolutionary analysis of glycosyl hydrolase family 28 (GH28) suggests lineage-specific expansions in necrotrophic fungal pathogens

“…This topology supports an analysis by Gotesson et al (2002) showing that GH28s from the Stramenopile Phytophthora cinnamomi are more closely related to fungal GH28s than with those from plants. Furthermore, Phytophthora species have acquired multiple gene families laterally from distantly related plantdegrading fungi (Andersson, 2006;Soanes et al, 2007;Belbahri et al, 2007;Richards and Talbot, 2007), and similar processes likely resulted in the observed distribution of the pectinase gene family. Mucoromycotina is a basal group of fungi "incertae sedis" (Hibbett et al, 2007), and GH28s from this group form a well-supported clade of unannotated GH28 homologs (Supplementary File 2).…”