Bioinformatic characterisation of genes encoding cell wall degrading enzymes in the Phytophthora parasitica genome

Abstract

BackgroundA critical aspect of plant infection by the majority of pathogens is penetration of the plant cell wall. This process requires the production and secretion of a broad spectrum of pathogen enzymes that target and degrade the many complex polysaccharides in the plant cell wall. As a necessary framework for a study of the expression of cell wall degrading enzymes (CWDEs) produced by the broad host range phytopathogen, Phytophthora parasitica, we have conducted an in-depth bioinformatics analysis of the entire complement of genes encoding CWDEs in this pathogen’s genome.ResultsOur bioinformatic analysis indicates that 431 (2%) of the 20,825 predicted proteins encoded by the P. parasitica genome, are carbohydrate-active enzymes (CAZymes) involved in the degradation of cell wall polysaccharides. Of the 431 proteins, 337 contain classical N-terminal secretion signals and 67 are predicted to be targeted to the non-classical secretion pathway. Identification of CAZyme catalytic activity based on primary protein sequence is difficult, nevertheless, detailed comparisons with previously characterized enzymes has allowed us to determine likely enzyme activities and targeted substrates for many of the P. parasitica CWDEs. Some proteins (12%) contain more than one CAZyme module but, in most cases, multiple modules are from the same CAZyme family. Only 12 P. parasitica CWDEs contain both catalytically-active (glycosyl hydrolase) and non-catalytic (carbohydrate binding) modules, a situation that contrasts with that in fungal phytopathogens. Other striking differences between the complements of CWDEs in P. parasitica and fungal phytopathogens are seen in the CAZyme families that target cellulose, pectins or β-1,3-glucans (e.g. callose). About 25% of P. parasitica CAZymes are solely directed towards pectin degradation, with the majority coming from pectin lyase or carbohydrate esterase families. Fungal phytopathogens typically contain less than half the numbers of these CAZymes. The P. parasitica genome, like that of other Oomycetes, is rich in CAZymes that target β-1,3-glucans.ConclusionsThis detailed analysis of the full complement of P. parasitica cell wall degrading enzymes provides a framework for an in-depth study of patterns of expression of these pathogen genes during plant infection and the induction or repression of expression by selected substrates.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-785) contains supplementary material, which is available to authorized users.

Phytophthora cinnamomi

“…Initial penetration and subsequent colonization of the plant are made possible by the action of a wide range of pathogen degradative enzymes that digest components of the plant cell wall. Phytophthor a genomes contain large multigene families encoding CWDEs that contain one or more Carbohydrate‐Active enZyme (CAZyme) modules (Blackman et al ., ; Götesson et al ., ; Larroque et al ., ; Ospina‐Giraldo et al ., ).…”

“…Gene‐by‐gene analysis of predicted P. cinnamomi transcripts included in the FungiDB database using dbCAN (http://csbl.bmb.uga.edu/dbCAN/) indicates that there are 438 CWDE genes in the P. cinnamomi genome (Tables ), a number similar to the 431 and 423 CWDE genes identified in P. parasitica and P. infestans , respectively, using the same approach (Blackman et al ., ) (Table S1, see Supporting Information). The 438 CWDEs in P. cinnamomi include 271 proteins containing a glycoside hydrolase (GH) module (Table ), 17 proteins containing an auxiliary activity (AA) module (Table ), 53 proteins containing a carbohydrate esterase (CE) module (Table ), 42 proteins containing a polysaccharide lyase (PL) module (Table ) and 64 proteins containing only a non‐catalytic carbohydrate‐binding module (CBM) (Table ).…”

Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses

“…In several of the CAZy families (e.g., arabinose family GH93, poorly characterized family GH89 [70]) single members are missing from one of the three BCG species. It remains to be shown however whether these differences reflect differences in the composition of the targeted cell walls and, thus, adaptations to the host.…”

Depiction of carbohydrate-active enzyme diversity in Caldicellulosiruptor sp. F32 at the genome level reveals insights into distinct polysaccharide degradation features

“…42,43 A panel of CAZymes, distributing in GHs, CEs, and PLs, is required for complete deconstruction of the complex pectin. 42,43 A panel of CAZymes, distributing in GHs, CEs, and PLs, is required for complete deconstruction of the complex pectin.…”

“…Usually, GH28 endopolygalacturonases (EC 3.2.1.15) and exopolygalacturonases (EC 3.2.1.67) can cleave a-1,4-linkages and a-1,2-linkages in pectin, respectively. 43 Starch degradation a-Amylase (1,4-a-D-glucan-4 glucanohydrolase; EC 3.2.1.1) catalyzes the hydrolysis of the a-1,4 glycosidic linkages of starch, thereby generating dextrins and oligosaccharides with low polymerization. 43 In the genome of Caldicellulosiruptor sp.…”