Comparative genome analysis of plant ascomycete fungal pathogens with different lifestyles reveals distinctive virulence strategies

Abstract

Background Pathogens have evolved diverse lifestyles and adopted pivotal new roles in both natural ecosystems and human environments. However, the molecular mechanisms underlying their adaptation to new lifestyles are obscure. Comparative genomics was adopted to determine distinct strategies of plant ascomycete fungal pathogens with different lifestyles and to elucidate their distinctive virulence strategies. Results We found that plant ascomycete biotrophs exhibited lower gene gain and loss events and loss of CAZyme-encoding genes involved in plant cell wall degradation and biosynthesis gene clusters for the production of secondary metabolites in the genome. Comparison with the candidate effectome detected distinctive variations between plant biotrophic pathogens and other groups (including human, necrotrophic and hemibiotrophic pathogens). The results revealed the biotroph-specific and lifestyle-conserved candidate effector families. These data have been configured in web-based genome browser applications for public display (http://lab.malab.cn/soft/PFPG). This resource allows researchers to profile the genome, proteome, secretome and effectome of plant fungal pathogens. Conclusions Our findings demonstrated different genome evolution strategies of plant fungal pathogens with different lifestyles and explored their lifestyle-conserved and specific candidate effectors. It will provide a new basis for discovering the novel effectors and their pathogenic mechanisms.

Genome Analyses of Two Blueberry Pathogens: Diaportheamygdali CAA958 and Diaporthe eres CBS 160.32

“…Moreover, CBMs that bind to glycoside hydrolases to enhance plant cell wall degradation (e.g., L-rhamnose-binding and starch-binding) and PLs degrading glycosaminoglycans and pectin were also detected among all species analyzed. Our results corroborate previous studies in which the capacity of plant cell wall degradation is linked to fungal lifestyle (necrotrophic, hemibiotrophic, and biotrophic) [ 93 , 94 ]. For instance, some authors have documented that higher numbers of hydrolytic enzymes are most prominent in hemibiotrophs (e.g., M. oryzae , D. longicolla , N. parvum ), necrotrophs (e.g., B. cinerea ), saprobes (e.g., Paraphaeosphaeria sporulosa ), and endophytes/latent pathogens (e.g., Periconia macrospinosa ) than in biotrophs [ 21 , 78 , 93 ].…”

Applying molecular and genetic methods to trees and their fungal communities

“…Despite the of loss of genes for key cell wall decomposing enzymes, there is still a functional fine-tuned attack of selective host cell wall polymers by specific enzymes in first host tissue colonization, which is in principle common with other fungal guilds of plant colonizing species, such as endophytes, biotrophic pathogens and hemi-biotrophic species in their growth phase with living plant cells before they enter their necrotrophic phase (Anasontzis et al 2019 ; Bellincampi et al 2014 ). Genome comparisons between different types of ascomycetous plant pathogens revealed that biotrophs have a lower number of genes for plant cell wall degrading than hemi-biotrophs and necrotrophs, as one possible adaptation to living in physiologically active plant tissues (Wang et al 2022 ). Interactions with plant cell walls and plant cell wall degradation abilities of different fungal guilds are certainly the most important topic in the ecology of all kinds of tree-associated fungi.…”

“…Likely also obtained by HGT, the poplar canker pathogen Mycosphaerella populorum expresses a chaetoglobosin-like BGC during growth on poplar wood (Dhillon et al 2015 ). Wang et al ( 2022 ) reported from comparative genomics a correlation with increasing numbers of gene SM clusters from biotrophic to hemi-biotrophic and necrotrophic pathogens. Typical for many ascomycetous plant pathogens, the North-American lethal laurel wilt Raffaelea lauricola and the Eucalyptus leaf blight pathogen Calonectria pseudoreteaudii have greatly increased numbers of distinctive BGCs as compared to the non-pathogenic Raffaelea aguacate and average levels generally found in ascomycetes (Ye et al 2018 ; Zhang et al 2020 ).…”

“…Some others act as host-specific toxins which are usually expressed by necrotrophs (Lo Presti et al 2015 ; see above). Overall, pathogens mostly tend to have a higher number and more diverse candidate effector-like SSPs than symbionts, these more than saprotrophs, and biotrophic more than necrotrophic pathogens (Kim et al 2016b ; Sperschneider et al 2018 ) but, possibly depending on relationships of selected species, there are also reports with observations to the opposite (Wang et al 2022 ). A recent software update of the machine-learning classifier to EffectorP 3.0 now distinguishes between apoplastic and cytoplasmic effectors and predicts biotrophs to have higher numbers of cytoplasmic effectors (Sperschneider and Dodds 2022 ).…”

Genome-Based Analysis of Verticillium Polyketide Synthase Gene Clusters

“…Genes in clusters are not constitutively expressed, and formerly actively expressed genes can become transcriptionally inactive with repeated culturing [ 31 ]. In addition, antiSMASH (a freely available online tool to investigate the presence and diversity of secondary metabolite biosynthesis gene clusters) analyses of fungal genomes showed that ascomycete biotrophs show a lower rate of SM and CAZyme-related gene gain and loss events in the genome [ 32 ]. Taylor et al [ 33 ] predicted SM biosynthetic gene clusters in the genome of Sclerotinia sclerotiorum and analyzed their gene expression during the infection of Brassica napus and reported 80 putative SM clusters.…”