Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens

Abstract

The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases.

Introgression and gene family contraction drive the evolution of lifestyle and host shifts of hypocrealean fungi

“…The utilisation of host-based nutrition is critical for fungal parasitism and includes or carbohydrate-activated enzymes (CAZymes) and as well as proteases, which are among key virulence factors involved in parasitism in various pathogenic fungi (Gao et al 2011; Klosterman et al 2011; Xiao et al 2012). The abundance and types of these enzymes should be key to the adaption to different host-based nutrition.…”

“…Most of the research on genomics in Hypocreales are mainly focused on gene function related to phylogeny, development and pathogenesis, and has revealed the sophisticated strategies associated with the adaption to various lifestyles (Klosterman et al 2011; Rouxel et al 2011). The subtilisins and chitinases, for example, have been shown to be involved in the pathogenesis of insects (Gao et al 2011).…”

“…The subtilisins and chitinases, for example, have been shown to be involved in the pathogenesis of insects (Gao et al 2011). Polysaccharide lyases (PLs) and glycoside hydrolases (GHs), enzymes involved in the breakdown of pectin and cellulose in plant cell walls play a role in the infection of plants (Klosterman et al 2011). However, the evolutionary history and potential mechanisms of lifestyle changes are not comprehensively understood at the genomic level.…”

Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics

“…67). Putative effectors in the U. virens secretomes were predicted based on the protein size (r 400 amino-acid residues) and the number of cysteine residues (Z4) 68 . The prediction of transmembrane proteins and domain calling were described in the Supplementary Methods.…”

The Vascular Pathogen Verticillium longisporum Requires a Jasmonic Acid-Independent COI1 Function in Roots to Elicit Disease Symptoms in Arabidopsis Shoots

“…Hemibiotrophic pathogens first colonize their hosts as biotrophs before killing them during the subsequent necrotrophic phase. Vascular pathogens like Fusarium oxysporum or Verticillium species, which persist during the first part of their life cycle in the xylem before causing severe tissue damage, can thus be regarded as hemibiotrophs (Thatcher et al, 2009;Klosterman et al, 2011).…”