Genomic Plasticity Mediated by Transposable Elements in the Plant Pathogenic Fungus Colletotrichum higginsianum

Abstract

Phytopathogen genomes are under constant pressure to change, as pathogens are locked in an evolutionary arms race with their hosts, where pathogens evolve effector genes to manipulate their hosts, whereas the hosts evolve immune components to recognize the products of these genes. Colletotrichum higginsianum ( Ch ), a fungal pathogen with no known sexual morph, infects Brassicaceae plants including Arabidopsis thaliana . Previous studies revealed that Ch differs in its virulence toward various Arabidopsis thaliana ecotypes, indicating the existence of coevolutionary selective pressures. However, between-strain genomic variations in Ch have not been studied. Here, we sequenced and assembled the genome of a Ch strain, resulting in a highly contiguous genome assembly, which was compared with the chromosome-level genome assembly of another strain to identify genomic variations between strains. We found that the two closely related strains vary in terms of large-scale rearrangements, the existence of strain-specific regions, and effector candidate gene sets and that these variations are frequently associated with transposable elements (TEs). Ch has a compartmentalized genome consisting of gene-sparse, TE-dense regions with more effector candidate genes and gene-dense, TE-sparse regions harboring conserved genes. Additionally, analysis of the conservation patterns and syntenic regions of effector candidate genes indicated that the two strains vary in their effector candidate gene sets because of de novo evolution, horizontal gene transfer, or gene loss after divergence. Our results reveal mechanisms for generating genomic diversity in this asexual pathogen, which are important for understanding its adaption to hosts.

Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens

“…sorokiniana isolate, WAI2406, contained a large segmental movement of 200 kb from one chromosome to another. Similar interchromosomal translocations were observed previously in the fungal plant pathogens Verticillium dahliae, Magnaporthe oryzae, and Colletotrichum higginsianum (46–48). While all three studies demonstrated that translocations occur in regions where transposons are prevalent, only the study by Faino et al (47) in the asexual species V.…”

Subtelomeric regions and a repeat-rich chromosome harbor multicopy effector gene clusters with variable conservation in multiple plant pathogenicColletotrichumspecies

“…dahliae and also C. higginsianum (Jonge et al 2013;Tsushima et al 2019). However, V. dahliae 316 and C. higginsianum are asexual pathogens, whereas CGSC members have known sexual morphs increased TE activity in Nara gc5, although this needs to be investigated.…”

Rapid evolution in plant–microbe interactions – an evolutionary genomics perspective

“…It has been proposed that TEs are instrumental for rapid adaptation in fungal and oomycete pathogens (Whisson et al , ; Kasuga & Gijzen, ; Frantzeskakis et al , ). TE expansion may facilitate gene gain or loss and thereby introduce genetic novelty (Yoshida et al , , Hartmann & Croll, , Tsuhima et al ). However, TE‐derived mutations can negatively impact fitness as well (e.g.…”