Pathogenic adaptations of Colletotrichum fungi revealed by genome wide gene family evolutionary analyses

Abstract

The fungal genus Colletotrichum contains hemibiotrophic phytopathogens being highly variable in host and tissue specificities. We sequenced a C. fructicola genome (1104–7) derived from an isolate of apple in China and compared it with the reference genome (Nara_gc5) derived from an isolate of strawberry in Japan. Mauve alignment and BlastN search identified 0.62 Mb lineage-specific (LS) genomic regions in 1104–7 with a length criterion of 10 kb. Genes located within LS regions evolved more dynamically, and a strongly elevated proportion of genes were closely related to non-Colletotrichum sequences. Two LS regions, containing nine genes in total, showed features of fungus-to-fungus horizontal transfer supported by both gene order collinearity and gene phylogeny patterns. We further compared the gene content variations among 13 Colletotrichum and 11 non-Colletotrichum genomes by gene function annotation, OrthoMCL grouping and CAFE analysis. The results provided a global evolutionary picture of Colletotrichum gene families, and identified a number of strong duplication/loss events at key phylogenetic nodes, such as the contraction of the detoxification-related RTA1 family in the monocot-specializing graminicola complex and the expansions of several ammonia production-related families in the fruit-infecting gloeosporioides complex. We have also identified the acquirement of a RbsD/FucU fucose transporter from bacterium by the Colletotrichum ancestor. In sum, this study summarized the pathogenic evolutionary features of Colletotrichum fungi at multiple taxonomic levels and highlights the concept that the pathogenic successes of Colletotrichum fungi require shared as well as lineage-specific virulence factors.

Comparative genome analysis indicates rapid evolution of pathogenicity genes inColletotrichum tanaceti

“…Duplication of pathogenicity and virulence genes and a higher mutation rate may allow more rapid pathogen responses to evolution of resistance in existing hosts or adaptation to new host species. Genus Colletotrichum Phylogenetic relationship throughout the genus was consistent with previous observations, with gloeosporioides complex members and C. orbiculare forming a clade separately from the destructivum, graminicola and acutatum clades [9][10][11]. One notable difference was in the divergence time estimates for the divergence of Colletotrichum species complexes which were more ancient than reported by Liang et al [11], despite using the same calibration times.…”

“…Genus Colletotrichum Phylogenetic relationship throughout the genus was consistent with previous observations, with gloeosporioides complex members and C. orbiculare forming a clade separately from the destructivum, graminicola and acutatum clades [9][10][11]. One notable difference was in the divergence time estimates for the divergence of Colletotrichum species complexes which were more ancient than reported by Liang et al [11], despite using the same calibration times. This could have been due to this study using cross-validation across 50 smoothing factors in CAFÉ as opposed to using 12 different constraints and smoothing factor combinations differences, as the use of the different data sets.…”

“…The final RAxML phylogenetic tree was used to generate an ultrametric tree in r8s v1.81 [86] applying the penalized likelihood method [87] and the truncated Newton (TN) algorithm [88]. Divergence times were estimated using previously derived estimates [8,11,89] Colletotrichum crown as calibrations. An optimal smoothing factor which was deduced using the cross validation process [86] among 50 values across 1 to 6.3e+09 was used in the divergence time estimation.…”

“…Many Colletotrichum species are known to cause major economic losses globally, and have been extensively used in the study of the molecular and cellular bases of fungal pathogenicity [4]. The publication of 25 whole genome sequences of Colletotrichum species has significantly improved understanding of the biology, genetics and evolution of this genus [5][6][7][8][9][10][11]. However, a large research gap still exists with this ever-expanding genus consisting of more than 200 accepted species [12] and 14 major species complexes [13,14].…”

“…Comparative genomics has enabled inference of patterns of speciation, pathogenesis and host determination within Colletotrichum lineages [31]. These studies have indicated that the gain and loss of putative pathogenicity gene families in Colletotrichum genomes are important determinants of host specificity and pathogenic adaptation of these species [7,11]. with an average insert size of bp was constructed using the KAPA Hyper Prep Library Preparation Kit [33] and was paired-end sequenced (2×300 bp reads) using the Illumina Miseq platform (San Diego, USA).…”