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Strawberry is a small fruit crop with high economic value. Anthracnose caused by Colletotrichum spp. poses a serious threat to strawberry production, particularly in warm and humid climates, but knowledge of pathogen populations in tropical and subtropical regions is limited. To investigate the diversity of infectious agents causing strawberry anthracnose in Taiwan, a disease survey was conducted from 2010 to 2018, and Colletotrichum spp. were identified through morphological characterization and multilocus phylogenetic analysis with internal transcribed spacer, glyceraldehyde 3-phosphate dehydrogenase, chitin synthase, actin, beta-tubulin, calmodulin, and the intergenic region between Apn2 and MAT1-2-1 (ApMAT). Among 52 isolates collected from 24 farms/nurseries in Taiwan, a new species, Colletotrichum miaoliense sp. nov. (6% of all isolates), a species not previously known to be associated with strawberry, Colletotrichum karstii (6%), and three known species, Colletotrichum siamense (75%), Colletotrichum fructicola (11%), and Colletotrichum boninense (2%), were identified. The predominant species C . siamense and C . fructicola exhibited higher mycelial growth rates on potato dextrose agar and caused larger lesions on wounded and non-wounded detached strawberry leaves. Colletotrichum boninense , C. karstii , and C. miaoliense only caused lesions on wounded leaves. Understanding the composition and biology of the pathogen population will help in disease management and resistance breeding.

Species limits in the fungal genus Colletotrichum are traditionally distinguished by appressorial and/or conidial morphology or through host plant association, but both criteria are criticized for their inability to resolve distinct taxa. In previous research eight novel falcate-spored Colletotrichum species were identified from graminicolous hosts using multilocus molecular phylogenetic analysis. In the present work formal descriptions and illustrations are provided for six of the new taxa: C. hanaui sp. nov., C. nicholsonii sp. nov., C. paspali sp. nov., C. jacksonii sp. nov., C. miscanthi sp. nov. and C. axonopodi sp. nov.; and an emended description with epitypification is provided for C. eleusines. Comparison of hyphopodial appressoria and host association against phylogenetic species boundaries and evolutionary relationships in the graminicolous Colletotrichum group demonstrate that, while these characters can be useful in combination for the purpose of species diagnosis, erroneous identification is possible and species boundaries might be underestimated if these characters are used independently, as exemplified by the polyphyletic taxa C. falcatum. Appressoria have been subject to convergent evolution and were not predictive of phylogenetic relationships. Despite these limitations, the results of this work establish that in combination appressorial and host range characters could be used to generate informative dichotomous identification keys for Colletotrichum species groups when an underlying framework of evolutionary relationships, taxonomic criteria and nomenclature have been satisfactorily derived from molecular systematic treatments.

The genome of the hemibiotrophic anthracnose fungus, Colletotrichum higginsianum, encodes a large repertoire of candidate-secreted effectors containing LysM domains, but the role of such proteins in the pathogenicity of any Colletotrichum species is unknown. Here, we characterized the function of two effectors, ChELP1 and ChELP2, which are transcriptionally activated during the initial intracellular biotrophic phase of infection. Using immunocytochemistry, we found that ChELP2 is concentrated on the surface of bulbous biotrophic hyphae at the interface with living host cells but is absent from filamentous necrotrophic hyphae. We show that recombinant ChELP1 and ChELP2 bind chitin and chitin oligomers in vitro with high affinity and specificity and that both proteins suppress the chitintriggered activation of two immune-related plant mitogen-activated protein kinases in the host Arabidopsis. Using RNAi-mediated gene silencing, we found that ChELP1 and ChELP2 are essential for fungal virulence and appressorium-mediated penetration of both Arabidopsis epidermal cells and cellophane membranes in vitro. The findings suggest a dual role for these LysM proteins as effectors for suppressing chitin-triggered immunity and as proteins required for appressorium function.

Understanding the factors that drive the evolution of pathogenic fungi is central to revealing the mechanisms of virulence and host preference, as well as developing effective disease control measures. Prerequisite to these pursuits is the accurate delimitation of species boundaries. Colletotrichum gloeosporioides s.l. is a species complex of plant pathogens and endophytic fungi for which reliable species recognition has only recently become possible through a multi-locus phylogenetic approach. By adopting an intensive regional sampling strategy encompassing multiple hosts within and beyond agricultural zones associated with cranberry (Vaccinium macrocarpon Aiton), we have integrated North America strains of Colletotrichum gloeosporioides s.l. from these habitats into a broader phylogenetic framework. We delimit species on the basis of genealogical concordance phylogenetic species recognition (GCPSR) and quantitatively assess the monophyly of delimited species at each of four nuclear loci and in the combined data set with the genealogical sorting index (gsi). Our analysis resolved two principal lineages within the species complex. Strains isolated from cranberry and sympatric host plants are distributed across both of these lineages and belong to seven distinct species or terminal clades. Strains isolated from V. macrocarpon in commercial cranberry beds belong to four species, three of which are described here as new. Another species, C. rhexiae Ellis & Everh., is epitypified. Intensive regional sampling has revealed a combination of factors, including the host species from which a strain has been isolated, the host organ of origin, and the habitat of the host species, as useful indicators of species identity in the sampled regions. We have identified three broadly distributed temperate species, C. fructivorum , C. rhexiae , and C. nupharicola , that could be useful for understanding the microevolutionary forces that may lead to species divergence in this important complex of endophytes and plant pathogens.

Richard O'Connell and colleagues report the genomes and transcriptomes of two Colletotrichum plant fungal pathogens. C. higginsianum infects Arabidopsis thaliana , and C. graminicola infects maize ( Zea mays ); comparative genomics in both species lead to molecular insights into the transition from biotrophic to necrotrophic life stages. Colletotrichum species are fungal pathogens that devastate crop plants worldwide. Host infection involves the differentiation of specialized cell types that are associated with penetration, growth inside living host cells (biotrophy) and tissue destruction (necrotrophy). We report here genome and transcriptome analyses of Colletotrichum higginsianum infecting Arabidopsis thaliana and Colletotrichum graminicola infecting maize. Comparative genomics showed that both fungi have large sets of pathogenicity-related genes, but families of genes encoding secreted effectors, pectin-degrading enzymes, secondary metabolism enzymes, transporters and peptidases are expanded in C. higginsianum . Genome-wide expression profiling revealed that these genes are transcribed in successive waves that are linked to pathogenic transitions: effectors and secondary metabolism enzymes are induced before penetration and during biotrophy, whereas most hydrolases and transporters are upregulated later, at the switch to necrotrophy. Our findings show that preinvasion perception of plant-derived signals substantially reprograms fungal gene expression and indicate previously unknown functions for particular fungal cell types.

The genus Colletotrichum comprises species with different lifestyles but is mainly known for phytopathogenic species that infect crops of agronomic relevance causing considerable losses. The fungi of the genus Colletotrichum are distributed in species complexes and within each complex some species have particularities regarding their lifestyle. The most commonly found and described lifestyles in Colletotrichum are endophytic and hemibiotrophic phytopathogenic. Several of these phytopathogenic species show wide genetic variability, which makes long-term maintenance of resistance in plants difficult. Different mechanisms may play an important role in the emergence of genetic variants but are not yet fully understood in this genus. These mechanisms include heterokaryosis, a parasexual cycle, sexual cycle, transposable element activity, and repeat-induced point mutations. This review provides an overview of the genus Colletotrichum, the species complexes described so far and the most common lifestyles in the genus, with a special emphasis on the mechanisms that may be responsible, at least in part, for the emergence of new genotypes under field conditions.

ABSTRACT Fungal plant pathogens cause major crop losses worldwide, with many featuring compartmentalised genomes that include both core and accessory regions, which are believed to drive adaptation. The highly host‐specific fungus Colletotrichum lupini greatly impacts lupin (Lupinus spp.) cultivation. This pathogen is part of clade 1 of the C. acutatum species complex and comprises four genetically uniform, presumably clonal, lineages (I–IV). Despite this, variation in virulence and morphology has been observed within these lineages. To investigate the potential sources of genetic variability in this asexual fungus, we compared the genomes of 16 C. lupini strains and 17 related Colletotrichum species. Phylogenomics confirmed the presence of four distinct lineages, but further examination based on genome size, gene content, transposable elements (TEs), and deletions revealed that lineage II could be split into two groups, II‐A and II‐B. TE content varied between lineages and correlated strongly with genome size variation, supporting a role for TEs in genome expansion in this species. Pangenome analysis revealed a highly variable accessory genome, including a minichromosome present in lineages II, III, and IV, but absent in lineage I. Accessory genes and effectors appeared to cluster in proximity to TEs. Presence/absence variation of putative effectors was lineage‐specific, suggesting that these genes play a crucial role in determining host range. Notably, no effectors were found on the TE‐rich minichromosome. Our findings shed light on the potential mechanisms generating genetic diversity in this asexual fungal pathogen that could aid future disease management. Comparative genomics of the lupin pathogen Colletotrichum lupini reveals low SNP diversity but highlights a dynamic accessory genome, including a variable accessory chromosome and diverse transposable element landscape.

Fragaria × ananassa (common name: strawberry) is a globally cultivated hybrid species belonging to Rosaceae family. Colletotrichum acutatum sensu lato (s.l.) is considered to be the second most economically important pathogen worldwide affecting strawberries. A collection of 148 Colletotrichum spp. isolates including 67 C. acutatum s.l. isolates associated with the phytosanitary history of UK strawberry production were used to characterize multi-locus genetic variation of this pathogen in the UK, relative to additional reference isolates that represent a worldwide sampling of the diversity of the fungus. The evidence indicates that three different species C. nymphaeae, C. godetiae and C. fioriniae are associated with strawberry production in the UK, which correspond to previously designated genetic groups A2, A4 and A3, respectively. Among these species, 12 distinct haplotypes were identified suggesting multiple introductions into the country. A subset of isolates was also used to compare aggressiveness in causing disease on strawberry plants and fruits. Isolates belonging to C. nymphaeae, C. godetiae and C. fioriniae representative of the UK anthracnose pathogen populations showed variation in their aggressiveness. Among the three species, C. nymphaeae and C. fioriniae appeared to be more aggressive compared to C. godetiae. This study highlights the genetic and pathogenic heterogeneity of the C. acutatum s.l. populations introduced into the UK linked to strawberry production.

Selection of a reliable internal control gene is critical for quantitative real-time PCR, which is a rapid, highly sensitive, and easy method for evaluating gene expression levels in different samples or tissues. Colletotrichum scovillei , which belongs to the C. acutatum species complex, is a common and aggressive species that can cause anthracnose in chili peppers. However, stable reference genes have not yet been identified for C. scovillei . In our study, reference genes were selected and validated in C. scovillei during different growth stages, including conidia, conidial germination, and mycelium growth, during host interactions, and after treatment with the common solvent 0.5% dimethyl sulfoxide (DMSO) and plant extracts with antifungal activity against C. scovillei . Eight candidate reference genes ( CsUCE , CsCK , CsTBP , CsTIF , CsPP2A , CsTUB , CsCAL , and CsNADH ) were selected from C. scovillei based on transcriptomic and genomic data. Several statistical methods, including the comparative quantification cycle threshold (Ct) method, geNorm, NormFinder, and Bestkeeper, were used to assess the stabilities of reference gene transcripts. The results indicated that CsPP2A had better stability during the C. scovillei growth stage, CsTUB had the best stability during host interactions, and CsUCE was more stable after treatment with the general solvent 0.5% DMSO and Cestrum glanduliferum kerber ex Francey extracts. Our study provides the most suitable reference gene for future studies to quantify target gene expression levels in C. scovillei under different conditions.

Apple bitter rot caused by Colletotrichum species is a growing problem worldwide. Colletotrichum spp. are economically important but taxonomically un-resolved. Identification of Colletotrichum spp. is critical due to potential species-level differences in pathogenicity-related characteristics. A 400-isolate collection from New York apple orchards were morphologically assorted to two groups, C. acutatum species complex ( CASC ) and C. gloeosporioides species complex ( CGSC ). A sub-sample of 44 representative isolates, spanning the geographical distribution and apple varieties, were assigned to species based on multi-locus phylogenetic analyses of nrITS, GAPDH and TUB2 for CASC , and ITS, GAPDH, CAL, ACT, TUB2, APN2, ApMat and GS genes for CGSC . The dominant species was C. fioriniae , followed by C. chrysophilum and a novel species, C. noveboracense , described in this study. This study represents the first report of C. chrysophilum and C. noveboracense as pathogens of apple. We assessed the enzyme activity and fungicide sensitivity for isolates identified in New York. All isolates showed amylolytic, cellulolytic and lipolytic, but not proteolytic activity. C. chrysophilum showed the highest cellulase and the lowest lipase activity, while C. noveboracense had the highest amylase activity. Fungicide assays showed that C. fioriniae was sensitive to benzovindiflupyr and thiabendazole, while C. chrysophilum and C. noveboracense were sensitive to fludioxonil, pyraclostrobin and difenoconazole. All species were pathogenic on apple fruit with varying lesion sizes. Our findings of differing pathogenicity-related characteristics among the three species demonstrate the importance of accurate species identification for any downstream investigations of Colletotrichum spp. in major apple growing regions.