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Genomic Characteristics and Comparative Genomics Analysis of Two Chinese Corynespora cassiicola Strains Causing Corynespora Leaf Fall (CLF) Disease.

ABSTRACT: Rubber tree Corynespora leaf fall (CLF) disease, caused by the fungus Corynespora cassiicola, is one of the most damaging diseases in rubber tree plantations in Asia and Africa, and this disease also threatens rubber nurseries and young rubber plantations in China. C. cassiicola isolates display high genetic diversity, and virulence profiles vary significantly depending on cultivar. Although one phytotoxin (cassicolin) has been identified, it cannot fully explain the diversity in pathogenicity between C. cassiicola species, and some virulent C. cassiicola strains do not contain the cassiicolin gene. In the present study, we report high-quality gapless genome sequences, obtained using short-read sequencing and single-molecule long-read sequencing, of two Chinese C. cassiicola virulent strains. Comparative genomics of gene families in these two stains and a virulent CPP strain from the Philippines showed that all three strains experienced different selective pressures, and metabolism-related gene families vary between the strains. Secreted protein analysis indicated that the quantities of secreted cell wall-degrading enzymes were correlated with pathogenesis, and the most aggressive CCP strain (cassiicolin toxin type 1) encoded 27.34% and 39.74% more secreted carbohydrate-active enzymes (CAZymes) than Chinese strains YN49 and CC01, respectively, both of which can only infect rubber tree saplings. The results of antiSMASH analysis showed that all three strains encode ~60 secondary metabolite biosynthesis gene clusters (SM BGCs). Phylogenomic and domain structure analyses of core synthesis genes, together with synteny analysis of polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS) gene clusters, revealed diversity in the distribution of SM BGCs between strains, as well as SM polymorphisms, which may play an important role in pathogenic progress. The results expand our understanding of the C. cassiicola genome. Further comparative genomic analysis indicates that secreted CAZymes and SMs may influence pathogenicity in rubber tree plantations. The findings facilitate future exploration of the molecular pathogenic mechanism of C. cassiicola.

SUBMITTER: Li B

PROVIDER: S-EPMC8235470 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Corynespora cassiicola is an Ascomycetes fungus with a broad host range and diverse life styles. Mostly known as a necrotrophic plant pathogen, it has also been associated with rare cases of human infection. In the rubber tree, this fungus causes the Corynespora leaf fall (CLF) disease, which increasingly affects natural rubber production in Asia and Africa. It has also been found as an endophyte in South American rubber plantations where no CLF outbreak has yet occurred. The C. cassiicola species is genetically highly diverse, but no clear relationship has been evidenced between phylogenetic lineage and pathogenicity. Cassiicolin, a small glycosylated secreted protein effector, is thought to be involved in the necrotrophic interaction with the rubber tree but some virulent C. cassiicola isolates do not have a cassiicolin gene. This study set out to identify other putative effectors involved in CLF. The genome of a highly virulent C. cassiicola isolate from the rubber tree (CCP) was sequenced and assembled. In silico prediction revealed 2870 putative effectors, comprising CAZymes, lipases, peptidases, secreted proteins and enzymes associated with secondary metabolism. Comparison with the genomes of 44 other fungal species, focusing on effector content, revealed a striking proximity with phylogenetically unrelated species (Colletotrichum acutatum, Colletotrichum gloesporioides, Fusarium oxysporum, nectria hematococca, and Botrosphaeria dothidea) sharing life style plasticity and broad host range. Candidate effectors involved in the compatible interaction with the rubber tree were identified by transcriptomic analysis. Differentially expressed genes included 92 putative effectors, among which cassiicolin and two other secreted singleton proteins. Finally, the genomes of 35 C. cassiicola isolates representing the genetic diversity of the species were sequenced and assembled, and putative effectors identified. At the intraspecific level, effector-based classification was found to be highly consistent with the phylogenomic trees. Identification of lineage-specific effectors is a key step toward understanding C. cassiicola virulence and host specialization mechanisms.

Project description:Numerous plant-pathogenic fungi secrete necrotrophic effectors (syn. host-selective toxins) that are important determinants of pathogenicity and virulence in species that have a necrotrophic lifestyle. Corynespora cassiicola is a necrotrophic fungus causing emerging target spot epidemics in the southeastern United States (US). Previous studies revealed that populations of C. cassiicola from cotton, soybean, and tomato are clonal, host specialized and genetically distinct. Additionally, cassiicolin - the necrotrophic effector identified in some C. cassiicola isolates - is an important toxin for virulence on rubber. It is encoded by seven Cas gene variants. Our goal was to conduct comparative genomic analyses to identify variation among putative necrotrophic effector genes and to determine if lack of one of the mating-types explained clonal populations in C. cassiicola causing outbreaks in the southeastern US and the apparent absence of sexual reproduction worldwide. A total of 12 C. cassiicola genomes, with four each from isolates from tomato, soybean, and cotton, were sequenced using an Illumina Next Seq platform. Each genome was assembled de novo, compared with the reference genome from rubber, and searched for known Cas, and other gene clusters with homologs of secondary metabolites. Cas2 and/or Cas6 were present in isolates from soybean in the southeastern US, whereas Cas1 and Cas2 were present in isolates from cotton in the southeastern US. In addition, several toxin genes, including the T-toxin biosynthetic genes were present in all C. cassiicola from cotton, soybean, and tomato. The mating-type locus was identified in all of the sequenced genomes, with the MAT1-1 idiomorph present in all cotton isolates and the rubber isolate, whereas the MAT1-2 idiomorph was present in all soybean isolates. We developed a PCR-based marker for mating-type in C. cassiicola. Both mating types were present in isolates from tomato. Thus, C. cassiicola has both mating-types necessary for sexual reproduction, but the absence of both mating-types within soybean and cotton populations could explain clonality in these populations. Variation in necrotrophic effectors may underlie host specialization and disease emergence of target spot on cotton, soybean, and tomato in the southeastern US.

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Genomic Characteristics and Comparative Genomics Analysis of Two Chinese Corynespora cassiicola Strains Causing Corynespora Leaf Fall (CLF) Disease.

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