Loss of Pathogenicity and Evidence of Horizontal Gene Transfer in Colletotrichum gloeosporioides From a Medicinal Plant.

Colletotrichum gloeosporioides is a major agricultural pathogen of crops that has also been identified as an endophyte of the medicinal plant Huperzia serrata. Both H. serrata and C. gloeosporioides produce huperzine A, a potential treatment for Alzheimer's disease. In this study, a nonpathogenic C. gloeosporioides strain (NWUHS001) was isolated and its genome sequenced. Gene structure prediction identified 15,413 protein-coding genes and 879 noncoding RNAs. Through PHI-base database prediction, we found that NWUHS001 lacks two key pathogenicity genes CgDN3 and cap20, which may be the cause of its nonpathogenicity. Comparative genomic analysis showed that the number of genes encoding pectin lyase B (pelB), pectin lyase (pnl) and polygalacturonase (pg) in NWUHS001 was significantly lower than that in pathogenic strains during the expansion of mycelium into host tissues. This caused slow growth and incapability to penetrate host cells. In contrast, in NWUHS001, genes involved in carbon acquisition such as ribose and amino sugar metabolic pathways were enriched, indicating active metabolite exchange with the host. In addition, by comparing the genome of NWUHS001 with that of the host H. serrata, we found that polyketosynthetase (pksIII), a key gene in the host huperzine A biosynthetic pathway, may possibly have been acquired from the fungus by horizontal gene transfer (HGT). This study explained the possible genetic evolution mechanism of C. gloeosporioides from pathogenicity to nonpathogenicity, which is of value for studying the interaction between microorganisms and plants. It also provided clues to the genetic evolution of the biosynthetic pathway of huperzine A.