Horizontal transfer of a subtilisin gene from plants into an ancestor of the plant pathogenic fungal genus Colletotrichum

PLoS One. 2013;8(3):e59078. doi: 10.1371/journal.pone.0059078. Epub 2013 Mar 15.

Abstract

The genus Colletotrichum contains a large number of phytopathogenic fungi that produce enormous economic losses around the world. The effect of horizontal gene transfer (HGT) has not been studied yet in these organisms. Inter-Kingdom HGT into fungal genomes has been reported in the past but knowledge about the HGT between plants and fungi is particularly limited. We describe a gene in the genome of several species of the genus Colletotrichum with a strong resemblance to subtilisins typically found in plant genomes. Subtilisins are an important group of serine proteases, widely distributed in all of the kingdoms of life. Our hypothesis is that the gene was acquired by Colletotrichum spp. through (HGT) from plants to a Colletotrichum ancestor. We provide evidence to support this hypothesis in the form of phylogenetic analyses as well as a characterization of the similarity of the subtilisin at the primary, secondary and tertiary structural levels. The remarkable level of structural conservation of Colletotrichum plant-like subtilisin (CPLS) with plant subtilisins and the differences with the rest of Colletotrichum subtilisins suggests the possibility of molecular mimicry. Our phylogenetic analysis indicates that the HGT event would have occurred approximately 150-155 million years ago, after the divergence of the Colletotrichum lineage from other fungi. Gene expression analysis shows that the gene is modulated during the infection of maize by C. graminicola suggesting that it has a role in plant disease. Furthermore, the upregulation of the CPLS coincides with the downregulation of several plant genes encoding subtilisins. Based on the known roles of subtilisins in plant pathogenic fungi and the gene expression pattern that we observed, we postulate that the CPLSs have an important role in plant infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Colletotrichum / genetics*
  • Gene Expression
  • Gene Transfer, Horizontal*
  • Host-Pathogen Interactions
  • Models, Molecular
  • Molecular Sequence Data
  • Phylogeny
  • Plant Diseases / genetics
  • Plant Diseases / microbiology
  • Plants / genetics*
  • Plants / microbiology*
  • Protein Conformation
  • Protein Interaction Domains and Motifs
  • Sequence Alignment
  • Subtilisin / chemistry
  • Subtilisin / genetics*

Substances

  • Subtilisin

Grants and funding

This research was supported by funds from the Ministerio de Ciencia e Innovación (MICINN) of Spain (grants AGL2011–29446 and AGL2012-34139). VDAJ was supported by a graduate fellowship from the Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación of Ecuador. W.A.V was supported by a fellowship from the Juan de la Cierva Program (JCI–2009–05364). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.