Multiple interkingdom horizontal gene transfers in Pyrenophora and closely related species and their contributions to phytopathogenic lifestyles

PLoS One. 2013;8(3):e60029. doi: 10.1371/journal.pone.0060029. Epub 2013 Mar 29.

Abstract

Many studies have reported horizontal gene transfer (HGT) events from eukaryotes, especially fungi. However, only a few investigations summarized multiple interkingdom HGTs involving important phytopathogenic species of Pyrenophora and few have investigated the genetic contributions of HGTs to fungi. We investigated HGT events in P. teres and P. tritici-repentis and discovered that both species harbored 14 HGT genes derived from bacteria and plants, including 12 HGT genes that occurred in both species. One gene coding a leucine-rich repeat protein was present in both species of Pyrenophora and it may have been transferred from a host plant. The transfer of genes from a host plant to pathogenic fungi has been reported rarely and we discovered the first evidence for this transfer in phytopathogenic Pyrenophora. Two HGTs in Pyrenophora underwent subsequent duplications. Some HGT genes had homologs in a few other fungi, indicating relatively ancient transfer events. Functional analyses indicated that half of the HGT genes encoded extracellular proteins and these may have facilitated the infection of plants by Pyrenophora via interference with plant defense-response and the degradation of plant cell walls. Some other HGT genes appeared to participate in carbohydrate metabolism. Together, these functions implied that HGTs may have led to highly efficient mechanisms of infection as well as the utilization of host carbohydrates. Evolutionary analyses indicated that HGT genes experienced amelioration, purifying selection, and accelerated evolution. These appeared to constitute adaptations to the background genome of the recipient. The discovery of multiple interkingdom HGTs in Pyrenophora, their significance to infection, and their adaptive evolution, provided valuable insights into the evolutionary significance of interkingdom HGTs from multiple donors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ascomycota / classification
  • Ascomycota / genetics*
  • Biological Evolution
  • Gene Transfer, Horizontal / genetics*
  • Phylogeny

Grants and funding

This project was supported by the National Natural Science Foundation of China (NSFC grant no. 31090253, 31210103912, 30900137), partially by Major Innovation Program of Chinese Academy of Sciences (KSCX2-EW-Z-2), a grant (No. O529YX5105) from the Key Laboratory of the Zoological Systematics and Evolution of the Chinese Academy of Sciences, National Science Fund for Fostering Talents in Basic Research (Special subjects in animal taxonomy, NSFC- J0930004), and the Natural Sciences and Engineering Research Council (Canada) Discovery Grant 3148. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.