Gene duplication and fragment recombination drive functional diversification of a superfamily of cytoplasmic effectors in Phytophthora sojae

PLoS One. 2013 Jul 29;8(7):e70036. doi: 10.1371/journal.pone.0070036. Print 2013.

Abstract

Phytophthora and other oomycetes secrete a large number of putative host cytoplasmic effectors with conserved FLAK motifs following signal peptides, termed crinkling and necrosis inducing proteins (CRN), or Crinkler. Here, we first investigated the evolutionary patterns and mechanisms of CRN effectors in Phytophthora sojae and compared them to two other Phytophthora species. The genes encoding CRN effectors could be divided into 45 orthologous gene groups (OGG), and most OGGs unequally distributed in the three species, in which each underwent large number of gene gains or losses, indicating that the CRN genes expanded after species evolution in Phytophthora and evolved through pathoadaptation. The 134 expanded genes in P. sojae encoded family proteins including 82 functional genes and expressed at higher levels while the other 68 genes encoding orphan proteins were less expressed and contained 50 pseudogenes. Furthermore, we demonstrated that most expanded genes underwent gene duplication or/and fragment recombination. Three different mechanisms that drove gene duplication or recombination were identified. Finally, the expanded CRN effectors exhibited varying pathogenic functions, including induction of programmed cell death (PCD) and suppression of PCD through PAMP-triggered immunity or/and effector-triggered immunity. Overall, these results suggest that gene duplication and fragment recombination may be two mechanisms that drive the expansion and neofunctionalization of the CRN family in P. sojae, which aids in understanding the roles of CRN effectors within each oomycete pathogen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biological Evolution
  • Gene Duplication / genetics
  • Phytophthora / classification
  • Phytophthora / genetics*

Grants and funding

This work was supported by grants from the National Natural Science Foundation of China (number 31171831), National Basic Research Program of China (number 2009CB119200), and Natural Science Foundation of Jiangsu Province (number BK2012027). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.