Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C4 and crassulacean acid metabolism plants

PeerJ. 2022 Jan 20:10:e12828. doi: 10.7717/peerj.12828. eCollection 2022.

Abstract

Phosphoenolpyruvate carboxylase (PEPC), as the key enzyme in initial carbon fixation of C4and crassulacean acid mechanism (CAM) pathways, was thought to undergo convergent adaptive changes resulting in the convergent evolution of C4 and CAM photosynthesis in vascular plants. However, the integral evolutionary history and convergence of PEPC in plants remain poorly understood. In the present study, we identified the members of PEPC gene family across green plants with seventeen genomic datasets, found ten conserved motifs and modeled three-dimensional protein structures of 90 plant-type PEPC genes. After reconstructing PEPC gene family tree and reconciled with species tree, we found PEPC genes underwent 71 gene duplication events and 16 gene loss events, which might result from whole-genome duplication events in plants. Based on the phylogenetic tree of the PEPC gene family, we detected four convergent evolution sites of PEPC in C4 species but none in CAM species. The PEPC gene family was ubiquitous and highly conservative in green plants. After originating from gene duplication of ancestral C3-PEPC, C4-PEPC isoforms underwent convergent molecular substitution that might facilitate the convergent evolution of C4 photosynthesis in Angiosperms. However, there was no evidence for convergent molecular evolution of PEPC genes between CAM plants. Our findings help to understand the origin and convergent evolution of C4 and CAM plants and shed light on the adaptation of plants in dry, hot environments.

Keywords: Carbon-concentrating mechanisms; Convergent evolution; PEPC; Photosynthetic convergence; Phylogeny.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Crassulacean Acid Metabolism*
  • Evolution, Molecular
  • Phosphoenolpyruvate Carboxylase* / genetics
  • Phylogeny
  • Protein Isoforms / genetics

Substances

  • Phosphoenolpyruvate Carboxylase
  • Protein Isoforms

Associated data

  • figshare/10.6084/m9.figshare.16943797
  • figshare/10.6084/m9.figshare.9911876
  • Dryad/10.5061/dryad.msbcc2ftv
  • Dryad/10.5061/dryad.0vm37

Grants and funding

This research was funded by the “Strategic Priority Research Program” of the Chinese Academy of Sciences (Grant No. XDA13020602). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.