Phylogeny of C4-photosynthesis enzymes based on algal transcriptomic and genomic data supports an archaeal/proteobacterial origin and multiple duplication for most C4-related genes

PLoS One. 2014 Oct 14;9(10):e110154. doi: 10.1371/journal.pone.0110154. eCollection 2014.

Abstract

Both Calvin-Benson-Bassham (C3) and Hatch-Slack (C4) cycles are most important autotrophic CO2 fixation pathways on today's Earth. C3 cycle is believed to be originated from cyanobacterial endosymbiosis. However, studies on evolution of different biochemical variants of C4 photosynthesis are limited to tracheophytes and origins of C4-cycle genes are not clear till now. Our comprehensive analyses on bioinformatics and phylogenetics of novel transcriptomic sequencing data of 21 rhodophytes and 19 Phaeophyceae marine species and public genomic data of more algae, tracheophytes, cyanobacteria, proteobacteria and archaea revealed the origin and evolution of C4 cycle-related genes. Almost all of C4-related genes were annotated in extensive algal lineages with proteobacterial or archaeal origins, except for phosphoenolpyruvate carboxykinase (PCK) and aspartate aminotransferase (AST) with both cyanobacterial and archaeal/proteobacterial origin. Notably, cyanobacteria may not possess complete C4 pathway because of the flawed annotation of pyruvate orthophosphate dikinase (PPDK) genes in public data. Most C4 cycle-related genes endured duplication and gave rise to functional differentiation and adaptation in different algal lineages. C4-related genes of NAD-ME (NAD-malic enzyme) and PCK subtypes exist in most algae and may be primitive ones, while NADP-ME (NADP-malic enzyme) subtype genes might evolve from NAD-ME subtype by gene duplication in chlorophytes and tracheophytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Archaea / genetics
  • Autotrophic Processes
  • Bacterial Proteins / genetics
  • Bayes Theorem
  • Cyanobacteria / enzymology
  • Cyanobacteria / genetics*
  • Evolution, Molecular
  • Gene Duplication
  • Genome, Bacterial
  • Molecular Sequence Data
  • Photosynthesis / genetics*
  • Photosynthetic Reaction Center Complex Proteins / chemistry
  • Photosynthetic Reaction Center Complex Proteins / genetics*
  • Phylogeny
  • Proteobacteria / genetics
  • Symbiosis
  • Transcriptome*

Substances

  • Bacterial Proteins
  • Photosynthetic Reaction Center Complex Proteins

Grants and funding

This work was supported by the National Natural Science Foundation of China (NSFC No. 41206116 and No. 31271397, China Postdoctoral Science Foundation (No. 2011M501167), National Public Benefit Research Foundation of China (No. 201105021). The algal transcriptome sequencing was supported by 1KP Project (www.onekp.com). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.