Phylogeny of Calvin cycle enzymes supports Plantae monophyly

Abstract

Photosynthesis is a critical biochemical process on our planet providing food for most life. The common ancestor of plants and their algal sisters gained photosynthesis through the engulfment and retention of a cyanobacterial primary endosymbiont that evolved into a photosynthetic organelle, the plastid (Bhattacharya et al., 2004). In photosynthetic eukaryotes, the essential series of reactions that capture the products of photosynthetic light reactions (ATP and NADPH2) to fix CO2 (Fig. 1), known as the Calvin cycle (CC; Calvin and Benson, 1948), takes place in the plastid stroma. The eukaryotic CC involves 11 different enzymes (Table 1) that are nuclear encoded and plastid targeted to express their function, with the exception of ribulose-1,5-bisphosphate carboxylase (RuBisCO) subunits (large and small) that remain plastid encoded in red and glaucophyte algae. In green algae (and land plants) the RuBisCO large subunit is encoded in the plastid genome but the small subunit is nuclear encoded. Photosynthetic eukaryotes also contain cytosolic enzymes involved in glycolysis and gluceoneogenesis that catalyze reactions similar to those in the CC and were present in eukaryotes before plastid origin (Martin and Schnarrenberger, 1997). Molecular phylogenetic analyses suggest that land plants (Martin and Schnarrenberger, 1997) and red algae acquired at least a subset of the CC enzymes via intracellular (endosymbiotic) gene transfer (EGT) from the captured cyanobacterium prior to the divergence of green and red algae (Matsuzaki et al., 2004). However, it is well known that some CC enzymes in land plants and red algae have a non-cyanobacterial origin (Martin and Schnarrenberger, 1997; Matsuzaki et al., 2004). A likely explanation is that