Origin and distribution of Calvin cycle fructose and sedoheptulose bisphosphatases in plantae and complex algae: a single secondary origin of complex red plastids and subsequent propagation via tertiary endosymbioses

Abstract

Sedoheptulose-1,7-bisphosphatase (SBPase) and fructose-1,6-bisphosphatase (FBPase) are essential nuclear-encoded enzymes involved in land plant Calvin cycle and gluconeogenesis. In this study, we cloned seven SBP and seven FBP cDNAs/genes and established sequences from all lineages of photosynthetic eukaryotes, in order to investigate their origin and evolution. Our data are best explained by a single recruitment of plastid-targeted SBP in Plantae after primary endosymbiosis and a further distribution to algae with complex plastids. While SBP is universally found in photosynthetic lineages, its presence in apicomplexa, ciliates, trypanosomes, and ascomycetes is surprising given that no metabolic function beyond the one in the plastid Calvin cycle is described so far. Sequences of haptophytes, cryptophytes, diatoms, and peridinin-containing dinoflagellates (complex red lineage) strongly group together in the SBP tree and the same assemblage is recovered for plastid-targeted FBP sequences, although this is less supported. Both SBP and plastid-targeted FBP are most likely of red algal origin. Including phosphoribulokinase, fructose bisphosphate aldolase, and glyceraldehyde-3-phosphate dehydrogenase, a total of five independent plastid-related nuclear-encoded markers support a common origin of all complex rhodoplasts via a single secondary endosymbiosis event. However, plastid phylogenies are incongruent with those of the host cell, as illustrated by the cytosolic FBP isoenzyme. These results are discussed in the context of Cavalier-Smith's far-reaching chromalveolate hypothesis. In our opinion, a more plausible evolutionary scenario would be the establishment of a unique secondary rhodoplast and its subsequent spread via tertiary endosymbioses.