Higher-plant chloroplast and cytosolic fructose-1,6-bisphophosphatase isoenzymes: origins via duplication rather than prokaryote-eukaryote divergence

Abstract

Full-size cDNAs encoding the precursors of chloroplast fructose-1,6-bisphosphatase (FBP), sedoheptulose-1,7-bisphosphatase (SBP), and the small subunit of Rubisco (RbcS) from spinach were cloned. These cDNAs complete the set of homologous probes for all nuclear-encoded enzymes of the Calvin cycle from spinach (Spinacia oleracea L.). FBP enzymes not only of higher plants but also of non-photosynthetic eukaryotes are found to be unexpectedly similar to eubacterial homologues, suggesting a eubacterial origin of these eukaryotic nuclear genes. Chloroplast and cytosolic FBP isoenzymes of higher plants arose through a gene duplication event which occurred early in eukaryotic evolution. Both FBP and SBP of higher plant chloroplasts have acquired substrate specificity, i.e. have undergone functional specialization since their divergence from bifunctional FBP/SBP enzymes of free-living eubacteria.

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

“…SBPase was previously described as an essential enzyme of green plants that was acquired after primary endosymbiosis (Martin et al 1996). In this study, we document the presence of SBPase in all lineages of photosynthetic eukaryotes containing primary plastids including green plants, rhodophytes, and glaucophytes (Plantae) as well as in all lineages with complex green (euglenophytes, chlorarachniophytes) or complex red plastids (haptophytes, cryptophytes, diatoms, dinoflagellates) (Fig.…”

“…Several phylogenetic analyses of SBP and FBP sequences have shown that they are homologous and demonstrated the highly distinct nature of the monophyletic SBP subtree (Hannaert et al 2003;Martin et al 1996;Rogers and Keeling 2004). Figure 2 shows the maximum likelihood tree (PhyML) of 37 eukaryotic SBP sequences based on 197 aa positions.…”

“…The plastid-targeted FBP is a duplicate of the closely related cytosolic FBP (Fig. 1), whereas the very divergent SBP displays no close affinity to any of the other FBP sequences (Martin et al 1996). …”

“…Eukaryotic SBP and FBP are distantly related and nuclear-encoded genes that are both of bacterial ancestry (Martin et al 1996). Chloroplast SBPase and FBPase of land plants have replaced the bispecific enzyme of cyanobacteria that either uses sedoheptulose-1,7-bisphosphate or fructose-1,6-bisphosphate as a substrate (Gerbling et al 1986).…”

Plant-like traits associated with metabolism of Trypanosoma parasites

“…We have used genomic information to search for the presence of genes coding for potential glycosomal proteins as identified by the presence of so-called peroxisometargeting signals (PTSs), either at their C terminus (PTS1) or near their N terminus (PTS2). Most strikingly, we identified in T. brucei, a gene with a complete ORF for a homolog of SBPase, an enzyme typical of the Calvin cycle of photosynthetic organisms and has been thus far encountered only in the chloroplasts of green algae and plants (18). The inferred protein sequence has a PTS1 (-SKL) at its C terminus, suggestive of a glycosomal localization.…”