Abstract

BackgroundThe CO2-concentrating mechanism associated to Crassulacean acid metabolism (CAM) alters the catalytic context for Rubisco by increasing CO2 availability and provides an advantage in particular ecological conditions. We hypothesized about the existence of molecular changes linked to these particular adaptations in CAM Rubisco. We investigated molecular evolution of the Rubisco large (L-) subunit in 78 orchids and 144 bromeliads with C3 and CAM photosynthetic pathways. The sequence analyses were complemented with measurements of Rubisco kinetics in some species with contrasting photosynthetic mechanism and differing in the L-subunit sequence.ResultsWe identified potential positively selected sites and residues with signatures of co-adaptation. The implementation of a decision tree model related Rubisco specific variable sites to the leaf carbon isotopic composition of the species. Differences in the Rubisco catalytic traits found among C3 orchids and between strong CAM and C3 bromeliads suggested Rubisco had evolved in response to differing CO2 concentration.ConclusionsThe results revealed that the variability in the Rubisco L-subunit sequence in orchids and bromeliads is composed of coevolving sites under potential positive adaptive signal. The sequence variability was related to δ13C in orchids and bromeliads, however it could not be linked to the variability found in the kinetic properties of the studied species.

Highlights

  • The CO2-concentrating mechanism associated to Crassulacean acid metabolism (CAM) alters the catalytic context for Rubisco by increasing CO2 availability and provides an advantage in particular ecological conditions

  • The CAM pathway is characterized by the temporal separation of carbon fixation: CO2 is initially fixed by phosphoenolpyruvate carboxylase at night [1,2,3]

  • Our hypothesis was that a large variability in the L-subunit exists in bromeliads and orchids, and that part of this molecular variability was positively selected to improve the catalytic performance of Rubisco according to the specific physiology of CAM and C3 species

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Summary

Results

Variation of leaf traits and their correlation with the photosynthetic mechanism As for the purposes of the present study, the classification of the photosynthetic mechanism of the studied species and varieties into different CAM levels is required. Strong CAM plants presented significantly (p < 0.05) higher LMA than C3 plants (Additional file 2: Table S2). 23 amino acidic sites were identified under co-evolution in the L-subunit of Rubisco, distributed in 11 coevolution groups (Additional file 3: Table S3). 20 amino acidic sites were identified under co-evolution, distributed in 2 coevolution groups, being the residues 449 and 478 the ones with two interactions and the rest of co-evolving sites appeared in only one group (Additional file 3: Table S3). Differences in the relative abundance of Rubisco over leaf total soluble protein ([Rubisco]/[TSP]) were observed among bromeliads (Table 4), with the strong CAM A. nudicaulis and T. bermejoensis presenting the lowest values. [Rubisco]/ [TSP] was inversely correlated with LMA, leaf thickness and leaf δ13C

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