Molecular evolution of rbcL in three gymnosperm families: identifying adaptive and coevolutionary patterns

Abstract

BackgroundThe chloroplast-localized ribulose-1, 5-biphosphate carboxylase/oxygenase (Rubisco), the primary enzyme responsible for autotrophy, is instrumental in the continual adaptation of plants to variations in the concentrations of CO2. The large subunit (LSU) of Rubisco is encoded by the chloroplast rbcL gene. Although adaptive processes have been previously identified at this gene, characterizing the relationships between the mutational dynamics at the protein level may yield clues on the biological meaning of such adaptive processes. The role of such coevolutionary dynamics in the continual fine-tuning of RbcL remains obscure.ResultsWe used the timescale and phylogenetic analyses to investigate and search for processes of adaptive evolution in rbcL gene in three gymnosperm families, namely Podocarpaceae, Taxaceae and Cephalotaxaceae. To understand the relationships between regions identified as having evolved under adaptive evolution, we performed coevolutionary analyses using the software CAPS. Importantly, adaptive processes were identified at amino acid sites located on the contact regions among the Rubisco subunits and on the interface between Rubisco and its activase. Adaptive amino acid replacements at these regions may have optimized the holoenzyme activity. This hypothesis was pinpointed by evidence originated from our analysis of coevolution that supported the correlated evolution between Rubisco and its activase. Interestingly, the correlated adaptive processes between both these proteins have paralleled the geological variation history of the concentration of atmospheric CO2.ConclusionsThe gene rbcL has experienced bursts of adaptations in response to the changing concentration of CO2 in the atmosphere. These adaptations have emerged as a result of a continuous dynamic of mutations, many of which may have involved innovation of functional Rubisco features. Analysis of the protein structure and the functional implications of such mutations put forward the conclusion that this evolutionary scenario has been possible through a complex interplay between adaptive mutations, often structurally destabilizing, and compensatory mutations. Our results unearth patterns of evolution that have likely optimized the Rubisco activity and uncover mutational dynamics useful in the molecular engineering of enzymatic activities.ReviewersThis article was reviewed by Prof. Christian Blouin (nominated by Dr W Ford Doolittle), Dr Endre Barta (nominated by Dr Sandor Pongor), and Dr Nicolas Galtier.

Plastome organization and evolution of chloroplast genes in Cardamine species adapted to contrasting habitats

“…The observed rates of positive selection on neutral hydrophobic residues such A (alanine) and V (valine) are consistent with previous estimates of selection sites across land plants [ 62 ]. As compared to RUBISCO adaptive selection in gymnosperms, where previous reports suggest 7 sites under positive selection (A11V, Q14K, K30Q, S95N, V99A, I133L, and L225I) [ 63 ], the low frequency of the sites under positive selection observed in Brassicaceae, which belongs to Angiosperms, could be a consequence of the more recent origin of the latter group. The fact that the long series of geological variations of atmospheric CO 2 concentrations experienced by gymnosperms seem to parallel adaptive bursts of co-evolution between RUBISCO and RUBISCO activase lend support to this view [ 63 ].…”

Exploring molecular evolution of Rubisco in C3 and CAM Orchidaceae and Bromeliaceae

“…Previous studies reported residues under positive selection in Rubisco L-subunit in different groups of plants Fig. 1 Frequency diagram according to the leaf carbon isotope composition (δ 13 C, ‰) of the 78 orchids and 144 bromeliads studied (see Table 1 and Additional file 1: Table S1) [28-30, 33, 34, 59-62] and revealed that amino acid coevolution is common in Rubisco of land plants [62,63]. Kapralov and Filatov (2007) [28] reported a number of amino acid sites under positive selection in families sharing C 3 and CAM species.…”

Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

“…The initial molecular-phylogenetic analysis of rbcL showed that positive selection is widespread among all main lineages of land plants, but is restricted to a relatively small number of Rubisco amino acid residues within functionally important sites [6]. Following studies showed that rbcL is under positive selection in particular taxonomic groups [26], [27], [51], [52], [53], [54], [55], [56]. Coevolution of residues is common in Rubisco of land plants as well as positive selection and there is an overlap between coevolving and positively selected residues [57].…”