Adaptive evolution of cytochrome c oxidase: Infrastructure for a carnivorous plant radiation

Abstract

Much recent attention in the study of adaptation of organismal form has centered on developmental regulation. As such, the highly conserved respiratory machinery of eukaryotic cells might seem an unlikely target for selection supporting novel morphologies. We demonstrate that a dramatic molecular evolutionary rate increase in subunit I of cytochrome c oxidase (COX) from an active-trapping lineage of carnivorous plants is caused by positive Darwinian selection. Bladderworts (Utricularia) trap plankton when water-immersed, negatively pressured suction bladders are triggered. The resetting of traps involves active ion transport, requiring considerable energy expenditure. As judged from the quaternary structure of bovine COX, the most profound adaptive substitutions are two contiguous cysteines absent in Ϸ99.9% of databased COX I sequences from Eukaryota, Archaea, and Bacteria. This motif lies directly at the docking point of COX I helix 3 and cytochrome c, and modeling of bovine COX I suggests the possibility of an unprecedented helix-terminating disulfide bridge that could alter COX͞cytochrome c dissociation kinetics. Thus, the key adaptation in Utricularia likely lies in molecular energetic changes that buttressed the mechanisms responsible for the bladderworts' radical morphological evolution. Along with evidence for COX evolution underlying expansion of the anthropoid neocortex, our findings underscore that important morphological and physiological innovations must often be accompanied by specific adaptations in proteins with basic cellular functions. molecular adaptation ͉ positive selection ͉ cellular energetics ͉ protein structure ͉ developmental regulation

The role of mitochondrial respiration in physiological and evolutionary adaptation

“…In these plants, two consecutive amino acids, Leu 113 and Ala 114 located at the docking site of cytochrome c, have both been replaced by cysteine residues. (99) The formation of a disulfide bridge between these residues is theoretically possible, which could change the structure of COX I and alter the kinetics of the interaction to allow the high respiratory rate required for the ATP-dependent trapping mechanism.…”

Molecular evolution of the OrcPI locus in natural populations of Mediterranean orchids

“…Evolutionary forces shape the patterns of genetic diversity that vary greatly within and among species and populations (Small et al, 1999;Vieira and Charlesworth, 2001), and the adaptation at the molecular level can be detected by genetic evidence of the past positive selection (Yang and Bielawski, 2000;Jobson et al, 2004).…”

Phylogenetic Ecology at World Scale, a New Fusion Between Ecology and Evolution

“…So far, comparative plant ecology has worked with physical and chemical traits, or with assays like potential relative growth rates (Cornelissen et al 2003). It is now becoming feasible to compare selected proteins and their function across large numbers of species (Driskell et al 2004, Jobson et al 2004. This is opening up metabolic and developmental traits that would be impractical to bioassay across thousands of species.…”