Adaptive diversity in structure and function of C₄ photosynthetic components

Many tropical and subtropical plant lineages have independently evolved C₄ photosynthesis. The convergent evolution of this complex functional trait from different ancestors is reflected in variations in the structural and biochemical characteristics of C₄ components such as enzymes and cellular specializations. The mechanism of C₄ carbon concentration mostly involves coordinated function of mesophyll and bundle sheath cells. Important adaptations of the C₄ syndrome include increased vein density and the development of photosynthetic bundle sheath cells with low gas conductance. In addition, the enzymes and transporters of the C₄ pathway evolved via the co-option of multiple genes, each derived from a specific lineage of isoforms present in nonC₄-ancestors. In particular, the adaptation of C₄ enzymes resulted in a variety of structural and biochemical modifications, generally leading to increased catalytic efficiency and regulation by metabolites and post-translational modifications. Differences in these adaptations are particularly evident in the C₄-acid decarboxylation step, which can be catalyzed by three decarboxylases that define the C₄ subtypes. Associated with the biochemical subtypes, there are also differences in the extend of grana staking and localization of bundle sheath cells chloroplasts. The presence of a suberin layer and symplastic connections also likely vary among the different C₄-subtypes. This review examines the current understanding of the diversity of structural and functional changes in key components of the C₄ carbon concentration mechanism. This knowledge is necessary not only to identify divergent solutions for convergent optimization of C₄ components in different C₄ lineages, but also to guide their creation for rational synthetic biology approaches.