Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis

Abstract

Summary Are evolutionary outcomes predictable? Adaptations that show repeated evolutionary convergence across the Tree of Life provide a special opportunity to dissect the context surrounding their origins, and identify any commonalities that may predict why certain traits evolved many times in particular clades and yet never evolved in others. The remarkable convergence of C4 and Crassulacean Acid Metabolism (CAM) photosynthesis in vascular plants makes them exceptional model systems for understanding the repeated evolution of complex phenotypes. This review highlights what we have learned about the recurring assembly of C4 and CAM, focusing on the increasingly predictable stepwise evolutionary integration of anatomy and biochemistry. With the caveat that we currently understand C4 evolution better than we do CAM, I propose a general model that explains and unites C4 and CAM evolutionary trajectories. Available data suggest that anatomical modifications are the ‘rate‐limiting step’ in each trajectory, which in large part determines the evolutionary accessibility of both syndromes. The idea that organismal structure exerts a primary influence on innovation is discussed in the context of other systems. Whether the rate‐limiting step occurs early or late in the evolutionary assembly of a new phenotype may have profound implications for its distribution across the Tree of Life.

CAM emerges in a leaf metabolic model under water-saving constraints in different environments

“…Secondly, CAM has evolved many times independently and it is believed to be present in well over 5% of vascular plant species 42,43 . These observations can be attributed to the fact that CAM most likely evolved on a ‘biochemistry first, anatomy second’ trajectory 44 in which ‘C 3 +CAM’ is an evolutionarily accessible phenotype on the trajectory to strong CAM 45,46 . Our model demonstrates the water-saving potential of a partial CAM or CAM-like mode for plants grown in temperate climates, while maintaining a high net metabolic output.…”

C4 and crassulacean acid metabolism within a single leaf: deciphering key components behind a rare photosynthetic adaptation

“…Crassulacean acid metabolism is found in at least 35 families mainly distributed in arid environments (Winter, 2019), and is also commonly, but not exclusively, associated with higher leaf succulence (Nelson et al, 2005;Silvera et al, 2010;Edwards 2019). In contrast to C 4 , CAM occurs in each individual MC and relies on temporal coordination of primary and secondary CO 2 fixation by the circadian clock (Hartwell, 2006).…”

Model approaches to advance crassulacean acid metabolism system integration

“…Similar approaches could also be used to model phylogenetic transitions within major CAM families and address the ‘cause or effect’ of tissue succulence in driving the commitment to CAM shown across the CAM trait space (Males and Griffiths, ; Edwards, ). Here, we stress the need for CAM syndromes to be assessed in their entirety: the regulation of CO 2 supply and evaporative demand as expressed by stomata, the mesophyll metabolic processes and the limitations imposed by low mesophyll conductance in dense tissues with low airspaces.…”

“…The answer to these questions may not lie in a single linear progression from a typical C3 leaf (high air space, low succulence, facultative CAM) to strong CAM in dense, succulent tissues, particularly given recent findings on the extent of intermediate C3-CAM forms (Winter et al, 2015;Earles et al, 2018;Edwards, 2019). Such evidence might be compelling within single clades of annual or perennial herbs with similar growth forms, or when inferred from indirect proxies such as air spaces and vasculature (Earles et al, 2018;Males and Griffiths, 2018) or carbon isotope compositions (Edwards, 2019).…”