Stomatal Biology of CAM Plants1[CC-BY]

Crassulacean acid metabolism (CAM) is a major physiological syndrome that has evolved independently in numerous land plant lineages. CAM plants are of great ecological significance, and there is increasing interest for their water-use efficiency and drought resistance. Integral to the improvement in water-use efficiency that CAM affords is a unique pattern of stomatal conductance, distinguished by primarily nocturnal opening and often extensive diurnal flexibility in response to environmental factors. Here, we assess how recent research has shed new light on the functional biology of CAM plant stomata and integration within the broader physiology and ecology of succulent organisms. Divergences in stomatal sensitivity to environmental and endogenous factors relative to C3 species have been a key aspect of the evolution of functional CAM. Stomatal traits of CAM plants are closely coordinated with other leaf functional traits, and structural specialization of CAM stomatal complexes may be of undiagnosed functional relevance.We also highlight how salient results from ongoing work on C3 plant stomatal biology could apply to CAM species. Key questions remaining relate to the interdependence between stomatal and mesophyll responses and are particularly relevant for bioengineering of CAM traits or bioenergy crops to exploit enhanced water-use efficiency and productivity on marginal land. With the increasing availability of powerful analytical tools and the emergence of new model systems for the study of the molecular basis of physiological traits in CAM plants, many exciting avenues for future research are open to intrepid investigators. CAM is a celebrated example of a convergent physiological syndrome (i.e. a characteristic combination of traits), having evolved independently on numerous occasions across the land plants (Smith and Winter, 1996). Furthermore, thanks in part to their ability to withstand multiple, synergistic stressors (Lüttge, 2010), CAM plants have successfully invaded diverse environmental spaces ranging from deserts to cloud forests. In many tropical and subtropical vegetation types, CAM is a dominant ecophysiological syndrome, and CAM plants represent at least 6% of higher plant species richness (Dodd et al., 2002). The physiological mechanisms and ecological significance of the gas exchange rhythms of plants performing CAM have been the subject of curiosity and investigation for not just decades, but centuries (De Saussure, 1804; Heyne, 1815; Osmond, 1978; Ting, 1987; Faak, 2000). The quintessential feature of CAM is nocturnal primary carbon assimilation by the enzyme phospho-enol-pyruvate carboxylase (PEPC), producing malic acid that is stored in mesophyll cell vacuoles and subsequently decarboxylated during the light period to provide CO2 for refixation by Rubisco (Winter and Smith, 1996). While a few lineages are capable of performing CAM in tissues lacking stomata, including some aquatic plants with leaves with no stomata (“astomatous”; Keeley, 1998) and epiphytic orchids with astomatous chlorophyllous roots (Goh et al., 1983), in most cases, CAM involves the delivery of CO2 to the mesophyll via stomata that are open in the dark (Winter and Smith, 1996). Nonnegligible nocturnal stomatal conductance is increasingly recognized as an important physiological phenomenon in many C3 plants (Zeppel et al., 2012; de Dios et al., 2013; Forster, 2014; Matimati et al., 2014; Zeppel et al., 2014; Cirelli et al., 2016; Resco de Dios et al., 2016), but stomata of CAM plants displaying primarily nocturnal CO2 assimilation clearly must differ from those of C3 plants in their responsiveness to environmental and endogenous stimuli. The global CAM flora combines great ecological diversity with a wide variety of evolutionary backgrounds,