The CAM lineages of planet Earth

Abstract

Background and Scope The growth of experimental studies of crassulacean acid metabolism (CAM) in diverse plant clades, coupled with recent advances in molecular systematics, presents an opportunity to re-assess the phylogenetic distribution and diversity of species capable of CAM. It has been more than two decades since the last comprehensive lists of CAM taxa were published, and an updated survey of the occurrence and distribution of CAM taxa is needed to facilitate and guide future CAM research. We aimed to survey the phylogenetic distribution of these taxa, their diverse morphology, physiology, and ecology, and the likely number of evolutionary origins of CAM based on currently known lineages. Results and Conclusions We found direct evidence – in the form of experimental or field observations of gas exchange, day–night fluctuations in organic acids, carbon isotope ratios, and enzymatic activity – for CAM in 370 genera of vascular plants, representing 38 families. Further assumptions about the frequency of CAM species in CAM clades, and the distribution of CAM in the Cactaceae and Crassulaceae, bring the currently estimated number of CAM-capable species to nearly 7% of all vascular plants. The phylogenetic distribution of these taxa suggests a minimum of 66 independent origins of CAM in vascular plants, with possibly dozens more. To achieve further insight into CAM origins, there is a need for more extensive and systematic surveys of previously unstudied lineages, particularly in living material to identify low-level CAM activity, and for denser sampling to increase phylogenetic resolution in CAM-evolving clades. This should allow further progress in understanding the functional significance of this pathway by integration with studies on the evolution and genomics of CAM in its many forms.

Predicting photosynthetic pathway from anatomy using machine learning

“…We binned each taxon into three CAM phenotypes based on Gilman et al . (2023) and references therein: C 3 , C 3 –C 4 , and C 4 taxa were coded as ‘non‐CAM’; taxa that fix the minority of their daily CO 2 with CAM (C 3 + CAM, C 3 –C 4 + CAM, and C 4 + CAM) were coded as mCAM; and taxa that primarily use CAM to fix CO 2 (i.e. over 50%, resulting in δ 13 C ratios ≥ −18.7‰; Winter & Holtum, 2002) as pCAM.…”

“…To reduce our data set to one observation per species, we took the mean of each feature where multiple accessions were measured; these mean species values were used as the basis for analysis throughout. We binned each taxon into three CAM phenotypes based on Gilman et al (2023) and references therein: C 3 , C 3 -C 4 , and C 4 taxa were coded as 'non-CAM'; taxa that fix the minority of their daily CO 2 with CAM (C 3 + CAM, C 3 -C 4 + CAM, and C 4 + CAM) were coded as mCAM; and taxa that primarily use CAM to fix CO 2 (i.e. over 50%, resulting in d 13 C ratios ≥ À18.7&; Winter & Holtum, 2002) as pCAM.…”

“…However, there are many recognized CAM phenotypes that differ in pattern and magnitude of CAM activity. CAM activity varies along multiple axes, including the degree to which is it facultative or constitutive, the extent of nocturnal stomatal conductance, and the amount of CO 2 sequestered as malic acid (Winter, 2019; Gilman et al ., 2023). Despite the diversity in CAM activity, most CAM‐capable species either use CAM as their primary method of carbon fixation or use CAM for a small minority of carbon fixation, as evidenced by carbon isotope ratios (Messerschmid et al ., 2021).…”

Mesophyll-Specific Circadian Dynamics of CAM Induction in the Ice Plant Unveiled by Single-Cell Transcriptomics

“…CAM holds potential economic and environmental value due to its unique mechanism of fixing CO2 at night. This process involves nocturnal stomatal opening, leading to lower evapotranspiration rates and higher water retention in leaves compared to C3 and C4 plants that fix CO2 during the day 1,[3][4][5][6] . CAM plants demonstrate remarkable drought tolerance, exhibiting up to 20 times greater water-use efficiency than C3 plants 6 .…”

Closely related facultative and constitutive CAM phenotypes show little transcriptomic overlap in the subgenusTillandsia

“…Indeed, instances where similar phenotypes have evolved without a common genetic basis have been observed across a broad spectrum of life including beach mice (Steiner et al, 2009), conifers (Yeaman et al, 2016), lab-reared Drosophila (Barghi et al, 2019) and cacao plants. (Hämälä et al, 2020) An example of a complex but highly evolvable trait is Crassulacean Acid Metabolism (CAM), a carbon-concentrating mechanism that has evolved independently in at least 38 plant families, amounting to a minimum of 66 independent origins (Gilman et al, 2023). CAM plants restructure part of the photosynthetic metabolism across the diel cycle by assimilating CO2 at night, rather than during the day as C3 plants do.…”