Dissecting Succulence: Crassulacean Acid Metabolism and Hydraulic Capacitance are Independent Adaptations in Clusia Leaves

Abstract

Succulence is found across the world as an adaptation to water-limited niches. The fleshy organs of succulent plants develop via enlarged photosynthetic chlorenchyma and/or achlorophyllous water storage hydrenchyma cells. The precise mechanism by which anatomical traits contribute to drought tolerance is unclear, as the effect of succulence is multifaceted. Large cells are believed to provide space for nocturnal storage of malic acid fixed by crassulacean acid metabolism (CAM), whilst also buffering water potentials by elevating hydraulic capacitance (CFT). Furthermore, the effect of CAM and elevated CFT on growth and water conservation have not been compared, despite the assumption that these adaptations often occur together. We assessed the relationship between succulent anatomical adaptations, CAM and CFT, across the genus Clusia. In addition, we simulated the effects of CAM and CFT on growth and water conservation during drought using the Photo3 model. Within Clusia leaves, CAM and CFT are independent traits: CAM requires large palisade chlorenchyma cells, whereas hydrenchyma tissue governs interspecific differences in CFT. In addition, our model suggests that CAM supersedes CFT as a means to maximise CO2 assimilation and minimise transpiration during drought. Our study challenges the assumption that CAM and CFT are mutually dependent traits within succulent leaves.

Exploring Xylem Anatomical Adaptations Associated with Crassulacean Acid Metabolism and Hydraulic Capacitance in Clusia Leaves: Lessons for CAM Bioengineering

“…Estimates of leaf bulk hydraulic capacitance (CFT) were taken from Leverett et al (2022). Pressure-volume curve data were used to calculate CFT with the equation…”

“…Crassulacean acid metabolism (CAM) is a photosynthetic adaptation that minimises water loss via reorganised stomatal dynamics, so that stomata open at night and close during the middle of the day, (Borland et al ., 2014, 2015; Yang et al ., 2015). By decreasing transpiration, CAM prevents leaf water potentials (Ψ L ) from falling low enough to cause mechanical damage to vascular and mesophyll tissues (Haag-Kerwer et al ., 1996; Winter et al ., 2005; Leverett et al ., 2022). Elevated bulk hydraulic capacitance (C FT : see equation 1 in Materials and Methods) is another strategy for coping with water limitation which allows leaves to maintain a stable Ψ L when tissues dehydrate (Smith et al ., 1987; Ogburn and Edwards, 2010, 2012; Luo et al ., 2021).…”

“…Elevated bulk hydraulic capacitance (C FT : see equation 1 in Materials and Methods) is another strategy for coping with water limitation which allows leaves to maintain a stable Ψ L when tissues dehydrate (Smith et al ., 1987; Ogburn and Edwards, 2010, 2012; Luo et al ., 2021). Consequently, leaves with high C FT rely less on the influx of water to prevent transpiration-induced drops in Ψ L (Leverett et al ., 2022). Hence, like CAM, elevated C FT minimises the rate at which water flows through transpiring leaves.…”

“…These tropical trees, epiphytes and hemiepiphytes exhibit a wide variety of photosynthetic phenotypes, including obligate C 3 and constitutive CAM species as well as C 3 -CAM intermediates, where CAM accounts for only a fraction of total carbon assimilation (Barrera-Zambrano et al ., 2014; Borland et al ., 2018; Leverett et al ., 2021; Luján et al ., 2021; Pachon et al ., 2022). In addition, a > 5-fold variation in C FT exists across Clusia (Leverett et al ., 2022). CAM and C FT appear to be independent traits in this genus, as the former is associated with deep chlorenchyma tissue, whereas the latter is the consequence of investment in adaxial hypodermal hydrenchyma tissue (Leverett et al ., 2022).…”

“…In addition, a > 5-fold variation in C FT exists across Clusia (Leverett et al ., 2022). CAM and C FT appear to be independent traits in this genus, as the former is associated with deep chlorenchyma tissue, whereas the latter is the consequence of investment in adaxial hypodermal hydrenchyma tissue (Leverett et al ., 2022). As CAM and C FT are independent adaptations in Clusia leaves, this genus is ideal for exploring which trait is more influential on vascular architecture and xylem anatomy.…”