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 (C FT ). The effect of CAM and elevated C FT 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 C FT , across the genus Clusia. We also simulated the effects of CAM and C FT on growth and water conservation during drought using the Photo3 model. Within Clusia leaves, CAM and C FT are independent traits: CAM requires large palisade chlorenchyma cells, whereas hydrenchyma tissue governs interspecific differences in C FT . In addition, our model suggests that CAM supersedes C FT as a means to maximise CO 2 assimilation and minimise transpiration during drought. Our study challenges the assumption that CAM and C FT are mutually dependent traits within succulent leaves.

Bringing CAM photosynthesis to the table: Paving the way for resilient and productive agricultural systems in a changing climate

“…It has been defined primarily by nocturnal gas exchange and C 4 acid accumulation ( Haag-Kerwer et al., 1996 ; Cushman and Borland, 2002 ; Owen et al., 2016 ; Winter and Smith, 2022 ), tight regulation of key CAM genes by the circadian clock ( Borland et al., 1999 ; Lüttge, 2000 ; Taybi et al., 2002 ; Dodd et al., 2003 ; Borland and Taybi, 2004 ; Boxall et al., 2005 , 2017 , 2020 ), and leaf succulence ( Koch and Kennedy, 1980 ; Maxwell et al., 1997 ; Griffiths et al., 2008 ; Guan et al., 2020 ; Heyduk, 2021 ). Nevertheless, it is noteworthy that this last attribute does not show a definitive positive correlation with CAM in several taxa ( Heyduk et al., 2016b ; Martin et al., 2019 ; Leverett et al., 2023 ).…”

Exogenous Sodium and Calcium Alleviate Drought Stress by Promoting the Succulence of Suaeda salsa

“…Typically, succulent tissues (i.e., the tissues responsible for water storage) are caused by the growth of enlarged cells in either the photosynthetic tissue (chlorenchyma), a specialised achlorophyllous water storage tissue (hydrenchyma), or a combination of both [ 25 , 50 , 51 ]. In this study, electron microscopy was used to measure the size and number of epidermal cells in S. salsa leaves ( Figure 3 ).…”

Revisiting an ecophysiological oddity: Hydathode‐mediated foliar water uptake in Crassula species from southern Africa

“…This makes Crassula one of the few plant groups in which laminar hydathodes and leaf succulence converge. Succulent organs are characterised by high values of hydraulic capacitance ( C ) (i.e., the change in water content relative to the change in Ψ), which reflects their ability to maintain relatively high Ψ values even during periods of net water loss (Fradera‐Soler et al, 2022; Leverett et al, 2023; Ogburn & Edwards, 2010). As hypothesised by Berry et al (2019), differences in C should influence FWU, with high values of C resulting in relatively constant FWU rates that can be sustained for longer.…”