Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia

Abstract

Succulence and leaf thickness are important anatomical traits in CAM plants, resulting from the presence of large vacuoles to store organic acids accumulated overnight. A higher degree of succulence can result in a reduction in intercellular air space which constrains internal conductance to CO2. Thus, succulence presents a trade-off between the optimal anatomy for CAM and the internal structure ideal for direct C3 photosynthesis. This study examined how plasticity for the reversible engagement of CAM in the genus Clusia could be accommodated by leaf anatomical traits that could facilitate high nocturnal PEPC activity without compromising the direct day-time uptake of CO2 via Rubisco. Nine species of Clusia ranging from constitutive C3 through C3/CAM intermediates to constitutive CAM were compared in terms of leaf gas exchange, succulence, specific leaf area, and a range of leaf anatomical traits (% intercellular air space (IAS), length of mesophyll surface exposed to IAS per unit area, cell size, stomatal density/size). Relative abundances of PEPC and Rubisco proteins in different leaf tissues of a C3 and a CAM-performing species of Clusia were determined using immunogold labelling. The results indicate that the relatively well-aerated spongy mesophyll of Clusia helps to optimize direct C3-mediated CO2 fixation, whilst enlarged palisade cells accommodate the potential for C4 carboxylation and nocturnal storage of organic acids. The findings provide insight on the optimal leaf anatomy that could accommodate the bioengineering of inducible CAM into C3 crops as a means of improving water use efficiency without incurring detrimental consequences for direct C3-mediated photosynthesis.

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

“…However, altering the latter two parameters could potentially limit photosynthesis in C 3 mode due to reduced CO 2 diffusion through the mesophyll and a lower C i 47 and therefore disadvantage flexible CAM. Barrera Zambrano et al proposed that Clusia might overcome this discrepancy by having a high % IAS in the spongy mesophyll for efficient CO 2 diffusion in C 3 mode, and large palisade cells for carboxylic acid storage in CAM mode and suggested this as a potential engineering strategy for transferring inducible CAM into a C 3 plant 48 . Of particular relevance is a study which attempted to increase leaf cell size by overexpressing a grape berry transcription factor ( VvCEB1 opt ) in Arabidopsis thaliana and Nicotiana sylvestris 49 .…”

Mining from transcriptomes: 315 single‐copy orthologous genes concatenated for the phylogenetic analyses of Orchidaceae

“…; Barrera Zambrano et al. ). Given the number of diversified species in Epidendroideae, such as terrestrial and epiphytic, sympodial and monopodial, and achlorophyllous and autotrophic orchids, we selected five species to represent this large subfamily.…”

“…The showy flowers of some of these plant species are important parents in hybridization. Despite the cosmopolitan distribution of these plants, most species are tropical epiphytes, typically with succulent and swollen leaves or stems, likely associated with crassulacean acid metabolism plants (Winter et al 1983;Silvera et al 2005;Griffiths et al 2008;Barrera Zambrano et al 2014). Given the number of diversified species in Epidendroideae, such as terrestrial and epiphytic, sympodial and monopodial, and achlorophyllous and autotrophic orchids, we selected five species to represent this large subfamily.…”

Altered Gene Regulatory Networks are Associated with the Transition from C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)

“…CO 2 is temporarily stored as malic acid in the vacuoles until day time, when stomata close and malic acid is moved back into the cytosol for decarboxylation. The resulting increase of CO 2 levels near ribuslose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) results in highly efficient CO 2 reduction via C 3 photosynthesis CAM is associated with a number of anatomical, physiological and genetic change, including alterations to leaf anatomy (Nelson and Sage, 2008; Zambrano et al, 2014), stomatal opening at night, and tight regulation of metabolic genes within day/night cycles. Despite the complexity of these evolutionary novelties, CAM plants are found in a wide range of plant families, including eudicot species in the Euphorbiaceae (Horn et al, 2014) and Caryophyllales (Guralnick et al, 1984; Moore et al, 2017; Winter and Holtum, 2011) and monocot lineages in Agavoideae (Abraham et al, 2016; Heyduk et al, 2016), Orchidaceae (Silvera et al, 2009, 2010), and Bromeliaceae (Crayn et al, 2004).…”