Succulence and Crassulacean Acid Metabolism in the Genus Clusia

Ph. D. Thesis.Succulent plants can be found across the world in semi-arid and seasonally dry ecosystems. Succulent anatomy exists in different forms; either via large chlorenchyma cells, specialised water-storage tissue called hydrenchyma, or some combination of the two. In addition, succulent chlorenchyma tissue is often accompanied by Crassulacean acid metabolism (CAM); an altered form of photosynthesis which minimises transpirational water loss. By comparing the hydrenchyma to the large photosynthetic chlorenchyma cells, it was shown that only succulence in the hydrenchyma provides capacitance to the leaf. In addition, the degree to which succulence and CAM contribute to leaf turgor loss point (TLP) was explored. The presence of hydrenchyma drives the TLP up, whereas the presence of CAM does not. To develop this, the ecological significance of hydrenchyma and CAM was tested, by investigating how these adaptations affect species’ climatic niches. CAM, and not hydrenchyma, is an important adaptation for species ability to inhabit arid environments. As hydrenchyma and CAM were deemed to be playing discretely different, non-overlapping roles in both the physiology and ecology of CAM, it was expected that they would have different impacts on the vascular architecture of Clusia. Vein density was significantly lower in CAM leaves, whilst hydrenchyma has no impact, suggesting that the lower diel stomatal conductance of CAM plants requires less hydraulic conductance to replace lost water, but that the capacitance generated by hydrenchyma does not have this effect. Finally, as CAM plays an ecologically important role in species distributions, but does not affect the TLP, it was hypothesised that the relevance of this adaptation lies outside of maintaining cell turgor during drought. Accordingly, the CAM drought response was characterised by higher photosynthetic assimilation and mitochondrial respiration rates, suggesting that the purpose of CAM is to sustain metabolic rates during drought, rather than prevent drops in water potential

Low Internal Air Space In Plants With Crassulacean Acid Metabolism May Be An Anatomical Spandrel

Crassulacean Acid Metabolism (CAM) is a photosynthetic adaptation found in at least 38 plant families. Typically, the anatomy of CAM plants is characterised by large photosynthetic cells and a low percentage of leaf volume comprised of internal air space (% IAS). It has been suggested that reduced mesophyll conductance (gm) arising from low % IAS benefits CAM plants by preventing the movement of CO2 out of cells and ultimately minimising leakage of CO2 from leaves into the atmosphere during day-time decarboxylation. Here, we propose that low % IAS does not provide any adaptive benefit to CAM plants, because stomatal closure during phase III of CAM will result in internal concentrations of CO2 becoming saturated, meaning low gm will not have any meaningful impact on the flux of gasses within leaves. We suggest that low % IAS is more likely an indirect consequence of maximising the cellular volume within a leaf, to provide space for the overnight storage of malic acid during the CAM cycle

Dissecting succulence: Crassulacean acid metabolism and hydraulic capacitance are independent adaptations in Clusia leaves

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). 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. We also 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

The long and tortuous path towards improving photosynthesis by engineering elevated mesophyll conductance

Publication status: PublishedFunder: Novo Nordisk Fonden; doi: http://dx.doi.org/10.13039/501100009708The growing demand for global food production is likely to be a defining issue facing humanity over the next 50 years. To tackle this challenge, there is a desire to bioengineer crops with higher photosynthetic efficiencies, to increase yields. Recently, there has been a growing interest in engineering leaves with higher mesophyll conductance, which would allow CO2 to move more efficiently from the substomatal cavities to the chloroplast stroma. However, if crop yield gains are to be realised through this approach, it is essential that the methodological limitations associated with estimating are fully appreciated. In this review, we summarise these limitations, and outline the uncertainties and assumptions that can affect the final estimation of. Furthermore, we critically assess the predicted quantitative effect that elevating will have on assimilation rates in crop species. We highlight the need for more theoretical modelling to determine whether altering is truly a viable route to improve crop performance. Finally, we offer suggestions to guide future research on, which will help mitigate the uncertainty inherently associated with estimating this parameter

The long and tortuous path towards improving photosynthesis by engineering elevated mesophyll conductance

AbstractThe growing demand for global food production is likely to be a defining issue facing humanity over the next 50 years. To tackle this challenge, there is a desire to bioengineer crops with higher photosynthetic efficiencies, to increase yields. Recently, there has been a growing interest in engineering leaves with higher mesophyll conductance (gm), which would allow CO2 to move more efficiently from the substomatal cavities to the chloroplast stroma. However, if crop yield gains are to be realised through this approach, it is essential that the methodological limitations associated with estimating gm are fully appreciated. In this review, we summarise these limitations, and outline the uncertainties and assumptions that can affect the final estimation of gm. Furthermore, we critically assess the predicted quantitative effect that elevating gm will have on assimilation rates in crop species. We highlight the need for more theoretical modelling to determine whether altering gm is truly a viable route to improve crop performance. Finally, we offer suggestions to guide future research on gm, which will help mitigate the uncertainty inherently associated with estimating this parameter.</jats:p

Forty years of research into Crassulacean Acid Metabolism in the genus Clusia : anatomy, ecophysiology and evolution.

Clusia is the only genus containing dicotyledonous trees with a capacity to perform Crassulacean acid metabolism (CAM). Since the discovery of CAM in Clusia, 40 years ago, several studies have highlighted the extraordinary plasticity and diversity of life forms, morphology, and photosynthetic physiology of this genus. In this review we revisit aspects of CAM photosynthesis in Clusia and hypothesize about the timing, the environmental conditions and potential anatomical characteristics that led to the evolution of CAM in the group. We discuss the role of physiological plasticity in influencing species distribution and ecological amplitude in the group. We also explore patterns of allometry of leaf anatomical traits and their correlations with CAM activity. Finally, we identify opportunities for further research of CAM in Clusia, such as the role of elevated nocturnal accumulation of citric acid, and gene expression in C3-CAM intermediate phenotypes

Are cell wall traits a component of the succulent syndrome?

Succulence is an adaptation to low water availability characterised by the presence of water-storage tissues that alleviate water stress under low water availability. The succulent syndrome has evolved convergently in over 80 plant families and is associated with anatomical, physiological and biochemical traits. Despite the alleged importance of cell wall traits in drought responses, their significance in the succulent syndrome has long been overlooked. Here, by analyzing published pressure–volume curves, we show that elastic adjustment, whereby plants change cell wall elasticity, is uniquely beneficial to succulents for avoiding turgor loss. In addition, we used comprehensive microarray polymer profiling (CoMPP) to assess the biochemical composition of cell walls in leaves. Across phylogenetically diverse species, we uncover several differences in cell wall biochemistry between succulent and non-succulent leaves, pointing to the existence of a ‘succulent glycome’. We also highlight the glycomic diversity among succulent plants, with some glycomic features being restricted to certain succulent lineages. In conclusion, we suggest that cell wall biomechanics and biochemistry should be considered among the characteristic traits that make up the succulent syndrome