Johan Ceusters

The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world

SUMMARY The photosynthetic specialization of crassulacean acid metabolism (CAM) has evolved many times in response to selective pressures imposed by water limitation. Integration of circadian and metabolite control over nocturnal C₄ and daytime C₃ carboxylation processes in CAM plants provides plasticity for optimizing carbon gain and water use by extending or curtailing the period of net CO₂ uptake over any 24-h period. Photosynthetic plasticity underpins the ecological diversity of CAM species and contributes to the potential for high biomass production in water-limited habitats. Perceived evolutionary constraints on the dynamic range of CO₂ acquisition strategies in CAM species can be reconciled with functional anatomical requirements and the metabolic costs of maintaining the enzymatic machinery required for C₃ and C₄ carboxylation processes. Succulence is highlighted as a key trait for maximizing biomass productivity in water-limited habitats by serving to buffer water availability, by maximizing the magnitude of nocturnal CO₂ uptake and by extending the duration of C₄ carboxylation beyond the night period. Examples are discussed where an understanding of the diverse metabolic and ecological manifestations of CAM can be exploited for the sustainable productivity of economically and ecologically important species.

A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world

Crassulacean acid metabolism (CAM) is a specialized mode of photosynthesis that features nocturnal CO2 uptake, facilitates increased water-use efficiency (WUE), and enables CAM plants to inhabit water-limited environments such as semi-arid deserts or seasonally dry forests. Human population growth and global climate change now present challenges for agricultural production systems to increase food, feed, forage, fiber, and fuel production. One approach to meet these challenges is to increase reliance on CAM crops, such as Agave and Opuntia, for biomass production on semi-arid, abandoned, marginal, or degraded agricultural lands. Major research efforts are now underway to assess the productivity of CAM crop species and to harness the WUE of CAM by engineering this pathway into existing food, feed, and bioenergy crops. An improved understanding of CAM has potential for high returns on research investment. To exploit the potential of CAM crops and CAM bioengineering, it will be necessary to elucidate the evolution, genomic features, and regulatory mechanisms of CAM. Field trials and predictive models will be required to assess the productivity of CAM crops, while new synthetic biology approaches need to be developed for CAM engineering. Infrastructure will be needed for CAM model systems, field trials, mutant collections, and data management.

Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism

Summary Besides the acknowledged roles of red light, blue light is a key determinant for synchronizing the metabolic and physiological components of CAM over the day/night cycle.

Sedoheptulose accumulation under CO2 enrichment in leaves of Kalanchoë pinnata: a novel mechanism to enhance C and P homeostasis?

In contrast to the well-documented roles of its mono- and bisphosphate esters, the occurrence of free sedoheptulose in plant tissues remains a matter of conjecture. The present work sought to determine the origin of sedoheptulose formation in planta, as well as its physiological importance. Elevated CO2 and sucrose induction experiments were used to study sedoheptulose metabolism in the Crassulacean acid metabolism (CAM) plants Kalanchoë pinnata and Sedum spectabile. Experimental evidence suggested that sedoheptulose is produced from the oxidative pentose phosphate pathway intermediate sedoheptulose-7-phosphate, by a sedoheptulose-7-phosphate phosphatase. Carbon flux through this pathway was stimulated by increased triose-phosphate levels (elevated CO2, compromised sink availability, and sucrose incubation of source leaves) and attenuated by ADP and inorganic phosphate (Pi). The accumulation of free sedoheptulose is proposed to act as a mechanism contributing to both C and P homeostasis by serving as an alternative carbon store under elevated CO2 or a compromised sink capacity to avoid sucrose accumulation, depletion of inorganic phosphate, and suppression of photosynthesis. It remains to be established whether this acclimation-avoiding mechanism is confined to CAM plants, which might be especially vulnerable to Pi imbalances, or whether some C3 and C4 plants also dispose of the genetic capacity to induce and accelerate sedoheptulose synthesis upon CO2 elevation.

Drought adaptation in plants with crassulacean acid metabolism involves the flexible use of different storage carbohydrate pools

Nocturnal CO2 uptake in CAM plants is sustained by the degradation of storage carbohydrate which provides the acceptor (PEP) for the nocturnal carboxylase (PEPc). The investment of resources into a transient storage carbohydrate pool unavoidably places restriction on other metabolic activities including dark respiration, growth and acclimation to abiotic stress. In our recent report the flexible use of different storage carbohydrate pools is shown to be involved in the acclimation process to drought and recovery from dehydration. While starch breakdown stoichiometrically accounts for nocturnal CO2 uptake under well-watered conditions, the sucrose pool is maintained in preference to starch during progressing drought and sucrose becomes the major source of carbon fuelling the dark reactions after 45 days of water deprivation. Re-watering plants results in a recovery to the original situation, with starch constituting the main carbohydrate reserve for nocturnal provision of PEP. However, substantial amounts of starch are also retained in the leaves of re-watered plants by restricting export/respiration and thus provides a potential buffer capacity against a return to water deprivation. This significant conservation of starch suggests the ability to perceive, remember and anticipate the formerly encountered drought stress in some way, with the adaptation of the equilibrium of carbohydrate balance as a central factor underpinning the physiological homeostasis of CAM plants.

Glucuronoarabinoxylan structure in the walls of Aechmea leaf chlorenchyma cells is related to wall strength

In CAM-plants rising levels of malic acid in the early morning cause elevated turgor pressures in leaf chlorenchyma cells. Under specific conditions this process is lethal for sensitive plants resulting in chlorenchyma cell burst while other species can cope with these high pressures and do not show cell burst under comparable conditions. The non-cellulosic polysaccharide composition of chlorenchyma cell walls was investigated and compared in three cultivars of Aechmea with high sensitivity for chlorenchyma cell burst and three cultivars with low sensitivity. Chlorenchyma layers were cut from the leaf and the non-cellulosic carbohydrate fraction of the cell wall fraction was analyzed by gas-liquid chromatography. Glucuronoarabinoxylans (GAXs) were the major non-cellulosic polysaccharides in Aechmea. The fine structure of these GAXs was strongly related to chlorenchyma wall strength. Chlorenchyma cell walls from cultivars with low sensitivity to cell burst were characterized by an A/X ratio of ca. 0.13 while those from cultivars with high sensitivity showed an A/X ratio of ca. 0.23. Xylose chains from cultivars with high cell burst sensitivity were ca. 40% more substituted with arabinose compared to cultivars with low sensitivity for cell burst. The results indicate a relationship in vivo between glucuronoarabinoxylan fine structure and chlorenchyma cell wall strength in Aechmea. The evidence obtained supports the hypothesis that GAXs with low degrees of substitution cross-link cellulose microfibrils, while GAXs with high degrees of substitution do not. A lower degree of arabinose substitution on the xylose backbone implies stronger cell walls and the possibility of withstanding higher internal turgor pressures without cell bursting.

Impacts of Elevated CO2 on the Growth and Physiology of Plants with Crassulacean Acid Metabolism

The photosynthetic specialization of crassulacean acid metabolism (CAM) employs both Rubisco and phosphoenolpyruvate carboxylase (PEPC) for uptake of CO2 over the day and night. Temporal separation of the C3 and C4 carboxylases optimizes photosynthetic performance and carbon gain under water-limited environments. The water-conserving attributes of CAM has highlighted the potential of plants with this photosynthetic pathway as a means of carbon sequestration and biomass production on marginal lands. Sustainable agronomic and horticultural production of CAM species requires an understanding of how exposure to elevated atmospheric concentrations of CO2 will affect growth and productivity. In this review, the physiological responses of CAM plants to [CO2] elevation will be assessed in terms of net carbon gain, growth, anatomy, morphology, and water use efficiency. Photosynthetic responses to elevated [CO2] will be specifically discussed on a background of carbohydrate metabolism and partitioning toward the potentially competing sinks of nocturnal acid synthesis, respiration, and export for growth in CAM species.

Exploration of Sweet Immunity to Enhance Abiotic Stress Tolerance in Plants: Lessons from CAM

The concept of ‘sweet immunity’ or ‘sugar-enhanced defence’ is based on the accumulating evidence that sweet, endogenous saccharides might act as signalling molecules that are activated by exposure to stress and hence initiate signal amplification and lead to more rapid and robust activation of defence, immunity and stress tolerance. Sugars such as glucose, fructose and sucrose have acquired important regulatory functions in evolution and are becoming more and more recognized as signalling molecules in plants controlling gene expression related to plant metabolism, stress resistance and development. This offers opportunities for ‘sweet priming’, defined as a physiological process that prepares plants for a faster and/or stronger defence response to future stress conditions, but does not impose the costs associated with full implementation of an induced defence response. Future possibilities to substitute toxic agrochemicals with biodegradable sugar-(like) compounds in agricultural and horticultural practice requires a thorough understanding of how sugars can play a crucial role in perceiving, anticipating and counteracting abiotic stresses. In this review, the physiological responses of crassulacean acid metabolism (CAM) plants to different conditions of abiotic stress will be discussed with particular attention to sucrose dynamics. CAM plants are ideally suited to different abiotic stress conditions and carbohydrate cycling and availability are of paramount importance for plant growth, photosynthesis and homeostasis. By evaluating the plethora of effects sugars can exert on plant metabolism, growth and development the possibilities for sugars as potential priming agents to enhance abiotic stress tolerance will be explored.

Impact of developmental stage on CAM expression and growth in an Aechmea hybrid under greenhouse conditions

Summary Besides environmental factors, expression of crassulacean acid metabolism (CAM) and the related production of malic acid may depend on plant developmental stage. This topic has not yet been investigated under commercial greenhouse conditions. In CAM plant cultivation, malic acid is a central determinant of plant growth, but can also cause physiological leaf damage problems. Here, we present data on diurnal leaf malic acid contents, relative water content dynamics, and measurements of growth at four stages of the plant growth cycle (i.e., ex vitro-acclimated plantlets, 6-month, 12-month, and 18-month-old plants) of Aechmea ‘Maya’. The results obtained showed that Aechmea ‘Maya’ was an obligate CAM plant at all developmental stages during cultivation. Nevertheless, there was some developmental control on the expression of CAM. Under the same environmental conditions, 6-month-old plants accumulated significantly higher amounts of malic acid in their leaves, thus supporting higher growth rates, than in the other growth stages. This larger malic acid pool implied a higher risk of physiological leaf damage, but since remobilisation of malic acid in the early morning remained unaffected during growth, physiological leaf damage might occur throughout vegetative growth.

Impact of fertiliser level on plant growth, plant shape, and physiological leaf damage in two cultivars of Aechmea characterised by crassulacean acid metabolism.

Summary The efficacy of different fertiliser levels was evaluated in terms of plant growth, plant shape, and leaf quality. Experiments were conducted on two cultivars of Aechmea of known sensitivity (high and low, respectively) to physiological leaf damage. Plants were grown under two fertiliser levels (a fertigation solution of 1.2 mS cm−1, or a fertigation solution of 2.4 mS cm−1) over a 9-month treatment period. In general, the lower level of fertiliser resulted in more desirable, compact plants, with leaf length as the major parameter determining plant shape. The higher level of fertiliser improved the growth rate significantly, but also increased the risk of leaf quality problems. The extent of this effect was strongly cultivar-dependent. In practice, growers will have to compromise between plant shape and leaf quality on the one hand, and growth rate on the other. Based on this work, either of two plant-related parameters can be used to evaluate the risk of leaf quality problems when changing fertiliser levels: (i) chlorenchymal cell dimensions at the leaf anatomical level, or (ii) turgor pressure at the leaf physiological level.