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More than 200 years ago, Alexander von Humboldt described a tree of the genus Clusia for its ability to perform crassulacean acid metabolism (CAM). This drought-adaptive metabolism allows plants to maintain photosynthesis under water limitation by temporally separating CO₂ uptake and fixation. The diversity of CAM physiotypes has fueled a debate about evolutionary constraints and the feasibility of engineering CAM into C₃ crops. The genus Clusia displays an exceptional diversity of photosynthetic physiotypes, yet genome sequences and genomic mechanisms generating this diversity remain unresolved. Here, we sequence and compare the genomes of three Clusia species spanning weak, inducible, and strong CAM. We show that polyploidization followed by transposon-mediated genic diploidization could have shaped CAM-related gene families, particularly those controlling phosphoenol-pyruvate recycling via phosphorolytic leaf starch metabolism. Our results indicate that whole-genome duplication coupled to diploidization might have driven diversification of CAM physiotypes in Clusia , providing a genomic framework for understanding CAM diversity and evolution. Clusia species exhibit diverse photosynthetic physiotypes. The authors present genome assemblies for C. major (weak CAM), C. minor s.l. (facultative CAM), and C. rosea (strong CAM), and speculate that polyploidization and subsequent diploidization could have shaped the emergence of extant C3 + CAM physiotypes.

Chronologies of the shifts between photosynthetic modes are provided for a range of facultative CAM species. Combined with new sequencing technologies, facultative systems will contribute towards understanding the principles of CAM.

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.

Key messageRestricted access of light for stems reduced carbon acquisition there and limited the biomass growth of the roots.Light access can affect the microatmosphere within stems, creating favourable conditions for photosynthesis. We tested the hypothesis that stem photosynthesis modifies carbon allocation within plants and also can affect root growth. To verify this hypothesis, parts of Clusia minor L. stems were covered with dark material for 8 months to block light access to stems, and then, we compared morphological traits, biomass increment, photosynthetic activity and carbon isotopic signature (δ13C) in plants with dark- and light-exposed stems. Clusia minor stems were characterized by chlorophyll presence from pith to cortex, active photosystem II and 79% re-assimilation of respired CO2. We also revealed 24-h changes in the δ13C of carbohydrates exported from leaves. Keeping stems in darkness led to a significant lowering in root biomass and shoot-to-root weight index (Iw). Moreover, reductions in stem CO2 efflux and the δ13C in the roots and stems were also observed. Our results indicate that the lack of stem photosynthesis affects photosynthate flux to heterotrophic organs, such as roots, stems and probably expanding leaves.

It is the aim of this review to present a monographic survey of the neotropical genus Clusia on scaling levels from molecular phylogeny, metabolism, photosynthesis and autecological environmental responses to ecological amplitude and synecological habitat impact. Clusia is the only dicotyledonous genus with real trees performing crassulacean acid metabolism (CAM). By way of introduction, a brief historical reminiscence describes the discovery of CAM in Clusia and the consequent increase in interest in studying this particular genus of tropical shrubs and trees. The molecular phylogeny of CAM in the genus is compared with that in$Kalancho\\ddot{e}$and the Bromeliaceae. At the level of metabolism and photosynthesis, the great plasticity of expression of photosynthetic physiotypes, i.e. (i) C3photosynthesis, (ii) CAM including CAM idling, (iii) CAM cycling and (iv)$C_3/CAM-intermediate$behaviour, as well as metabolic flexibility in Clusia is illustrated. At the level of autecology, the factors water, irradiance and temperature, which control photosynthetic flexibility, are assessed. The phenotypic plasticity of physiotypes and morphotypes is described. At the level of synecology, the ecological amplitude of Clusia in the tropics and the relations to habitat are surveyed.

In some internal valleys of the northern Andes, precipitation at treeline elevation is seasonal, with one or two dry periods that could exert a strong control on tree seedling survival. However, little is known about (1) the severity of the dry periods, due to a lack of climate data, or (2) the effect of drought on tree seedling demographic dynamics and how this is modulated by local plant interactions in these tropical-alpine ecosystems. We studied annual precipitation variation and seedling demography and ecophysiology in relation to microclimate and neighboring plants in a dry treeline ecotone at 3100 m a.s.l in the Venezuelan Andes. We selected seedlings of the dominant tree species Cybianthus marginatus and Clusia multiflora at three sites, each with three adjacent 10 × 10-m plots within the forest, forest border, and páramo. For both species, seedling density was zero in the páramo and did not differ between border and forest. Growth rates were low for both species, but higher for Cybianthus in the border than in the forest. Survival rates were high in both environments. Low assimilation and transpiration rates were found in both species regardless of the environment. The spatial association of seedlings with moisture-regulating elements such as mosses, ferns and basal rosettes may indicate a benefit of better hydric conditions in their neighborhood. Our study shows a strong limitation for tree establishment in the páramo, but high rates of survival at the edge of the forest. This suggests a scenario of slow potential forest expansion at this tropical treeline, tree cover advancing in a closed front by the successive formation of forest-edge vegetation allowing tree seedling establishment outside of the forest.

Photon flux density (PFD) and water availability, the daily and seasonal factors that vary most in tropical environments, were examined to see how they influenced expression of crassulacean acid metabolism (CAM) in 3-year-old Clusia shrubs native to Panama. Instead of the commonly used single-leaf approach, diel CO2 exchange was measured for whole individual canopies of plants in large soil containers inside a naturally illuminated 8.8 m3 chamber. In well-watered C. rosea, a mainly constitutive CAM species, nocturnally fixed CO2 contributed about 50% to 24 h carbon gain on sunny days but the contribution decreased to zero following overcast days. Nonetheless, CO2 fixation in the light responded in such a way that 24 h carbon gain was largely conserved across the range of daily PFDs. The response of C. rosea to drought was similarly buffered. A facultative component of CAM expression led to reversible increases in nocturnal carbon gain that offset drought-induced reductions of CO2 fixation in the light. Clusia cylindrica was a C3 plant when well-watered but exhibited CAM when subjected to water stress. The induction of CAM was fully reversible upon rewatering. C. cylindrica joins C. pratensis as the most unambiguous facultative CAM species reported in the genus Clusia.

Tropical montane forests are threatened by uncontrolled fire events because of agricultural expansion. Consequently, deforested areas frequently are dominated by the bracken fern, Pteridium spp., for long periods, and forest regeneration is limited. Despite considerable research on bracken-dominated ecosystems, little is known about the relationship between bracken mycorrhizal fungi and tree seedlings. Arbuscular mycorrhizal fungi (AMF) form symbiotic relationships with terrestrial plants, providing nutrients and protection against pathogens and promoting seedling growth and establishment. Therefore, AMF inoculum have high potential for forest restoration programs. Here, we compare the species diversity of AMF spores, root colonization, and seedling growth of Clusia trochiformis 1 year after the addition of different liquefied root inocula: forest conspecific, forest heterospecific, and from Pteridium rhizomes. Thirteen morphospecies of arbuscular mycorrhizal fungi were identified on the roots of C. trochiformis, and Glomus spp. were the most abundant in all treatments. No differences were observed in spore species richness and diversity among treatments, but spore density was the highest subsequent to the Pteridium inoculum. There was no significant difference in mycorrhizal root colonization and seedling growth of C. trochiformis among inoculated treatments. We found a positive relation between root colonization and total biomass. This study shows that the AMF communities in bracken areas and forests present similar characteristics and that the bracken fern does not limit AMF inoculum potential, favouring seedling growth of Clusia.

Aiming to evaluate responses in terms of growth rates, physiological parameters, and degree of sensitivity to SO sub(2) and SPM sub(Fe) in Eugenia uniflora L. (Myrtaceae, a C sub(3) species) and Clusia hilariana Schlecht (Clusiaceae, a CAM species); saplings were exposed to emissions from a pelletizing factory for 7 months. The species were distributed along a transect (200, 500, 800, 1400, and 1700 m away from the emission source), and analyses were performed after 71, 118, and 211 days of exposure to the pollutants. E. uniflora received higher superficial deposition of particulate iron. The highest total iron foliar contents were observed 200 m away from the emission source in both plant species, while the highest total sulfur foliar contents were observed 200 m away in C. hilariana and 800 m away in E. uniflora. E. uniflora presented decreased values of height growth rate, number of necrotic leaves, chlorophyll analysis (SPAD index) and transpiration, in relation to the distances from the emission source. C. hilariana showed decreased values of height growth rate, number of leaves, number of necrotic leaves, total ionic permeability, stomatal conductance, transpiration, net CO sub(2) assimilation, and total dry matter, in relation to distances from the emission source. In relation to the days of exposure, both species presented increased number of necrotic leaves and foliar phytotoxicity index, and decreased values in the chlorophyll analysis. The two native plant species, both of which occur in the Brazilian Restinga, showed damage when exposed to emissions from an iron ore pelletizing factory. C. hilariana was considered the most sensitive species due to the decreased values in a higher number of variables after exposition.

In plants with crassulacean acid metabolism (CAM), dark CO2 uptake is mediated by phosphoenolpyruvate carboxylase (PEPC), an enzyme that can be regulated at transcriptional and posttranslational levels. Reversible phosphorylation of PEPC is catalyzed by a dedicated PEPC kinase, which in turn is regulated at the transcriptional level over the 24-h cycle in CAM plants. PEPC kinase controls the day/night regulation of PEPC during the CAM cycle, thus facilitating plasticity for optimizing CO2 uptake under different environmental conditions. To understand the importance of PEPC kinase in relation to its target PEPC in terms of CAM performance, the expression of the genes encoding the two enzymes was investigated in four species of Clusia that have photosynthetic patterns ranging from C3 photosynthesis to constitutive CAM. By linking changes in the expression of PEPC and PEPC kinase to day/night patterns of leaf gas exchange, organic acid, and soluble sugar contents under different environmental conditions, the genetic and metabolic limitations to CAM plasticity were assessed. The results indicate that PEPC expression is a major factor underpinning the genotypic capacity for CAM and that PEPC kinase expression does not appear to limit CAM. The day/night regulation of Ppck transcript abundance was found to be a consequence of CAM and the day/night cycling of associated metabolites, rather than the primary controlling factor for the temporal separation of carboxylation processes.