A life of drought and flood in the canopy

Epiphytic orchids are one of the most species-rich and diverse groups of plants and they inhabit a wide range of niches, varying from almost constantly humid to seasonally dry habitats. Despite the abundance of orchid species occupying the canopy, the epiphytic habitat is the most severe niche in tropical forests because the availability of water and nutrients is sporadic and dependent on atmospheric sources. Survival and adaptive success of these plants rely largely on their flexible developmental and metabolic responses to environmental conditions. A high number of epiphytic species perform crassulacean acid metabolism (CAM) photosynthesis, an important ecophysiological adaptation that allows plants to reside in habitats with scarce, intermittent and/or seasonal water availability. The drought endurance observed in the majority of epiphytes is frequently provided by a stronger CAM photosynthetic behaviour that promotes maximum carbon gain combined with minimum water loss. This is feasible because CAM photosynthesis usually acts as a CO₂-concentrating mechanism through nocturnal CO₂ fixation by phosphoenolpyruvate carboxylase (PEPC) and subsequent vacuolar storage of the fixed CO₂ in the form of organic acids. The following daytime decarboxylation of organic acids releases CO₂, which is refixed by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and assimilated in the Calvin cycle behind closed stomata.

One essential structural adaptation of most epiphytic orchids against severe drought is a certain degree of tissue succulence, mainly by their leaves and pseudobulbs. Besides being an efficient way to store water and nutrients during the dry season, succulence is also suggested as an important requirement for CAM expression. A number of reports have indicated a positive correlation between leaf thickness and CAM activity in epiphytic orchids. Orchid leaves can show either CAM or C3 photosynthesis depending on the presence of thick and thin leaves. The higher leaf thickness of plants performing CAM is also related to an increased capacity to nocturnally store organic acids inside the vacuoles during the CAM cycle.

A recent paper in Annals of Botany sets out to discover whether distinct regimes of water availability influence the photosynthetic mode (C3 and/or CAM) in leaves and non-leaf organs of thick-leaved Cattleya walkeriana and thin-leaved Oncidium ‘Aloha’, and if so, how drought specifically affects the photosynthetic pathway in leaves of these species. The authors also investigate whether there is a particular degree of compartmentalization in CAM expression among different organs of such epiphytic orchids under either drought or well-watered treatments. They demonstrate that water availability is a powerful signal capable of modulating CAM expression in an organ/tissue-compartmented manner in the epiphytic orchids studied. The data highlights the importance of studying the range of CAM expression/modulation in specific plant tissues while taking into consideration the physiological responses under different environmental conditions and/or developmental phases.

Spatial patterns of photosynthesis in thin- and thick-leaved epiphytic orchids: unravelling C3–CAM plasticity in an organ-compartmented way. Annals of Botany (2013) 112 (1): 17-29. doi: 10.1093/aob/mct090
A positive correlation between tissue thickness and crassulacean acid metabolism (CAM) expression has been frequently suggested. Therefore, this study addressed the question of whether water availability modulates photosynthetic plasticity in different organs of two epiphytic orchids with distinct leaf thickness. Tissue morphology and photosynthetic mode (C3 and/or CAM) were examined in leaves, pseudobulbs and roots of a thick-leaved (Cattleya walkeriana) and a thin-leaved (Oncidium ‘Aloha’) epiphytic orchid. Morphological features were studied comparing the drought-induced physiological responses observed in each organ after 30 d of either drought or well-watered treatments. Cattleya walkeriana, which is considered a constitutive CAM orchid, displayed a clear drought-induced up-regulation of CAM in its thick leaves but not in its non-leaf organs (pseudobulbs and roots). The set of morphological traits of Cattleya leaves suggested the drought-inducible CAM up-regulation as a possible mechanism of increasing water-use efficiency and carbon economy. Conversely, although belonging to an orchid genus classically considered as performing C3 photosynthesis, Oncidium ‘Aloha’ under drought seemed to express facultative CAM in its roots and pseudobulbs but not in its leaves, indicating that such photosynthetic responses might compensate for the lack of capacity to perform CAM in its thin leaves. Morphological features of Oncidium leaves also indicated lower efficiency in preventing water and CO₂ losses, while aerenchyma ducts connecting pseudobulbs and leaves suggested a compartmentalized mechanism of nighttime carboxylation via phosphoenolpyruvate carboxylase (PEPC) (pseudobulbs) and daytime carboxylation via Rubisco (leaves) in drought-exposed Oncidium plants. Water availability modulated CAM expression in an organ-compartmented manner in both orchids studied. As distinct regions of the same orchid could perform different photosynthetic pathways and variable degrees of CAM expression depending on the water availability, more attention should be addressed to this in future studies concerning the abundance of CAM plants.