Crassulacean acid metabolism under severe light limitation: a matter of plasticity in the shadows?

Abstract

Despite the increased energetic costs of CAM compared with C(3) photosynthesis, it is hypothesized that the inherent photosynthetic plasticity of CAM allows successful acclimation to light-limiting conditions. The present work sought to determine if CAM presented any constraints to short and longer term acclimation to light limitation and to establish if and how metabolic and photosynthetic plasticity in the deployment of the four phases of CAM might facilitate acclimation to conditions of deep shade. Measurements of leaf gas exchange, organic acids, starch and soluble sugar (glucose, fructose, and sucrose) contents were made in the leaves of the constitutive CAM bromeliad Aechmea 'Maya' over a three month period under severe light limitation. A. 'Maya' was not particularly tolerant of severe light limitation in the short term. A complete absence of net CO(2) uptake and fluctuations in key metabolites (i.e. malate, starch or soluble sugars) indicated a dampened metabolism whilst cell death in the most photosynthetically active leaves was attributed to an over-acidification of the cytoplasm. However, in the longer term, plasticity in the use of the different phases of gas exchange and different storage carbohydrate pools, i.e. a switch from starch to sucrose as the major carbohydrate source, ensured a positive carbon balance for this CAM species under extremely low levels of irradiance. As such, co-ordinated plasticity in the use of C(3) and C(4) carboxylases and different carbohydrate pools together with an increase in the abundance of light-harvesting complexes, appear to underpin the adaptive radiation of the energetically costly CAM pathway within light-limiting environments such as wet cloud forests and shaded understoreys of tropical forests.

Effect of low irradiance on the photosynthetic performance and spiking of Phalaenopsis

“…For example, Aechmea 'Maya', an obligate CAM plant, significantly decreased PN, the concentrations of sucrose and starch, and the day-night fluctuations of starch and malic acid under severe irradiance limitation for 6 d (Ceusters et al 2011). In our experiment, lowering of irradiance also significantly reduced g s and delayed stomata opening ( Fig.…”

“…This mitigation of malate and citrate concentration changes also occurred in A. 'Maya' under severe irradiance limitation (approximately 15% of mean control daily integrated irradiance) for 6 d (Ceusters et al 2011) and in two Phalaenopsis-type orchids under low irradiance (approximately 15% of mean control irradiance) for 15 weeks (Wu et al 2013). Citrate and malate are important intermediates of the Krebs cycle that serves as the biochemical hub of the cell and closely relates with respiration capacity.…”

“…Lower irradiance decreases photosynthetic performance: Numerous studies showed that the photosynthetic rate significantly declined with shading, which resulted in a reduced content of total soluble carbohydrates and lesser fluctuation in the starch concentration (Souza et al 2004, Chang et al 2008, Ceusters et al 2011, Wu et al 2013. For example, Aechmea 'Maya', an obligate CAM plant, significantly decreased PN, the concentrations of sucrose and starch, and the day-night fluctuations of starch and malic acid under severe irradiance limitation for 6 d (Ceusters et al 2011).…”

CAM Photosynthesis in Bromeliads and Agaves: What Can We Learn from These Plants?

“…The extra CO 2 absorbed in those phases was used for the synthesis of hexoses that were not exported from the leaves. A later work on the same species showed that when these plants were transferred to low luminosity conditions, CAM was strongly dampened in the short term [107]. In fact, there is an acidification of the cytosol, which seems to be the result of an incapacity of the cells to degrade the malic acid formed during the previous night.…”

“…In fact, some Type III bromeliads have been intensively studied in terms of photosynthetic plasticity. For instance, Aechmea 'Maya', which is a cross between A. fasciata and A. tessmanii, expresses CAM photosynthesis and has been used as a model for analyzing the impacts of several environmental factors (e.g., light, nutrition, CO 2 availability) on the CAM behavior and carbohydrate partitioning [106][107][108]. Interestingly, when maintained under elevated concentrations of CO 2 , this species increased the CO 2 uptake during Phases II and IV, but the nocturnal uptake of CO 2 remained similar to control conditions [106].…”