Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands

Abstract

Crassulacean acid metabolism (CAM) is a photosynthetic adaptation that facilitates the uptake of CO(2) at night and thereby optimizes the water-use efficiency of carbon assimilation in plants growing in arid habitats. A number of CAM species have been exploited agronomically in marginal habitats, displaying annual above-ground productivities comparable with those of the most water-use efficient C(3) or C(4) crops but with only 20% of the water required for cultivation. Such attributes highlight the potential of CAM plants for carbon sequestration and as feed stocks for bioenergy production on marginal and degraded lands. This review highlights the metabolic and morphological features of CAM that contribute towards high biomass production in water-limited environments. The temporal separation of carboxylation processes that underpins CAM provides flexibility for modulating carbon gain over the day and night, and poses fundamental questions in terms of circadian control of metabolism, growth, and productivity. The advantages conferred by a high water-storage capacitance, which translate into an ability to buffer fluctuations in environmental water availability, must be traded against diffusive (stomatal plus internal) constraints imposed by succulent CAM tissues on CO(2) supply to the cellular sites of carbon assimilation. The practicalities for maximizing CAM biomass and carbon sequestration need to be informed by underlying molecular, physiological, and ecological processes. Recent progress in developing genetic models for CAM are outlined and discussed in light of the need to achieve a systems-level understanding that spans the molecular controls over the pathway through to the agronomic performance of CAM and provision of ecosystem services on marginal lands.

Phosphorylation of Phosphoenolpyruvate Carboxylase Is Essential for Maximal and Sustained Dark CO2 Fixation and Core Circadian Clock Operation in the Obligate Crassulacean Acid Metabolism Species Kalanchoë fedtschenkoi

“…CO 2 fixation via Rubisco and older leaves developing nocturnal CO 2 fixation associated with increasing CAM (Jones, 1975;Borland et al, 2009;Dever et al, 2015;Hartwell et al, 2016). Using a multi-cuvette, gas switching, infrared gas analyzer system (described in detail in Dever et al, 2015), we investigated the 24 h pattern of CO 2 exchange for detached, full-CAM leaves (leaf pair 6 [LP6]) from rPPCK1-1, rPPCK1-3, and the wild type that had been entrained in 12-h-light/12-h-dark cycles (Figure 2).…”

“…It is particularly noteworthy for its high water-use efficiency (WUE) relative to C 3 and C 4 photosynthesis (Borland et al, 2009;Cushman et al, 2015). The functional genomics and evolutionary biology of CAM species has recently received a dramatic upsurge in interest due to the potential of CAM crops, such as agaves and opuntias, as water-wise sources of biomass for biofuels, platform chemicals, and food Yang et al, 2015).…”

“…Based on our currently incomplete understanding of the molecular-genetic blueprint for CAM (Hartwell et al, 2016), C 3 species are believed to possess ancestral copies of all of the genes required for CAM (Cushman and Bohnert, 1999;Aubry et al, 2011;Ming et al, 2015). In principle, for CAM to evolve from the C 3 ancestral state in a leaf succulent CAM species such as Kalanchoë fedtschenkoi, the corresponding metabolic enzymes, metabolite transporters, and their cognate regulatory proteins must increase in abundance in leaf mesophyll cells and come under tight temporal control such that certain metabolic steps are confined to the dark period, and others are confined to the light (Cushman and Bohnert, 1999;Borland et al, 2009;Abraham et al, 2016;Brilhaus et al, 2016;Hartwell et al, 2016). However, only limited work has been reported testing this principle using a genetic approach, which represents a powerful method for in planta functional testing of candidate CAM genes when combined with detailed characterization of CAM-associated phenotypes in the resulting transgenic lines (Hartwell et al, 2016;Dever et al, 2015).…”

“…Primary CO 2 fixation is catalyzed by phosphoenolpyruvate carboxylase (PPC), which converts PEP and HCO 3 2 to OAA and inorganic phosphate (Chollet et al, 1996). Malate dehydrogenase reduces OAA to malate, which is transported to and stored in the vacuole as malic acid (Borland et al, 2009). In the light, malate decarboxylation generates CO 2 that is refixed by Rubisco in the Calvin cycle, referred to as secondary CO 2 fixation.…”

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

“…The nocturnally accumulated malic acid is stored overnight in a central vacuole, and during the subsequent day malate is decarboxylated to release CO 2 at an elevated concentration for Rubisco in the chloroplast. The diel separation of carboxylases in CAM is accompanied by an inverse (compared with C 3 and C 4 photosynthesis-performing species) day/night pattern of stomatal closure/ opening that results in improved water-use efficiency (CO 2 fixed per unit water lost) that is up to sixfold higher than that of C 3 photosynthesis plants and up to threefold higher than that of C 4 photosynthesis plants under comparable conditions 2 .…”