Discrimination Processes and Shifts in Carboxylation during the Phases of Crassulacean Acid Metabolism

Abstract

The magnitude and extent of Crassulacean acid metabolism (CAM) activity in two Clusia species was manipulated to investigate the regulation of the distinct CAM phases. First, in response to leaf-air vapor pressure deficit at night, changes in leaf conductance altered on-line carbon-isotope discrimination throughout the theoretical range for dark CO, uptake during CAM. These ranged from the limit set by phosphoenolpyruvate carboxylase (PEPc) (-6%0, 613C equivalent of -2%0) to that imposed by diffusion limitation (+4%0, 613C equivalent of -1 2%0), but the lowest carbon-isotope discrimination occurred when pJpa was only 0.7. Second, when the availability of external or internal sources of CO, was reduced for both field-and greenhouse-grown plants, CO, uptake by day via PEPc during phase I1 largely compensated. Third, by reducing the dark period, plants accumulated low levels of acidity, and CO, uptake occurred throughout the subsequent light period. Discrimination switched from being dominated by PEPc (phase II) to ribulose 1,s-bisphosphate carboxylase/oxygenase (phase III), with both enzymes active during phase IV. Under natural conditions, photochemical stability is maintained by extended PEPc activity in phase II, which enhances acid accumulation and delays decarboxylation until temperature and light stress are maximal at midday.

Modulation of Rubisco Activity during the Diurnal Phases of the Crassulacean Acid Metabolism Plant Kalanchoëdaigremontiana

“…Toward the end of the day the Rubisco carbamylation state remained relatively high compared with early phase II as the apparent activation state of PEPC increased. Therefore, there is an increased possibility for futile cycling through C 3 and C 4 carboxylation during this period, in agreement with earlier observations based on gas exchange and on-line carbon isotope discrimination (Osmond et al, 1996;Borland and Griffiths, 1997).…”

“…Exceptionally high PPFD tends to obfuscate those diurnal changes in ETR and nonphotochemical quenching that were central to our observations. High rates of gas exchange coupled to low Rubisco and high PEPC activities suggest that PEPC-mediated atmospheric CO 2 uptake was maintained for at least the first hour of the photoperiod, as confirmed by earlier studies using on-line carbon isotope discrimination (Borland et al, 1993;Roberts et al, 1997). Carbamylation increased during phase II as apparent PEPC activity declined to a minimum, suggesting a tight co-regulation of both carboxylase enzymes, with a reduced likelihood that Rubisco and PEPC compete for CO 2 during the early morning.…”

“…During the early morning, phase II marks the transition from C 4 to C 3 carboxylation and may be accompanied by considerable net atmospheric CO 2 uptake. Recently, it has been demonstrated in some species that PEPC activity may remain active for 3 to 4 h during phase II (Borland et al, 1993;Roberts et al, 1997), with the carbon fixed accounting for a considerable proportion of the net daily carbon gain Griffiths, 1996, 1997). Decarboxylation of malic acid and re-fixation of CO 2 by Rubisco occurs behind closed stomata during phase III.…”

Induction of Crassulacean acid metabolism by water limitation

“…Instantaneous measurements of carbon isotope discrimination during leaf gas exchange provide a noninvasive assessment of the relative fluxes of carbon through the C 3 and C 4 pathways throughout the day/night cycle. Under natural conditions, this approach has illustrated for C. minor how shifts in C 3 and C 4 carboxylation occur on a daily basis in response to changes in environmental parameters such as water availability and PFD (Roberts et al 1997). Moreover, in a number of facultative Clusia species, PEPC activity is not confined to the dark period and can substantially supplement daytime C 3 photosynthesis, as shown under laboratory-based manipulations and field conditions (Borland & Griffiths 1997).…”

Evolution along the crassulacean acid metabolism continuum

“…leaves and stems), although the extent of gas exchange and nocturnal acidification might be modulated by prevailing environmental conditions (Griffiths 1988 (Winter 1985;Griffiths 1988;Winter et al 2008). The expression of CAM in such C 3 -CAM species varies dynamically with experimentally manipulated conditions, such as photoperiod (Brulfert and Queiroz 1982), water status, light, temperature, nutritional status, salinity, anoxia, or atmospheric CO 2 concentration (Winter 1985;Lüttge 1987;Griffiths 1988;Roberts et al 1997). The common ice plant, Mesembryanthemum crystallinum L., a member of the Aizoaceae, is a well studied example of inducible CAM under strict environmental control (Winter 1985;Winter and Holtum 2007;Cushman et al 2008aCushman et al , 2008b.…”