Is crassulacean acid metabolism activity in sympatric species of hemi-epiphytic stranglers such as Clusia related to carbon cycling as a photoprotective process?

Abstract

A comparison of carbon isotope discrimination characteristics, crassulacean acid metabolism (CAM) activity and gas exchange together with concurrent analysis of photosystem II (PSII) chlorophyll fluorescence was conducted on leaves of sympatric species of Clusia from the restinga of Barra de Maricá, Brazil. The carbon isotope discrimination (Δ) and leaf-sap titratable acidity for leaves collected in the field indicated that the carbon metabolism of one species, C. lanceolata, was predominantly C3-like, and a second, C. fluminensis, constitutive CAM. When well-watered under glasshouse conditions C. lanceolata displayed a gas exchange pattern expected of a C3 plant, where values of instantaneous discrimination (Δ) rose from 13.5% shortly after dawn to 21.9‰ at midday, suggesting that all CO₂ uptake was mediated solely by ribulose 1,5-bisphosphate carboxylase (RUBISCO). C. fluminensis showed a gas exchange pattern which clearly exhibited all four phases of CAM. Δ values during phase II ranged from -0.4‰ at dawn to 5.9‰ some 3 h later, indicating that C4 carboxylation dominated CO₂ uptake during the morning with an increasing contribution by RUBISCO, suggested by the 5‰ shift in Δ at this time. The dominance of phosphoenol-pyruvate carboxylase (PEPc) activity was also found during phase IV, and extended throughout the dark period (phase I) in C. fluminensis, such that values of Δ measured were negative (-5.0 to -0.4‰). This is the first time that negative Δ values have been reported, close to those predicted theoretically for PEPc activity. The day-time uptake of CO₂ mediated by PEPc could lead to futile cycling through RUBISCO. In C. fluminensis organic acids were subjected to carbon turnover between PEPc and RUBISCO during phase II of CAM, serving perhaps to dissipate ATP and reductant at a time when excess photons are absorbed. Under low levels of photosynthetically active radiation (PAR) the two species displayed similar chlorophyll fluorescence characteristics, although for the CAM C. fluminensis a lower rate of decarboxylation of acids in the afternoon was reflected in changed quenching capacity. Under high PAR both species responded directly to changes in incident radiation, reflected by decreases in photon use efficiency (ΦPSII) and the intrinsic photochemical efficiency (F _V/F _M), together with high and reversible quenching of excess light by the means of radiationless or thermal dissipation (q _N). Both species, with such markedly different carboxylation characteristics achieve similar rates of electron transport and maintain photosynthetic integrity. Under field conditions, however the severity of a prolonged dry season caused the CAM species to become deciduous, whereas the "C3-like" species remained healthy. This suggests that the widely expected advantages of CAM do not extend to tolerance of extreme environmental conditions, in contrast to the more C3-like of these sympatric species.

Keywords: C. fluminensis; Carbon isotope discrimination (Δ); Clusia lanceolata; PEPc; RUBISCO.