Diurnal changes in chlorophyll a fluorescence, CO2-exchange and organic acid decarboxylation in the tropical CAM tree Clusia hilariana

Abstract

Crassulacean acid metabolism (CAM) plants are dependent on the organic acids that accumulate overnight in the vacuoles as a source of CO2 during the daylight deacidification period, when stomata are closed and high irradiances generally prevail. We performed an integrative analysis of diurnal changes in gas exchange, chlorophyll fluorescence parameters and organic acid decarboxylation to understand the adjustments in photochemical and non-photochemical processes during the different CAM phases in Clusia hilariana Schlecht., a dominant tree species in the sandy coastal plains of southeastern Brazil. A linear relationship was obtained between the quantum yields of photochemical and non-photochemical quenching, irrespective of the CAM phase and prevailing irradiance. Degradation of malic and citric acids during the midday stomatal closure period could lead to potential CO2 fixation rates of 23 μmol m-2 s-1, whereas CO2 losses, measured as CO2 evolution, corresponded to about 3% of this value. Thus, decarboxylation of malate and citrate provided high internal CO2 concentrations during phase III of CAM, even though the stomata were closed, allowing optimal utilization of light energy, as indicated by the non-saturating electron transport rates (ETR) in the light response curves, with highest rates of ETR occurring at midday in the diurnal curves. At the transition from phase III to IV of CAM, depletion of internal CO2 sources and low stomatal conductances, which restricted the supply of exogenous CO2, reduced the demand for photochemical energy to drive carbon assimilation. This was compensated by increases in thermal energy dissipation as indicated by higher rates of non-photochemical quenching, while high irradiances still prevailed. Shifts in the CAM phases and changes in protective thermal dissipation potential allowed C. hilariana to match changes in PPFD patterns for leaves of different orientations. Evidence that most of the decline in photochemical efficiency was probably related to the fast-relaxing component of non-photochemical quenching is provided by the high values of the quantum yield of photosystem II after 20 min of relaxation in darkness, and an almost complete recovery after sunset. These adjustments in photosynthetic machinery minimized the danger of photo-inhibition in C. hilariana, which is commonly found in fully exposed habitats.