The economic challenge of leaf gas exchange

Abstract

The exchange of water for carbon dioxide required for photosynthesis in the leaves of vascular plants couples the global terrestrial carbon and water cycles. It also acts as a selection pressure for the plant: on the one hand, gas exchange for photosynthesis is beneficial for survival and growth in a competitive environment, but the loss of too much water can lead to plant death. In this thesis, two aspects of leaf functioning in relation to gas exchange were investigated in terms of these selection pressures, to determine whether observed leaf functioning across species could be explained in terms of broad adaptive principles, based on the exchange of water and carbon (or the water-carbon economy). The two aspects were gas exchange dynamics under changing irradiance and the long-term coordination of photosynthesis, leaf water supply and gas exchange across species. Relations between steady-state and dynamic gas exchange in response to changes in irradiance were assessed across 15 species, encompassing ferns, gymnosperms and angiosperms. The aim was to determine whether angiosperms possessed innovations that could provide them with an adaptive advantage over earlier-diverging lineages in a dynamic light environment, or whether observed relations followed adaptive ecological trends to maximise light fleck use. There was no dynamic adaptive advantage of angiosperms, but instead observed durations of stomatal opening and closing followed that predicted to maximise light fleck use. However, adaptations allowing a less-conservative water-use strategy in angiosperms may have provided an adaptive advantage by allowing faster photosynthetic induction for a given stomatal opening speed. A consideration of the water-carbon economy was then used to explain the long-term coordination between the capacities of photosynthesis, leaf water supply and gas exchange across species. Through the development of an analytical optimal model, this coordination was shown to be consistent with the maximisation of leaf carbon gain, given carbon costs in the building and maintenance of the stomata, leaf water supply network and osmotic pressure required to support gas exchange. It also predicted turgor loss point to be independent of photosynthesis, and predicted trait trends qualitatively consistent with those expected under drier conditions. The relative cost of xylem was predicted to be significantly less than the costs of stomata and osmotic pressure and surprisingly close to an independent estimate based on the literature. A consideration of the impacts of gas exchange on photosynthesis naturally led to the question of how to calculate biochemical and stomatal limitations to photosynthesis, in particular during photosynthetic induction. Different methods to calculate limitations were compared, using the photosynthetic induction data collected earlier. A differential method that takes into account the time courses of stomatal and biochemical changes was the best method. If the time course is not known, a differential method is best if stomatal and biochemical changes between states are coordinated, while elimination methods are best if one limitation is more dominant. These results show that a consideration of selective pressures on the leaf in terms of water and carbon is powerful for predicting leaf gas exchange behaviour across species.