Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers.

Flowers are critical for angiosperm reproduction and the production of food, fiber, and pharmaceuticals, yet for unknown reasons, they appear particularly sensitive to combined heat and drought stress. A possible explanation for this may be the co-occurrence of leaky cuticles in flower petals and a vascular system that has a low capacity to supply water and is prone to failure under water stress. These characteristics may render reproductive structures more susceptible than leaves to runaway cavitation-an uncontrolled feedback cycle between rising water stress and declining water transport efficiency that can rapidly lead to lethal tissue desiccation. We provide modeling and empirical evidence to demonstrate that flower damage in the perennial crop pyrethrum (Tanacetum cinerariifolium), in the form of irreversible desiccation, corresponds with runaway cavitation in the flowering stem after a combination of heat and water stress. We show that tissue damage is linked to greater evaporative demand during high temperatures rather than direct thermal stress. High floral transpiration dramatically reduced the soil water deficit at which runaway cavitation was triggered in pyrethrum flowering stems. Identifying runaway cavitation as a mechanism leading to heat damage and reproductive losses in pyrethrum provides different avenues for process-based modeling to understand the impact of climate change on cultivated and natural plant systems. This framework allows future investigation of the relative susceptibility of diverse plant species to reproductive failure under hot and dry conditions.

Deadly acceleration in dehydration of Eucalyptus viminalis leaves coincides with high-order vein cavitation.

Xylem cavitation during drought is proposed as a major driver of canopy collapse, but the mechanistic link between hydraulic failure and leaf damage in trees is still uncertain. Here, we used the tree species manna gum (Eucalyptus viminalis) to explore the connection between xylem dysfunction and lethal desiccation in leaves. Cavitation damage to leaf xylem could theoretically trigger lethal desiccation of tissues by severing water supply under scenarios such as runaway xylem cavitation, or the local failure of terminal parts of the leaf vein network. To investigate the role of xylem failure in leaf death, we compared the timing of damage to the photosynthetic machinery (Fv/Fm decline) with changes in plant hydration and xylem cavitation during imposed water stress. The water potential at which Fv/Fm was observed to decline corresponded to the water potential marking a transition from slow to very rapid tissue dehydration. Both events also occurred simultaneously with the initiation of cavitation in leaf high-order veins (HOV, veins from the third order above) and the analytically derived point of leaf runaway hydraulic failure. The close synchrony between xylem dysfunction and the photosynthetic damage strongly points to water supply disruption as the trigger for desiccation of leaves in this hardy evergreen tree. These results indicate that runaway cavitation, possibly triggered by HOV network failure, is the tipping agent determining the vulnerability of E. viminalis leaves to damage during drought and suggest that HOV cavitation and runaway hydraulic failure may play a general role in determining canopy damage in plants.

Optimization can provide the fundamental link between leaf photosynthesis, gas exchange and water relations.

Tight coordination in the photosynthetic, gas exchange and water supply capacities of leaves is a globally conserved trend across land plants. Strong selective constraints on leaf carbon gain create the opportunity to use quantitative optimization theory to understand the connected evolution of leaf photosynthesis and water relations. We developed an analytical optimization model that maximizes the long-term rate of leaf carbon gain, given the carbon costs in building and maintaining stomata, leaf hydraulics and osmotic pressure. Our model demonstrates that selection for optimal gain should drive coordination between key photosynthetic, gas exchange and water relations traits. It also provides predictions of adaptation to drought and the relative costs of key leaf functional traits. Our results show that optimization in terms of carbon gain, given the carbon costs of physiological traits, successfully unites leaf photosynthesis and water relations and provides a quantitative framework to consider leaf functional evolution and adaptation.

Estimating stomatal and biochemical limitations during photosynthetic induction.

Understanding stomatal and biochemical components that limit photosynthesis under different conditions is important for both the targeted improvement of photosynthesis and the elucidation of how stomata and biochemistry affect plant performance in an ecological context. Limitation analyses have not yet been extensively applied to conditions of photosynthetic induction after an increase in irradiance. Moreover, few studies have systematically assessed how well various limitation analyses actually work. Here we build on two general ways of estimating limitations, one that sequentially removes the effect of a limitation (elimination) and one that uses a tangent plane approximation (differential), by including the ternary effect and boundary layer conductance so that they are consistent with gas exchange data. We apply them to the analysis of temporal and time-integrated limitations during photosynthetic induction, calculating limitations either independent of the time course (one-step) or make use of the entire time course (stepwise). We show that the stepwise differential method is the best method to use when time steps are small enough. We further show that the differential method predicts limitations near exact when the internal CO2 concentration stays constant. This last insight has important implications for the general use of limitation analyses beyond photosynthetic induction.

Plant water-use strategy mediates stomatal effects on the light induction of photosynthesis.

More efficient gas exchange strategies under dynamic light environments have been hypothesised to contribute to the dominance of angiosperms in the vascular plant flora. However, we still lack a clear understanding of how stomatal dynamics affect photosynthetic dynamics and whether differences exist between lineages. Stomatal and photosynthetic dynamics following changes in irradiance were studied in 15 species, encompassing ferns, gymnosperms and angiosperms. We determined the effect of stomatal speed on dynamic photosynthesis and water loss. Moreover, we assessed whether dynamic behaviour followed evolutionary lineage divisions, or whether ecological adaptation to maximise light fleck use could describe dynamic behaviour. We found that species with fast stomatal opening, such as ferns, forgo less photosynthesis during photosynthetic induction. By contrast, there was no relationship between stomatal closure speed and the water wasted by transiently more-open stomata, because species with higher rates of gas exchange also showed faster stomatal closure. Shade-adapted species possessed fast-opening but slow-closing stomata, consistent with ecological adaptation to maximise light fleck use. Our results suggest dynamic behaviour follows adaptive ecological trends more strongly than evolutionary ones, but angiosperms may benefit from relatively faster photosynthetic induction by adopting a less conservative water-use strategy.

Estimation of Photorespiratory Fluxes by Gas Exchange.

Photorespiratory fluxes can be easily estimated by photosynthetic gas exchange using an infrared gas analyzer and applying the Farquhar, von Caemmerer, and Berry (Farquhar et al. Planta 149:78-90, 1980) photosynthesis model. For a more direct measurement of photorespiratory CO2 release from glycine decarboxylation, infrared gas analysis can be coupled to membrane-inlet mass spectrometry, capable of separating the total CO2 concentration into its 12CO2 and 13CO2 components in a continuous online fashion. This chapter discusses how to calculate rates of photorespiration from Rubisco kinetics and describes in detail a method for measuring the CO2 release from glycine decarboxylation using 13CO2.

Stomatal dynamics are limited by leaf hydraulics in ferns and conifers: results from simultaneous measurements of liquid and vapour fluxes in leaves.

Stomatal responsiveness to vapour pressure deficit (VPD) results in continuous regulation of daytime gas-exchange directly influencing leaf water status and carbon gain. Current models can reasonably predict steady-state stomatal conductance (gs ) to changes in VPD but the gs dynamics between steady-states are poorly known. Here, we used a diverse sample of conifers and ferns to show that leaf hydraulic architecture, in particular leaf capacitance, has a major role in determining the gs response time to perturbations in VPD. By using simultaneous measurements of liquid and vapour fluxes into and out of leaves, the in situ fluctuations in leaf water balance were calculated and appeared to be closely tracked by changes in gs thus supporting a passive model of stomatal control. Indeed, good agreement was found between observed and predicted gs when using a hydropassive model based on hydraulic traits. We contend that a simple passive hydraulic control of stomata in response to changes in leaf water status provides for efficient stomatal responses to VPD in ferns and conifers, leading to closure rates as fast or faster than those seen in most angiosperms.