While traditionally considered important mainly in hypoxic roots during flooding, upregulation of fermentation pathways in plants has recently been described as an evolutionarily conserved drought survival strategy, with acetate signaling mediating reprograming of transcription and cellular carbon and energy metabolism from roots to leaves. The amount of acetate produced directly correlates with survival through potential mechanisms including defense gene activation, biosynthesis of primary and secondary metabolites, and aerobic respiration. Here, we review root ethanolic fermentation responses to hypoxia during saturated soil conditions and summarize studies highlighting acetate fermentation under aerobic conditions coupled with respiration during growth and drought responses. Recent work is discussed demonstrating long-distance transport of acetate via the transpiration stream as a respiratory substrate. While maintenance and growth respiration are often modeled separately in terrestrial models, here we propose the concept of 'Defense Respiration' fueled by acetate fermentation in which upregulation of acetate fermentation contributes acetate substrate for alternative energy production via aerobic respiration, biosynthesis of primary and secondary metabolites, and the acetylation of proteins involved in defense gene regulation. Finally, we highlight new frontiers in leaf-atmosphere emission measurements as a potential way to study acetate fermentation responses of individual leaves, branches, ecosystems, and regions.

Leaf thermoregulation has been documented in a handful of studies, but the generality and origins of this pattern are unclear. We suggest that leaf thermoregulation is widespread in both space and time, and originates from the optimization of leaf traits to maximize leaf carbon gain across and within variable environments. Here we use global data for leaf temperatures, traits and photosynthesis to evaluate predictions from a novel theory of thermoregulation that synthesizes energy budget and carbon economics theories. Our results reveal that variation in leaf temperatures and physiological performance are tightly linked to leaf traits and carbon economics. The theory, parameterized with global averaged leaf traits and microclimate, predicts a moderate level of leaf thermoregulation across a broad air temperature gradient. These predictions are supported by independent data for diverse taxa spanning a global air temperature range of ∼60 °C. Moreover, our theory predicts that net carbon assimilation can be maximized by means of a trade-off between leaf thermal stability and photosynthetic stability. This prediction is supported by globally distributed data for leaf thermal and photosynthetic traits. Our results demonstrate that the temperatures of plant tissues, and not just air, are vital to developing more accurate Earth system models.

Climate change is expected to pose a global threat to forest health by intensifying extreme events like drought and insect attacks. Carbon allocation is a fundamental process that determines the adaptive responses of long-lived late-maturing organisms like trees to such stresses. However, our mechanistic understanding of how trees coordinate and set allocation priorities among different sinks (e.g., growth and storage) under severe source limitation remains limited. Using flux measurements, isotopic tracing, targeted metabolomics, and transcriptomics, we investigated how limitation of source supply influences sink activity, particularly growth and carbon storage, and their relative regulation in Norway spruce (Picea abies) clones. During photosynthetic deprivation, absolute rates of respiration, growth, and allocation to storage all decline. When trees approach neutral carbon balance, i.e., daytime net carbon gain equals nighttime carbon loss, genes encoding major enzymes of metabolic pathways remain relatively unaffected. However, under negative carbon balance, photosynthesis and growth are down-regulated while sucrose and starch biosynthesis pathways are up-regulated, indicating that trees prioritize carbon allocation to storage over growth. Moreover, trees under negative carbon balance actively increase the turnover rate of starch, lipids, and amino acids, most likely to support respiration and mitigate stress. Our study provides molecular evidence that trees faced with severe photosynthetic limitation strategically regulate storage allocation and consumption at the expense of growth. Understanding such allocation strategies is crucial for predicting how trees may respond to extreme events involving steep declines in photosynthesis, like severe drought, or defoliation by heat waves, late frost, or insect attack.

High temperatures alter the thermal sensitivities of numerous physiological and biochemical processes that impact tree growth and productivity. Foliar and root applications of methanol have been implicated in plant acclimation to high temperature via the C1 pathway. Here, we characterized temperature acclimation at 35 °C of leaf gas exchange, chlorophyll fluorescence, and extractable metabolites of potted Populus trichocarpa saplings and examined potential influences of mM concentrations of methanol added during soil watering over a two-month period. Relative to plants grown under the low growth temperature (LGT), high growth temperature (HGT) plants showed a suppression of leaf water use and carbon cycling including transpiration (E), net photosynthesis (Pn), an estimate of photorespiration (Rp), and dark respiration (Rd), attributed to reductions in stomatal conductance and direct negative effects on gas exchange and photosynthetic machinery. In contrast, HGT plants showed an upregulation of nonphotochemical quenching (NPQt), the optimum temperature for ETR, and leaf isoprene emissions at 40 °C. A large number of metabolites (867) were induced under HGT, many implicated in flavonoid biosynthesis highlighting a potentially protective role for these compounds. Methanol application did not significantly alter leaf gas exchange but slightly reduced the suppression of Rd and Rp by the high growth temperature while slightly impairing ETR, Fv′/Fm′, and qp. However, we were unable to determine if soil methanol was sufficiently taken up by the plant to have a direct effect on foliar processes. A small number of extracted leaf tissue metabolites (55 out of 10 015) showed significantly altered abundances under LGT and methanol treatments relative to water controls, and this increased in compound number (222) at the HGT. The results demonstrate the large physiological and biochemical impacts of high growth temperature on poplar seedlings and highlight the enhancement of the optimum temperature of ETR as a rapid thermal acclimation mechanism. Although no large effect on leaf physiology was observed, the results are consistent with methanol both impairing photochemistry of the light reactions via formaldehyde toxicity and stimulating photosynthesis and dark respiration through formate oxidation to CO2.

Abstract Rapid and broad-scale forest mortality associated with recent droughts, rising temperature, and insect outbreaks has been observed over western North America (NA). Climate models project additional future warming and increasing drought and water stress for this region. To assess future potential changes in vegetation distributions in western NA, the Community Earth System Model (CESM) coupled with its Dynamic Global Vegetation Model (DGVM) was used under the future A2 emissions scenario. To better span uncertainties in future climate, eight sea surface temperature (SST) projections provided by phase 3 of the Coupled Model Intercomparison Project (CMIP3) were employed as boundary conditions. There is a broad consensus among the simulations, despite differences in the simulated climate trajectories across the ensemble, that about half of the needleleaf evergreen tree coverage (from 24% to 11%) will disappear, coincident with a 14% (from 11% to 25%) increase in shrubs and grasses by the end of the twenty-first century in western NA, with most of the change occurring over the latter half of the twenty-first century. The net impact is a ~6 GtC or about 50% decrease in projected ecosystem carbon storage in this region. The findings suggest a potential for a widespread shift from tree-dominated landscapes to shrub and grass-dominated landscapes in western NA because of future warming and consequent increases in water deficits. These results highlight the need for improved process-based understanding of vegetation dynamics, particularly including mortality and the subsequent incorporation of these mechanisms into earth system models to better quantify the vulnerability of western NA forests under climate change.

Leaf respiration in the dark (Rdark) and light (Rday) is poorly characterized in diverse tropical ecosystems, and little to no information exists on the degree of light suppression in common tree species within the Amazon basin, and their dependences upon plant functional traits and position within the canopy. We quantified Rdark and apparent Rday using the Kok method and measured key leaf traits in 26 tree individuals of different species distributed in three different canopy positions: canopy, lower canopy, and understory. To explore the relationships between the leaf traits we used the standardized major axis (SMA). We found that canopy trees had significantly higher rates of Rdark and Rday than trees in the understory. The difference between Rdark and Rday (the light suppression of respiration) was greatest in the understory (68 ± 9%, 95% CI) and lower canopy (49 ± 9%, 95% CI) when compared to the canopy (37 ± 10%, 95% CI). We also found that Rday was significantly and strongly correlated with Rdark (p < 0.001) for all the canopy positions. Also, leaf mass per area (LMA) and leaf Phosphorus concentration (P) had a significant relationship with Rdark (p < 0.001; p = 0.003), respectively. In addition, a significant relationship was found for LMA in the canopy and lower canopy positions (p = 0.009; p = 0.048) while P was only significant in the canopy (p = 0.044). Finally, no significant relationship was found between Rdark and nitrogen, sugars, and starch. Our results highlight the importance of including representation of the light suppression of leaf respiration in terrestrial biosphere models and also of accounting for vertical gradients within forest canopies and connections with functional traits.