Maciej Andrzej Zwieniecki

The evolution of plant hydraulics reflects a trade-off between efficiency and safety, between maximizing water transport while preventing embolism spread. Two major lineages achieved this balance differently: conifers and Gingko optimized safety through low resistance torus-margo pits, while angiosperms maximized hydraulic efficiency through long, wide vessels. It is therefore striking that no lineage evolved a “hybrid” design combining the efficiency of vessels with the low resistance of margo membranes with potential exception of Ephedraceae. Here we use a combination of experimental and theoretical approaches to show that the geometry of vessels inherently limits the pressure differentials required for torus-margo function.

Summary: Short‐term recovery from drought‐induced vessel embolism is an energy‐dependent biological process that requires a water source and solutes, both likely supplied by parenchyma cells. Despite fibers primarily providing structural support, their functional role as a reservoir of unbound water during and after stress remains unclear. In this study, Populus nigra plants were exposed to two drying regimes (slow and fast developing stress). At the end of the drought treatments and after stress relief, nondestructive structural observations were performed in vivo using synchrotron X‐ray microCT. Different drought progression rates did not affect the final extent of vessel embolism, but poplars subjected to slower drought development exhibited higher levels of air‐filled fibers. Following stress relief, faster hydraulic recovery was observed in plants exposed to rapid drought, which displayed lower occurrences of water‐depleted fibers. We suggest a novel functional role for xylem fibers during drought and recovery. We hypothesize that parenchyma cells can access water stored in completely mature fibers via pits, enhancing their survival during drought. Upon xylem tension relief, this stored water may be mobilized by living cells from fibers to vessels, facilitating the recovery of their transport function.

The global incidence of megafires is on the rise, leading to extensive areas being shrouded in dense smoke for prolonged periods, spanning days or weeks¹. Here, by integrating long-term regional observations of non-structural carbohydrate content in trees across California’s Central Valley with spatiotemporal satellite data, we present compelling evidence that dense smoke plumes negatively impact carbohydrate stores in three tree species: Prunus dulcis, Pistacia vera and Juglans regia. Our findings show that the presence of smoke causes a significant decrease in total non-structural carbohydrates, with reductions in the accumulation of both soluble sugar and starch reserves. This decline in carbohydrate levels persists through the trees’ dormancy period into the next season’s bloom, culminating in a reduced yield. Our results highlight a previously unrecognized wildfire threat that could affect plant health and ecosystem stability in both agricultural and natural environments.

Successful yield in orchards is the culmination of a series of events that start with plants entering dormancy with adequate energy reserves (non-structural carbohydrates; NSC). These NSC are responsible for the maintenance of activities during dormancy and extending onto the period of activeness. Using multi-year yield information and monthly NSC content in twigs, we show that high levels of carbohydrate in Prunus dulcis, Pistachio vera, and Juglans regia during the winter months are indeed associated with high yield, while high levels of the NSC in late summer often correlate with low yield. An evaluation of monthly NSC level importance on yield revealed that for P. dulcis high levels in February were a good predictor of yield and that low levels throughout summer were associated with high yield. In P. vera, high levels of NSC in December were best predictors of yield. J. regia exhibited peculiar patterns; while high pre-budbreak reserves were associated with high yields they only played a minor role in explaining crop, the most important months for predicting yields were June and July. Results suggest that NSC levels can serve as good predictors of orchard yield potential and should be monitored to inform orchard management.

Controlling fluid flow is a fundamental problem with applications from biomedicine to environmental engineering. Contemporary solutions combine electromechanical sensors, valves, and pumps; however, these are expensive and difficult to maintain. We report an autonomous flow control principle inspired by vascular transport in plants. Combining experiments on real and biomimetic tissues, we show that networks of cells linked by nonlinear valves permit the physical programming of a nearly arbitrary pressure drop versus flow rate relation. The nonlinearity is a consequence of fluid-structure interactions that allow a flexible element to selectively block the valve aperture. We report four applications: parallel connections that function as (i) a nonlinear flow controller, (ii) a constant flow controller, (iii) a reverse Ohm flow controller, and a serial connection that acts as (iv) a fluidic on-off switch.

Plants are frequently exposed to prolonged and intense drought events. To survive, species must implement strategies to overcome progressive drought while maintaining sufficient resources to sustain the recovery of functions. Our objective was to understand how stress rate development modulates energy reserves and affects the recovery process. Grenache Vitis vinifera cultivar was exposed to either fast‐developing drought (within few days; FDD), typical of pot experiments, or slow‐developing drought (few weeks, SDD), more typical for natural conditions. FDD was characterized by fast (2–3 days) stomatal closure in response to increased stress level, high abscisic acid (ABA) accumulation in xylem sap (>400 μg L⁻¹) without the substantial changes associated with stem priming for recovery (no accumulation of sugar or drop in xylem sap pH). In contrast, SDD was characterized by gradual stomatal closure, low ABA accumulation (−1) and changes that primed the stem for recovery (xylem sap acidification from 6 to 5.5 pH and sugar accumulation from 1 to 3 g L⁻¹). Despite FDD and SDD demonstrating similar trends over time in the recovery of stomatal conductance, they differed in their sensitivity to xylem ABA. Grenache showed near‐isohydric and near‐anisohydric behavior depending on the rate of drought progression, gauging the risk between hydraulic integrity and photosynthetic gain. The isohydry observed during FDD could potentially provide protection from large sudden swings in tension, while transitioning to anisohydry during SDD could prioritize the maintenance of photosynthetic activity over hydraulic security.

The green leaves of plants are optimized for carbon fixation and the production of sugars, which are used as central units of carbon and energy throughout the plant. However, there are physical limits to this optimization that remain insufficiently understood. Here, quantitative anatomical analysis combined with mathematical modeling and sugar transport rate measurements were employed to determine how effectively sugars are exported from the needle‐shaped leaves of conifers in relation to leaf length. Mathematical modeling indicated that phloem anatomy constrains sugar export in long needles. However, we identified two mechanisms by which this constraint is overcome, even in needles longer than 20 cm: i) the grouping of transport conduits, and ii) a shift in the diurnal rhythm of sugar metabolism and export in needle tips. The efficiency of sugar transport in the phloem can have a significant influence on leaf function. The constraints on sugar export described here for conifer needles are likely to also be relevant in other groups of plants, such as grasses and angiosperm trees.

Maintaining high rates of photosynthesis in leaves requires efficient movement of CO₂from the atmosphere to the mesophyll cells inside the leaf where CO₂is converted into sugar. CO₂diffusion inside the leaf depends directly on the structure of the mesophyll cells and their surrounding airspace, which have been difficult to characterize because of their inherently three-dimensional organization. Yet faster CO₂diffusion inside the leaf was probably critical in elevating rates of photosynthesis that occurred among angiosperm lineages. Here we characterize the three-dimensional surface area of the leaf mesophyll across vascular plants. We show that genome size determines the sizes and packing densities of cells in all leaf tissues and that smaller cells enable more mesophyll surface area to be packed into the leaf volume, facilitating higher CO₂diffusion. Measurements and modelling revealed that the spongy mesophyll layer better facilitates gaseous phase diffusion while the palisade mesophyll layer better facilitates liquid-phase diffusion. Our results demonstrate that genome downsizing among the angiosperms was critical to restructuring the entire pathway of CO₂diffusion into and through the leaf, maintaining high rates of CO₂supply to the leaf mesophyll despite declining atmospheric CO₂levels during the Cretaceous.

Summary: In drought‐stressed plants a coordinated cascade of chemical and transcriptional adjustments occurs at the same time as embolism formation. While these processes do not affect embolism formation during stress, they may prime stems for recovery during rehydration by modifying apoplast pH and increasing sugar concentration in the xylem sap. Here we show that in vivo treatments modifying apoplastic pH (stem infiltration with a pH buffer) or reducing stem metabolic activity (infiltration with sodium vanadate and sodium cyanide; plant exposure to carbon monoxide) can reduce sugar accumulation, thus disrupting or delaying the recovery process. Application of the vanadate treatment (NaVO_3, an inhibitor of many ATPases) completely halted recovery from drought‐induced embolism for up to 24 h after re‐irrigation, while partial recovery was observed in vivo in control plants using X‐ray microcomputed tomography. Our results suggest that stem hydraulic recovery in poplar is a biological, energy‐dependent process that coincides with accumulation of sugars in the apoplast during stress. Recovery and damage are spatially coordinated, with embolism formation occurring from the inside out and refilling from the outside in. The outside‐in pattern highlights the importance of xylem proximity to the sugars within the phloem to the embolism recovery process.