Plants require the capacity for quick and precise recognition of external stimuli within their environment for survival. Upon exposure to biotic (herbivores and pathogens) or abiotic stressors (environmental conditions), plants can activate hydraulic, chemical, or electrical long-distance signals to initiate systemic stress responses. A plant's stress reactions can be highly precise and orchestrated in response to different stressors or stress combinations. To date, an array of information is available on plant responses to single stressors. However, information on simultaneously occurring stresses that represent either multiple, within, or across abiotic and biotic stress types is nascent. Likewise, the crosstalk between hydraulic, chemical, and electrical signaling pathways and the importance of each individual signaling type requires further investigation in order to be fully understood. The overlapping presence and speed of the signals upon plant exposure to various stressors makes it challenging to identify the signal initiating plant systemic stress/defense responses. Furthermore, it is thought that systemic plant responses are not transmitted by a single pathway, but rather by a combination of signals enabling the transmission of information on the prevailing stressor(s) and its intensity. In this review, we summarize the mode of action of hydraulic, chemical, and electrical long-distance signals, discuss their importance in information transmission to biotic and abiotic stressors, and suggest future research directions.
Summary Signal coordination in response to changes in water availability remains unclear, as does the role of embolism events in signaling drought stress. Sunflowers were exposed to two drought treatments of varying intensity while simultaneously monitoring changes in stomatal conductance, acoustic emissions (AE), turgor pressure, surface‐level electrical potential, organ‐level water potential and leaf abscisic acid (ABA) concentration. Leaf, stem and root xylem vulnerability to embolism were measured with the single vessel injection technique. In both drought treatments, it was found that AE events and turgor changes preceded the onset of stomatal closure, whereas electrical surface potentials shifted concurrently with stomatal closure. Leaf‐level ABA concentration did not change until after stomata were closed. Roots and petioles were equally vulnerable to drought stress based on the single vessel injection technique. However, anatomical analysis of the xylem indicated that the increased AE events were not a result of xylem embolism formation. Additionally, roots and stems never reached a xylem pressure threshold that would initiate runaway embolism throughout the entire experiment. It is concluded that stomatal closure was not embolism‐driven, but, rather, that onset of stomatal closure was most closely correlated with the hydraulic signal from changes in leaf turgor.
Background Recent reports of extreme levels of undersaturation in the internal leaf air spaces have called into question one of the foundational assumptions of leaf gas exchange analysis, that leaf air spaces are effectively saturated with water vapor at leaf surface temperature. Historically, inferring the biophysical states controlling assimilation and transpiration from the fluxes directly measured by gas exchange systems has presented a number of challenges, including: 1) a mismatch in scales between the area of flux measurement, the biochemical cellular scale, and the meso-scale introduced by the localization of the fluxes to stomatal pores; 2) the inaccessibility of the internal states of CO2 and water vapor required to define conductances; and 3) uncertainties about the pathways these internal fluxes travel. In response, plant physiologists have adopted a set of simplifying assumptions that define phenomenological concepts such as stomatal and mesophyll conductances. Scope Investigators have long been concerned that a failure of basic assumptions could be distorting our understanding of these phenomenological conductances, and the biophysical states inside leaves. Here we review these assumptions and historical efforts to test them. We then explore whether artifacts in analysis arising from the averaging of fluxes over macroscopic leaf areas could provide alternative explanations for some part, if not all, of reported extreme states of undersaturation. Conclusions Spatial heterogeneities can, in some cases, create the appearance of undersaturation in the internal air spaces of leaves. Further refinement of experimental approaches will be required to separate undersaturation from the effects of spatial variations in fluxes or conductances. Novel combinations of current and emerging technologies hold promise for meeting this challenge.
The weather variations around the world are already having a profound impact on agricultural production. This impacts apple production and the quality of the product. Through agricultural precision, growers attempt to optimize both yield and fruit size and quality. Two experiments were conducted using field-grown “Gala” apple trees in Geneva, NY, USA, in 2021 and 2022. Mature apple trees (Malus × domestica Borkh. cv. Ultima “Gala”) grafted onto G.11 rootstock planted in 2015 were used for the experiment. Our goal was to establish a relationship between stem water potential (Ψtrunk), which was continuously measured using microtensiometers, and the growth rate of apple fruits, measured continuously using dendrometers throughout the growing season. The second objective was to develop thresholds for Ψtrunk to determine when to irrigate apple trees. The economic impacts of different irrigation regimes were evaluated. Three different water regimes were compared (full irrigation, rainfed and rain exclusion to induce water stress). Trees subjected the rain-exclusion treatment were not irrigated during the whole season, except in the spring (April and May; 126 mm in 2021 and 100 mm in 2022); that is, these trees did not receive water during June, July, August and half of September. Trees subjected to the rainfed treatment received only rainwater (515 mm in 2021 and 382 mm in 2022). The fully irrigated trees received rain but were also irrigated by drip irrigation (515 mm in 2021 and 565 mm in 2022). Moreover, all trees received the same amount of water out of season in autumn and winter (245 mm in 2021 and 283 mm in 2022). The microtensiometer sensors detected differences in Ψtrunk among our treatments over the entire growing season. In both years, experimental trees with the same trunk cross-section area (TCSA) were selected (23–25 cm−2 TCSA), and crop load was adjusted to 7 fruits·cm−2 TCSA in 2021 and 8.5 fruits·cm−2 TCSA in 2022. However, the irrigated trees showed the highest fruit growth rates and final fruit weight (157 g and 70 mm), followed by the rainfed only treatment (132 g and 66 mm), while the rain-exclusion treatment had the lowest fruit growth rate and final fruit size (107 g and 61 mm). The hourly fruit shrinking and swelling rate (mm·h−1) measured with dendrometers and the hourly Ψtrunk (bar) measured with microtensiometers were correlated. We developed a logistic model to correlate Ψtrunk and fruit growth rate (g·h−1), which suggested a critical value of −9.7 bars for Ψtrunk, above which there were no negative effects on fruit growth rate due to water stress in the relatively humid conditions of New York State. A support vector machine model and a multiple regression model were developed to predict daytime hourly Ψtrunk with radiation and VPD as input variables. Yield and fruit size were converted to crop value, which showed that managing water stress with irrigation during dry periods improved crop value in the humid climate of New York State.
The water status of the living tissue in leaves between the xylem and stomata (outside xylem zone - OXZ) play a critical role for plant function and global mass and energy balance but has remained largely inaccessible. We resolve the local water relations of OXZ tissue using a nanogel reporter of water potential (ψ), AquaDust, that enables an in-situ, non-destructive measurement of bothψof xylem and highly localizedψat the terminus of transpiration in the OXZ. Working in maize, these localized measurements reveal gradients in the OXZ that are several fold larger than those based on conventional methods, and values ofψin the mesophyll apoplast well below the macroscopic turgor loss potential. We find a strong loss of hydraulic conductance in both the bundle sheath and the mesophyll with decreasing xylem potential but not with evaporative demand. Our measurements suggest an active role played by the OXZ in regulating the transpiration path, and our methods provide novel means to study this phenomenon.
The xylem network, the water conduction system in wood determines the ability of trees to avoid hydraulic failure during drought stress. The capability to withstand embolisms, disruptions of the water column by gas bubbles that contribute to hydraulic failure, is mainly determined by the anatomical arrangement and connectedness (topology) of xylem vessels. However, the quantification of xylem network characteristics has been difficult, so that relating network properties and topology to hydraulic vulnerability and predicting xylem function remains challenging. We studied the xylem vessel networks of three diffuse- (Fagus sylvatica, Liriodendron tulipifera, Populus x canadensis) and three ring-porous (Carya ovata, Fraxinus pennsylvatica, Quercus montana) tree species using volumetric images of xylem from laser ablation tomography (LATscan). Using convolutional neural networks for image segmentation, we generated three-dimensional, high-resolution maps of xylem vessels, with detailed measurements of morphology and topology. We studied the network topologies by incorporating multiple network metrics into a multidimensional analysis and simulated the robustness of these networks against the loss of individual vessel elements that mimic the obstruction of water flow from embolisms. This analysis suggested that networks in Populus x canadensis and Carya ovata are quite similar despite being different wood types. Similar networks had comparable experimental measurements of P50 values (pressure inducing 50% hydraulic conductivity loss) obtained from hydraulic vulnerability curves, a common tool to quantify the cavitation resistance of xylem networks. This work produced novel data on plant xylem vessel networks and introduces new methods for analyzing the biological impact of these network structures.
The relationship between root, stem, and leaf hydraulic status and stomatal conductance during drought (Field capacities: 100-25%) and drought recovery was studied in Helianthus annuus, and five tree species (Populus x canadensis, Acer saccharum, A. saccharinum, Picea glauca, and Tsuga canadensis). Measurements of stomatal conductance (gs), organ water potential and vessel embolism were performed and the following was observed: 1. Cavitation only occurred in the petioles and not the roots or stems of tree species regardless of drought stress; 2. In contrast, all H. annuus organs exhibited cavitation to an increasing degree from root to petiole; and 3. All species initiated stomatal closure before cavitation events occurred or expected turgor loss point was reached. After rewatering: 1. Cavitated vessels in petioles of Acer species recovered whereas those of P. x canadensis did not and leaves were shed; 2. In H. annuus cavitated xylem vessels were refilled in roots and petioles, but not in stems; and 3. Despite refilled embolisms in petioles of some species during drought recovery, gs never returned to pre-drought conditions. Conclusions are drawn with respect to the hydraulic segmentation hypothesis for above and below-ground organs, and the timeline of embolism occurrence and repair is discussed.
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