Stomatal closure during water deficit is controlled by below-ground hydraulics.

BACKGROUND AND AIMS: Stomatal closure allows plants to promptly respond to water shortage. Although the coordination between stomatal regulation, leaf and xylem hydraulics has been extensively investigated, the impact of below-ground hydraulics on stomatal regulation remains unknown. METHODS: We used a novel root pressure chamber to measure, during soil drying, the relation between transpiration rate (E) and leaf xylem water pressure (ψleaf-x) in tomato shoots grafted onto two contrasting rootstocks, a long and a short one. In parallel, we also measured the E(ψleaf-x) relation without pressurization. A soil-plant hydraulic model was used to reproduce the measurements. We hypothesize that (1) stomata close when the E(ψleaf-x) relation becomes non-linear and (2) non-linearity occurs at higher soil water contents and lower transpiration rates in short-rooted plants. KEY RESULTS: The E(ψleaf-x) relation was linear in wet conditions and became non-linear as the soil dried. Changing below-ground traits (i.e. root system) significantly affected the E(ψleaf-x) relation during soil drying. Plants with shorter root systems required larger gradients in soil water pressure to sustain the same transpiration rate and exhibited an earlier non-linearity and stomatal closure. CONCLUSIONS: We conclude that, during soil drying, stomatal regulation is controlled by below-ground hydraulics in a predictable way. The model suggests that the loss of hydraulic conductivity occurred in soil. These results prove that stomatal regulation is intimately tied to root and soil hydraulic conductances.

Activation of the root xylem proton pump by hydraulic signals from leaves under suppressed transpiration.

Long term field observations have revealed that the inhibition of transpiration by heavy rainfall promotes immediate positive shift in the trans-root electric potential (TRP), indicating activation of the xylem proton pump in the tree root system presumably participating in acropetal water transport. This phenomenon is indicative of signal transmission from the aerial part to the root system via change in the xylem hydraulic pressure. To test this hypothesis, we constructed a new device that enables the simultaneous recording of artificially applied xylem hydraulic pressure and the change in the TRP of tree saplings. With the application of artificial pressure to the xylem vessels (20-62 kPa), TRP shifted towards positive potential by 20-80 mV, which indicates the activation of the proton pump in the root xylem. The reaction was observed in 11 tree species, six deciduous and five evergreen, although only during the resting phase of the xylem proton pump (May to October) when the transpiration rates were high. Contrastingly the application of tension (negative pressure) produced no reaction. Simultaneous determination of the two components of the TRP, i.e. Vps (electric membrane potential difference across root surface cell membrane) and Vpx (electric membrane potential difference between root symplast and xylem vessel), are performed using the intra-cellular micro-electrode technique throughout the four seasons. Application of excess xylem hydraulic pressure had no significant effect on Vps, while it brought about hyper-polarisation of Vpx except during the winter season, most significantly during summer when transpiration is vigorous and the xylem pump is in a resting state. Such effect of excess xylem pressure was, however, not observed under anoxia.

Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge.

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.

The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding.

Jasmonates are lipid mediators that control defence gene expression in response to wounding and other environmental stresses. These small molecules can accumulate at distances up to several cm from sites of damage and this is likely to involve cell-to-cell jasmonate transport.Also, and independently of jasmonate synthesis, transport and perception, different long distance wound signals that stimulate distal jasmonate synthesis are propagated at apparent speeds of several cm min­1 to tissues distal to wounds in a mechanism that involves clade 3 GLUTAMATE RECEPTOR-LIKE (GLR) genes. A search for jasmonate synthesis enzymes that might decode these signals revealed LOX6, a lipoxygenase that is necessary for much of the rapid accumulation of jasmonic acid at sites distal to wounds. Intriguingly, the LOX6 promoter is expressed in a distinct niche of cells that are adjacent to mature xylem vessels,a location that would make these contact cells sensitive to the release of xylem water column tension upon wounding. We propose a model in which rapid axial changes in xylem hydrostatic pressure caused by wounding travel through the vasculature and lead to slower,radially dispersed pressure changes that act in a clade 3 GLR-dependent mechanism to promote distal jasmonate synthesis.

Analysis of the Mechanisms Underlying the Specificity of the Variation Potential Induced by Different Stimuli.

Plants are able to perceive diverse environmental factors and form an appropriate systemic functional response. Systemic responses are induced by stimulus-specific long-distance signals that carry information about the stimulus. Variation potential is proposed as a candidate for the role of such a signal. Here, we focus on the mechanisms that determine the specificity of the variation potential under the action of different local stimuli. Local stimuli such as heating, burning and wounding cause variation potential, the parameters of which differ depending on the type of stimulus. It was found that the stimulus-specific features of the hydraulic signal monitored by changes in leaf thickness and variation potential, such as a greater amplitude upon heating and burning and a significant amplitude decrement upon burning and wounding, were similar. The main features of these signals are the greater amplitude upon heating and burning, and a significant amplitude decrement upon burning and wounding. Together with the temporal correspondence of signal propagation, this evidence indicates a role for the hydraulic signal in the induction of stimulus-specific variation potential. Experiments using mechanosensitive channel inhibitors have demonstrated that the hydraulic signal contributes more to the induction of the variation potential in the case of rapidly growing stimuli, such as burning and wounding, than in the case of gradual heating. For thermal stimuli (gradual heating and burning), a greater contribution, compared to wounding, of the chemical signal related to reactive oxygen species to the induction of the variation potential was demonstrated. Thus, the specificity of the parameters of the variation potential is determined by the different contributions of hydraulic and chemical signals.