Global climate changes are expected to intensify drought-events in the near future causing plant death across natural ecosystems. One cause of tree mortality is xylem hydraulic failure due to formation of embolism (air-filled conduits).
Trees have evolved several mechanisms to mitigate the loss of water transport capacity and many species seem to counter embolism with a fast recovery after rainfalls. This process requires that empty vessels fill with water against existing energy gradients, as the bulk of water in xylem may remain under low tension. Thus, recovery cannot happen spontaneously and physiological activity of parenchyma cells is necessary to generate the osmotic gradient needed to force water influx into the void vessels.
The xylem of poplar trees was previously shown to respond to embolism by accumulating carbohydrates in the apoplast and dropping xylem sap pH, thus revealing specific changes in parenchyma cell activity in response to stress. We hypothesized that sap acidification is one of the symptom/signal of severe water stress in trees and that the resulting accumulation of sugars can prime stems for embolism recovery when stress is relieved.
Dynamics of plant responses to recovery from drought-induced loss of hydraulic capacity were monitored through physiological, transcriptional and chemical analyses.
Results/Conclusions
To test our hypothesis, we followed in vivo changes of apoplastic pH in trees exposed to drought. Severely stressed poplars showed a drop of xylem sap pH, stomata closure and an increase in abscisic acid (ABA) content. Moreover, we proved, in vitro and in vivo, that in a lower pH environment, the xylem apoplast continuously accumulates carbohydrates mostly in form of glucose and fructose. Therefore, we suggest that drop in pH stimulates the activity of acidic cell wall invertases responsible for the splitting of sucrose into monosaccharides, thus inducing sucrose efflux by lowering its apoplastic concentration. Moreover, treatments with vanadate and ATP assay suggest that drop of pH is countered by inward rectifying proton pump activity.
After recovery from severe water stress, poplars showed high stomatal conductance, low ABA content and an increase of apoplastic pH. In this higher pH environment, sugar accumulation was significantly reduced and sucrose was the primary component. We thus propose that, as soon as transpiration is restored, new water would be delivered from roots and cellular stress reaction would be ‘triggered off’ by washing away sugars and changing xylem pH to more neutral values.