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.

Automated summary

Long-term field observations have shown that heavy rainfall inhibits transpiration and activates the xylem proton pump in tree root systems, resulting in a positive shift in the trans-root electric potential. A new device was constructed to test this hypothesis, and the results confirmed that artificial pressure applied to xylem vessels activates the proton pump. The reaction was observed in various tree species during the resting phase of the proton pump, but not under anoxia.