When a man-made hydraulic system needs repair, the system has to be shut down by relieving the pressure that drives flow in the system. In plants, hydraulic failure is caused by formation of embolisms in xylem conduits. It has been known for some time that plants can repair embolisms even while their hydraulic systems are under considerable negative pressure, but the underlying mechanisms have remained one of the most puzzling mysteries of plant science, prompting Holbrook and Zwieniecki in 1999 to pose the question whether we might need a miracle to explain it. We propose that the new paradigm needed to solve the problem is to ask how air exits the embolized conduit rather than asking first how the conduit is refilled with water. The objective of this research was to test the hypothesis that angiosperm xylem operates as a liquid-gas membrane contactor and that air from embolized vessels diffuses through pit membranes into adjacent vessels, where it is carried away, dissolved in the transpiration stream. We further hypothesized that this process would be associated with nocturnal transpiration and take place under conditions of increasing, but below-atmospheric, xylem water potentials.
Results/Conclusions
Using the desert shrub Encelia farinosa as a model system, we found that (1.) embolism repair under negative pressure occurs usually at night while the stomata are open and while water potentials are below those potentially generated by root pressure, and (2.) that inhibition of nighttime transpiration by bagging of leaves inhibits embolism repair. These findings show that a transpiration stream is required for embolism repair under negative pressure. The hypothesis of air dissolution into the transpiration stream was tested successfully, first using a microporous hollow-fiber membrane contactor as an artificial model system, and then for branches of Encelia farinosa by determining air contents in embolized vessels before and after embolism repair, by measuring dissolved air contents in the xylem sap, and quantifying sap flow during the period of embolism repair. We hypothesize that vessel refilling from adjacent, living cells could be aided by air being pulled into the transpiration stream and that aquaporins may be involved in this process. The findings suggest that there may be a structural tradeoff between resistance to embolism formation and the ability to repair embolisms under negative pressure, and that hydraulic integration between vessels may be the key to both resistance and repair.
