Water ascent in tall trees: does evolution of land plants rely on a highly metastable state?

Abstract

The Cohesion Theory considers plant xylem as a 'vulnerable pipeline' isolated from the osmotically connected tissue cells, phloem and mycorrhizas living in symbiosis with plant roots. It is believed that water is pulled exclusively by transpiration-induced negative pressure gradients of several megapascals through continuous water columns from the roots to the foliage. Water under such negative pressures is extremely unstable, particularly given the hydrophobicity of the inner xylem walls and sap composition (lipids, proteins, mucopolysaccharides, etc.) that prevents the development of stable negative pressures larger than about -1 MPa. However, many plant physiologists still view the Cohesion Theory as the absolute and universal truth because clever wording from the proponents of this theory has concealed the recent breakdown of the Scholander pressure bomb (and other indirect methods) as qualified tools for measuring negative pressures in transpiring plants. Here we show that the arguments of the proponents of the Cohesion Theory are completely misleading. We further present an enormous bulk of evidence supporting the view that - depending on the species and ecophysiological context - many other forces, additional to low tensions, can be involved in water ascent and that water can be lifted by a series of watergates (like ships in staircase locks). Contents I. Introduction 576 II. Can water sustain negative pressures? 577 III. Negative xylem pressures of several megapascals: fact or mystery? 579 IV. The continuity of the xylem water columns: fact or hypothesis? 588 V. The 'Multi-Force' or 'Watergate' Theory 590 VI. Conclusions 604 Acknowledgements 605 References 605 Appendix 1 612 Appendix 2 613.