A Quest for Mechanisms of Plant Root Exudation Brings New Results and Models, 300 Years after Hales

Abstract

The review summarizes some of our current knowledge on the phenomenon of exudation from the cut surface of detached roots with emphasis on results that were mostly established over the last fifty years. The phenomenon is quantitatively documented in the 18th century (by Hales in 1727). By the 19th century, theories mainly ascribed exudation to the secretion of living root cells. The 20th century favored the osmometer model of root exudation. Nevertheless, growing insights into the mechanisms of water transport and new or rediscovered observations stimulated the quest for a more adequate exudation model. The historical overview shows how understanding of exudation changed with time following experimental opportunities and novel ideas from different areas of knowledge. Later theories included cytoskeleton-dependent micro-pulsations of turgor in root cells to explain the observed water exudation. Recent progress in experimental biomedicine led to detailed study of channels and transporters for ion transport via cellular membranes and to the discovery of aquaporins. These universal molecular entities have been incorporated to the more complex models of water transport via plant roots. A new set of ideas and explanations was based on cellular osmoregulation by mechanosensitive ion channels. Thermodynamic calculations predicted the possibility of water transport against osmotic forces based on co-transport of water with ions via cation-chloride cotransporters. Recent observations of rhizodermis exudation, exudation of roots without an external aqueous medium, segments cut from roots, pulses of exudation, a phase shifting of water uptake and exudation, and of effects of physiologically active compounds (like ion channel blockers, metabolic agents, and cytoskeletal agents) will likely refine our understanding of the phenomenon. So far, it seems that more than one mechanism is responsible for root pressure and root exudation, processes which are important for refilling of embolized xylem vessels. However, recent advances in ion and water transport research at the molecular level suggest potential future directions to understanding of root exudation and new models awaiting experimental testing.

The Importance of Microorganisms for Sustainable Agriculture—A Review

“…Among several transporters involved in the secretion of exudates by roots are ABC (ATP-binding cassette) transporters which transport lipids and flavonoids [160], and anion channels are involved in secreting carbohydrates [161]. Moreover, for the secretion of root exudates transmembrane proteins aquaporins (AQPs) that are related to the membrane reflection coefficient and root hydraulic conductivity seem to be of great importance, as reviewed in [162]. Aquaporins are present in endogenous and exogenous membranes of eukaryotes and prokaryotes and are responsible for symplastic transport of not only water but also low molecular weight compounds and non-charged molecules including urea, glycerol, hydrogen peroxide, ammonium ions, and some elements, e.g., silicon and boron, as reviewed in [163].…”

An analytical complete model of root pressure generation: Theoretical bases for studying hydraulics of bamboo

“…Root pressure, first discovered by Stephen Hales in 1727, is the positive hydrostatic pressure developed in the roots of plants, causing exudation of sap from cut stems and/or guttation of water from leaves (Singh, 2016). Root pressure is assumed to be generated in combination by osmotically and energetically driven uphill transport of water across the plasma membrane of xylem parenchyma cells, possibly taking advantage of the free energy gradients of ions and sugars (Singh, 2016; Volkov & Schwenke, 2020; Wegner, 2014). So far, there is still no unanimous agreement about the mechanism of root pressure generation in plants (Singh, 2016; Volkov & Schwenke, 2020; Wegner, 2014; Zholkevich et al, 2007), albeit the concepts of ‘two‐compartments’, ‘three‐interphases’ (Pickard, 2003a, 2003b), ‘plant heart theory’ (Kundt & Gruber, 2006), ‘pushing water upward‐like mechanism’ (Singh et al, 2009) and ‘water cotransport theory’ (Wegner, 2014) were proposed to explain the generation of root pressure.…”

“…Root pressure is assumed to be generated in combination by osmotically and energetically driven uphill transport of water across the plasma membrane of xylem parenchyma cells, possibly taking advantage of the free energy gradients of ions and sugars (Singh, 2016; Volkov & Schwenke, 2020; Wegner, 2014). So far, there is still no unanimous agreement about the mechanism of root pressure generation in plants (Singh, 2016; Volkov & Schwenke, 2020; Wegner, 2014; Zholkevich et al, 2007), albeit the concepts of ‘two‐compartments’, ‘three‐interphases’ (Pickard, 2003a, 2003b), ‘plant heart theory’ (Kundt & Gruber, 2006), ‘pushing water upward‐like mechanism’ (Singh et al, 2009) and ‘water cotransport theory’ (Wegner, 2014) were proposed to explain the generation of root pressure. Typically, root pressure most likely occurs when soil water potentials are high and transpiration rates are low, especially at night or during rainstorms (Cochard et al, 1994; Taiz & Zeiger, 2010; Wegner, 2014).…”