The role of pores for water transport in plants

Water transport in plants is tightly associated with growth, primary productivity, plant performance, and various physiological processes in plants, such as transport of photosynthetic products. In most cases, water is transported from the roots to the leaves, driven by the phase change of liquid water to water vapour near tiny openings (stomata) in leaves. Foliar water uptake, however, has also been reported in many species, and may well be more common than previously thought. The amount of water transpired by plants, which varies from very small amounts to hundreds of liters on a daily basis, depends strongly on environmental conditions, access to soil water, the plant species, and its size. Despite the global importance of plant transpiration in hydrological cycles, and its major consequences for the functioning of our biosphere, hydrology, and agriculture, our understanding about the actual mechanisms behind water transport remain incompletely understood (Jansen and Schenk, 2015). It remains indeed a longstanding question in biology how plants are able to transport water under negative pressure without continuously developing large gas bubbles in their transport system that reduce the transport capacity. In fact, engineers are unable to mimic water transport under negative pressure in a similar way as plants do, especially without using pure and completely degassed water.

A good grasp of plant anatomy combined with physics of porous media and chemistry is needed to understand the multiphase interactions between water, gas, plant tissues and cells. Capillarity, cohesion, adhesion, and, in case of very tall trees, gravity represent the major forces that are able to hold up continuous columns of water across many plant organs and thousands of cells, well above the atmospheric pressure limit of ca. 10.33 m. The xylem tissue represents about 99% of the entire distance of the hydraulic pathway from the roots to the leaves, and is characterised by apoplastic transport through tracheary elements (including multicellular vessel elements, and unicellular, imperforate tracheids), which are dead when functional (see Fig. 1 for a conceptual picture). The remaining 1%, however, includes both apoplastic transport and symplastic barriers, such as plasmodesmata and aquaporins, which may provide some control over the transport efficiency (Tyree and Zimmermann, 2002). 

The pore dimensions encountered by water molecules from the xylem tissue in roots to the minor leaf veins include macroporous conduits, which vary in diameter from a few µm to > 500 µm, and have a length from several mm to several m. Cell walls of water conducting cells, which are lignified and typically a few µm thick, show pores < 2 nm, and provide considerable resistance to transport of water and gas. However, there are also mesoporous media with pores < 50 nm between neighbouring cell walls, which provide important pathways due to the finite length of conduits. Hence, water has to cross thousands of cell walls from root xylem to the tiny veins in leaves, which is typically reflected in a water potential gradient in transpiring plants. These mesoporous media occur where no secondary wall is deposited, represent modified primary cell walls, and are mainly composed of cellulose fibrillar aggregates (Kaack et al., 2019, 2021). They function as important safety valves to avoid fast propagation of large air-bubbles (embolism), but at the same time are the main openings for an efficient, relatively fast transport of sap, with sap flow from ca. 1 to 40 meters per hour. Gas cannot be excluded from the system, and xylem sap is found to be saturated or even oversaturated with dissolved gas. Moreover, xylem sap was recently found to include insoluble, amphiphilic lipids (mainly phospholipids and galactolipids), which likely originate from cytoplasmic remnants, and have a potent surface activity in sap. 

Open questions in understanding water transport in plants include the exact mechanisms associated with the formation of large gas bubbles (embolism), which are known to be induced under severe drought and freeze-thawing cycles. A major challenge is to understand how gas-water-solid interfaces behave under negative pressure, with a dynamic surface tension, and possibly local pressure differences. There is solid experimental evidence that embolism largely spreads from an embolised, gas-filled conduit to a neighbouring, sap-filled conduit under negative pressure, but we do not know the exact mechanisms that trigger a sap-filled conduit to become embolised. More research on gas diffusion across cell walls, and the functional role of xylem sap lipids appear to be promising avenues that may shed novel light on water transport in plants, which remains a longstanding question in biology.

Figure 1: Water transport in a tree includes sap movement across various types of porous media. The process is driven by transpiration at the leaf level, along a xylem water potential gradient, with capillarity, adhesion, cohesion, and gravity representing the major forces. A: transverse section through a root. After entering via root hairs, water crosses symplastically or apoplastically the cortex (C), the largely impermeable endodermis (E), and then reaches conduits in the xylem tissue (X). B. Transverse section through wood, showing water transport (red arrows) across adjacent cell walls. C. Section through a leaf, showing the hydraulic pathway from a small vein (1), with an apoplastic pathway across mesophyll cells to a substomatal cavity (2), where a phase change from liquid to gas phase may occur, and water vapour leaves the leaf tissue via a stoma (3).