In the autumn droughts when soils are powdery dry, when fires rage across the landscape, when the grasses have cured and the forbs have dried and blown away, and even deep-rooted trees and shrubs are drought stressed, Pisolithus sp. fruits in the most inhospitable dry soils, through cement sidewalk cracks and between rocky outcrops (Fig. 1). Fruiting of some of these mycorrhizal fungi poses one of the most intriguing questions in these drought-plagued regions. The new paper by Erik Lilleskov and his colleagues in this issue of New Phytologist (pp. 483–494) takes the step of demonstrating the importance of the complex transport of water from deep in the soil to the mycorrhizal sporocarps. Understanding the results presented in this paper, and the laboratory and field studies on hydraulic redistribution preceding it, underscores the dynamic and important complex structural elements that actually comprise the soil–fungal–plant interface.
‘... that Amanita muscaria may even parasitize the water of B. edulis is intriguing, only adding to the complexity of organism interactions occurring despite the drought conditions ...’
The summer of 2005 saw some of the most severe droughts ever recorded in Europe. Climate projections from the Intergovernmental Panel on Climate Change (IPCC) and other sources show increasing drought in southern Europe, the southwestern USA and northwestern Mexico, the Sahel, South Africa and Australia. Understanding drought stress responses by plants and their symbiotic partners, from the atmosphere into the bedrock, is the basis for the careful management of fire intensity, drought and marginal land production. Research on the plant–atmosphere interface of the soil–plant–atmosphere continuum (SPAC) has made major advancements over the past few decades to the point where predictions from satellite data are relatively accurate. Predictability breaks down, however, at the soil–plant interface. Much of the work remains based on irrigation technology, with a focus on saturated flows under high levels of soil water, and the work is often based on diffusion models and on laboratory-measured flow properties. However, in unsaturated soils, flow models become highly complex because of the microscale variation in soil pores and in solid materials, in dynamic roots and in even more dynamic microbes. Work on mycorrhizas, particularly over the past decade, has altered our understanding of the mechanisms whereby mycorrhizal fungi and their host plants exchange resources, and the complex array of ever-shifting water flux directions, flux rates and interdependencies (Allen, 2007). Stahl (1900) first postulated that water uptake is a major regulator of mycorrhizal functioning. Little did he anticipate how complex that process actually was! Mycorrhizal fungi not only cover the portion of the root where absorption of nutrients predominates, but create an extensive and dynamic mycelial network ranging far from the root tip and even into the bedrock.
Water moves in response to energy gradients. As soils fill with water as a result of rain or snowmelt, first small pores, and then large pores, fill, creating a high water content (θ). That water absorbs nutrients and salts, creating an energy difference from the comparatively pure rainwater. This difference in energy is called the osmotic potential (ψπ). Plants extract water from the soil at a rate equal to the transpiration from the leaves, first from the larger pores. As it is depleted, water in the pores forms a thin meniscus along the surface of the soil particles, organic micelles and soil organisms and is left in ever-smaller pores. As roots extract water from these pores, and the larger ones are depleted, gradients in water form between the filled pores and the emptied pores. The energy to extract that water bound to the soil particles is called the matric potential (ψm). These gradients are expressed in units of energy (mega-pascals, MPa) as the energy difference between two solutions on opposite sides of a membrane or between two locations. Water potential is a function of the concentration of solutes (ψπ), the adhesion to a surface (ψm) and gravity (ψg).
Water flow from soil to the leaves is also dependent upon adhesion between water molecules forming a hydraulic continuum from the soil pores through the plant and into the atmosphere (Fig. 2). Any break, or cavitation, can result in the death of the plant. In an irrigated cropland or mesic environment, water in the macropores (i.e. those > 80 µm) is extracted by roots and then replenished by irrigation or precipitation. However, in arid lands, that replenishment often occurs infrequently. Water retreats back to smaller pores (mesopores). Just as importantly, as soils dry to that of the wilting point (−1.5 MPa), roots shrink, creating air gaps between the root surface and the soil particles. Root hairs, if present, can penetrate the mesopores (down to 30 µm), but rarely smaller. In Mediterranean and semi-arid climates, the proportion of the growing season where soil dryness is lower than the wilting point can exceed 40% of the year, including most of the year when soil temperatures support growth. Thus, the portion of the growing season when the root surface is not directly in contact with soil water can be high. Mycorrhizal fungal hyphae bridge these air gaps, and rhizomorphs and individual hyphae radiate into the smaller soil pores, including micropores, with gaps of only a few mm3. This is one mechanism whereby mycorrhizas can increase water uptake from the surface soils (Allen, 2007). This remaining soil water becomes even more concentrated in solutes, including nitrogen (N) and phosphorus (P), and becomes inaccessible to roots; eventually even the hyphae should dry out. However, growth and metabolism continues in the many evergreen plants and their mycorrhizal fungi. The question is, how?
Tracking water movements has been aided by important technologies not available until recently. Dyes have become far more specific, and isotopic tracers facilitate the identification of important transport mechanisms. Just as importantly, the use of natural-abundance isotopes allows researchers to quantify transport rates in the field, not just to postulate mechanisms based on glasshouse chamber studies. However, these methods require extensive calibration of potential sources and modeling of differential fractionation to be carried out during the transport and transpiration process. Lighter isotopes (H and 16O) transpire more rapidly than heavier isotopes (D and 18O).
In the course of these studies, researchers have found that in many arid environments, plants (especially shrubs and trees) develop deep roots that penetrate into fractures in the bedrock and even form mycorrhizas with fungi that penetrate decomposing rock material (Egerton-Warburton et al., 2003; Bornyasz et al., 2005), extracting deep water (you can get water from a stone!). In southern California and eastern Oregon, woody evergreen plants require access to this water stored in granite or they would die from drought because there is not enough soil water to sustain them through the dry season (Sternberg et al., 1996; Warren et al., 2007).
Another process was discovered when studying the importance of deep water, namely hydraulic redistribution (Richards & Caldwell, 1987). In hydraulic redistribution, the water is transpired normally during the day; however, at night, when stomata close, if the surface soils have a ψ that is lower than that of the vascular tissue, water flows horizontally into fine roots. If there were no mycorrhizas, then the water would diffuse into the air gaps surrounding the shrunken roots. However, most of these roots are mycorrhizal. With their intimate contact with dry soil, the mycorrhizal fungal hyphae and soil have a more negative ψ than does the plant vascular system. Because of the lower ψ, this redistributed water is transported along and into the hyphae (Querejeta et al., 2003), and even into a neighboring root, if that root has a compatible mycorrhiza (Egerton-Warburton et al., 2007; Warren et al., 2008).
While small amounts of water are needed to sustain the hyphae of mycorrhizal fungi (Querejeta et al., 2007, in press; Warren et al., 2008), Lilleskov et al. demonstrated that, in fact, rather large amounts of water can move by this mechanism – so much so that it can create enough osmotic force to push sporocarps through crusts, rock and cement fractures, during the most extreme dry season.
Lilleskov et al. found that particular fungi have adapted this mechanism for sporulation, particularly Boletus edulis, whereas others with less well developed rhizomorphs (Russula spp.) did not show this extensive use of deep water. Their finding that Amanita muscaria may even parasitize the water of B. edulis is intriguing, only adding to the complexity of organism interactions occurring despite the drought conditions of these highly diverse ecosystems.
In California, Pisolithus sp. and Rhizopogon sp. both form rhizomorphs, and both were found forming ectomycorrhizas deep in the decomposing granite bedrock (Egerton-Warburton et al., 2003). Along with B. edulis, these fungi are also common among semi-arid woodlands and Mediterranean-type habitats worldwide. Access to deep water directly, or by hydraulic lift, has the potential to alter dramatically how we think about phenology and mycorrhizas in semi-arid regions of the globe, as well as forestry and agriculture in marginal lands. Simple assumptions, such as nutrient acquisition being limited to periods of wet soils, the importance of dry deposition of N to the soil surface, and soil respiration and carbon fluxes during the dry season, will all take on new dimensions as the physiological activities of mycorrhizal hyphae during hydraulic lift are further explored.