Partial root-zone drying (PRD) occurs when a part of the root system dries out, while water remains available to other portions of the root system. Plant responses to PRD have been studied primarily in agricultural settings, in attempts to reduce irrigation while maintaining crop yields and quality (Davies et al., 2002; Kang & Zhang, 2004). However, heterogeneity of water availability around root systems is a far more general phenomenon, occurring widely in natural environments. River banks provide an extreme example of a heterogeneous environment, although most if not all plants may experience some degree of heterogeneity of water supply throughout their lifespan. Riparian trees can be subject to natural cycles of drying and re-wetting of portions of their root systems, especially in arid and semi-arid environments where stream flows are often intermittent or strongly seasonal (Dettinger & Diaz, 2000). This heterogeneous water availability around root systems, both spatially and temporally, can result in frequent PRD events.
PRD often results in partial stomatal closure, leading to increased water use efficiency. In some cases, stomatal closure appears to be caused by a chemical signal from the drying roots, and not simply water deficit, as the stomata re-open when the dried root portion is severed (Gowing et al., 1990; Liu et al., 2001). Increased abscisic acid (ABA) content of the dried roots and shoot xylem sap and increased xylem sap pH have been observed during stomatal responses to PRD, and are considered likely signalling mechanisms (Davies et al., 2002; Dodd et al., 2008). However, the extent of the stomatal response to PRD varies considerably. For example, the stomatal conductance (gs) of Citrus aurantium subject to PRD was c. 70% that of fully watered control plants (Zekri & Parsons, 1990), while in another study the gs of Acer pseudoplatanus saplings under PRD declined to c. 30% of that of controls (Khalil & Grace, 1993). In other experiments using Lupinus cosentinii, Quercus robur, Betula pendula, Olea europaea, Phaseolus vulgaris and Persea americana, no stomatal response to PRD was observed; instead gs and rates of water use consistent with pre-PRD conditions were maintained (Gallardo et al., 1994; Fort et al., 1997, 1998; Centritto et al., 2005; Wakrim et al., 2005; Neuhaus et al., 2007). While differences in PRD response can be partly explained by the variable conditions used within each study, some of the variation may also reflect species differences (e.g. Croker et al., 1998). We hypothesize that differences among species in PRD response reflect adaptations to environmental heterogeneity or homogeneity. If this hypothesis is correct, we would expect gs and water use to be unaffected by PRD in species commonly subjected to natural PRD events, including some riparian trees, provided that adequate water is available to other parts of the root system. If a plant is able to maintain water uptake via the remaining hydrated zones, the best adaptive strategy may be to continue water use, and therefore photosynthesis and growth, at a constant rate.
The mechanisms by which plants maintain water uptake via only a portion of the root system are unclear. Even when total water use is reduced in response to PRD, the uptake rates of the wet roots can increase, thus compensating partly for reduced uptake from the dried parts of the root system (Lawlor, 1973; Zekri & Parsons, 1990; Kang et al., 2003; Mingo et al., 2004). The increased flow rates in the wet root portion during PRD may result solely from changes in hydrostatic gradients, or the roots might also adjust their hydraulic conductance (Lp) according to demand. Kang et al. (2003) found that pear (Pyrus communis) tree roots may have increased Lp in response to PRD, although this result was inferred from sap flux data and not measured directly. However, there are many examples of roots rapidly adjusting Lp to match demand under other circumstances. Partial root excision in wheat (Triticum aestivum) plants resulted in increased Lp of the remaining roots (Vysotskaya et al., 2004). Lp is known to fluctuate diurnally, in synchrony with transpirational demand (Henzler et al., 1999; Beaudette et al., 2007; Vandeleur et al., 2009). Shading can also induce a reduction in fine root Lp (McElrone et al., 2007). If plants do increase Lp under PRD, then the adjustment must be rapid, and localized to the watered root portion.
Root water uptake occurs via parallel apoplastic, symplastic and transcellular pathways (Steudle, 1994). The relative conductance of these pathways depends heavily on the extent of hydrophobic apoplastic barriers and the nature of the gradients involved (i.e. hydrostatic or osmotic), but the apoplast is generally considered the path of least resistance (Steudle & Peterson, 1998; Steudle, 2000). Rapid adjustment in apparent Lp can either result directly from changes in the gradients driving water flow, by changing the contribution of each flow pathway (Steudle, 2000), or through changes in the permeability of the root tissues themselves. Although anatomical changes can affect apoplastic Lp over longer timescales (Enstone et al., 2003), the only known means of rapid permeability adjustment is via transcellular Lp, through changes in the quantity or activity of root cell plasma membrane intrinsic protein (PIP) aquaporins. There is growing evidence that short-term changes in Lp may be generated primarily through aquaporins (Maurel et al., 2010). Transient increases in root Lp during early drought may be caused by increased PIP permeability (Hose et al., 2000), reduction of root Lp under anoxia can occur through proton gating of PIPs by cytosolic acidification (Tournaire-Roux et al., 2003), and the reduction and subsequent recovery of root Lp during chilling is associated with changes in expression and phosphorylation states of PIPs (Aroca et al., 2005). If rapid root Lp adjustments do occur in the wet root portion during PRD, aquaporins may be involved.
The riparian tree Melaleuca argentea is widespread across northern Australia, in locations where permanent shallow ground water is accessible. Following flood events, M. argentea commonly grows extensive aquatic root mats within temporary pools that form in the creek beds. Sap flux studies have shown that these aquatic roots can provide the majority of the water used by the tree, especially when adjacent bank soils are relatively dry (Graham, 2001). However, as the pools dry out, the aquatic roots die back and water uptake must occur via different parts of the root system. Given the natural frequency of drying events, we hypothesized that M. argentea would not respond to PRD with stomatal closure but would maintain water uptake by compensating with other parts of the root system. We also hypothesized that such a compensatory effect would involve rapid increases in root hydraulic conductance, which may be mediated by changes in aquaporin content or permeability. We tested these hypotheses with seedlings of M. argentea in a split-root system, mimicking the conditions frequently observed in the field with a portion of the roots in soil, and a portion in an aquatic pool. This design allowed us to test the effects of draining the aquatic pool on the shoot, and on the remaining hydrated part of the root system.