Augé RM. 2003. Stomatal behavior of forest trees in relation to hydraulic, chemical and environmental factors. In: Hanson P, Wullschleger SD (ed) North American Temperate Deciduous Forest Responses to Changing Precipitation Regimes. Springer-Verlag, New York. ISBN 0-387-00309-6. Stomata regulate plant carbon gain, water loss, and other physiological determinants of forest productivity. Our ability to assess impacts of environmental changes on forest ecosystems relies heavily, therefore, on understanding stomatal function and control. The recent discovery of nonhydraulic, root-sourced stress signals is changing our understanding of how plants "sense" and how stomata respond to fluctuations in soil moisture. Formerly, it had been widely held that stomatal conductance (gs) was hydraulically regulated by leaf water potential (Y) or turgor potential (Yp; Kramer and Boyer 1995), at least in anisohydric plants (Tardieu et al. 1996; Tardieu and Simmoneau 1998). However, there are several instances in which gs was inhibited in drying soils even in the absence of perturbations in leaf water status (Davies et al. 1994). Such studies suggest that stomatal closure resulting from soil-water depletion can be mediated by changes in root water status through effects on the chemical flow of information from root to shoot. This behavior has been explained as follows. Soil dehydration alters root metabolism, which results in the production of a nonhydraulic, chemical signal, probably a positive inhibitor (Gowing et al. 1990) that moves via the transpiration stream to leaves where it affects various physiological responses. A drop in the water status of part of the root system (e.g., roots near the soil surface) may trigger or elevate the signal, which then reduces gs, even though other portions of the root system are exposed to sufficient moisture to fully supply shoot needs. Nonhydraulic inhibition of stomatal opening can be substantial. Declines in gs of up to 50% or more (relative to well-watered controls) have been reported for both woody (Khalil and Grace 1993) and herbaceous species (Zhang and Davies 1989a, 1990a; Figure 7.1). Concentrations or rates of flow of several components of xylem sap have been suggested to play a role in chemical root-to-shoot signaling of soil drying: abscisic acid (ABA; Davies et al. 1994), pH (Hartung et al. 1998), malate (Patonnier et al. 1999), cation/anion balance (Hartung and Radin 1989), cytokinins (Neuman et al. 1990; Fußeder et al. 1992). Most evidence implicates the involvement of ABA. ABA is synthesized in increasing quantities in dehydrating root tips (Liu et al. 2001a,b), where it or its conjugates (Hansen and Dorffling 1999; Sauter and Hartung 2000) move into xylem, to shoots, and to the leaf apoplast surrounding guard cells. It has long been recognized that ABA is a potent stomatal-closing agent [e.g., Jones and Mansfield (1970)]. Roots produce ABA in increasing amounts as soil water declines [e.g., Cornish and Zeevaart (1985); Zhang and Davies (1987)], and these increases have been correlated with subsequent increases in ABA content of stem and petiole xylem sap (Zhang and Davies 1990a,b; Tardieu et al. 1993). Stomatal conductance is often more closely correlated with xylem ABA concentrations ([ABA]) than with leaf or soil water status. Stomata may also be responding to root-sourced changes in xylem-sap pH that occur in response to changes in soil moisture (Hartung et al. 1998; Holbrook et al. 2002). Small changes in the flux of H+ to leaves via xylem can create large changes in apoplastic pH, with alkalization of leaf apoplast in turn enhancing the release of ABA from leaf mesophyll cells into the apoplast surrounding guard cells (Hartung et al. 1988; Netting 2000). pH gradients in leaf tissues control ABA distribution in the leaf and ABA concentrations at the primary site(s) of action at guard-cell complexes and hence influence stomatal aperture and transpirational water loss (Hartung et al. 1998). Much evidence implicates both ABA and xylem-sap pH in the regulation of gs [e.g., Jia and Zhang (1997); Zhang et al. (1997); Hartung et al. (1998); Wilkinson et al. (1998)]. Current thought is that hydraulic signals, whether originating in response to changes in atmospheric or soil water content, probably act in concert with chemical signals to regulate gs (Davies et al. 1994; Saliendra et al. 1995; Thomas and Eamus 1999; Netting 2000). Whether the ABA moving to guard-cell complexes is predominantly of leaf or root origin (Saliendra et al. 1995; Liang et al. 1997; Thompson et al. 1997; Hartung et al. 1998), changes in gs have been correlated with foliar ABA levels (Thomas and Eamus 1999) and more specifically with [ABA] in leaf epidermis (Zhang et al. 1987) and xylem sap (Davies et al. 1994). Stomatal sensitivity to xylem [ABA] can be altered by leaf Y, temperature, cytokinin activity, or light intensity, and changes in stomatal sensitivity to xylem [ABA] may play as important a role as actual xylem [ABA] in regulating gs during drought (Tardieu et al. 1993; Tardieu and Davies 1993; Heckenberger et al. 1996; Correia et al. 1997; Socias et al. 1997). Often, gs during diurnal time course studies is not correlated with leaf Y or xylem [ABA] but is better correlated with these hydraulic and chemical parameters from day to day [e.g., Socias et al. (1997)]. Although the mechanism of action is still being elucidated, nonhydraulic, root-to-shoot signaling appears to be an important component of plant response to drought conditions (Davis et al. 1994). The ability to respond dynamically to changes in available soil moisture usually improves a plant's long-term water-use efficiency and survival (Ludlow et al. 1989; Mansfield and McAinsh 1995). We conducted a series of experiments to (1) characterize stomatal response of temperate, deciduous tree species to nonhydraulic root-to-shoot signals of soil drying; (2) measure the foliar dehydration tolerance of these tree species; (3) determine whether seasonal gs of forest trees is better correlated with hydraulic, chemical, or environmental variables; and (4) determine if gs of forest trees is inhibited during soil drying episodes before leaf water status is affected.