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The apoplastic pH of intact Forsythiaxintermedia (cv. Lynwood) and tomato (Solanum lycopersicum) …

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- Manipulation of the apoplastic pH of intact plants mimics stomatal and growth responses to water availability and microclimatic variation

Plants in drying soil and/or air must limit water loss to sustaina positive water balance in shoots and roots. Stomata are inducedto close, and leaf growth is reduced in order to limit the surfacearea from which water can be lost, and these changes occur verysensitively in response to changes in rhizospheric (Sobeih et al., 2004)and aerial microclimatic (Tardieu and Davies, 1992, 1993) conditions.An increase in xylem and/or bulk leaf abscisic acid (ABA) concentrationis often associated with the drying of the soil around the root(Zhang and Davies, 1989, 1990), or of the air around the shoot[measured as an increase in vapour pressure deficit (VPD), Trejo et al., 1995;Nejad and Van Meeteren, 2007]. The synthesis of ABA is stimulatedby the dehydration of root and/or leaf cells (Zhang and Tardieu, 1996;Nambara and Marion-Poll, 2005), and/or ABA can be translocatedaround the plant in response to environmental perturbation (seebelow). Roots sensing a loss of soil moisture often transportmore ABA to the shoot via the xylem vessels before the waterstatus of the shoot becomes reduced (Zhang and Davies, 1989).In the shoot, ABA sourced from roots, stems, and/or leaves interactswith guard cells to close stomata (Israelsson et al., 2006),and with the growing cells of the leaf to reduce expansion (Bacon, 1999),although there is still some controversy over the growth-regulatoryrole of ABA (Sharp, 2002).

However, it is important to note the variability in the apparentsensitivity of stomatal conductance (gs) and growth to a givenconcentration of ABA in the xylem stream (Trejo and Davies, 1991;Gollan et al., 1992; Schurr et al., 1992; Tardieu and Davies, 1992,1993). Zhang and Outlaw (2001a) determined that changes in theABA concentration of the apoplastic fluid immediately adjacentto a single guard cell pair were correlated with the stomatalresponse to mild stress in Vicia faba L. in the absence of morewidespread changes in ABA concentration. Trejo et al. (1993)detected a linear relationship between the ABA concentrationin the leaf epidermal subcompartment and the stomatal responsein Commelina communis L., whereas only a very poor relationshipexisted between the bulk leaf ABA concentration and stomatalaperture. Such sensitive and localized changes in ABA concentration,to which stomata respond, arise partly as a result of environment-inducedchanges in the ability of the cells of the stem and of the differentleaf tissues to filter out and remove ABA from, or to releaseABA into the apoplastic stream as it travels from the root tothe leaf, or as it traverses a single leaf (Slovik and Hartung, 1992a,b; Slovik et al., 1995; Wilkinson and Davies, 1997).

The amount of ABA that is removed by the symplast (i.e. thatenters the cells to become stored or metabolized) from the xylemand the leaf apoplast, before the transpiration stream reachesits target cells, depends in part on the pH of these compartments(Kaiser and Hartung, 1981; Hartung and Radin, 1989), which hasalso been shown to be sensitive to the environment in some species(see below). Apoplastic pH can thereby determine the concentrationof ABA that finally arrives at the guard cells or growing cells(Slovik and Hartung, 1992a, b; and see Wilkinson and Davies, 2002;Wilkinson, 2004). In general, a more acidic xylem/apoplasticpH (usually between 5.0 and 6.0) exists in the sap of unstressedplants and allows the greatest removal of ABA from the xylemand leaf apoplast, such that less reaches the guard cells. Morealkaline sap pH values have been detected when plants are exposedto ‘stress’ (see below), usually between 6.4 and7.2. Under these circumstances, the pH gradient over the cellmembrane that normally drives ABA removal from the apoplastis reduced, and ABA can accumulate to concentrations high enoughto affect stomatal guard cells by the time that the transpirationstream reaches their distant locality, even in the absence ofde novo synthesis. Thus pH changes generated by the root thatare propagated along the xylem vessels to penetrate to the leafapoplast (Jia and Davies, 2007), or that are generated withinthe leaf (see below), can function as chemical messengers thatalert the shoot of the need to conserve water, by adjustingthe amount of ABA that finally reaches the guard cells or thegrowing cells of the leaf.

Increases in root and/or shoot xylem sap pH have most commonlybeen shown to occur in response to soil drying (Gollan et al., 1992;Wilkinson and Davies, 1997; Bacon et al., 1998; Wilkinson et al., 1998;and see Wilkinson, 2004), although this is not a universal phenomenon(Thomas and Eamus, 2002). Alterations in pH can be one of thefirst chemical changes measurable in xylem sap from plants exposedto drying soil (Bahrun et al., 2002; Sobeih et al., 2004), evenwhen moisture tensions are low enough that a supply of wateris still freely available. Sap pH also increases in plants withroots that are exposed to soil flooding (Jackson et al., 2003;Else et al., 2006), to changes in soil nutrient status (Kirkby and Armstrong, 1980;Dodd et al., 2003; Jia and Davies, 2007; and see Wilkinson et al., 2007),and in response to salt stress (Gao et al., 2004). These changescan occur before the shoot water status of the plant is affectedby perturbation at the roots (Schurr et al., 1992; Dodd et al., 2003),within 1–2 d of the onset of perturbation (Mingo et al., 2003),or even within a few hours (Jackson et al., 2003; Gao et al., 2004;Else et al., 2006), often prior to, or coincident with, theassociated environmentally induced change in plant physiology(gs or growth).

That xylem pH can alter shoot physiology via an ABA-mediatedmechanism has been experimentally demonstrated by Wilkinson and Davies (1997),Wilkinson et al. (1998), and Bacon et al. (1998). Artificialbuffers adjusted to relatively alkaline pH values, equivalentto those found in the xylem of plants experiencing soil drying,did not reduce transpiration or growth when supplied to thexylem stream of detached shoots or leaves of ABA-deficient mutantsor ABA-depleted wild-type plants, unless ABA was also suppliedvia the transpiration stream, even at a concentration whichwas not sufficient alone to affect physiology.

More recently, changes in shoot or leaf xylem/apoplastic sappH have also been detected in response to natural or imposedchanges in the aerial environment (Savchenko et al., 2000; Hedrich et al., 2001—CO2;Felle and Hanstein, 2002—light, CO2; Mühling and Lauchli, 2000;Stahlberg et al., 2001—light; Davies et al., 2002; Wilkinson and Davies, 2002—light,VPD, and/or temperature; Jia and Davies, 2007—VPD). Photonflux density (PFD—a measure of light intensity), VPD,and air temperature are positively correlated under most ambientconditions, and as stated above stomatal closure is often associatedwith high VPD. High PFD/VPD/temperature was associated withincreased xylem pH and reduced gs in Forsythiaxintermedia (cv.Lynwood) and Hydrangea macrophylla (cv. Bluewave) when intactplants were exposed to natural fluctuations in the summer microclimateover the course of several weeks (Davies et al., 2002; Wilkinson and Davies, 2002).In related work, Tardieu and Davies (1992, 1993) observed thatstomata and growing leaves became more responsive to the ABAconcentration in the xylem as the VPD increased around leavesof field-grown maize. Since it is known that ABA can be involvedin the stomatal closure response to low humidity (Xie et al., 2006;but see Assmann et al., 2000), it is tempting to suggest a rolefor ABA-based pH signalling in stomatal regulation when theaerial microclimate becomes potentially stressful. As well asmediating changes in foliar compartmentalization of incomingroot-sourced xylem-borne ABA, microclimate-induced changes inpH may also regulate ABA release from symplastic stores in stemsand/or leaves, and/or ABA removal from the leaf via the phloem,and recirculation via the root to the shoot (Jia and Zhang, 1997;Sauter and Hartung, 2002; Else et al., 2006; see Wilkinson and Davies 2002).

Here it is demonstrated that changes in foliar apoplastic pHcan function as ABA-mediated signals of perturbations in therhizospheric and/or the aerial environment that can be adaptivein the face of stress in the intact plant. Evidence is providedfor a novel pH-based link between the aerial environment andstomatal aperture. Foliar sprays of phosphate buffer iso-osmoticallyadjusted to a range of pH values are used to manipulate leafapoplastic pH and plant physiology artificially in intact unstressedForsythia and tomato plants, and in intact plants of the ABA-deficientflacca mutant of tomato (Imber and Tal, 1970).

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