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The Role of ABA and the Transpiration Stream in the Regulation of the Osmotic Water Permeability of Leaf Cells

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The Role of ABA and the Transpiration Stream in the Regulation of the Osmotic Water Permeability of Leaf Cells The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells Raphae¨ l Morillon and Maarten J. Chrispeels* Division of Biology, University of California at San Diego, La Jolla, CA 92093-0116 Contributed by Maarten J. Chrispeels, September 5, 2001 The transpiration stream that passes through a plant may follow an pressed PIPs are in the PIP1 and PIP2 subfamilies. These apoplastic route, with low resistance to flow, or a cell-to-cell route, subgroups also have a conserved phosphorylation site that may in which cellular membranes impede water flow. However, pas- be a target for regulation of aquaporin activity and overall sage of water through membranes can be facilitated by aquaporins plasma membrane hydraulic conductivity (7, 8). thereby decreasing resistance. We investigated the relationship In the study presented here we questioned how the magnitude between transpiration, which can be down-regulated by abscisic of the transpiration stream affects the hydraulic conductivity of acid (ABA) or by high humidity, and the osmotic water permeability the membranes. The transpiration stream can be modulated by (Pos) of protoplasts. By using leaf protoplasts of wild-type (wt) changing the relative humidity (RH) of the atmosphere or by the Arabidopsis thaliana plants and of mutants that are low in ABA application of the hormone abscisic acid (ABA), which causes (aba1) or insensitive to ABA (abi1 and abi2), we found that stomatal closure. For plants growing at 20°C, the transpiration protoplasts from aba1 and abi mutants have very low Pos values stream will decrease more than 80% when the RH is raised from compared with those from wt plants when the plants are grown at 45% to 85%. Plants sense this change in humidity and open their 45% relative humidity. High values of Pos were found 3 h after the stomates further (9). Although not all of the plants react in the addition of ABA to the culture medium of aba1 plants; addition of same way, the most common response consists of sensing of the ABA to abi plants did not restore the Pos to wt levels. There was no stomatal transpiration rate through the guard cells (10). Other such increase in Pos when excised leaves of aba1 plants were mechanisms, such as cuticular transpiration (11, 12) or leaf water treated with ABA. When the transpiration stream was attenuated potential (12, 13), could also be involved in sensing RH. All of by growing the plants at 85% relative humidity, the Pos of proto- these mechanisms find experimental support in the literature. plasts from all plants (wt and mutants) was higher. We suggest However, ABA is not involved in this sensing mechanism (14). that attenuation of the transpiration stream in whole plants is This is in contrast to its role in bringing about stomatal closure required for the up-regulation of the P of the membranes, and os in response to a decrease in soil water potential. that this up-regulation, which does not require ABA, is mediated by The synthesis of ABA is enhanced in response to soil water the activation of aquaporins in the plasma membrane. deficit, causing the rapid closure of stomates and thereby de- creasing the intensity of the transpiration stream. In addition, lant growth requires a tradeoff between the need to acquire ABA, which is involved in long-distance signaling between root PCO2 for photosynthesis and the need to minimize water loss and shoot (15), may directly affect the hydraulic conductivity of from the leaves. Water lost through the transpiration stream is both root and shoot tissues. A number of studies carried out with replaced by water that is taken up from the soil. The force that decapitated root systems show that ABA applied to the roots drives this water uptake is the tension created by the evaporation increases the exudation volume from the cut stump of the stem of water from the leaf cells. Water that moves through living by increasing the hydraulic conductivity (Lr) of the root system tissues can follow an apoplastic or cell-to-cell path. Careful about 2-fold. ABA thus functions to allow faster uptake of water measurements of the hydraulic properties of plant tissues and by the roots and better transport of water within the plant organs show that the relative contribution of each pathway to (16–18). This effect of ABA appears to be rapid (within 30 min) overall hydraulic conductivity may change substantially depend- and long lasting (17). ing on the intensity of water flow and other factors (1). When the ABA-deficient mutants are very useful for investigating the rate of water flow is high (open stomates, low relative humidity), role of this hormone in plant water relations. The cut stump of water flows along the apoplast and around the protoplasts a plant of the wilty tomato mutant flacca has an exudation rate because the apoplastic path has the lower hydraulic resistance. that is only half that of a control plant (19). By using this same Conversely, when the rate of water flow is small, a larger mutant, Bradford (20) showed that spraying the shoot with ABA proportion of water follows the cell-to-cell path and needs to pass not only caused stomatal closure, but also raised the hydraulic through cellular membranes (and possibly through plasmodes- conductivity of the root system. mata). Water flow along this path has a much higher hydraulic Application of the cell pressure probe allows a direct approach resistance and can be modulated by aquaporins, proteins that to studying the effect of ABA on transmembrane water trans- facilitate transmembrane water transport (2–4). An important et al. unanswered question is whether the magnitude of flow in the port. With this technique, Hose (21) investigated the effect apoplastic path affects the resistance in the cell-to-cell path. of ABA on the hydraulic conductivity of maize roots and cortex In plants, aquaporins form a family of 35–37 sequence-related cells. They found that ABA facilitates the cell-to-cell component proteins (5, 6) that transport water and neutral solutes, such as of water transport across the root cylinder. The effects on glycerol, across membranes. Aquaporins have been found in the tonoplast (vacuolar membrane) and the plasma membrane, and Abbreviations: ABA, abscisic acid; PIP, plasma membrane intrinsic protein; Pos, osmotic many among them can increase the Pos of the Xenopus laevis water permeability; RH, relative humidity; wt, wild type. oocyte plasma membrane by 10- to 20-fold. Sequence compar- *To whom reprint requests should be addressed. E-mail: [email protected]. isons show that they fall into four different clades, and the The publication costs of this article were defrayed in part by page charge payment. This plasma membrane intrinsic protein (PIP) clade has about a article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. dozen members. The most abundantly and ubiquitously ex- §1734 solely to indicate this fact. 14138–14143 ͉ PNAS ͉ November 20, 2001 ͉ vol. 98 ͉ no. 24 www.pnas.org͞cgi͞doi͞10.1073͞pnas.231471998 Downloaded by guest on October 2, 2021 cellular hydraulic conductivity were large (7- to 27-fold) but mis stuck to the glass. Then, under the microscope, stomatal highly transient and postulated to be mediated by aquaporins. apertures were recorded with a video recorder for 10 min, To understand how the transpiration stream affects the hy- allowing the image capture of more than 100 stomata. Measure- draulic conductivity of cellular membranes, we used the tech- ments of the stomatal apertures were performed subsequently nique of Ramahaleo et al. (22) to measure the Pos of leaf on the filmed images. In each case more than 100 measure- protoplasts derived from wild-type (wt) Arabidopsis ecotype ments were performed. Landsberg erecta (Ler) plants and from mutants that are im- paired in ABA synthesis (aba1) or are insensitive to ABA (abi1 Preparation of Protoplasts and Pos Measurements. Leaf protoplast and abi2) (23, 24). In these mutants, the stomates are wide open. preparation and osmotic water permeability measurements on As a result, the apoplastic water flow, with its low hydraulic isolated protoplasts were performed as described (22). resistance, dominates the water transport path. What happens to To determine whether ABA affects the permeability of pro- the permeability of the membranes in these plants? Our results toplasts, Pos was measured on leaf protoplasts from aba1 plants. show that attenuating the transpiration stream by closing the The protoplasts were incubated for 10 min with 1 or 10 ␮MABA stomates with ABA or increasing the RH causes an increase in in the measuring solutions. the Pos of the protoplasts. Aba1 and abi mutant plants have very Ϯ low Pos values compared with wt. When ABA was added to the Statistical Analysis. The Pos values are given as the mean SD or growth medium of the aba1 plants, stomatal closure preceded a as frequency histograms. We used SIGMASTAT from SPSS (Chi- ͞ ͞ dramatic increase in Pos of the leaf protoplasts up to the levels cago; www.spss.com software science) to analyze the data. The found in wt plants. ABA had no effect on the Pos of protoplasts t test and ANOVA test were used to detect differences between isolated from excised leaves that were incubated in ABA solu- the lines and the growing conditions at the usual probability level ϭ tion. We conclude that leaves regulate the Pos of the plasma of P 0.05. membrane in response to the magnitude of the transpiration stream. Results aba and abi Mutants of Arabidopsis Have Plasma Membranes with a Materials and Methods Low Pos.
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