High Molecular Weight Organic Compounds in the Xylem Sap of Mangroves: Implications for Long‐Distance Water Transport

Abstract

The rise of sap in mangroves has puzzled plant physiologists for many decades. The current consensus is that negative pressures in the xylem exist which are sufficiently high to exceed the osmotic pressure of seawater (2.5 MPa). This implies that the radial reflection coefficients of the mangrove roots are equal to unity. However, direct pressure probe measurements in xylem vessels of the roots and stems of mangrove (Rhizophora mangle) grown in the laboratory or in the field yielded below‐atmospheric, positive (absolute) pressure values. Slightly negative pressure values were recorded only occasionally. Xylem pressure did not change significantly when the plants were transferred from tap water to solutions containing up to 1700 mOsmol kg−1 NaCl. This indicates that the radial reflection coefficient of the roots for salt, and therefore the effective osmotic pressure of the external solution, was essentially zero as already reported for other halophytes. The low values of xylem tension measured with the xylem pressure probe were consistent with previously published data obtained using the vacuum/leafy twig technique. Values of xylem tension determined with these two methods were nearly two orders of magnitude smaller than those estimated for mangrove using the pressure chamber technique (−3 to −6MPa). Xylem pressure probe measurements and staining experiments with alcian blue and other dyes gave strong evidence that the xylem vessels contained viscous, mucilage‐ and/or protein‐related compounds. Production of these compounds resulting from wound or other artifactual reactions was excluded. The very low sap flow rates of about 20–50 cm h−1 measured in these mangrove plants were consistent with the presence of high molecular weight polymeric substances in the xylem sap. The presence of viscous substances in the xylem sap of mangroves has the following implications for traditional xylem pressure measurement techniques, development of xylem tension, and longdistance water transport: (1) high external balancing pressures in the pressure chamber are needed to force xylem sap to the cut surface of the twig; (2) stable tensions much larger than 0.1 MPa can be developed only occasionally because viscous solutions provide nucleation sites for gas bubble formation; (3) the frequent presence of small gas bubbles in viscous solutions allows water transport by interfacial, gravity‐independent streaming at gas/water interfaces and (4) the increased density of viscous solutions creates (gravity‐dependent) convectional flows. Density‐driven convectional flows and interfacial streaming, but also the very low radial reflection coefficient of the roots to NaCl are apparently the means by which R. mangle maintains water transport to its leaves despite the high salinity of the environment.

Water relations of coastal and estuarine Rhizophora mangle: xylem pressure potential and dynamics of embolism formation and repair

“…When the values of P x using non-transpiring leaves, in this study, are further corrected by the osmotic potential of the xylem sap, then the estimated values of P x could be about 1.0 MPa more positive than estimates based on Ψ L measurements with transpiring leaves. The estimates of maximum (most positive) P x reported here (-0.72 MPa, Table 2) are still substantially lower than the most negative value of c. -0.2 MPa recorded with the xylem pressure probe in R. mangle in a previous study (Zimmermann et al 1994). The basis for the disparity between pressure-chamber and xylem-pressure-probe estimates of P x in R. mangle, despite the good agreement reported for maize and sugarcane (Melcher et al 1998a;Wei et al 1999) remains to be elucidated.…”

“…Substantial hydraulic resistance within leaves causes steep water potential gradients to develop in response to transpiration (Tyree et al 1974;Turner and Long 1980). Direct measurements of P x obtained with the xylem pressure probe (Balling and Zimmermann 1990), on the other hand, yielded much less negative values of P x (within the measuring range of the xylem pressure probe c. -1.0 MPa; Thürmer et al 1999;Wei et al 1999) than those estimated using a pressure chamber with transpiring leaves (Balling and Zimmermann 1990;Zimmermann et al 1994). Problems in reconciling measurements made with the xylem pressure probe and the pressure chamber remain in part because the measurement range of the pressure chamber extends beyond that of existing versions of the xylem pressure probe.…”

Long-term xylem pressure measurements in the liana Tetrastigma voinierianum by means of the xylem pressure probe

“…So far, transverse solute-reflecting barriers have not yet been reported, but they might be brought about by air bubbles (Sachs 1887;Zimmermann et al 1993a, b), mucilagious substances (Zimmermann et al 1994b) or other obstacles (e.g. living cells; M. McCully, Department of Biology, Carleton University, Ottawa, Canada, personal communication; see also Zimmermann 1983).…”

“…Convectional water flow requires a steady-state gradient in density in the vessels and thus depends on transpiration (but negative pressures are not needed). Alternatively, convectional flow can be created by circulation of water between the phloem and the xylem as recently detected by non-invasive NMRimaging (K0ckenberger et al 1994;Kuchenbrod et al 1994; see also Tanner and Beevers 1990;Zimmermann et al 1994b). …”

“…This hypothesis, which was rejected soon after publication by several workers in the field (Hammel 1973;Richter 1973;Scholander 1973;Pickard 1981), quite recently gained convincing experimental support to explain water ascent. Dye staining and xylem pressure-probe measurements in the xylem of mangroves have shown that the vessels apparently contain substantial amounts of (viscous) organic high polymers (Zimmermann et al 1994b). In addition, scanning electron microscopy by M.J.…”