Calcium is a major determinant of xylem vulnerability to cavitation

Abstract

Xylem vulnerability to cavitation is a key parameter in the drought tolerance of trees, but little is known about the control mechanisms involved. Cavitation is thought to occur when an air bubble penetrates through a pit wall, and would hence be influenced by the wall's porosity. We first tested the role of wall-bound calcium in vulnerability to cavitation in Fagus sylvatica. Stems perfused with solutions of oxalic acid, EGTA, or sodium phosphate (NaPO(4)) were found to be more vulnerable to cavitation. The NaPO(4)-induced increase in vulnerability to cavitation was linked to calcium removal from the wall. In contrast, xylem hydraulic conductance was unaffected by the chemical treatments, demonstrating that the mechanisms controlling vulnerability to cavitation and hydraulic resistance are uncoupled. The NaPO(4) solution was then perfused into stems from 13 tree species possessing highly contrasted vulnerability to cavitation. Calcium was found to be a major determinant of between-species differences in vulnerability to cavitation. This was evidenced in angiosperms as well as conifer species, thus supporting the hypothesis of a common mechanism in drought-induced cavitation.

Figure 1.

Vulnerability to cavitation (A) and retention (B) curves of beech stems perfused with NaPO₄ solutions. Fagus stems were perfused with a NaPO₄ solution at pH 4 (black circles) or pH 10 (white circles). Then, the vulnerability (A) and retention (B) curves were established. As a control, a vulnerability curve was scored from stems perfused with a control (CaCl₂ 1 mm + KCl 10 mm, triangles up) and a retention curve was scored from nonperfused stems (triangles down). The data for the vulnerability and retention curves are means (±se) of three and four samples, respectively.

Figure 2.

Effect of NaPO₄ solutions at different pH on both xylem hydraulic conductance and vulnerability to cavitation. For vulnerability to cavitation measures, stems from Fagus (circles), Salix (triangles), or Betula (squares) were perfused with a NaPO₄ solution (pH from 2–12) and then the P₅₀ value (white symbols) was determined. Data are means (±se) of three to four samples. For conductance measures, Fagus stems were perfused with a solution of KCl 10 mm and CaCl₂ 1 mm and conductance was scored under a pressure of 4 kPa. The stems were then perfused with a NaPO₄ solution (pH from 2–12), and conductance (black circles) was scored and expressed relative to initial conductance. Data are means (±se) of five samples. Data sharing different letters are significantly different according to a Tukey's HSD test (P < 0.05).

Figure 3.

Role of xylem calcium in vulnerability to cavitation in different woody species. For each species, stems were perfused with NaPO₄ solutions at pH 4 or pH 10, and the P₅₀ values were scored. Each dot represents the data for one angiosperm species (black symbols) or for one coniferophyte species (white symbols). The top section (A) shows P₅₀ values at pH 4 versus P₅₀ values at pH 10. The bottom section (B) shows the P₅₀ values at pH 4 versus the shift in P₅₀ values calculated as P_{50 pH4} − P_{50 pH10}. Data are means (±se) of three to four samples. The solid line is a regression on the mean values, with r² = 0.88 and P_{50 pH4} − P_{50 pH10} = 0.707 P_{50 pH4} + 1.055 (P < 0. 001). The dashed line is the function P_{50 pH4} = P_{50 pH10}.

Figure 4.

Role of xylem calcium in the light-induced increase in vulnerability to cavitation. Full sunlight-grown (white symbols) and shade-grown (black symbols) stems were sampled on four beech trees (four different symbols). They were perfused with NaPO₄ solutions at pH 4 or pH 10, and the P₅₀ values were scored. The section shows P₅₀ values at pH 4 versus the shift in P₅₀ values calculated as P_{50 pH4} − P_{50 pH10}. Data are means (±se) of three to four samples. According to a repeated ANOVA analysis, the P_{50 pH4} means was significantly different between trees and between sunlight- and shade-grown stems, with P < 0.01. However, the means of P₅₀ shift were not significantly different between trees (P = 0.226) and between full sunlight- and shade-grown stems (P = 0.899).