Anatomical regulation of ice nucleation and cavitation helps trees to survive freezing and drought stress

Abstract

Water in the xylem, the water transport system of plants, is vulnerable to freezing and cavitation, i.e. to phase change from liquid to ice or gaseous phase. The former is a threat in cold and the latter in dry environmental conditions. Here we show that a small xylem conduit diameter, which has previously been shown to be associated with lower cavitation pressure thus making a plant more drought resistant, is also associated with a decrease in the temperature required for ice nucleation in the xylem. Thus the susceptibility of freezing and cavitation are linked together in the xylem of plants. We explain this linkage by the regulation of the sizes of the nuclei catalysing freezing and drought cavitation. Our results offer better understanding of the similarities of adaption of plants to cold and drought stress, and offer new insights into the ability of plants to adapt to the changing environment.

Figure 1. Schematic presentation of conduits of a deciduous tree species and inter-conduit pits (a) between two water-filled conduits and (b) between a gas-filled and a water-filled conduit.

In (a), impurities and other solid particles can enter a conduit through a pit membrane in the case of large enough pores, and become potential ice nuclei. In (b), gas penetrates from a gas-filled conduit to adjacent water-filled conduit through a pit membrane in the case of large enough pores, and induces cavitation.

Figure 2. Schematic presentation of the used terminology related to temperature (T) and pressure (P).

Freezing temperature and cavitation pressure refer to heterogeneous nucleation; homogeneous freezing takes place at approximately −40°C and homogeneous cavitation at approximately −140 MPa.

Figure 3

(a) Measurements (N = 70) of ice nucleation temperature of water in trees and maximum conduit radius.The narrowest conduits were found in conifers and the widest in deciduous species. Curve for the theoretical relationship is drawn. (b) Theoretical relationship between ice nucleation temperature and ice nucleus radius with varying particle surface properties denoted with θ (equation 5) in the insert. The ice nucleation temperature is calculated to be reached when the nucleation probability exceeds 0.5 in one minute for a sample of 3 cm³ in volume (a cylinder of 1 cm in radius and 1 cm in height).

Figure 4. Empirical results concerning the relationship between drought cavitation pressure and conduit radius are compared with the theoretical relationship between ice nucleation temperature and conduit radius that is also supported by the empirical data (R² = 0.35, P < 0.0001).

Drought cavitation is described with the pressure reducing 50% of the hydraulic conductivity (P₅₀). The linear regression line of Wilson and Jackson was drawn visually from the original figure. The definition of conduit radius was different in different studies: mean conduit radius, hydraulically weighted mean radius (Σr⁵/Σr⁴) and mean radius of conduits responsible for 95% of water flow were used. In this study we used maximum conduit radius.

Figure 5. Relationship of ice nucleation temperature with (a) sample volume, (b) cooling rate and (c) maximum conduit radius.

The lines represent statistical prediction between ice nucleation temperature and sample volume (a) and ice nucleation temperature and maximum conduit radius (c) when the effect of other variables in the multivariate model were fixed to data averages. There was no significant dependency between ice nucleation temperature and cooling ratio (b).

Figure 6. Schematic presentation of the relationship between conduit anatomy and the trade-off between water transport safety and efficiency at whole tree level.

Conduit size scales with the degree of metastability the tree can experience before spreading of cavitation or freezing. Different sized conduits are favoured in different environmental conditions.