Threading the white spruce needle: hydraulic foliar adaptive traits stitch a story of diffusion trade-offs between growth maintenance, drought resistance, and needle water uptake

Although evidence of the incidence of foliar water uptake has previously been documented in white spruce (Picea glauca), its eco-physiological importance remains unclear. Our aim was to evaluate the ecological significance of functional differences in foliar water uptake between populations relative to their climate of origin, foliar anatomy, and aquaporin expression.

To investigate needle radial anatomies, micrographs were made using new growth needles collected from 11 provenances growing in a range-wide common garden experiment near Athabasca Alberta. Correlations were then performed to determine relationships between the anatomies and climatic parameters of origin. A foliar water uptake experiment was then conducted on twigs with new growth needles from 6 representative provenances, 3 pairs, each from a different climatic ecozone to best capture a gradient of differences in latitude and marked differences in climate of origin and needle anatomy. The experiment was run using two initial desiccation levels on the 3 ecozones selected—mild, and severe—and mass measurements and tissue samples for RT-qPCR of PIP aquaporins were taken before dehydration, and at t=0, 30, 60, and 240 minutes.

Provenances with thinner Casparian strips and hypodermis layers lost more water during needle dehydration but were also able to take up water faster when wet. Dry climate, Boreal Plains provenances, were anatomically maladapted to drought but had a greater water influx than the others over the first 30 minutes of wetting, which may be explained by their greater aquaporin expression levels during uptake. Expression rates of PIP aquaporins 1;1, and 2;2 were strongly positively correlated with RWC and 1;2 was negatively correlated with the hypodermis thickness.

We conclude that population level differences in foliar water uptake are facilitated by needle anatomy and mediated by aquaporin expression. Our results suggest that there are inherent trade-offs between productivity maintenance in cold climates, drought tolerance, and foliar water uptake. Colder climate populations are anatomically maladapted to drought, but some may be able to compensate with foliar water uptake.