White spruce (Picea glauca) population differences in needle anatomy, foliar water uptake and aquaporin expression indicate trade-offs between hydraulic safety and productivity.

White spruce is a leading species across nearly the entirety of the North American boreal forest, occurs under a wide range of climate conditions and has been reported to take up water through its needles. As such, the species represents a good model organism in which to research adaptation to climatic factors through structural and physiological mechanisms. We used branch samples obtained from a 40-year-old range-wide provenance experiment to relate the climate of origin to needle anatomy, foliar water uptake and aquaporin expression under simulated drought conditions. Provenances with cold and dry source climates generally had thinner needle hypodermis layers and Casparian strips, and lost more water during dehydration. However, foliar water uptake, which involved the regulation of aquaporin water channel gene expression, was also highest in these provenances. We propose that the absence of foliar anatomical traits that would typically be associated with drought adaptation represents a previously undocumented drought adaptation strategy: a thin hypodermis and Casparian strip with aquaporin-mediated water uptake enables distinct spruce populations to leverage foliar wetting events such as snowmelt, dew or light rain, when water uptake in roots is seasonally restricted by low soil temperatures. However, this strategy is vulnerable to severe or prolonged drought events.