Phytochrome B and phytochrome-interacting-factor4 modulate tree seasonal growth in cold environments

Plants that live at high latitudes and altitudes must adapt to growth in cold environments. Trees survive freezing winter conditions by ceasing growth and forming protective winter buds at the end of the growing season. To optimize growth and adaptation, the timing of growth cessation and bud set is critical. Like the well-studied Populus species (poplars, aspens, cottonwoods), many trees respond to the shortening photoperiods of fall to induce growth cessation. Temperature also has a role in this process, but the mechanism is unknown. Here, we show that the PHYTOCHROME B (PHYB)-PHYTOCHROME INTERACTING FACTOR4 (PIF4) module controls the interplay between photoperiod cues and temperature to prevent premature growth cessation and bud set at cooler temperatures. PHYB is essential for the ability of aspen trees to maintain growth under lower temperatures in permissive long days. This is mediated through PIF4, which promotes growth cessation, specifically in response to low temperatures rather than to changes in photoperiod. PIF4 can directly bind to the promoter region of the vegetative growth marker gene FLOWERING LOCUS T2 (FT2). In contrast to annual plants, it does so to suppress its transcription. Furthermore, lower temperatures can suppress PIF4 function at the transcriptional and protein levels to prevent premature growth cessation. These data show how poplar trees balance the antagonistic roles of PHYB and PIF4 to optimise the timing of growth cessation and bud set in cold environments, and this has been achieved with contrasting mechanisms compared to the annual plant model.