Growth-limiting drought stress induces time-of-day-dependent transcriptome and physiological responses in hybrid poplar

Drought is a life-changing event for long-lived forest trees. It influences all aspects of their growth and development; it limits their ability to capture carbon and increases their susceptibility to other stressors. In this study, we showed that poplar trees could experience the same amount of available water as a stress at one time of day, but not at another; we also showed that droughts of different severities affect the transcriptome in quantitatively and qualitatively different ways. Our findings suggest that responses to drought stress are temporally heterogeneous and are calibrated to account for the duration and severity of the drought. Drought stress negatively impacts the health of long-lived trees. Understanding the genetic mechanisms that underpin response to drought stress is requisite for selecting or enhancing climate change resilience. We aimed to determine how hybrid poplars respond to prolonged and uniform exposure to drought; how responses to moderate and more severe growth-limiting drought stresses differed; and how drought responses change throughout the day. We established hybrid poplar trees (Populus x 'Okanese') from unrooted stem cutting with abundant soil moisture for 6 weeks. We then withheld water to establish well-watered, moderate and severe growth-limiting drought conditions. These conditions were maintained for 3 weeks during which growth was monitored. We then measured photosynthetic rates and transcriptomes of leaves that had developed during the drought treatments at two times of day. The moderate and severe drought treatments elicited distinct changes in growth and development, photosynthetic rates and global transcriptome profiles. Notably, the time of day of sampling produced the strongest effect in the transcriptome data. The moderate drought treatment elicited global transcriptome changes that were intermediate to the severe and well-watered treatments in the early evening but did not elicit a strong drought response in the morning. Stable drought conditions that are sufficient to limit plant growth elicit distinct transcriptional profiles depending on the degree of water limitation and on the time of day at which they are measured. There appears to be a limited number of genes and functional gene categories that are responsive to all of the tested drought conditions in this study emphasizing the complex nature of drought regulation in long-lived trees.