Storage of carbon reserves in spruce trees is prioritized over growth in the face of carbon limitation

Significance Forest decline due to climate change is increasing worldwide. Accurate forecasting of forest dynamics requires a mechanistic understanding of carbon allocation strategies that can link molecular process regulation to whole-tree responses. However, dedicated transdisciplinary investigations spanning these scales are lacking. Here we used a unique experimental platform to manipulate the whole-tree carbon balance and combine metabolic flux measurements with transcriptional information to reveal tree resource allocation priorities under reduced carbon supply. In contrast to current understanding and model implementations, we show that trees prioritize carbon allocation to storage and mobilization of storage to support respiration rather than growth to ensure immediate and future survival under negative carbon balance that may occur during critical periods of stress. Climate change is expected to pose a global threat to forest health by intensifying extreme events like drought and insect attacks. Carbon allocation is a fundamental process that determines the adaptive responses of long-lived late-maturing organisms like trees to such stresses. However, our mechanistic understanding of how trees coordinate and set allocation priorities among different sinks (e.g., growth and storage) under severe source limitation remains limited. Using flux measurements, isotopic tracing, targeted metabolomics, and transcriptomics, we investigated how limitation of source supply influences sink activity, particularly growth and carbon storage, and their relative regulation in Norway spruce (Picea abies) clones. During photosynthetic deprivation, absolute rates of respiration, growth, and allocation to storage all decline. When trees approach neutral carbon balance, i.e., daytime net carbon gain equals nighttime carbon loss, genes encoding major enzymes of metabolic pathways remain relatively unaffected. However, under negative carbon balance, photosynthesis and growth are down-regulated while sucrose and starch biosynthesis pathways are up-regulated, indicating that trees prioritize carbon allocation to storage over growth. Moreover, trees under negative carbon balance actively increase the turnover rate of starch, lipids, and amino acids, most likely to support respiration and mitigate stress. Our study provides molecular evidence that trees faced with severe photosynthetic limitation strategically regulate storage allocation and consumption at the expense of growth. Understanding such allocation strategies is crucial for predicting how trees may respond to extreme events involving steep declines in photosynthesis, like severe drought, or defoliation by heat waves, late frost, or insect attack.