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

Abstract

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.

Feasibility of enhancing carbon sequestration and stock capacity in temperate and boreal European forests via changes to management regimes

“…In addition, stand rejuvenation through harvesting and the replanting of saplings, with less 'respiring' (live) biomass per unit of photosynthetic leaf area (because of a shift toward younger stands), and combined with the fertilization effects of increased atmospheric CO 2 concentration can potentially drives to more productive and efficient forests. This is mirrored in the observed capability of trees to partition more of the photosynthetically assimilated carbon into new woody biomass rather than into nonstructural 19 carbon pools (Campioli et al, 2015;Pappas et al, 2020;Collalti et al, 2020a;Huang et al, 2021). This aspect is reflected in the increasing Harvested Wood Products (HWP; Figure S7) over time with more frequent thinning, reduced tree density, replacement and presence of younger forest stands that potentially can remain in the system as standing biomass over the long-term (Figure S8).…”

“…This outcome, combined with the fertilization effects of increased atmospheric CO 2 concentration and less 'respiring' (live) biomass per unit of photosynthetic (leaf) area (because of shift toward younger stands), potentially drives more productive and efficient forests. This is mirrored in the capability for trees to allocate (partition) more of the photosynthetically assimilated carbon into new woody biomass rather than into nonstructural carbon pools to maintain living woody tissues (Vicca et al 2012;Campioli et al, 2015;Malhi et al, 2015;Pappas et al, 2020;Martínez-Vilalta et al, 2016;Collalti et al, 2020a;Huang et al, 2021). This is directly mirrored by the increasing HWP over time with more frequent thinning, reduced tree density, replacement and presence of younger forest stands (a component of the pCWS, see for HWP dynamic Figure S7) which potentially can remain in the system (the other component of the pCWS, see for standing woody biomass dynamic preprint (which was not certified by peer review) is the author/funder.…”

Contrasting drought legacy effects on gross primary productivity in a mixed versus pure beech forest

“…Yu et al: Contrasting drought legacy effects on GPP in a mixed vs. pure beech forest Drought impacts on terrestrial ecosystems are not limited to concurrent effects but also include legacy effects during the following seasons and years (Anderegg et al, 2015;Frank et al, 2015;Kannenberg et al, 2020;Müller and Bahn, 2022). Legacy effects at tree and/or stand scale can be caused by the higher vulnerability to drought due to previous water depletion of the soil (Krishnan et al, 2006, Galvagno et al, 2013, reduced or delayed leaf development (Migliavacca et al, 2009;Rocha and Goulden, 2010;Kannenberg et al, 2019), drought-induced hydraulic damage of the xylem (Anderegg et al, 2013), adjustments in carbon allocation within the trees (Huang et al, 2021), depletion of non-structural carbohydrates (Peltier et al, 2022) due to reduced carbon availability and adjustments in carbon allocation (Hartman and Trumbore, 2016), and tree mortality (Allen et al, 2015), as well as reduced resistance to disturbances (e.g. insect outbreaks) due to depleted non-structural carbohydrates (Erbilgin et al, 2021).…”

Aspen growth is not limited by starch reserves

“…6,7 However, there is also experimental evidence indicating that trees actively store starch at the expense of growth. [7][8][9] Multiple studies have indicated a role for starch in providing carbon and energy when photosynthesis or sugar transport is limited, e.g., during dormancy, bud flush, or stress. 8,[10][11][12][13][14] A genetic link between seasonal starch content variation and stress has been observed for genomic variation connected to carbon storage in Populus trichocarpa.…”