Large seasonal fluctuations in whole-tree carbohydrate reserves: is storage more dynamic in boreal ecosystems?

BACKGROUND AND AIMS: Carbon reserves are a critical source of energy and substrates that allow trees to cope with periods of minimal carbon gain and/or high carbon demands, conditions which are prevalent in high-latitude forests. However, we have a poor understanding of carbon reserve dynamics at the whole-tree level in mature boreal trees. We therefore sought to quantify the seasonal changes in whole-tree and organ-level carbon reserve pools in mature boreal Betula papyrifera. METHODS: Non-structural carbohydrate (NSC; soluble sugars and starch) tissue concentrations were measured at key phenological stages throughout a calendar year in the roots, stem (inner bark and xylem), branches and leaves, and scaled up to estimate changes in organ and whole-tree NSC pool sizes. Fine root and stem growth were also measured to compare the timing of growth processes with changes in NSC pools. KEY RESULTS: The whole-tree NSC pool increased from its spring minimum to its maximum at bud set, producing an average seasonal fluctuation of 0.96 kg per tree. This fluctuation represents a 72 % change in the whole-tree NSC pool, which greatly exceeds the relative change reported for more temperate conspecifics. At the organ level, branches accounted for roughly 48-60 % of the whole-tree NSC pool throughout the year, and their seasonal fluctuation was four to eight times greater than that observed in the stemwood, coarse roots and inner bark. CONCLUSIONS: Branches in boreal B. papyrifera were the largest and most dynamic storage pool, suggesting that storage changes at the branch level largely drive whole-tree storage dynamics in these trees. The greater whole-tree seasonal NSC fluctuation in boreal vs. temperate B. papyrifera may result from (1) higher soluble sugar concentration requirements in branches for frost protection, and/or (2) a larger reliance on reserves to fuel new leaf and shoot growth in the spring.

Viewing forests from below: fine root mass declines relative to leaf area in aging lodgepole pine stands.

In the continued quest to explain the decline in productivity and vigor with aging forest stands, the most poorly studied area relates to root system change in time. This paper measures the wood production, root and leaf area (and mass) in a chronosequence of fire-origin lodgepole pine (Pinus contorta Loudon) stands consisting of four age classes (12, 21, 53, and ≥100 years), each replicated ~ five times. Wood productivity was greatest in the 53-year-old stands and then declined in the ≥100-year-old stands. Growth efficiency, the quantity of wood produced per unit leaf mass, steadily declined with age. Leaf mass and fine root mass plateaued between the 53- and ≥100-year-old stands, but leaf area index actually increased in the older stands. An increase in the leaf area index:fine root area ratio supports the idea that older stand are potentially limited by soil resources. Other factors contributing to slower growth in older stands might be lower soil temperatures and increased self-shading due to the clumped nature of crowns. Collectively, the proportionally greater reduction in fine roots in older stands might be the variable that predisposes these forests to be at a potentially greater risk of stress-induced mortality.

Low root reserve accumulation during drought may lead to winter mortality in poplar seedlings.

Climate models suggest that more frequent drought events of greater severity and length, associated with climate change, can be expected in the coming decades. Although drought-induced tree mortality has been recognized as an important factor modulating forest demography at the global scale, the mechanisms underlying drought-induced tree mortality remain contentious. Above- and below-ground growth, gas exchange, water relations and carbon reserve accumulation dynamics at the organ and whole-plant scale were quantified in Populus tremuloides and P. balsamifera seedlings in response to severe drought. Seedlings were maintained in drought conditions over one growing and one dormant winter season. Our experiment presents a detailed description of the effect of severe drought on growth and physiological variables, leading to seedling mortality after an extended period of drought and dormancy. After re-watering following the dormant period, drought-exposed seedlings did not re-flush, showing that the root system had died off. The results of this study suggest a complex series of physiological feedbacks between the measured variables in both Populus species. Further, they reveal that reduced reserve accumulation in the root system during drought decreases the conversion of starch to soluble sugars in roots, which may contribute to the root death of drought-exposed seedlings during the dormant season by compromising the frost tolerance of the root system.

Populus root salicinoid phenolic glycosides are not mobilized to support metabolism and regrowth under carbon limited conditions.

Remobilization of carbon storage compounds in trees is crucial for the resilience to disturbances, stress, and the requirements of their perennial lifestyle, all of which can impact photosynthetic carbon gain. Trees contain abundant non-structural carbohydrates (NSC) in the form of starch and sugars for long term carbon storage, yet questions remain about the ability of trees to remobilize non-conventional carbon compounds under stress. Aspens, like other members of the genus Populus, have abundant specialized metabolites called salicinoid phenolic glycosides, which contain a core glucose moiety. In this study, we hypothesized that the glucose-containing salicinoids could be remobilized as an additional carbon source during severe carbon limitation. We made use of genetically modified hybrid aspen (Populus tremula x P. alba) with minimal salicinoid content and compared these to control plants with high salicinoid content during resprouting (suckering) in dark (carbon limited) conditions. As salicinoids are abundant anti-herbivore compounds, identification of such a secondary function for salicinoids may provide insight to the evolutionary pressures that drive their accumulation. Our results show that salicinoid biosynthesis is maintained during carbon limitation and suggests that salicinoids are not remobilized as a carbon source for regenerating shoot tissue. However, we found that salicinoid-producing aspens had reduced resprouting capacity per available root biomass when compared to salicinoid-deficient aspens. Therefore, our work shows that the constitutive salicinoid production in aspens can reduce the capacity for resprouting and survival in carbon limited conditions.

Seasonal dynamics of non-structural carbon pools and their relationship to growth in two boreal conifer tree species.

In an attempt to comprehensively study the dynamics of non-structural carbon compounds (NCCs), we measured the seasonal changes of soluble sugars, starch, lipids and sugar alcohols in the leaves, branches, stem and roots of the fast-growing Pinus contorta (Loudon) (pine) and slow-growing Picea glauca (Moench) Voss (spruce) trees growing in a boreal climate. In addition to measuring the seasonal concentrations of these compounds, the relative contribution of these compounds to the total NCC pool within the organs of trees (~8 m tall) was estimated and compared across different phenological and growth stages. Both species showed large seasonal shifts from starch to sugars from spring to fall in nearly all organs and tissues; most likely an adaptation to the cold winters. For both species, the total fluctuation of sugar + starch across the year (i.e., the difference between the minimum and maximum observed across collection times) was estimated to be between 1.6 and 1.8 kg for all NCCs. The fluctuation, however, was 1.40 times greater than the minimum reserves in pine, while only 0.72 times the minimum reserves in spruce. By tissue type, NCC fluctuations were greatest in the roots of both species. Roots showed a large build-up of reserves in late spring, but these reserves were depleted over summer and fall. Storage reserves in needles and branches declined over the summer, and this decline may be linked to the sink strength of the stem during diameter growth. Some notable highlights of this holistic study: a late winter build-up of sugars in the stem xylem of both species, but especially spruce; and an increase in sugar alcohols in the bark of spruce in very late winter, which could indicate mobilization to support early growth in spring and high lipid reserves in the bark of pine, which appeared not to be impacted by seasonal changes between summer and winter. Collectively, these observations point toward a more conservative NCC reserve strategy in spruce compared with pine, which is consistent with its stress tolerance and greater longevity.

Photosynthesis and carbon allocation of six boreal tree species grown in understory and open conditions.

One-year-old seedlings of Abies balsamea (L.) Mill, Picea glauca (Moench) Voss, Pinus contorta Loudon, Betula papyrifera Marsh., Populus tremuloides Michx. and Populus balsamifera L. were transplanted in the spring, in pots, to the understory of a mixed P. tremuloides-P. balsamifera stand or to an adjacent open site. Growth and leaf characteristics were measured and photosynthetic light response curves determined in mid-August. Overall, the coniferous seedlings showed less photosynthetic plasticity in response to growth conditions than the deciduous species. Abies balsamea, P. glauca and B. papyrifera responded to the understory environment with higher leaf area ratios, and lower photosynthetic light saturation points and area-based leaf respiration relative to values for open-grown seedlings, while they matched or exceeded the height growth of open-grown seedlings. In contrast, seedlings of Pinus contorta, P. tremuloides and P. balsamifera displayed characteristics that were not conducive to survival in the understory. These characteristics included a high light saturation point and leaf dark respiration rate in P. contorta, and lower leaf area variables combined with higher carbon allocation to roots in P. tremuloides and P. balsamifera. By the second growing season, all seedlings of P. tremuloides and P. balsamifera growing in the understory had died.

Hydraulic conductance in aspen (Populus tremuloides) seedlings exposed to low root temperatures.

Low root temperatures significantly reduced root hydraulic conductivity and increased resistance to water flow through the roots of aspen (Populus tremuloides Michx.) seedlings. Increased resistance to water flow could not be fully explained by the corresponding increase in water viscosity at low temperatures. The shapes of Arrhenius plots of root water flow and the activation energies were dependent on the direction, sequence and extent of temperature change. The Arrhenius plots suggested that the effect of low root temperature on root water flow was mediated by an effect on root metabolism. The low root temperatures tested did not induce root electrolyte leakage normally associated with cell membrane injury. Although a decrease in root temperatures to 7 or 4 degrees C induced a reduction in stomatal conductance, this reduction lagged the decline in root water flow by several hours. In contrast, when soil temperatures were raised from 4 or 7 degrees C to 25 degrees C, root water flow presumably increased, and stomatal conductance responded rapidly and was temporarily higher than before the cold treatment was imposed.

Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation?

In a greenhouse study we quantified the gradual change of gas exchange, water relations and root reserves of aspen (Populus tremuloides Michx.) seedlings growing over a 3-month period of severe water stress. The aim of the study was to quantify the complex interrelationship between growth, water and gas exchange, and root carbon (C) dynamics. Various growth, gas exchange and water relations variables in combination with root reserves were measured periodically on seedlings that had been exposed to a continuous drought treatment over a 12-week period and compared with well-watered seedlings. Although gas exchange and water relations parameters significantly decreased over the drought period in aspen seedlings, root reserves did not mirror this trend. During the course of the experiment roots of aspen seedlings growing under severe water stress showed a two orders of magnitude increase in sugar and starch content, and roots of these seedlings contained more starch relative to sugar than those in non-droughted seedlings. Drought resulted in a switch from growth to root reserves storage which indicates a close interrelationship between growth and physiological variables and the accumulation of root carbohydrate reserves. Although a severe 3-month drought period created physiological symptoms of C limitation, there was no indication of a depletion of root C reserve in aspen seedlings.