skip to main content


Title: Global variation in nonstructural carbohydrate stores in response to climate
Abstract

Woody plant species store nonstructural carbohydrates (NSCs) for many functions. While known to buffer against fluctuations in photosynthetic supply, such as at night, NSC stores are also thought to buffer against environmental extremes, such as drought or freezing temperatures by serving as either back‐up energy reserves or osmolytes. However, a clear picture of how NSCs are shaped by climate is still lacking. Here, we update and leverage a unique global database of seasonal NSC storage measurements to examine whether maximum total NSC stores and the amount of soluble sugars are associated with clinal patterns in low temperatures or aridity, indicating they may confer a benefit under freezing or drought conditions. We examine patterns using the average climate at each study site and the unique climatic conditions at the time and place in which the sample was taken. Altogether, our results support the idea that NSC stores act as critical osmolytes. Soluble Sugars increase with both colder and drier conditions in aboveground tissues, indicating they can plastically increase a plants' tolerance of cold or arid conditions. However, maximum total NSCs increased, rather than decreased, with average site temperature and had no relationship to average site aridity. This result suggests that the total amount of NSC a plant stores may be more strongly determined by its capacity to assimilate carbon than by environmental stress. Thus, NSCs are unlikely to serve as reservoir of energy. This study is the most comprehensive synthesis to date of global NSC variation in relation to climate and supports the idea that NSC stores likely serve as buffers against environmental stress. By clarifying their role in cold and drought tolerance, we improve our ability to predict plant response to environment.

 
more » « less
Award ID(s):
2010781
NSF-PAR ID:
10390537
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Global Change Biology
Volume:
29
Issue:
7
ISSN:
1354-1013
Page Range / eLocation ID:
p. 1854-1869
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Nonstructural carbohydrates (NSCs) are carbon compounds that serve a large variety of purposes, which makes it hard to disentangle how their concentrations change in response to environmental stress. Soluble sugars can accumulate in plants as metabolic demand decreases, e.g., in response to drought or as seasonal temperatures decrease. Alternatively, actively allocating to NSCs could be beneficial in cold acclimation (CA) or in periods of increased aridity because soluble sugars serve non-metabolic functions as cryoprotectants and in osmoregulation. We used Juniperus virginiana L., a woody plant currently expanding its range, to investigate whether plants sourced from colder and more arid locations maintained higher concentrations of NSCs. We sourced three populations of J. virginiana from across an environmental gradient, and we compared these with the closely related Juniperus scopulorum Sarg. We grew the plants in a common garden in north-east OH, part of J. virginiana’s historic range. We exposed the plants to a drought treatment during the summer and then measured the NSC concentrations and cold-hardiness as the plants acclimated to colder temperatures and shorter days. We found that individuals originating from the warmer, more southern range edge were initially not as cold-hardy as plants from the other source populations and that they only reached similar hardiness after prolonged low temperatures. We did not find an effect of drought on NSCs, although this may be due to other traits conferring a high level of drought tolerance in J. virginiana. Across all plants, the NSC concentration increased over the CA period, specifically as sugars. Although the highest concentrations of sugars were found in plants from southern populations, the plants from colder environments maintained higher sugar-to-starch ratios. These results highlight the importance of NSCs in CA and that plants sourced from different climates showed different physiological responses to shortening days and low temperatures.

     
    more » « less
  2. Abstract

    Trees'totalamount of non‐structural carbohydrate (NSC) stores and theproportionof these stores residing as insoluble starch are vital traits for individuals living in variable environments. However, our understanding of how stores vary in response to environmental stress is poorly understood as the genetic component of storage is rarely accounted for in studies. Here, we quantified variation in NSC traits in branch samples taken from over 600 clonally transplanted black cottonwood (Populus trichocarpa)trees grown in two common gardens. We found heritable variation in both total NSC stores and the proportion of stores in starch (H2TNC = 0.19, H2PropStarch = 0.31), indicating a substantial genetic component of variation. In addition, we found high amounts of plasticity in both traits in response to cold temperatures and significant genotype‐by‐environment (GxE) interactions in the total amount of NSC stored (54% of P is GxE). This finding of high GxE indicates extensive variation across trees in their response to environment, which may explain why previous studies of carbohydrate stores' responses to stress have failed to converge on a consistent pattern. Overall, we found high amounts of environmental and genetic variation in NSC storage concentrations, which may bolster species against future climate change.

     
    more » « less
  3. NA (Ed.)
    Abstract

    Interactions between water and carbon dynamics underlie drought-related tree mortality. While whole-tree water relations have been shown to play a key role in the response to and recovery from drought, the role of nonstructural carbohydrates (NSC) and how their storage and allocation changes surrounding drought events deserves further attention and is critical for understanding tree survival. Here, we quantified in situ NSC responses of temperate forest trees to the 2016 drought in the northeastern United States. Sugar and starch concentrations were measured in the stemwood of five tree species from 2014 to 2019, which allowed us to monitor NSCs in relation to climatic conditions before, during, and after the natural drought. We found that immediately following the drought, measured stemwood NSC concentrations decreased. However, NSC concentrations rebounded quickly within three years. Notably, trees allocated proportionally more to starch than to sugars following the 2016 drought. In winter 2017, starch comprised 45% of total stemwood stores, whereas starch made up only 1–2% in other years. Further, we modeled and assessed the climatic drivers of total NSC concentrations in the stem. Variation in total NSC concentrations was significantly predicted by the previous year’s temperature, precipitation, and standardized precipitation-evapotranspiration index (SPEI), with stemwood concentrations decreasing following hotter, drier periods and increasing following cooler, wetter periods. Overall, our work provides insight into the climatic drivers of NSC storage and highlights the important role that a tree’s carbon economy may play in its response and recovery to environmental stress.

     
    more » « less
  4. Cernusak, Lucas (Ed.)
    Abstract Nonstructural carbohydrates (NSCs) play a critical role in plant physiology and metabolism, yet we know little about their distribution within individual organs such as the stem. This leaves many open questions about whether reserves deep in the stem are metabolically active and available to support functional processes. To gain insight into the availability of reserves, we measured radial patterns of NSCs over the course of a year in the stemwood of temperate trees with contrasting wood anatomy (ring porous vs diffuse porous). In a subset of trees, we estimated the mean age of soluble sugars within and between different organs using the radiocarbon (14C) bomb spike approach. First, we found that NSC concentrations were the highest and most seasonally dynamic in the outermost stemwood segments for both ring-porous and diffuse-porous trees. However, while the seasonal fluctuation of NSCs was dampened in deeper stemwood segments for ring-porous trees, it remained high for diffuse-porous trees. These NSC dynamics align with differences in the proportion of functional sapwood and the arrangement of vessels between ring-porous and diffuse-porous trees. Second, radial patterns of 14C in the stemwood showed that sugars became older when moving toward the pith. The same pattern was found in the coarse roots. Finally, when taken together, our results highlight how the radial distribution and age of NSCs relate to wood anatomy and suggest that while deeper, and likely older, reserves in the stemwood fluctuated across the seasons, the deepest reserves at the center of the stem were not used to support tree metabolism under usual environmental conditions. 
    more » « less
  5. Summary

    Under prolonged drought and reduced photosynthesis, plants consume stored nonstructural carbohydrates (NSCs). Stored NSC depletion may impair the regulation of plant water balance, but the underlying mechanisms are poorly understood, and whether such mechanisms are independent of plant water deficit is not known. If so, carbon costs of fungal symbionts could indirectly influence plant drought tolerance through stored NSC depletion.

    We connected well‐wateredPinus ponderosaseedling pairs via ectomycorrhizal (EM) networks where one seedling was shaded (D) and the other kept illuminated (LD) and compared responses to seedling pairs in full light (L). We measured plant NSCs, osmotic and water potential, and transfer of13CO2through EM to explore mechanisms linking stored NSCs to plant water balance regulation and identify potential tradeoffs between plant water retention and EM fungi under carbon‐limiting conditions.

    NSCs decreased from L to LD to D seedlings. Even without drought, NSC depletion impaired osmoregulation and turgor maintenance, both of which are critical for drought tolerance. Importantly, EM networks propagated NSC depletion and its negative effects on water retention from carbon stressed to nonstressed hosts.

    We demonstrate that NSC storage depletion influences turgor maintenance independently of plant water deficit and reveal carbon allocation tradeoffs between supporting fungal symbionts and retaining water.

     
    more » « less