Nonstructural carbohydrates predict survival in saplings of temperate trees under carbon stress

Piper, Frida I.; Moreno, Paulo C.; Fajardo, Alex

doi:10.1111/1365-2435.14158

Cited by 11 publications

(9 citation statements)

References 68 publications

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“…In addition, despite the usefulness of using the absolute maxima, it does implicitly assume that absolute NSC levels have similar implications for survival across species. While this may not be true, as suggested by the variability in minimum NSC thresholds reported across species (Barker Plotkin et al, 2021;Piper et al, 2022;Weber et al, 2019), at this scale of study it is a reasonable assumption.…”

Section: F I G U R Ementioning

confidence: 85%

Global variation in nonstructural carbohydrate stores in response to climate

Blumstein

Gersony

Vilalta

et al. 2023

Global Change Biology

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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.

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Section: F I G U R Ementioning

confidence: 85%

Global variation in nonstructural carbohydrate stores in response to climate

Blumstein

Gersony

Vilalta

et al. 2023

Global Change Biology

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“…Our findings of seasonal acclimation in both stem and leaf drought tolerance also underscore the extent to which prolonged soil water deficits in the late growing season may lead to damage caused not just by hydraulic dysfunction and carbon starvation, but also by their interaction (Piper et al ., 2022). Nonstructural carbohydrate accumulation, which is reduced as plants downregulate or halt photosynthesis under dry conditions, has been shown to support xylem resistance to cavitation and recovery from cavitation in black poplar ( Populus nigra L.; Tomasella et al ., 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Bypassing water deficit stress in this way carries a price: avoidant plants generally cannot fix carbon when they do not have leaves or have closed their stomata and, therefore, risk carbon starvation (McDowell et al ., 2008; Sevanto et al ., 2014). Persistent carbon starvation not only interferes with plants' primary metabolic functioning but can also impair their ability to resist tissue desiccation and hydraulic dysfunction by reducing stocks of starches and sugars (nonstructural carbohydrates; NSCs; Sapes et al ., 2021; Tomasella et al ., 2021; Piper et al ., 2022).…”

Section: Introductionmentioning

confidence: 99%

Temperate woody species across the angiosperm phylogeny acquire tolerance to water deficit stress during the growing season

Grossman,

Coe,

Fey

et al. 2024

New Phytologist

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Summary Understanding the capacity of temperate trees to acclimate to limited soil water has become essential in the face of increasing drought risk due to climate change. We documented seasonal – or phenological – patterns in acclimation to water deficit stress in stems and leaves of tree species spanning the angiosperm phylogeny. Over 3 yr of field observations carried out in two US arboreta, we measured stem vulnerability to embolism (36 individuals of 7 Species) and turgor loss point (119 individuals of 27 species) over the growing season. We also conducted a growth chamber experiment on 20 individuals of one species to assess the mechanistic relationship between soil water restriction and acclimation. In three‐quarters of species measured, plants became less vulnerable to embolism and/or loss of turgor over the growing season. We were able to stimulate this acclimatory effect by withholding water in the growth chamber experiment. Temperate angiosperms are capable of acclimation to soil water deficit stress, showing maximum vulnerability to soil water deficits following budbreak and becoming more resilient to damage over the course of the growing season or in response to simulated drought. The species‐specific tempo and extent of this acclimatory potential constitutes preadaptive climate change resilience.

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“…Such levels might not be correlated to those at the time of budbreak. In addition, species differ in the minimum NSC concentrations required to survive under C stress (Piper et al, 2022). Therefore, the concentrations of NSC, starch, and TSS might not truly reflect the levels of such compounds that are effectively involved in budbreak responses.…”

Section: Discussionmentioning

confidence: 99%

“…The datasets generated by this study are available in Figshare: https://doi.org/10.6084/m9.figshare.21740177.v1 (Piper and Fajardo, 2022).…”

Section: Data Availability Statementmentioning

confidence: 99%

Carbon stress causes earlier budbreak in shade‐tolerant species and delays it in shade‐intolerant species

Piper

Fajardo

2023

American J of Botany

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Premise: Climate change may lead to C stress (negative C balance) in trees. Because nonstructural carbohydrates (NSC) are required during metabolic reactivation in the spring, C stress might delay budbreak timing. This effect is expected to be greater in shade-intolerant than in shade-tolerant species, owing to the faster C economy in the shade-intolerant. Methods: We experimentally induced C stress in saplings of six temperate tree species that differed in their light requirements by exposing them to either full light or shade from summer to spring, then recorded the date of first budbreak for the individuals. Because the levels of C reserves that represent effective C stress may differ among species, we estimated the degree of C stress by recording survival during the experiment and measuring whole-sapling NSC concentrations after budbreak. Results: Shade reduced NSC concentrations and increased the sugar fraction in the NSC in all species. In the shade, shade-intolerant species had higher mortality and generally lower NSC concentrations than the shade-tolerant species, indicating a trend for more severe C stress in species with faster C economy. In shade-intolerant species, budbreak started earlier and proceeded faster in full light than in shade, but in shade-tolerant species budbreak was delayed in full light. The effects of the light environments on budbreak were not greater in shade-intolerant than in shadetolerant species. Conclusions: Our study reveals a correspondence between budbreak responses to light and the light requirements of the species. This finding confirms that C metabolism has a significant role in triggering budbreak and demonstrates that whether C stress accelerates or delays budbreak depends on the species' light requirements.

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Nonstructural carbohydrates predict survival in saplings of temperate trees under carbon stress

Cited by 11 publications

References 68 publications

Global variation in nonstructural carbohydrate stores in response to climate

Global variation in nonstructural carbohydrate stores in response to climate

Temperate woody species across the angiosperm phylogeny acquire tolerance to water deficit stress during the growing season

Carbon stress causes earlier budbreak in shade‐tolerant species and delays it in shade‐intolerant species

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