Adaptive variation and plasticity in non‐structural carbohydrate storage in a temperate tree species

Blumstein, Meghan; Hopkins, Robin

doi:10.1111/pce.13959

Adaptive variation and plasticity in non‐structural carbohydrate storage in a temperate tree species

Journal Article · Thu Apr 29 00:00:00 EDT 2021 · Plant, Cell and Environment

DOI:https://doi.org/10.1111/pce.13959· OSTI ID:1787078

^[1]; Hopkins, Robin ^[2]

Department of Organismic and Evolutionary Biology Harvard University Cambridge Massachusetts USA
Department of Organismic and Evolutionary Biology Harvard University Cambridge Massachusetts USA, The Arnold Arboretum Boston Massachusetts USA

Abstract

Trees' total amount of non‐structural carbohydrate (NSC) stores and the proportion of 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 (H ² _TNC = 0.19, H ² _PropStarch = 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.

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0014664

OSTI ID:: 1787078

Journal Information:: Plant, Cell and Environment, Journal Name: Plant, Cell and Environment Journal Issue: 8 Vol. 44; ISSN 0140-7791

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (67)

Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis Martínez-Vilalta, Jordi; Sala, Anna; Asensio, Dolores Ecological Monographs, Vol. 86, Issue 4 https://doi.org/10.1002/ecm.1231	journal	November 2016
Non-structural carbohydrate pools in a tropical forest Würth, Mirjam K. R.; Peláez-Riedl, Susanna; Wright, S. Joseph. Oecologia, Vol. 143, Issue 1 https://doi.org/10.1007/s00442-004-1773-2	journal	December 2004
Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones Landh�usser, Simon M.; Lieffers, Victor J. Trees - Structure and Function, Vol. 17, Issue 6 https://doi.org/10.1007/s00468-003-0263-1	journal	November 2003
Defoliation increases risk of carbon starvation in root systems of mature aspen Landhäusser, Simon M.; Lieffers, Victor J. Trees, Vol. 26, Issue 2 https://doi.org/10.1007/s00468-011-0633-z	journal	October 2011
Molecular regulation of starch accumulation in rice seedling leaves in response to salt stress Chen, Huai-Ju; Chen, Jia-Yi; Wang, Shu-Jen Acta Physiologiae Plantarum, Vol. 30, Issue 2 https://doi.org/10.1007/s11738-007-0101-y	journal	October 2007
A New Perspective on Ecological Prediction Reveals Limits to Climate Adaptation in a Temperate Tree Species Blumstein, Meghan; Richardson, Andrew; Weston, David Current Biology, Vol. 30, Issue 8 https://doi.org/10.1016/j.cub.2020.02.001	journal	April 2020
Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests Hartmann, Henrik; Adams, Henry D.; Hammond, William M. Environmental and Experimental Botany, Vol. 152 https://doi.org/10.1016/j.envexpbot.2018.03.011	journal	August 2018
A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests Allen, Craig D.; Macalady, Alison K.; Chenchouni, Haroun Forest Ecology and Management, Vol. 259, Issue 4 https://doi.org/10.1016/j.foreco.2009.09.001	journal	February 2010
Rapid degradation of starch in chloroplasts and concomitant accumulation of soluble sugars associated with ABA-induced freezing tolerance in the moss Physcomitrella patens Nagao, Manabu; Minami, Anzu; Arakawa, Keita Journal of Plant Physiology, Vol. 162, Issue 2 https://doi.org/10.1016/j.jplph.2004.06.012	journal	February 2005
Osmoregulation in Dunaliella, Part II: Photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta Goyal, Arun Plant Physiology and Biochemistry, Vol. 45, Issue 9 https://doi.org/10.1016/j.plaphy.2007.05.009	journal	September 2007
Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels O’Brien, Michael J.; Leuzinger, Sebastian; Philipson, Christopher D. Nature Climate Change, Vol. 4, Issue 8 https://doi.org/10.1038/nclimate2281	journal	June 2014
Genomic insights into salt adaptation in a desert poplar Ma, Tao; Wang, Junyi; Zhou, Gongke Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3797	journal	November 2013
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli Nature Genetics, Vol. 46, Issue 10 https://doi.org/10.1038/ng.3075	journal	August 2014
A multi-species synthesis of physiological mechanisms in drought-induced tree mortality Adams, Henry D.; Zeppel, Melanie J. B.; Anderegg, William R. L. Nature Ecology & Evolution, Vol. 1, Issue 9 https://doi.org/10.1038/s41559-017-0248-x	journal	August 2017
Temperature gradients assist carbohydrate allocation within trees Sperling, Or; Silva, Lucas C. R.; Tixier, Aude Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-03608-w	journal	June 2017
The genetics of phenotypic plasticity I. Heritability Scheiner, Samuel M.; Lyman, Richard F. Journal of Evolutionary Biology, Vol. 2, Issue 2 https://doi.org/10.1046/j.1420-9101.1989.2020095.x	journal	March 1989
Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe Anderegg, William R. L.; Klein, Tamir; Bartlett, Megan Proceedings of the National Academy of Sciences, Vol. 113, Issue 18 https://doi.org/10.1073/pnas.1525678113	journal	April 2016
Moving beyond Common‐Garden and Transplant Designs: Insight into the Causes of Local Adaptation in Species Interactions Nuismer, Scott L.; Gandon, Sylvain The American Naturalist, Vol. 171, Issue 5 https://doi.org/10.1086/587077	journal	May 2008
Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Spitze, K. Genetics, Vol. 135, Issue 2 https://doi.org/10.1093/genetics/135.2.367	journal	October 1993
Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks Krasensky, J.; Jonak, C. Journal of Experimental Botany, Vol. 63, Issue 4 https://doi.org/10.1093/jxb/err460	journal	January 2012
The Effect of Low Temperature upon Starch, Sucrose and Fructan Synthesis in Leaves Pollock, C. J.; Lloyd, E. J. Annals of Botany, Vol. 60, Issue 2 https://doi.org/10.1093/oxfordjournals.aob.a087441	journal	August 1987
Genetic and environmental control of seasonal carbohydrate dynamics in trees of diverse Pinus sylvestris populations Oleksyn, J.; Zytkowiak, R.; Karolewski, P. Tree Physiology, Vol. 20, Issue 12 https://doi.org/10.1093/treephys/20.12.837	journal	June 2000
A method for routine measurements of total sugar and starch content in woody plant tissues Chow, P. S.; Landhausser, S. M. Tree Physiology, Vol. 24, Issue 10 https://doi.org/10.1093/treephys/24.10.1129	journal	October 2004
Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe Wortemann, R.; Herbette, S.; Barigah, T. S. Tree Physiology, Vol. 31, Issue 11 https://doi.org/10.1093/treephys/tpr101	journal	October 2011
Carbon dynamics in trees: feast or famine? Sala, A.; Woodruff, D. R.; Meinzer, F. C. Tree Physiology, Vol. 32, Issue 6 https://doi.org/10.1093/treephys/tpr143	journal	February 2012
Standardized protocols and procedures can precisely and accurately quantify non-structural carbohydrates Landhäusser, Simon M.; Chow, Pak S.; Dickman, L. Turin Tree Physiology, Vol. 38, Issue 12 https://doi.org/10.1093/treephys/tpy118	journal	October 2018
Phenotypic plasticity and genetic adaptation of functional traits influences intra-specific variation in hydraulic efficiency and safety Pritzkow, Carola; Williamson, Virginia; Szota, Christopher Tree Physiology, Vol. 40, Issue 2 https://doi.org/10.1093/treephys/tpz121	journal	December 2019
Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change Anderson, Jill T.; Inouye, David W.; McKinney, Amy M. Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1743 https://doi.org/10.1098/rspb.2012.1051	journal	June 2012
β -Amylase Induction and the Protective Role of Maltose during Temperature Shock Kaplan, Fatma; Guy, Charles L. Plant Physiology, Vol. 135, Issue 3 https://doi.org/10.1104/pp.104.040808	journal	July 2004
Diurnal Variation in Nonstructural Carbohydrate Storage in Trees: Remobilization and Vertical Mixing Tixier, Aude; Orozco, Jessica; Roxas, Adele Amico Plant Physiology, Vol. 178, Issue 4 https://doi.org/10.1104/pp.18.00923	journal	October 2018
Lethal drought leads to reduction in nonstructural carbohydrates in N orway spruce tree roots but not in the canopy Hartmann, Henrik; Ziegler, Waldemar; Trumbore, Susan Functional Ecology, Vol. 27, Issue 2 https://doi.org/10.1111/1365-2435.12046	journal	February 2013
An integrated phenology modelling framework in r Hufkens, Koen; Basler, David; Milliman, Tom Methods in Ecology and Evolution, Vol. 9, Issue 5 https://doi.org/10.1111/2041-210X.12970	journal	February 2018
The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change Valladares, Fernando; Matesanz, Silvia; Guilhaumon, François Ecology Letters, Vol. 17, Issue 11 https://doi.org/10.1111/ele.12348	journal	September 2014
Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications Valladares, Fernando; Sanchez-Gomez, David; Zavala, Miguel A. Journal of Ecology, Vol. 94, Issue 6 https://doi.org/10.1111/j.1365-2745.2006.01176.x	journal	November 2006
Coordination of carbon supply and plant growth Smith, Alison M.; Stitt, Mark Plant, Cell & Environment, Vol. 30, Issue 9 https://doi.org/10.1111/j.1365-3040.2007.01708.x	journal	September 2007
Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods Gibon, Yves; Pyl, Eva-Theresa; Sulpice, Ronan Plant, Cell & Environment, Vol. 32, Issue 7 https://doi.org/10.1111/j.1365-3040.2009.01965.x	journal	July 2009
Changes in light intensity reveal a major role for carbon balance in Arabidopsis responses to high temperature: Light modulates plant response to high temperature Vasseur, FranÇOis; Pantin, Florent; Vile, Denis Plant, Cell & Environment, Vol. 34, Issue 9 https://doi.org/10.1111/j.1365-3040.2011.02353.x	journal	June 2011
RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress: BMY8 and freezing stress Kaplan, Fatma; Guy, Charles L. The Plant Journal, Vol. 44, Issue 5 https://doi.org/10.1111/j.1365-313X.2005.02565.x	journal	November 2005
Adaptive responses for seed and leaf phenology in natural populations of sessile oak along an altitudinal gradient: Variation of phenological traits in Q. petraea Alberto, F.; Bouffier, L.; Louvet, J. -M. Journal of Evolutionary Biology, Vol. 24, Issue 7 https://doi.org/10.1111/j.1420-9101.2011.02277.x	journal	April 2011
Common reed produces starch granules at the shoot base in response to salt stress Kanai, Masatake; Higuchi, Kyoko; Hagihara, Takashi New Phytologist, Vol. 176, Issue 3 https://doi.org/10.1111/j.1469-8137.2007.02188.x	journal	August 2007
Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? McDowell, Nate; Pockman, William T.; Allen, Craig D. New Phytologist, Vol. 178, Issue 4 https://doi.org/10.1111/j.1469-8137.2008.02436.x	journal	June 2008
A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth: Letters Wiley, Erin; Helliker, Brent New Phytologist, Vol. 195, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04180.x	journal	May 2012
Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa Slavov, Gancho T.; DiFazio, Stephen P.; Martin, Joel New Phytologist, Vol. 196, Issue 3, p. 713-725 https://doi.org/10.1111/j.1469-8137.2012.04258.x	journal	August 2012
THE COMPARISON OF PHENOTYPIC PLASTICITY AND GENETIC VARIATION IN POPULATIONS OF THE GRASS DANTHONIA SPICATA Scheiner, Samuel M.; Goodnight, Charles J. Evolution, Vol. 38, Issue 4 https://doi.org/10.1111/j.1558-5646.1984.tb00356.x	journal	July 1984
Adaptive Population Differentiation in Phenology Across a Latitudinal Gradient in European Aspen (Populus Tremula, l.): a Comparison of Neutral Markers, Candidate Genes and Phenotypic Traits Hall, David; Luquez, Virginia; Garcia, Victoria M. Evolution, Vol. 61, Issue 12 https://doi.org/10.1111/j.1558-5646.2007.00230.x	journal	December 2007
Shared Spatial Effects on Quantitative Genetic Parameters: Accounting for Spatial Autocorrelation and home Range Overlap Reduces Estimates of Heritability in wild red deer Stopher, Katie V.; Walling, Craig A.; Morris, Alison Evolution, Vol. 66, Issue 8 https://doi.org/10.1111/j.1558-5646.2012.01620.x	journal	April 2012
Adaptation, migration or extirpation: climate change outcomes for tree populations: Climate change outcomes for tree populations Aitken, Sally N.; Yeaman, Sam; Holliday, Jason A. Evolutionary Applications, Vol. 1, Issue 1 https://doi.org/10.1111/j.1752-4571.2007.00013.x	journal	January 2008
Q _ST in a hierarchically structured population Whitlock, Michael C.; Gilbert, Kimberly J. Molecular Ecology Resources, Vol. 12, Issue 3 https://doi.org/10.1111/j.1755-0998.2012.03122.x	journal	February 2012
Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees Richardson, Andrew D.; Carbone, Mariah S.; Keenan, Trevor F. New Phytologist, Vol. 197, Issue 3 https://doi.org/10.1111/nph.12042	journal	November 2012
Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality Mitchell, Patrick J.; O'Grady, Anthony P.; Tissue, David T. New Phytologist, Vol. 197, Issue 3 https://doi.org/10.1111/nph.12064	journal	December 2012
Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism Adams, Henry D.; Germino, Matthew J.; Breshears, David D. New Phytologist, Vol. 197, Issue 4 https://doi.org/10.1111/nph.12102	journal	January 2013
Does carbon storage limit tree growth? Palacio, Sara; Hoch, Günter; Sala, Anna New Phytologist, Vol. 201, Issue 4 https://doi.org/10.1111/nph.12602	journal	October 2013
Tree mortality from drought, insects, and their interactions in a changing climate Anderegg, William R. L.; Hicke, Jeffrey A.; Fisher, Rosie A. New Phytologist, Vol. 208, Issue 3 https://doi.org/10.1111/nph.13477	journal	June 2015
Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know Hartmann, Henrik; Trumbore, Susan New Phytologist, Vol. 211, Issue 2 https://doi.org/10.1111/nph.13955	journal	March 2016
Starch as a determinant of plant fitness under abiotic stress Thalmann, Matthias; Santelia, Diana New Phytologist, Vol. 214, Issue 3 https://doi.org/10.1111/nph.14491	journal	March 2017
Drivers and mechanisms of tree mortality in moist tropical forests McDowell, Nate; Allen, Craig D.; Anderson-Teixeira, Kristina New Phytologist, Vol. 219, Issue 3 https://doi.org/10.1111/nph.15027	journal	February 2018
Whole‐tree nonstructural carbohydrate storage and seasonal dynamics in five temperate species Furze, Morgan E.; Huggett, Brett A.; Aubrecht, Donald M. New Phytologist, Vol. 221, Issue 3 https://doi.org/10.1111/nph.15462	journal	October 2018
How do trees die? A test of the hydraulic failure and carbon starvation hypotheses: How do trees die? Sevanto, Sanna; Mcdowell, Nate G.; Dickman, L. Turin Plant, Cell & Environment, Vol. 37, Issue 1 https://doi.org/10.1111/pce.12141	journal	June 2013
Subcellular reprogramming of metabolism during cold acclimation in Arabidopsis thaliana Hoermiller, Imke I.; Naegele, Thomas; Augustin, Hanna Plant, Cell & Environment, Vol. 40, Issue 5 https://doi.org/10.1111/pce.12836	journal	October 2016
Nonstructural Carbon in Woody Plants Dietze, Michael C.; Sala, Anna; Carbone, Mariah S. Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040054	journal	April 2014
Genotype-by-Environment Interaction and Plasticity: Exploring Genomic Responses of Plants to the Abiotic Environment Des Marais, David L.; Hernandez, Kyle M.; Juenger, Thomas E. Annual Review of Ecology, Evolution, and Systematics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110512-135806	journal	November 2013
A Central Role of Abscisic Acid in Stress-Regulated Carbohydrate Metabolism Kempa, Stefan; Krasensky, Julia; Dal Santo, Silvia PLoS ONE, Vol. 3, Issue 12 https://doi.org/10.1371/journal.pone.0003935	journal	December 2008
Detecting Adaptive Differentiation in Structured Populations with Genomic Data and Common Gardens Josephs, Emily B.; Berg, Jeremy J.; Ross-Ibarra, Jeffrey Genetics, Vol. 211, Issue 3 https://doi.org/10.1534/genetics.118.301786	journal	January 2019
Evolutionary Responses to Changing Climate Davis, Margaret B.; Shaw, Ruth G.; Etterson, Julie R. Ecology, Vol. 86, Issue 7 https://doi.org/10.1890/03-0788	journal	July 2005
Non-structural Carbohydrates in Dormant Woody Perennials; The Tale of Winter Survival and Spring Arrival Tixier, Aude; Gambetta, Gregory A.; Godfrey, Jessie Frontiers in Forests and Global Change, Vol. 2 https://doi.org/10.3389/ffgc.2019.00018	journal	May 2019
Climate-driven local adaptation of ecophysiology and phenology in balsam poplar, Populus balsamifera L. (Salicaceae) Keller, Stephen R.; Soolanayakanahally, Raju Y.; Guy, Robert D. American Journal of Botany, Vol. 98, Issue 1 https://doi.org/10.3732/ajb.1000317	journal	January 2011
Temperature-assisted redistribution of carbohydrates in trees Zwieniecki, Maciej A.; Tixier, Aude; Sperling, Or American Journal of Botany, Vol. 102, Issue 8 https://doi.org/10.3732/ajb.1500218	journal	August 2015

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