Warming nondormant tree roots advances aboveground spring phenology in temperate trees.
Betula pendula
Fagus sylvatica
Populus nigra
below- vs aboveground dormancy
root-to-leaf communication
root-zone temperature
soil insulation
soil warming
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
23
06
2023
accepted:
07
09
2023
medline:
17
11
2023
pubmed:
28
10
2023
entrez:
28
10
2023
Statut:
ppublish
Résumé
Climate warming advances the onset of tree growth in spring, but above- and belowground phenology are not always synchronized. These differences in growth responses may result from differences in root and bud dormancy dynamics, but root dormancy is largely unexplored. We measured dormancy in roots and leaf buds of Fagus sylvatica and Populus nigra by quantifying the warming sum required to initiate above- and belowground growth in October, January and February. We furthermore carried out seven experiments, manipulating only the soil and not air temperature before or during tree leaf-out to evaluate the potential of warmer roots to influence budburst timing using seedlings and adult trees of F. sylvatica and seedlings of Betula pendula. Root dormancy was virtually absent in comparison with the much deeper winter bud dormancy. Roots were able to start growing immediately as soils were warmed during the winter. Interestingly, higher soil temperature advanced budburst across all experiments, with soil temperature possibly accounting for c. 44% of the effect of air temperature in advancing aboveground spring phenology per growing degree hour. Therefore, differences in root and bud dormancy dynamics, together with their interaction, likely explain the nonsynchronized above- and belowground plant growth responses to climate warming.
Substances chimiques
Soil
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2276-2287Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : DFG MA 8130/1#x2010;1
Organisme : Deutsche Forschungsgemeinschaft
ID : KR 3309/9#x2010;1
Informations de copyright
© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.
Références
Abramoff RZ, Finzi AC. 2015. Are above- and below-ground phenology in sync? New Phytologist 205: 1054-1061.
Balduzzi S, Rücker G, Schwarzer G. 2019. How to perform a meta-analysis with R: a practical tutorial. Evidence-Based Mental Health 22: 153-160.
Baumgarten F, Zohner CM, Gessler A, Vitasse Y. 2021. Chilled to be forced: the best dose to wake up buds from winter dormancy. New Phytologist 230: 1366-1377.
Beil I, Kreyling J, Meyer C, Lemcke N, Malyshev AV. 2021. Late to bed, late to rise - warmer autumn temperatures delay spring phenology by delaying dormancy. Global Change Biology 27: 5806-5817.
Blume-Werry G. 2022. The belowground growing season. Nature Climate Change 12: 11-12.
Blume-Werry G, Jansson R, Milbau A. 2017. Root phenology unresponsive to earlier snowmelt despite advanced above-ground phenology in two subarctic plant communities. Functional Ecology 31: 1493-1502.
Blume-Werry G, Wilson SD, Kreyling J, Milbau A. 2016. The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient. New Phytologist 209: 978-986.
Camut L, Regnault T, Sirlin-Josserand M, Sakvarelidze-Achard L, Carrera E, Zumsteg J, Heintz D, Leonhardt N, Lange MJP, Lange T et al. 2019. Root-derived GA12 contributes to temperature-induced shoot growth in Arabidopsis. Nature Plants 5: 1216-1221.
Champagnat P. 1989. Rest and activity in vegetative buds of trees. Annales des Sciences Forestières 46: 9s-26s.
Choi G, Robinson DA, Kang S. 2010. Changing northern hemisphere snow seasons. Journal of Climate 23: 5305-5310.
Cooke JEK, Eriksson ME, Junttila O. 2012. The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant, Cell & Environment 35: 1707-1728.
Delpierre N, Vitasse Y, Chuine I, Guillemot J, Bazot S, Rutishauser T, Rathgeber CBK. 2016. Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models. Annals of Forest Science 73: 5-25.
Fu YH, Piao S, Vitasse Y, Zhao H, De Boeck HJ, Liu Q, Yang H, Weber U, Hänninen H, Janssens IA. 2015. Increased heat requirement for leaf flushing in temperate woody species over 1980-2012: effects of chilling, precipitation and insolation. Global Change Biology 21: 2687-2697.
Fu YH, Zhang X, Piao S, Hao F, Geng X, Vitasse Y, Zohner C, Peñuelas J, Janssens IA. 2019. Daylength helps temperate deciduous trees to leaf-out at the optimal time. Global Change Biology 25: 2410-2418.
Gaul D, Hertel D, Leuschner C. 2008. Effects of experimental soil frost on the fine-root system of mature Norway spruce. Journal of Plant Nutrition and Soil Science 171: 690-698.
Greer DH, Wünsche JN, Norling CL, Wiggins HN. 2006. Root-zone temperatures affect phenology of bud break, flower cluster development, shoot extension growth and gas exchange of ‘Braeburn’ (Malus domestica) apple trees. Tree Physiology 26: 105-111.
Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL. 2001. Colder soils in a warmer world: a snow manipulation study in a northern hardwood forest ecosystem. Biogeochemistry 56: 135-150.
Harrington CA, Gould PJ, St.Clair JB. 2010. Modeling the effects of winter environment on dormancy release of Douglas-fir. Forest Ecology and Management 259: 798-808.
Harris GA. 1977. Root phenology as a factor of competition among grass seedlings. Journal of Range Management 30: 172.
Hegland SJ, Nielsen A, Lázaro A, Bjerknes A-L, Totland Ø. 2009. How does climate warming affect plant-pollinator interactions? Ecology Letters 12: 184-195.
IPCC. 2022. Climate change 2022: impacts, adaptation, and vulnerability. In: Pörtner H-O, Roberts DC, Tignor M, Poloczanska ES, Mintenbeck K, Alegría A, Craig M, Langsdorf S, Löschke S, Möller V et al., eds. Contribution of Working Group II to the sixth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press, 3056.
Isard SA, Schaetzl RJ. 1998. Effects of winter weather conditions on soil freezing in southern Michigan. Physical Geography 19: 71-94.
Jones DL, Nguyen C, Finlay RD. 2009. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant and Soil 321: 5-33.
Keuper F, Wild B, Kummu M, Beer C, Blume-Werry G, Fontaine S, Gavazov K, Gentsch N, Guggenberger G, Hugelius G et al. 2020. Carbon loss from northern circumpolar permafrost soils amplified by rhizosphere priming. Nature Geoscience 13: 1-6.
Kindermann J, Würth G, Kohlmaier GH, Badeck F-W. 1996. Interannual variation of carbon exchange fluxes in terrestrial ecosystems. Global Biogeochemical Cycles 10: 737-755.
Kreyling J, Henry HAL. 2011. Vanishing winters in Germany: soil frost dynamics and snow cover trends, and ecological implications. Climate Research 46: 269-276.
Kreyling J, Schumann R, Weigel R. 2020. Soils from cold and snowy temperate deciduous forests release more nitrogen and phosphorus after soil freeze-thaw cycles than soils from warmer, snow-poor conditions. Biogeosciences 17: 4103-4117.
Kuzyakov Y. 2010. Priming effects: interactions between living and dead organic matter. Soil Biology and Biochemistry 42: 1363-1371.
Lacombe B, Achard P. 2016. Long-distance transport of phytohormones through the plant vascular system. Current Opinion in Plant Biology 34: 1-8.
Lahti M, Aphalo PJ, Finér L, Ryyppö A, Lehto T, Mannerkoski H. 2005. Effects of soil temperature on shoot and root growth and nutrient uptake of 5-year-old Norway spruce seedlings. Tree Physiology 25: 115-122.
Laube J, Sparks TH, Estrella N, Höfler J, Ankerst DP, Menzel A. 2014. Chilling outweighs photoperiod in preventing precocious spring development. Global Change Biology 20: 170-182.
Lavender DP, Sweet GB, Zaerr JB, Hermann RK. 1973. Spring shoot growth in Douglas-fir may be initiated by gibberellins exported from the roots. Science 182: 838-839.
Lenth R. 2022. emmeans: estimated marginal means, aka least-squares means. R Package Version 1: 2.
Lian X, Piao S, Li LZX, Li Y, Huntingford C, Ciais P, Cescatti A, Janssens IA, Peñuelas J, Buermann W et al. 2020. Summer soil drying exacerbated by earlier spring greening of northern vegetation. Science Advances 6: 1-12.
Liu H, Wang H, Li N, Shao J, Zhou X, van Groenigen KJ, Thakur MP. 2022. Phenological mismatches between above- and belowground plant responses to climate warming. Nature Climate Change 12: 97-102.
Lopushinsky W, Max TA. 1990. Effect of soil temperature on root and shoot growth and on budburst timing in conifer seedling transplants. New Forests 4: 107-124.
Ma H, Mo L, Crowther TW, Maynard DS, van den Hoogen J, Stocker BD, Terrer C, Zohner CM. 2021. The global distribution and environmental drivers of aboveground versus belowground plant biomass. Nature Ecology and Evolution 5: 1110-1122.
Makoto K, Wilson SD, Sato T, Blume-Werry G, Cornelissen JHC. 2020. Synchronous and asynchronous root and shoot phenology in temperate woody seedlings. Oikos 129: 643-650.
Malyshev AV, Henry HAL, Bolte A, Arfin Khan MAS, Kreyling J. 2018. Temporal photoperiod sensitivity and forcing requirements for budburst in temperate tree seedlings. Agricultural and Forest Meteorology 248: 82-90.
Marchi M, Castellanos-Acuña D, Hamann A, Wang T, Ray D, Menzel A. 2020. ClimateEU, scale-free climate normals, historical time series, and future projections for Europe. Scientific Data 7: 1-9.
Matamala R, Gonzàlez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH. 2003. Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302: 1385-1387.
McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM. 2014. Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95: 2224-2235.
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB et al. 2015. Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytologist 207: 505-518.
Piao S, Liu Q, Chen A, Janssens IA, Fu Y, Dai J, Liu L, Lian X, Shen M, Zhu X. 2019. Plant phenology and global climate change: current progresses and challenges. Global Change Biology 25: 1922-1940.
Pliura A, Suchockas V, Sarsekova D, Gudynaitė V. 2014. Genotypic variation and heritability of growth and adaptive traits, and adaptation of young poplar hybrids at northern margins of natural distribution of Populus nigra in Europe. Biomass and Bioenergy 70: 513-529.
Pritchard SG, Strand AE, McCormack ML, Davis MA, Finzi AC, Jackson RB, Matamala R, Rogers HH, Oren R. 2008. Fine root dynamics in a loblolly pine forest are influenced by free-air-CO2-enrichment: a six-year-minirhizotron study. Global Change Biology 14: 588-602.
R Core Team. 2021. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Radville L, McCormack ML, Post E, Eissenstat DM. 2016. Root phenology in a changing climate. Journal of Experimental Botany 67: 3617-3628.
Radville L, Post E, Eissenstat DM. 2018. On the sensitivity of root and leaf phenology to warming in the Arctic. Arctic, Antarctic, and Alpine Research 50: S100020.
Reich PB, Teskey RO, Johnson PS, Hinckley TM. 1980. Periodic root and shoot growth in oak. Forest Science 26: 590-598.
Reinmann AB, Susser JR, Demaria EMC, Templer PH. 2019. Declines in northern forest tree growth following snowpack decline and soil freezing. Global Change Biology 25: 420-430.
Richardson AD, Black TA, Ciais P, Delbart N, Friedl MA, Gobron N, Hollinger DY, Kutsch WL, Longdoz B, Luyssaert S et al. 2010. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 365: 3227-3246.
Rogiers SY, Clarke SJ, Schmidtke LM. 2009. Elevated root-zone temperature hastens vegetative and reproductive development in Shiraz grapevines. Australian Journal of Grape and Wine Research 20: 123-133.
Schenker G, Lenz A, Körner C, Hoch G. 2014. Physiological minimum temperatures for root growth in seven common European broad-leaved tree species. Tree Physiology 34: 302-313.
Solly EF, Brunner I, Helmisaari HS, Herzog C, Leppälammi-Kujansuu J, Schöning I, Schrumpf M, Schweingruber FH, Trumbore SE, Hagedorn F. 2018. Unravelling the age of fine roots of temperate and boreal forests. Nature Communications 9: 1-8.
Steinaker DF, Wilson SD, Peltzer DA. 2010. Asynchronicity in root and shoot phenology in grasses and woody plants. Global Change Biology 16: 2241-2251.
Sturm M, Holmgren J, König M, Morris K. 1997. The thermal conductivity of seasonal snow. Journal of Glaciology 43: 26-41.
Tagliavini M, Looney NE. 2019. Response of peach seedlings to root-zone temperature and root-applied growth regulators. HortScience 26: 870-872.
Takeshima N, Sozu T, Tajika OY, Hayasaka Y, Fukurawa T. 2014. Which is more generalizable, powerful and interpretable in meta-analyses, mean difference or standardized mean difference? BMC Medical Research Methodology 14: 30.
Vitasse Y, Basler D. 2013. What role for photoperiod in the bud burst phenology of European beech. European Journal of Forest Research 132: 1-8.
Vitasse Y, Lenz A, Körner C. 2014. The interaction between freezing tolerance and phenology in temperate deciduous trees. Frontiers in Plant Science 5: 1-12.
Vitra A, Lenz A, Vitasse Y. 2017. Frost hardening and dehardening potential in temperate trees from winter to budburst. New Phytologist 216: 113-123.
Weigel R, Henry HAL, Beil I, Gebauer G, Jurasinski G, Klisz M, van der Maaten E, Muffler L, Kreyling J. 2021. Ecosystem processes show uniform sensitivity to winter soil temperature change across a gradient from central to cold marginal stands of a major temperate forest tree. Ecosystems 24: 1545-1560.
Weigel R, Muffler L, Klisz M, Kreyling J, van der Maaten-Theunissen M, Wilmking M, van der Maaten E. 2018. Winter matters: sensitivity to winter climate and cold events increases toward the cold distribution margin of European beech (Fagus sylvatica L.). Journal of Biogeography 45: 2779-2790.
Wickham H. 2016. ggplot2: elegant graphics for data analysis. New York, NY, USA: Springer.
Wickham H, François R, Henry L, Müller K. 2022. dplyr: a grammar of data manipulation. R Package Version 1.0.9.