Abstract
Background and aims
In temperate conifer forests, soil temperature is an important driver of fine root growth and winter root growth can occur during aerial dormancy. We hypothesize that in conifers, stocks of non-structural carbohydrates (NSC) in fine roots are high enough to provide energy for root growth and production throughout the year, even when photosynthesis is reduced.
Methods
We measured monthly root production (i.e. the number of roots undergoing elongation) and their elongation rate (RER) in mature Picea abies for one year, along a soil temperature gradient (three altitudes of 1400, 1700 and 2000 m). Every two months we harvested needles, branches, stem, large, medium and fine roots, and quantified starch and soluble sugars in each organ using analytical methods and near infra-red spectroscopy (NIRS). Soil water potential was monitored continuously. We analysed RER data with regard to climate variables and NSC levels of the current and preceding month.
Results
NIRS was a reliable method for measuring starch and soluble sugars. NSC was high in the crown and roots but very low in the trunk all year round. Soil temperature was positively correlated to RER (of the current month) between 0 and 8 °C, above which RER stabilised and was not explained by NSC levels or soil water potential. However, mean RER of fine roots in the month following the measurement of NSC was significantly and negatively correlated to soluble sugar and positively correlated with starch content. Very fine root starch content was also positively correlated with root production in the month following the starch measurement.
Conclusion
Soil temperature was a major driver of fine root elongation, but at low temperatures only. At soil temperatures >8 °C, no particular driver was dominant. NSC levels were negligible in the stem and root-bases, suggesting that wood production is a major sink that depletes carbohydrates. A large pool of NSC, principally in the form of starch, existed in fine roots of P. abies, and acted as an energy supply for root production throughout the year, even when photosynthesis was limited. Soluble sugars were depleted in fine roots during the growing season, but no relationship was found between fine root production and soluble sugars. The physiological mechanism by which NSC accumulation actively or passively occurs in fine roots is not known but could be due to the symplastic pathway of phloem unloading in conifer root tips, which suggests a passive mechanism.
Similar content being viewed by others
References
Abramoff RZ, Finzi AC (2015) Are above and below ground phenology in sync? New Phytol 205:1054–1061
Alvarez Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Funct Ecol 21:211–218
Améglio T, Bodet C, Lacointe A, Cochard H (2002) Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees. Tree Physiol 22(17):1211–1220. https://doi.org/10.1093/treephys/22.17.1211
Barbaroux C, Bréda N, Dufrêne E (2003) Distribution of above ground and below ground carbohydrate reserves in adult trees of two contrasting broad leaved species (Quercus petraea and Fagus sylvatica). New Phytol 157:605–615
Batten G, Blakeney A, McGrath V, Ciavarella S (1993) Non-structural carbohydrate: analysis by near infrared reflectance spectroscopy and its importance as an indicator of plant growth. Plant nutrition—from genetic engineering to field practice. Springer, pp 269–272
Bohm W (1979) Methods of studying root systems. Springer-Verlag, Berlin, Heidelberg, New York 188 pp
Delucia EH (1986) Effect of low root temperature on net photosynthesis, stomatal conductance and carbohydrate concentration in Engelmann spruce (Picea engelmannii Parry ex Engelm.) seedlings. Tree Physiol 2:143–154
Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687
Druart N, Johansson A, Baba K, Schrader J, Sjödin A, Bhalerao RR, Resman L, Trygg J, Moritz T, Bhalerao RP (2007) Environmental and hormonal regulation of the activity–dormancy cycle in the cambial meristem involves stage specific modulation of transcriptional and metabolic networks. Plant J 50:557–573
Ek M, Gellerstedt G, Henriksson G (2009) Wood chemistry and wood biotechnology. Walter de Gruyter GmbH & Co KG, Berlin
Ericsson A (1978) Seasonal changes in translocation of 14C from different age classes of needles on 20 year old Scots pine trees (Pinus silvestris). Physiol Plant 43:351–358
Fajardo A, Piper FI, Pfund L, Körner C, Hoch G (2012) Variation of mobile carbon reserves in trees at the alpine treeline ecotone is under environmental control. New Phytol 195:794–802
Fajardo A, Piper FI, Hoch G (2013) Similar variation in carbon storage between deciduous and evergreen treeline species across elevational gradients. Ann Bot 112:623–631
Fukami T, Wardle DA (2005) Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients. Proc R Soc Lond B Biol Sci 272:2105–2115
Gaul D, Hertel D, Leuschner C (2008) Effects of experimental soil frost on the fine-root system of mature Norway spruce. J Plant Nutr Soil Sci 171:690–698
Germon A, Cardinael R, Prieto I, Mao Z, Kim J, Stokes A, Dupraz C, Laclau J-P, Jourdan C (2015) Unexpected phenology and lifespan of shallow and deep fine roots of walnut trees grown in a silvoarable Mediterranean agroforestry system. Plant Soil 1–18
Göttlicher S, Knohl A, Wanek W, Buchmann N, Richter A (2006) Short term changes in carbon isotope composition of soluble carbohydrates and starch: from canopy leaves to the root system. Rapid Commun Mass Spectrom 20:653–660
Heide O, Prestrud A (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol 25:109–114
Hein PR, Clair B, Brancheriau L, Chaix G (2010) Predicting microfibril angle in Eucalyptus wood from different wood faces and surface qualities using near infrared spectra. J Near Infrared Spectrosc 18:455
Hoch G, Körner C (2012) Global patterns of mobile carbon stores in trees at the high elevation tree line. Glob Ecol Biogeogr 21:861–871
Hoch G, Richter A, Körner C (2003) Non structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Huck MG, Taylor HM (1982) The rhizotron as a tool for root research. Adv Agron 35:1–35
Keel SG, Campbell CD, Högberg MN, Richter A, Wild B, Zhou X, Hurry V, Linder S, Näsholm T, Högberg P (2012) Allocation of carbon to fine root compounds and their residence times in a boreal forest depend on root size class and season. New Phytol 194:972–981
Kell DB (2012) Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Philos Trans R Soc Lond Ser B Biol Sci 5(367):1589–1597
Koller EK, Phoenix GK (2017) Seasonal dynamics of soil and plant nutrients at three environmentally contrasting sites along a sub-Arctic catchment sequence. Polar Biol 40(9):1821–1834. https://doi.org/10.1007/s00300-017-2105-4
Kollmann FF, Côté Jr WA (1968) Principles of wood science and technology, vol I. Solid wood principles of wood science and technology, vol I solid wood. Springer-Verlag
Körner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115:445–459
Lambers H, Nagel OW, van Arendonk JJCM (1995) The control of biomass partitioning in plants from “favourable” and “stressful” environments: a role for gibberellins and cytokinins. Bulg. J Plant Physiol 21:24–32
Lambers H, Pons T, Chapin F (2008) Plant physiological ecology, 1st ed. Springer Verlag, New York
Li MH, **ao WF, Shi P, Wang SG, Zhong YD, Liu XL, Wang XD, Cai XH, Shi ZM (2008) Nitrogen and carbon source–sink relationships in trees at the Himalayan treelines compared with lower elevations. Plant Cell Environ 31:1377–1387
Lintunen A, Paljakka T, Jyske T et al (2016) Osmolality and non-structural carbohydrate composition in the secondary phloem of trees across a latitudinal gradient in Europe. Front Plant Sci 7:726. https://doi.org/10.3389/fpls.2016.00726
Liu X, Nie Y, Luo T, Yu J, Shen W, Zhang L (2016) Seasonal shift in climatic limiting factors on tree transpiration: evidence from sap flow observations at alpine treelines in Southeast Tibet. Front Plant Sci 7:1018. https://doi.org/10.3389/fpls.2016.01018
Lyr H, Hoffmann G (1967) Growth rates and growth periodicity of tree roots. Int Rev For Res (NY) 2:181–236
Magel E, Jay-Allemand C, Ziegler H (1994) Formation of heartwood substances in the stemwood of Robinia pseudoacacia L. II. Distribution of nonstructural carbohydrates and wood extractives across the trunk. Trees 8:165–171
Mao Z, Bonis M-L, Rey H, Saint-André L, Stokes A, Jourdan C (2013a) Which processes drive fine root elongation in a natural mountain forest ecosystem? Plant Ecolog Divers 6:231–243
Mao Z, Jourdan C, Bonis M-L, Pailler F, Rey H, Saint-André L, Stokes A (2013b) Modelling root demography in heterogeneous mountain forests and applications for slope stability analysis. Plant Soil 363:357–382
Mao Z, Wang Y, Jourdan C, Cécillon L, Nespoulous J, Rey H, Saint-André L, Stokes A (2015) Characterizing above-and belowground carbon partitioning in forest trees along an altitudinal gradient using area-based indicators. Arct Antarct Alp Res 47:59–69
Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London
Martens H, Jensen SA (1983) Partial least squares regression: a new two-stage NIR calibration method. In: Progress in cereal chemistry and technology, vol. 5a. Elsevier, Amsterdam, pp 607–647
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari H-S, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of belowground contributions to terrestrial biosphere processes. New Phytol 207:505–518
Mei L, **ong Y, Gu J, Wang Z, Guo D (2015) Whole-tree dynamics of non-structural carbohydrate and nitrogen pools across different seasons and in response to girdling in two temperate trees. Oecologia 177:333–344
Millard P, Sommerkorn M, Grelet GA (2007) Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol 175:11–28
Mohamed A, Monnier Y, Mao Z, Lobet G, Maeght JL, Ramel M, Stokes A (2017) An evaluation of methods for root image acquisition when using rhizotrons. Plant Methods. https://doi.org/10.1186/s13007-017-0160z
Nehls U (2008) Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot 59:1097–1108
Noland TL, Mohammed GH, Scott M (1996) The dependance of root growth potential on light level, photosynthetic rate, and root starch content in jack pine seedlings. New For 13:105–119
Ögren E (2000) Maintenance respiration correlates with sugar but not nitrogen concentration in dormant plants. Physiol Plant 108:295–299. https://doi.org/10.1034/j.1399-3054.2000.108003295.x
Ögren E, Nilsson T, Sundblad LG (1997) Relationship between respiratory depletion of sugars and loss of cold hardiness in coniferous seedlings over-wintering at raised temperatures: indications of different sensitivities of spruce and pine. Plant Cell Environ 20:247–253
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4–2. https://CRAN.R-project.org/package=vegan
Palacio S, Maestro M, Montserrat-Martí G (2007) Relationship between shoot-rooting and root-sprouting abilities and the carbohydrate and nitrogen reserves of Mediterranean dwarf shrubs. Ann Bot 100:865–874
Palacio S, Hoch G, Sala A, Körner C, Millard P (2014) Does carbon storage limit tree growth? New Phytol 201:1096–1100
Pallardy SG (2010) Physiology of woody plants. Academic Press
Pett-Ridge J, Firestone MK (2017) Using stable isotopes to explore root-microbe-mineral interactions in soil. Rhizosphere 3:244–253
Pinheiro J, Bates D, DebRoy S, Sarkar D (2017) Package ‘nlme’. URL http://cran.r-project.org/web/packages/nlme/nlme.pdf
Quentin AG, Pinkard EA, Ryan MG, Tissue DT, Baggett LS, Adams HD, Maillard P, Marchand J, Landhäusser SM, Lacointe A (2015) Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol 35:1146–1165
R Core Team (2013) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL: www.R-project.org/
Ramirez JA, Posada JM, Handa IT, Hoch G, Vohland M, Messier C, Reu B (2015) Near infrared spectroscopy (NIRS) predicts non structural carbohydrate concentrations in different tissue types of a broad range of tree species. Methods Ecol Evol 6:1018–1025
Reid CPP, Mexal JG (1977) Water stress effects on root exudation by lodgepole pine. Soil Biol Biochem 9:417–422
Rocha AV (2013) Tracking carbon within the trees. New Phytol 197:685–686
Rodríguez-Calcerrada J, Buatois B, Chiche E, Shahin O, Staudt M (2013) Leaf isoprene emission declines in Quercus pubescens seedlings experiencing drought–any implication of soluble sugars and mitochondrial respiration? Environ Exp Bot 85:36–42
Roumet C, Picon Cochard C, Dawson LA, Joffre R, Mayes R, Blanchard A, Brewer MJ (2006) Quantifying species composition in root mixtures using two methods: near infrared reflectance spectroscopy and plant wax markers. New Phytol 170:631–638
Schädel C, Blöchl A, Richter A, Hoch G (2009) Short-term dynamics of nonstructural carbohydrates and hemicelluloses in young branches of temperate forest trees during bud break. Tree Physiol 29:901–911
Sellin A (1994) Sapwood-heartwood proportion related to tree diameter, age, and growth rate in Picea abies. Can J For Res 24:1022–1028
Shenk JS, Westerhaus MO (1993) Near infrared reflectance analysis with single and multiproduct calibrations. Crop Sci 33:582–584
Shi P, Körner C, Hoch G (2006) End of season carbon supply status of woody species near the treeline in western China. Basic Appl Ecol 7:370–377
Simard S, Giovannelli A, Treydte K, Traversi ML, King GM, Frank D, Fonti P (2013) Intra-annual dynamics of non-structural carbohydrates in the cambium of mature conifer trees reflects radial growth demands. Tree Physiol 33:913–923
Stokes MA, Smiley TL (1968) An introduction to tree-ring dating. University of Chicago Press
Thaler P, Pagès L (1996) Root apical diameter and root elongation rate of rubber seedlings (Hevea brasiliensis) show parallel responses to photoassimilate availability. Physiol Plant 97:365–371
Tinus R, Burr K, Atzmon N, Riov J (2000) Relationship between carbohydrate concentration and root growth potential in coniferous seedlings from three climates during cold hardening and dehardening. Tree Physiol 20:1097–1104
Wang Y, Kim JH, Mao Z, Ramel M, Pailler F, Perez J, Rey H, Tron S., Jourdan C, Stokes A (2018) Tree root dynamics in montane and subalpine mixed forest patches. Ann Bot. https://doi.org/10.1093/aob/mcy021
Wiley E, Helliker B (2012) A re evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195:285–289
Zhu WZ, Cao M, Wang SG, **ao WF, Li MH (2012a) Seasonal dynamics of mobile carbon supply in Quercus aquifolioides at the upper elevational limit. PLoS One 7:e34213
Zhu WZ, **ang J-S, Wang S-G, Li M-H (2012b) Resprouting ability and mobile carbohydrate reserves in an oak shrubland decline with increasing elevation on the eastern edge of the Qinghai–Tibet Plateau. For Ecol Manag 278:118–126
Acknowledgements
Funding was received from the China Scholarship Council (YW) and the INRA metaprogram AAFCC (Adaptation of Agriculture and Forests to Climate Change). Thanks are due to S. Tron, M. Ramel and F. Pailler (INRA) for technical assistance. We thank the Mairie de Chamrousse and the ONF for allowing us access to the field sites. Thanks are also due to two anonymous reviewers and the Plant and Soil section editor Richard J. Simpson for their helpful comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Richard J. Simpson.
Electronic supplementary material
ESM 1
(DOCX 7067 kb)
Rights and permissions
About this article
Cite this article
Wang, Y., Mao, Z., Bakker, M.R. et al. Linking conifer root growth and production to soil temperature and carbon supply in temperate forests. Plant Soil 426, 33–50 (2018). https://doi.org/10.1007/s11104-018-3596-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3596-7