, Volume 31, Issue 6, pp 1745–1758 | Cite as

Dendrobiochemistry, a missing link to further understand carbon allocation during growth and decline of trees

  • Giuliano Maselli Locosselli
  • Marcos Silveira BuckeridgeEmail author


Key message

The combination of dendrochronology with biochemical features such as nonstructural and structural carbohydrate dynamics may lead to more reliable views of how tree growth correlates with changes in natural environments.


Carbon is fixed in forests worldwide, where large pools are stored in the woody tissues of trees. After assimilation via photosynthesis, its products are transported through the phloem to support metabolism, storage, and the construction of new tissues. The metabolic dynamics of the assimilated carbon of trees have been studied by plant biochemistry and physiology approaches, mostly in young trees. On the other hand, dendrochronology rarely employs these approaches. It has been used mostly for growth quantification related to mature trees. Therefore, both fields of tree science could be merged to bring new inferences about how the internal plant metabolic processes correlate with tree growth in their inhabiting environments. Here we review the current knowledge about (1) nonstructural and structural carbohydrates of trees, as studied by plant biochemistry and physiology; and (2) tree-ring analysis as a proxy for tree growth studied by dendrochronology. We further discuss the current evidence available in the literature and the perspectives of merging these plant science fields here named dendrobiochemistry. We expect that this compilation can provide additional insights into some unresolved issues related to tree biochemistry, physiology, and dendrochronology and consequently improve current understanding of terrestrial carbon cycle.


Dendrochronology Monosaccharides Wood Nonstructural carbohydrates Starch Sucrose Cell wall Climate 



Authors thank Dr. Veronica Angyalossy for assisting in Fig. 1 production as well as providing materials for its development and Edgar Matsuda for valuable inputs in the manuscript. We also thank the valuable inputs of the reviewers. MSB thanks the Conselho Nacional de Ciência e Tecnologia/(CNPq) for financial support (Grant number 302804/2016-1). GL thanks for the financial support for postdoctoral fellowship (FAPESP 2013/21728-2, 2015/25511-3). Authors thank financial support from Microsoft Research-FAPESP Institute (FAPESP 2011/52065-3).

Compliance with ethical standards

Conflict of interest

Authors declare that they have no conflict of interest.


  1. Alfieri FJ, Evert RF (1968) Seasonal development of the secondary phloem in pinus. Am J Bot 55(4):518–528CrossRefGoogle Scholar
  2. Amano E (2007) Pau-brasil, madeira e casca: formação, desenvolvimento e estrutura, Ph.D. thesis. University of São Paulo, São PauloGoogle Scholar
  3. Anderegg WRL, Kane JM, Anderegg DL (2012) Consequences of widespread tree mortality triggered by drought and temperature stress. Nat Clim Change 3:30–36CrossRefGoogle Scholar
  4. Anderegg WRL, Matinez-Vilalta J, Cailleret M, Camarero JJ, Ewers BE, Galbraith D, Gessler A, Grote R, Huang C, Levick SR, Powell TL, Rowland L, Sánchez-Salguero R, Trostiuk V (2016) When a tree dies in the forest: scaling climate-driven tree mortality to ecosystem water and carbon fluxes. Ecosystems 19:1133–1147CrossRefGoogle Scholar
  5. Arx G, Arzac A, Fonti P, Frank D, Zweifel R, Rigling A, Galiano L, Gessler A, Olano JM (2017) Responses of sapwood ray parenchyma and non-structural carbohydrates of Pinus sylvestris to drought and long-term irrigation. Funct Ecol. doi: 10.1111/1365-2435.12860 Google Scholar
  6. Babst F, Alexander MR, Szejner P, Bouriaud O, Klesse S, Roden J, Ciais P, Poulter B, Frank D, Moore DJP, Trouet V (2014) A tree-ring perspective on the terrestrial carbon cycle. Oecologia 176:307–322PubMedCrossRefGoogle Scholar
  7. Barbaroux C, Bréda N (2002) Contrasting distribution and seasonal dynamics of carbohydrate reserves in stem wood of adult ring-porous sessile oak and diffuse porous beech trees. Tree Physiol 22:1201–1210PubMedCrossRefGoogle Scholar
  8. Bertaud F, Holmbom B (2004) Chemical composition of earlywood and latewood in Norway spruce heartwood, sapwood and transition zone. Wood Sci Technol 38:245–256CrossRefGoogle Scholar
  9. Bidhendi AJ, Geitmann A (2015) Relating the mechanics of primary plant cell wall to morphogenesis. J Exp Bot 67:449–461PubMedCrossRefGoogle Scholar
  10. Bigler C (2016) Trade-offs between growth rate, tree size and lifespan of mountain pine (Pinus montana) in the Swiss National Park. PLoS One 11:e0150402PubMedPubMedCentralCrossRefGoogle Scholar
  11. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546PubMedCrossRefGoogle Scholar
  12. Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forest. Science 320:1444–1449PubMedCrossRefGoogle Scholar
  13. Boudet AM (2000) Lignins and lignification: selected issues. Plant Physiol Biochem 28(1/2):81–96CrossRefGoogle Scholar
  14. Bowman DMJS, Brienen RJW, Gloor E, Phillips OL, Prior LD (2013) Detecting trends in tree growth: not so simple. Trends Plant Sci 18(1):11–17PubMedCrossRefGoogle Scholar
  15. Brienen RJW, Zuidema PA (2006) Lifetime growth patterns and ages of Bolivian rain forest trees obtained by tree ring analysis. J Ecol 94:481–493CrossRefGoogle Scholar
  16. Brienen RJW, Zuidema PA, Martínez-Ramos M (2010) Attaining the canopy in dry and moist tropical forests: strong differences in tree growth trajectories reflect variation in growing conditions. Oecologia 163:485–496PubMedCrossRefGoogle Scholar
  17. Brienen RJW, Wanek W, Hietz P (2011) Stable carbon isotopes in tree rings indicate improved water use efficiency and drought responses of tropical dry forest tree species. Trees Struct Funct 25:103–113CrossRefGoogle Scholar
  18. Brienen JW, Gloor M, Ziv G (2017) Tree demography dominates long-term growth trends from tree rings. Glob Change Biol 23:474–484CrossRefGoogle Scholar
  19. Briffa KR, Osborn TJ, Schweingruber FH (2002) Tree-ring width and density data around the Northern Hemisphere: part 1, local and regional climate signals. Holocene 12(6):737–757CrossRefGoogle Scholar
  20. Buckeridge MS, Santos HP, Tiné MAS (2000) Mobilisation of storage cell wall polysaccharides in seeds. Plant Physiol Biochem 38(1/2):141–156CrossRefGoogle Scholar
  21. Buckley BM, Duangsthaporn K, Palakit K, Butler S, Syhapanya V, Xaybouangeun N (2007) Analyses of growth rings of Pinus merkusii from Lao P.D.R. For Ecol Manag 253:120–137CrossRefGoogle Scholar
  22. Caffall KH, Mohnen D (2009) The structure, function and biosynthesis of plant cell wall pectic polysaccharies. Carbohyd Res 344:1879–1900CrossRefGoogle Scholar
  23. Cailleret M et al (2016) A synthesis of radial growth patterns preceding tree mortality. Glob Change Biol. doi: 10.1111/gcb.13535 Google Scholar
  24. Camarero JJ, Gazol A, Sangüesa-Barreda G, Oliva J, Vicente-Serrano SM (2015) To die or not to die: early warnings of tree dieback in response to severe drought. J Ecol 103:44–57CrossRefGoogle Scholar
  25. Carbone MS, Czimczik CI, Keenan TF, Murakami PF, Pederson N, Schaberg PG, Xu X, Richardson AD (2013) Age, Allocation and availability of nonstructural carbon in mature red maple trees. New Phytol 200:1145–1155PubMedCrossRefGoogle Scholar
  26. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3(1):1–30PubMedCrossRefGoogle Scholar
  27. Chapin FS (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447CrossRefGoogle Scholar
  28. Coomes DA, Allen RB (2007) Effects of size, competition and altitude on growth. J Ecol 95:1084–1097CrossRefGoogle Scholar
  29. Corlett RT (2016) The impacts of droughts in tropical forests. Trends Plant Sci 21(7):584–593PubMedCrossRefGoogle Scholar
  30. Cornuault V, Manfield IW, Ralet M, Knox JP (2014) Epitope detection chromatography: a method to dissect the structural heterogeneity and inter-connections of plant cell wall matrix glycans. Plant J 78:715–722PubMedCrossRefGoogle Scholar
  31. Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326PubMedCrossRefGoogle Scholar
  32. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev 6(11):850–861CrossRefGoogle Scholar
  33. Cosgrove DJ (2016) Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot 67:463–473PubMedCrossRefGoogle Scholar
  34. Delaporte A, Bazot S, Damesin C (2016) Reduced stem growth but no reserve depletion or hydraulic impairment in beech suffering from long-term decline. Trees Struct Funct 30:265–279CrossRefGoogle Scholar
  35. Delpierre N, Barveiller D, Granda E, Dufrêne E (2016) Wood phenology, not carbon input, controls the interannual variability of wood growth in a temperate oak forest. New Phytol 210:459–470PubMedCrossRefGoogle Scholar
  36. DeMartini JD, Wyman CE (2011) Changes in composition and sugar release across the annual rings of wood and implications on recalcitrance. Biores Technol 102:1352–1358CrossRefGoogle Scholar
  37. Dietze MC, Sala M, Carbone MS, Czimczik CI, Mantooth JÁ, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687PubMedCrossRefGoogle Scholar
  38. Doughty CE, Matcalfe DB, Girardin CAJ, Amezquita FF, Durand L, Huasco WH, Silva-Espejo JE, Araujo-Murakami A, Costa MC, Costa ACL, Rocha W, Meir P, Galbraith D, Malhi Y (2015) Source and sink carbon dynamics and carbon allocation in the Amazon basin. Glob Biogeochem Cycles 29(5):645–655CrossRefGoogle Scholar
  39. Evert RF (2006) Esau’s plant anatomy: meristems, cells and tissues of plant body: their structure, function and development. Wiley-Interscience, New JerseyCrossRefGoogle Scholar
  40. Fajardo A, Piper FI, Pfund L, Körner C, Hoch G (2012) Variation of mobile carbon reserves in trees at the alpine tree line ecotone is under environmental control. New Phytol 195:749–802CrossRefGoogle Scholar
  41. Fajardo A, Piper FI, Hoch G (2013) Similar variation in carbon storage between deciduous and evergreen treeline species across elevational gradients. Ann Bot 112:623–631PubMedPubMedCentralCrossRefGoogle Scholar
  42. Fardusi MJ, Ferrio JP, Comas C, Voltas J, Dios VR, Serrano L (2016) Intra-specific association between carbon isotope composition and productivity in woody plants: a meta-analysis. Plant Sci 251:110–118PubMedCrossRefGoogle Scholar
  43. Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon–water relations. Academic Press, New York, pp 47–70CrossRefGoogle Scholar
  44. Fonti P, Jansen S (2013) Xylem plasticity in response to climate. New Phytol 195:734–736CrossRefGoogle Scholar
  45. Gérard B, Bréda N (2014) Radial distribution of carbohydrate reserves in the trunk of declining European beech trees (Fagus sylvatica L.). Ann For Sci 71:657–682CrossRefGoogle Scholar
  46. Gessler A, Trydet K (2016) The fate and age of carbon- insights into the storage and remobilization dynamics in trees. New Phytol 209:1338–1340PubMedCrossRefGoogle Scholar
  47. Gessler A, Ferrio JP, Hommel R, Treydte K, Werner RA, Monson RK (2014) Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the leaves to the wood. Tree Physiol 34:796–818PubMedCrossRefGoogle Scholar
  48. Gibson LJ (2012) The hierarchical structure and mechanics of plant materials. J R Soc Interface 9:2749–2766PubMedPubMedCentralCrossRefGoogle Scholar
  49. Groenendijk P, Sass-Klaassen U, Bongers F, Zuidema PA (2014) Potential of tree-ring analysis in a wet tropical forest: a case study on 22 commercial tree species in Central Africa. For Ecol Manag 323:65–78CrossRefGoogle Scholar
  50. Groenendijk P, Van Der Sleen P, Vlam M, Bunyavejchewin S, Bongers F, Zuidema PA (2015) No evidence for consistent long-term growth stimulation of 13 tropical tree species: results from tree-ring analysis. Glob Change Biol 21:3762–3776CrossRefGoogle Scholar
  51. Gruber A, Pirkebner D, Oberhuber W (2014) Seasonal dynamics of mobile carbohydrate pools in phloem and xylem of two alpine timberline conifers. Tree Physiol 33:1076–1083CrossRefGoogle Scholar
  52. Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees- from what we can measure to what we want to know. New Phytol. doi: 10.1111/nph.13955 Google Scholar
  53. Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168CrossRefGoogle Scholar
  54. Hayashi T, Kaida R (2011) Functions of xyloglucan in plant cells. Mol Plant 4(1):17–24PubMedCrossRefGoogle Scholar
  55. Helle G, Scheleser GH (2004) Beyond CO2-fixation by Rubisco—an interpretation of 13C/12C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant Cell Environ 27:367–380CrossRefGoogle Scholar
  56. Hoch G (2007) Cell wall hemicelluloses as mobile carbon stores in non-reproductive plant tissues. Funct Ecol 21:823–834CrossRefGoogle Scholar
  57. Hoch G (2015) Carbon reserves as indicators for carbon limitation in trees. In: Lüttge U, Beyschlag W (eds) Progress in botany, vol 76. Springer, Cham, pp 321–346Google Scholar
  58. Hoch G, Körner C (2012) Global patterns of mobile carbon stores in trees at the high-elevation tree line. Glob Ecol Biogeogr 21:861–871CrossRefGoogle Scholar
  59. Hoch G, Richter A, Körner C (2003) Nonstructural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081CrossRefGoogle Scholar
  60. Hughes MK (2002) Dendrochronology in climatology—the state of the art. Dendrochronologia 10(1–2):95–116CrossRefGoogle Scholar
  61. Iglesias DJ, Lliso I, Tadeo FR, Talon M (2002) Regulation of photosynthesis through source: sink imbalance in citrus is mediated by carbohydrate content in leaves. Physiol Plant 116:563–572CrossRefGoogle Scholar
  62. Johnson MO, Galbraith D, Gloor M et al (2016) Variation in stem mortality rates determines patterns of above-ground biomass in Amazonian forests: implications for dynamic global vegetation models. Glob Change Biol 22:2996–4013CrossRefGoogle Scholar
  63. Kagawa A, Sugimoto A, Maximov TC (2006) Seasonal course of translocation, storage and remobilization of 13C pulse-labeled photoassimilate in naturally growing Larix gmelinii saplings. New Phytol 171:793–804PubMedCrossRefGoogle Scholar
  64. King DA, Davies SJ, Tan S, Noor NSM (2006) The role of wood density and stem support costs in the growth and mortality of tropical trees. J Ecol 94:670–680CrossRefGoogle Scholar
  65. Klein T, Hoch G (2015) Tree carbon allocation dynamics determined using a carbon mass balance approach. New Phytol 205:147–159PubMedCrossRefGoogle Scholar
  66. Klein T, Hoch G, Yakir D, Körner C (2014) Drought stress, growth and nonstructural carbohydrate dynamics of pine trees in a semi-arid forest. Tree Physiol 34(9):981–992PubMedCrossRefGoogle Scholar
  67. Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17CrossRefGoogle Scholar
  68. Körner C (2013) Growth controls photosynthesis—mostly. Nova Acta Leopold 114:273–283Google Scholar
  69. Kozlowski C (1992) Carbohydrate sources and sinks in woody plants. Bot Rev 58:107–222CrossRefGoogle Scholar
  70. Landis RM, Peart DR (2005) Early performance predicts canopy attainment across life histories in subalpine forest trees. Ecology 88(1):63–72CrossRefGoogle Scholar
  71. Lanner RM (2002) Why do trees live so long? Ageing Res Rev 1:653–671PubMedCrossRefGoogle Scholar
  72. Larson PR (1994) The vascular cambium: development and structure. Springer, BerlinCrossRefGoogle Scholar
  73. Lempereur M, Martin-StPaul NK, Damesin C, Joffre R, Ourcival J, Rocheteau A, Rambal S (2015) Grwoth is a better predictor of stem increment than carbon supply in a Mediterranean oak forest: implications for assessing forest productivity under climate change. New Phytol 207:579–590PubMedCrossRefGoogle Scholar
  74. Li G, Harrison SP, Prentice IC (2016) A model analysis of climate and CO2 controls on tree growth and carbon allocation in a semi-arid woodland. Ecol Model 342:175–185CrossRefGoogle Scholar
  75. Locosselli GM, Buckeridge MS, Moreira MZ, Ceccantini G (2013) A multi-proxy dendroecological analysis of two tropical species (Hymenaea spp., Leguminosae) growing in a vegetation mosaic. Trees Struct Funct 27:25–36CrossRefGoogle Scholar
  76. Locosselli GM, Cardim RH, Ceccantini G (2016a) Rock outcrops reduce temperature-induced stress for tropical conifer by decoupling regional climate in the semiarid environment. Int J Biometeorol 60(5):639–649PubMedCrossRefGoogle Scholar
  77. Locosselli GM, Schongart J, Ceccantini G (2016b) Climate/growth relations and teleconnections for a Hymenaea courbaril (Leguminosae) population inhabiting the dry forest on karst. Trees Struct Funct 30(4):1127–1136CrossRefGoogle Scholar
  78. Locosselli GM, Krottenthaler S, Pitsch P, Anhuf D, Ceccantini G (2017) Age and growth rate of congeneric tree species (Hymenaea spp.—Leguminosae) inhabiting different tropical biomes. Erdkunde. doi: 10.3112/erdkunde.2017.01.03 Google Scholar
  79. López BC, Gracia CA, Sabatée S, Keenan T (2009) Assessing the resilience of Mediterranean holm oaks to disturbances using selective thinning. Acta Oecol 35:849–854CrossRefGoogle Scholar
  80. Mahli Y (2011) The productivity, metabolism and carbon cycle of tropical forest vegetation. J Ecol 100:65–75Google Scholar
  81. McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801CrossRefGoogle Scholar
  82. McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26(10):523–532PubMedCrossRefGoogle Scholar
  83. Millard P, Sommerkorn M, Grelet G (2007) Environmental change and carbon limitation in trees: a biochemical ecophysiological and ecosystem appraisal. New Phytol 175:11–28PubMedCrossRefGoogle Scholar
  84. Muhr J, Angert A, Negrón-Juárez RI, Muñoz WA, Kraemer G, Chambers JQ, Trumbore SE (2013) Carbon dioxide emitted from live stems of tropical trees is several year old. Tree Physiol 33(7):743–752PubMedCrossRefGoogle Scholar
  85. Newell EA, Mulkey SS, Wright SJ (2002) Seasonal patterns of carbohydrate storage in four tropical tree species. Oecologia 131:333–342PubMedCrossRefGoogle Scholar
  86. O’Sullivan AC (1997) Cellulose: the structure slowly unravels. Cellulose 4:173–207CrossRefGoogle Scholar
  87. Obeso JR (2002) The cost of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  88. Olano JM, Arzac A, García-Cervigón AI, Arx G, Rozas V (2013) New star on the stage: amount of ray parenchyma in tree rings shows a link to climate. New Phytol 198:486–495PubMedCrossRefGoogle Scholar
  89. Palacio S, Hoch G, Sala A, Körner C, Millard P (2014) Does carbon storage limit tree growth? New Phytol 201:1096–1100PubMedCrossRefGoogle Scholar
  90. Pattathil S, Avci U, Baldwin D, Swennes AG, McGill JA et al (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153:514–525PubMedPubMedCentralCrossRefGoogle Scholar
  91. Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214CrossRefGoogle Scholar
  92. Piper FL (2011) Dorught induces opposite changes in the concentration of nonstructural carbohydrates of two evergreen Nothofagus species of differential drought resistence. Ann For Sci 68(2):415–424CrossRefGoogle Scholar
  93. Plavcová L, Jansen S (2015) The role of xylem parenchyma in the storage and utilization of nonstructural carbohydrates. In: Hacke U (ed) Functional and ecological xylem anatomy. Springer, Cham, pp 209–234Google Scholar
  94. Reichenbacker RR, Schultz RC, Hart ER (1996) Artificial defoliation effect on Populus growth, biomass production, and total nonstructural carbohydrate concentration. Environ Entomol 25:632–642CrossRefGoogle Scholar
  95. Reichstein M, Bahn M, Ciais P, Frank D, Mahecha MD, Senevirante SI, Zscheischlwe J, Beer C, Buchmann N, Frank DC (2013) Climate extremes and the carbon cycle. Nature 500:287–295PubMedCrossRefGoogle Scholar
  96. Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY, Murakami P, Schaberg PG, Xu X (2013) Seasonal dynamics and age of stem wood nonstructural carbohydrates in temperate forest trees. New Phytol 197:850–861PubMedCrossRefGoogle Scholar
  97. Richardson AD, Carbone MS, Huggett BA, Furze ME, Czimczik CI, Walker JC, Xu X, Schaberg PG, Murakami P (2015) Distribution and mixing of old and new nonstructural carbon in two temperate trees. New Phytol 206:590–597PubMedPubMedCentralCrossRefGoogle Scholar
  98. Rocha AV, Goulden ML, Dunn AL, Wofsy SC (2006) On linking interannual tree ring variability with observations of whole-forest CO2 flux. Glob Change Biol 12:1378–1389CrossRefGoogle Scholar
  99. Schädel C, Richter A, Blöchl A, Hoch G (2009a) Quantification and monosaccharide composition of hemicelluloses from different plant functional types. Plant Physiol Biochem 48(1):1–8PubMedCrossRefGoogle Scholar
  100. Schädel C, Richter A, Blöchl A, Hoch G (2009b) Short-term dynamics of nonstructural carbohydrates and hemicelluloses in young branches of temperate forest trees during bud break. Tree Physiol 29:901–911PubMedCrossRefGoogle Scholar
  101. Schädel C, Richter A, Blöchl A, Hoch G (2010) Hemicellulose concentration and composition in plant cell walls under extreme carbon source-sink imbalances. Physiol Palnt 139:241–255Google Scholar
  102. Scharlemann JPW, Tanner EVJ, Hiederer R, Kapos V (2014) Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Manag 5(1):81–91CrossRefGoogle Scholar
  103. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedCrossRefGoogle Scholar
  104. Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Glob Change Biol 1(1):77–91CrossRefGoogle Scholar
  105. Schippers P, Vlam M, Zuidema PA, Sterck F (2015) Sapwood allocation in tropical trees: a test of hypotheses. Funct Plant Biol 42:697–719CrossRefGoogle Scholar
  106. Schweingruber FH (1988) Tree rings. Basics and applications of dendrochronology. Kluwer, DordrechtGoogle Scholar
  107. Shibata R, Kurokawa H, Shibata M, Tanaka H, Lida S, Masaki T, Nakashizuka T (2016) Relations between resprouting ability, species traits and resource allocation patterns in woody species in a temperate forest. Funct Ecol 30:1205–1215CrossRefGoogle Scholar
  108. Tavares EQP, Buckeridge MS (2015) Do cell walls have a code? Plant Sci 241:286–294PubMedCrossRefGoogle Scholar
  109. Thomas SC, Martin AR (2012) Carbon content of tree tissues: a synthesis. Forests 3:332–352CrossRefGoogle Scholar
  110. Timell TE (1967) Recent progress in the chemistry of wood hemicelluloses. Wood Sci Technol 1:45–70CrossRefGoogle Scholar
  111. Tognetti R, Lombardi F, Lasserre B, Cherubini P, Marchetti M (2014) Tree-ring stable isotopes reveal twentieth-century increases in water-use efficiency of Fagus sylvatica and Nothofagus spp. in Italian and Chilean Mountains. PLoS One 9(11):e113136PubMedPubMedCentralCrossRefGoogle Scholar
  112. Tschaplinski TJ, Blake TJ (1994) Carbohydrate mobilization following shoot defoliation and decapitation in hybrid poplar. Tree Physiol 14:141–151PubMedCrossRefGoogle Scholar
  113. Van Der Sleen P, Groenendijk P, Vlam M et al (2015) No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nat Geosci 8:24–28CrossRefGoogle Scholar
  114. Van Der Sleen P, Gorenendijk P, Vlam M, Anten NPR, Bongers F, Zuidema PA (2016) Trends in tropical tree growth: re-analyses confirm earlier findings. Glob Change Biol. doi: 10.1111/gcb.13572 Google Scholar
  115. Würth MR, Peláez-Riedl S, Wright SJ, Körner C (2005) Nonstructural carbohydrates pools in a tropical forest. Oecologia 143:11–24PubMedCrossRefGoogle Scholar
  116. Ye Z, Zhong R (2015) Molecular control of wood formation in trees. J Exp Bot 66:4119–4131PubMedCrossRefGoogle Scholar
  117. Zhou T, Luo Y (2008) Spatial patterns of ecosystem carbon residence time and NPP-driven carbon uptake in the conterminous United States. Glob Biogeochem Cycles 22(3):GB3032. doi: 10.1029/2007GB002939 CrossRefGoogle Scholar
  118. Zykwinska AW, Ralet M, Garnier CD, Thibault JJ (2005) Evidence for in vitro binding of pectins side chains to cellulose. Plant Physiol 139(1):397–407PubMedPubMedCentralCrossRefGoogle Scholar
  119. Zykwinska A, Thibault J, Ralet M (2008) Competitive binding of pectin and xyloglucan with primary cell wall cellulose. Carbohyd Polym 74:957–961CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Giuliano Maselli Locosselli
    • 1
  • Marcos Silveira Buckeridge
    • 1
    Email author
  1. 1.Laboratory of Plant Physiological Ecology (LAFIECO), Department of Botany, Institute of BiosciencesUniversity of São PauloSão PauloBrazil

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