Nonstructural carbon (NSC) provides the carbon and energy for plant growth and survival. In woody plants, fundamental questions about NSC remain unresolved: Is NSC storage an active or passive process? Do older NSC reserves remain accessible to the plant? How is NSC depletion related to mortality risk? Herein we review conceptual and mathematical models of NSC dynamics, recent observations and experiments at the organismal scale, and advances in plant physiology that have provided a better understanding of the dynamics of woody plant NSC. Plants preferentially use new carbon but can access decade-old carbon when the plant is stressed or physically damaged. In addition to serving as a carbon and energy source, NSC plays important roles in phloem transport, osmoregulation, and cold tolerance, but how plants regulate these competing roles and NSC depletion remains elusive. Moving forward requires greater synthesis of models and data and integration across scales from -omics to ecology.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Ainsworth EA, Long SP. 1.  2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol. 163:351–72 [Google Scholar]
  2. Allen MT, Prusinkiewicz P, DeJong TM. 2.  2005. Using L-systems for modeling source-sink interactions, architecture and physiology of growing trees: the L-PEACH model. New Phytol. 166:869–80 [Google Scholar]
  3. Baldocchi D. 3.  2008. Breathing of the terrestrial biosphere: lessons learned from a global network of carbon dioxide flux measurement systems. Aust. J. Bot. 56:1–26 [Google Scholar]
  4. Barbaroux C, Bréda N. 4.  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. 22:1201–10 [Google Scholar]
  5. Barry KM, Quentin A, Eyles A, Pinkard EA. 5.  2012. Consequences of resource limitation for recovery from repeated defoliation in Eucalyptus globulus Labilladière. Tree Physiol. 32:24–35 [Google Scholar]
  6. Bell TL, Ojeda F. 6.  1999. Underground starch storage in Erica species of the Cape Floristic region—differences between seeders and resprouters. New Phytol. 144:143–52 [Google Scholar]
  7. Berninger F, Nikinmaa E, Sievanen R, Nygren P. 7.  2000. Modelling of reserve carbohydrate dynamics, regrowth and nodulation in a N2-fixing tree managed by periodic prunings. Plant Cell Environ. 23:1025–40 [Google Scholar]
  8. Bond WJ, Midgley JJ. 8.  2001. Ecology of sprouting in woody plants: the persistence niche. Trends Ecol. Evol. 16:45–51 [Google Scholar]
  9. Brunner I, Brodbeck S, Walthert L. 9.  2002. Fine root chemistry, starch concentration, and “vitality” of subalpine conifer forests in relation to soil pH. For. Ecol. Manag. 165:75–84 [Google Scholar]
  10. Canham CD, Kobe RK, Latty EF, Chazdon RL. 10.  1999. Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121:1–11 [Google Scholar]
  11. Cannell M, Dewar R. 11.  1994. Carbon allocation in trees: a review of concepts for modelling. Adv. Ecol. Res. 25:59–104 [Google Scholar]
  12. Carbone MS, Czimczik CI, Keenan TF, Murakami PF, Pederson N. 12.  et al.2014 Age, allocation and availability of nonstructural carbon in mature red maple trees. New Phytol. 200:1145–55 [Google Scholar]
  13. Carbone MS, Czimczik CI, McDuffee KE, Trumbore SE. 13.  2007. Allocation and residence time of photosynthetic products in a boreal forest using a low-level 14C pulse-chase labeling technique. Glob. Change Biol. 13:466–77 [Google Scholar]
  14. Carbone MS, Still CJ, Ambrose AR, Dawson TE, Williams AP. 14.  et al. 2011. Seasonal and episodic moisture controls on plant and microbial contributions to soil respiration. Oecologia 167:265–78 [Google Scholar]
  15. Carbone MS, Trumbore SE. 15.  2007. Contribution of new photosynthetic assimilates to respiration by perennial grasses and shrubs: residence times and allocation patterns. New Phytol. 176:124–35 [Google Scholar]
  16. Chantuma P, Lacointe A, Kasemsap P, Thanisawanyangkura S, Gohet E. 16.  et al. 2009. Carbohydrate storage in wood and bark of rubber trees submitted to different level of C demand induced by latex tapping. Tree Physiol. 29:1021–31 [Google Scholar]
  17. Chapin FS, Schulze E, Mooney HA. 17.  1990. The ecology and economics of storage in plants. Annu. Rev. Ecol. Syst. 21:423–47 [Google Scholar]
  18. Coley PD, Massa M, Lovelock CE, Winter K. 18.  2002. Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree. Oecologia 133:62–69 [Google Scholar]
  19. Cooper OR, Parrish DD, Stohl A, Trainer M, Nédélec P. 19.  et al. 2010. Increasing springtime ozone mixing ratios in the free troposphere over western North America. Nature 463:344–48 [Google Scholar]
  20. Cropper WP, Gholz HL. 20.  1993. Simulation of the carbon dynamics of a Florida slash pine plantation. Ecol. Model. 66:231–49 [Google Scholar]
  21. Curtis PS. 21.  1996. A meta-analysis of leaf gas exchange and nitrogen in trees grown under elevated carbon dioxide. Plant Cell Environ. 19:127–37 [Google Scholar]
  22. Czimczik CI, Trumbore SE, Carbone MS, Winston GC. 22.  2006. Changing sources of soil respiration with time since fire in a boreal forest. Glob. Change Biol. 12:957–71 [Google Scholar]
  23. Dannoura M, Maillard P, Fresneau C, Plain C, Berveiller D. 23.  et al. 2011. In situ assessment of the velocity of carbon transfer by tracing 13C in trunk CO2 efflux after pulse labelling: variations among tree species and seasons. New Phytol. 190:181–92 [Google Scholar]
  24. Del Tredici P. 24.  2001. Sprouting in temperate trees: a morphological and ecological review. Bot. Rev. 67:121–40 [Google Scholar]
  25. Dewar RC, Medlyn BE, McMurtrie RE. 25.  1999. Acclimation of the respiration photosynthesis ratio to temperature: insights from a model. Glob. Change Biol. 5:615–22 [Google Scholar]
  26. Dick JM, Dewar RC. 26.  1992. A mechanistic model of carbohydrate dynamics during adventitious root development in leafy cuttings. Ann. Bot. 70:371–77 [Google Scholar]
  27. Dietze MC, Clark JS. 27.  2008. Changing the gap dynamics paradigm: vegetative regeneration control on forest response to disturbance. Ecol. Monogr. 78:331–47 [Google Scholar]
  28. Dietze MC, Moorcroft PR. 28.  2011. Tree mortality in the eastern and central United States: patterns and drivers. Glob. Change Biol. 17:3312–26 [Google Scholar]
  29. Else MA, Tiekstra AE, Croker SJ, Davies WJ, Jackson MB. 29.  1996. Stomatal closure in flooded tomato plants involves abscisic acid and a chemically unidentified anti-transpirant in xylem sap. Plant Physiol. 112:239–47 [Google Scholar]
  30. Epron D, Bahn M, Derrien D, Lattanzi FA, Pumpanen J. 30.  et al. 2012. Pulse-labelling trees to study carbon allocation dynamics: a review of methods, current knowledge and future prospects. Tree Physiol. 32:776–98 [Google Scholar]
  31. Epron D, Ngao J, Dannoura M, Bakker MR, Zeller B. 31.  et al. 2011. Seasonal variations of belowground carbon transfer assessed by in situ 13CO2 pulse labelling of trees. Biogeosciences 8:1153–68 [Google Scholar]
  32. Felten S von, Hättenschwiler S, Saurer M, Siegwolf R. 32.  2007. Carbon allocation in shoots of alpine treeline conifers in a CO2 enriched environment. Trees 21:283–94 [Google Scholar]
  33. Fine PVA, Mesones I, Coley PD. 33.  2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663–65 [Google Scholar]
  34. Fischer C, Höll W. 34.  1991. Food reserves of Scots pine (Pinus sylvestris L.). Trees 5:187–95 [Google Scholar]
  35. Fisher R, McDowell N, Purves D, Moorcroft P, Sitch S. 35.  et al. 2010. Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations. New Phytol. 187:666–81 [Google Scholar]
  36. Friedlingstein P, Joel G, Field CB, Fung IY. 36.  1999. Toward an allocation scheme for global terrestrial carbon models. Glob. Change Biol. 5:755–70 [Google Scholar]
  37. Fu QS, Cheng LL, Guo YD, Turgeon R. 37.  2011. Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiol. 157:1518–27 [Google Scholar]
  38. Galiano L, Martínez-Vilalta J, Lloret F. 38.  2011. Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytol. 190:750–59 [Google Scholar]
  39. Galvez DA, Landhausser SM, Tyree MT. 39.  2013. Low root reserve accumulation during drought may lead to winter mortality in poplar seedlings. New Phytol. 198:139–48 [Google Scholar]
  40. Génard M, Dauzat J, Franck N, Lescourret F, Moitrier N. 40.  et al. 2008. Carbon allocation in fruit trees: from theory to modelling. Trees 22:269–82 [Google Scholar]
  41. Genet H, Bréda N, Dufrêne E. 41.  2010. Age-related variation in carbon allocation at tree and stand scales in beech (Fagus sylvatica L.) and sessile oak (Quercus petraea (Matt.) Liebl.) using a chronosequence approach. Tree Physiol. 30:177–92 [Google Scholar]
  42. Gholz H, Cropper W. 42.  1991. Carbohydrate dynamics in mature Pinus elliottii var. elliottii trees. Can. J. For. Res. 21:1742–47 [Google Scholar]
  43. Gough CM, Flower CE, Vogel CS, Dragoni D, Curtis PS. 43.  2009. Whole-ecosystem labile carbon production in a north temperate deciduous forest. Agric. For. Meteorol. 149:1531–40 [Google Scholar]
  44. Graf A, Smith AM. 44.  2011. Starch and the clock: the dark side of plant productivity. Trends Plant Sci. 16:169–75 [Google Scholar]
  45. Hartmann H, Ziegler W, Trumbore S. 45.  2013. Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct. Ecol. 27:413–27 [Google Scholar]
  46. Hättenschwiler S, Handa I, Egli L. 46.  2002. Atmospheric CO2 enrichment of alpine treeline conifers. New Phytol. 156:363–75 [Google Scholar]
  47. Hoch G, Körner C. 47.  2012. Global patterns of mobile carbon stores in trees at the high-elevation tree line. Glob. Ecol. Biogeogr. 21:861–71 [Google Scholar]
  48. Hoch G, Richter A, Körner C. 48.  2003. Non-structural carbon compounds in temperate forest trees. Plant Cell Environ. 26:1067–81 [Google Scholar]
  49. Hoffmann WA, Orthen B, Franco AC. 49.  2004. Constraints to seedling success of savanna and forest trees across the savanna-forest boundary. Oecologia 140:252–60 [Google Scholar]
  50. Högberg P, Högberg MN, Göttlicher SG, Betson NR, Keel SG. 50.  et al. 2008. High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol. 177:220–28 [Google Scholar]
  51. Hopkins F, Gonzalez-Meler MA, Flower CE, Lynch DJ, Czimczik C. 51.  et al. 2013. Ecosystem-level controls on root-rhizosphere respiration. New Phytol. 199:339–51 [Google Scholar]
  52. Ichie T, Igarashi S, Yoshida S, Kenzo T, Masaki T, Tayasu I. 52.  2013. Are stored carbohydrates necessary for seed production in temperate deciduous trees?. J. Ecol. 101:525–31 [Google Scholar]
  53. Keane RE, Austin M, Field C, Huth A, Lexer MJ. 53.  et al. 2001. Tree mortality in gap models: application to climate change. Clim. Change 51:509–40 [Google Scholar]
  54. Keel SG, Seidwolf RTW, Körner C. 54.  2006. Canopy CO2 enrichment permits tracing the fate of recently assimilated carbon in a mature deciduous forest. New Phytol. 172:319–29 [Google Scholar]
  55. Keel SG, Siegwolf RTW, Jaggi M, Körner C. 55.  2007. Rapid mixing between old and new C pools in the canopy of mature forest trees. Plant Cell Environ. 30:963–72 [Google Scholar]
  56. Keeley J. 56.  2004. Impact of antecedent climate on fire regimes in coastal California. Int. J. Wildland Fire 13:173–82 [Google Scholar]
  57. Keller JD, Loescher WH. 57.  1989. Nonstructural carbohydrate partitioning in perennial parts of sweet cherry. J. Am. Soc. Hortic. Sci. 114:969–75 [Google Scholar]
  58. Knox KJE, Clarke PJ. 58.  2005. Nutrient availability induces contrasting allocation and starch formation in resprouting and obligate seeding shrubs. Funct. Ecol. 19:690–98 [Google Scholar]
  59. Kobe RK. 59.  1997. Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80:226–33 [Google Scholar]
  60. Kobe RK, Iyer M, Walters MB. 60.  2010. Optimal partitioning theory revisited: nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology 91:166–79 [Google Scholar]
  61. Körner C. 61.  2003. Carbon limitation in trees. J. Ecol. 91:4–17 [Google Scholar]
  62. Körner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG. 62.  et al. 2005. Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309:1360–62 [Google Scholar]
  63. Kozlowski TT. 63.  1992. Carbohydrate sources and sinks in woody plants. Bot. Rev. 58:107–222 [Google Scholar]
  64. Kozlowski TT, Pallardy S. 64.  2002. Acclimation and adaptive responses of woody plants to environmental stresses. Bot. Rev. 68:279–334 [Google Scholar]
  65. Krepkowski J, Gebrekirstos A, Shibistova O, Bräuning A. 65.  2013. Stable carbon isotope labeling reveals different carry-over effects between functional types of tropical trees in an Ethiopian mountain forest. New Phytol. 199:441–51 [Google Scholar]
  66. Kreuzwieser J, Papadopoulou E, Rennenberg H. 66.  2004. Interaction of flooding with carbon metabolism of forest trees. Plant Biol. 6:299–306 [Google Scholar]
  67. Kuptz D, Fleischmann F, Matyssek R, Grams TEE. 67.  2011. Seasonal patterns of carbon allocation to respiratory pools in 60-yr-old deciduous (Fagus sylvatica) and evergreen (Picea abies) trees assessed via whole-tree stable carbon isotope labeling. New Phytol. 191:160–72 [Google Scholar]
  68. Kuzyakov Y, Gavrichkova O. 68.  2010. Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob. Change Biol. 16:3386–406 [Google Scholar]
  69. Lacointe A. 69.  2000. Carbon allocation among tree organs: a review of basic processes and representation in functional-structural tree models. Ann. For. Sci. 57:521–33 [Google Scholar]
  70. Landhäusser SM, Lieffers VJ. 70.  2012. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees 26:653–61 [Google Scholar]
  71. Landolt W, Günthardt-Goerg M, Pfenninger I, Scheidegger C. 71.  1994. Ozone-induced microscopical changes and quantitative carbohydrate contents of hybrid poplar (Populus×euramericana). Trees 8:183–90 [Google Scholar]
  72. Langley J, Drake B, Hungate BA. 72.  2002. Extensive belowground carbon storage supports roots and mycorrhizae in regenerating scrub oaks. Oecologia 131:542–48 [Google Scholar]
  73. Le Dizès S, Cruiziat P, Lacointe A, Sinoquet H, Le Roux X. 73.  et al. 1997. A model for simulating structure-function relationships in walnut tree growth processes. Silva Fenn. 31:313–28 [Google Scholar]
  74. Le Roux X, Lacointe A, Escobar-Gutiérrez A, Le Dizès S. 74.  2001. Carbon-based models of individual tree growth: a critical appraisal. Ann. For. Sci. 58:469–506 [Google Scholar]
  75. Leakey ADB, Bishop KA, Ainsworth EA. 75.  2012. A multi-biome gap in understanding of crop and ecosystem responses to elevated CO2. Curr. Opin. Plant Biol. 15:228–36 [Google Scholar]
  76. Levy PE, Lucas ME, McKay HM, Escobar-Gutierrez AJ, Rey A. 76.  2000. Testing a process-based model of tree seedling growth by manipulating [CO2] and nutrient uptake. Tree Physiol. 20:993–1005 [Google Scholar]
  77. Li J, Powell TL, Seiler TJ, Johnson DP, Anderson HP. 77.  et al. 2007. Impacts of Hurricane Frances on Florida scrub-oak ecosystem processes: defoliation, net CO2 exchange and interactions with elevated CO2. Glob. Change Biol. 13:1101–13 [Google Scholar]
  78. Li M, Hoch G, Körner C. 78.  2002. Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees 16:331–37 [Google Scholar]
  79. Litton CM, Raich JW, Ryan MG. 79.  2007. Carbon allocation in forest ecosystems. Glob. Change Biol. 13:2089–109 [Google Scholar]
  80. Luo Z-B, Calfapietra C, Liberloo M, Scarascia-Mugnozza G, Polle A. 80.  2006. Carbon partitioning to mobile and structural fractions in poplar wood under elevated CO2 (EUROFACE) and N fertilization. Glob. Change Biol. 12:272–83 [Google Scholar]
  81. Lux D, Leonardi S, Muller J, Wiemken A, Fluckiger W. 81.  1997. Effects of ambient ozone concentrations on contents of non-structural carbohydrates in young Picea abies and Fagus sylvatica. New Phytol. 137:399–409 [Google Scholar]
  82. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N. 82.  et al. 2008. Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought?. New Phytol. 178:719–39 [Google Scholar]
  83. McLaughlin SB, McConathy RK, Beste B. 83.  1979. Seasonal changes in within-canopy allocation of 14C-photosynthate by white oak. For. Sci. 25:361–70 [Google Scholar]
  84. McNeely R. 84.  1994. Long-term environmental monitoring of 14C levels in the Ottawa region. Environ. Int. 20:675–79 [Google Scholar]
  85. Mencuccini M, Hölttä T. 85.  2010. The significance of phloem transport for the speed with which canopy photosynthesis and belowground respiration are linked. New Phytol. 185:189–203 [Google Scholar]
  86. Mitchell PJ, O'Grady AP, Tissue DT, White DA, Ottenschlaeger ML, Pinkard EA. 86.  2013. Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol. 197:862–72 [Google Scholar]
  87. Muhr J, Angert A, Juárez RN, Muñoz WA, Kraemer G. 87.  et al. 2013. Carbon dioxide emitted from live stems of tropical trees is several years old. Tree Physiol. 33:743–52 [Google Scholar]
  88. Munch E. 88.  1927. Dynamik der Saftstromungen. Ber. Dtsch. Bot. Ges. 44:69–71 [Google Scholar]
  89. Myers JA, Kitajima K. 89.  2007. Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J. Ecol. 95:383–95 [Google Scholar]
  90. Nardini A, Lo Gullo MA, Salleo S. 90.  2011. Refilling embolized xylem conduits: Is it a matter of phloem unloading?. Plant Sci. 180:604–11 [Google Scholar]
  91. Nelson E, Dickson R. 91.  1981. Accumulation of food reserves in cottonwood stems during dormancy induction. Can. J. For. Res. 11:145–54 [Google Scholar]
  92. Newell EA, Mulkey SS, Wright SJ. 92.  2002. Seasonal patterns of carbohydrate storage in four tropical tree species. Oecologia 131:333–42 [Google Scholar]
  93. Nzunda EF, Griffiths ME, Lawes MJ. 93.  2008. Sprouting by remobilization of above-ground resources ensures persistence after disturbance of coastal dune forest trees. Funct. Ecol. 22:577–82 [Google Scholar]
  94. Ogee J, Barbour MM, Wingate L, Bert D, Bosc A. 94.  et al. 2009. A single-substrate model to interpret intra-annual stable isotope signals in tree-ring cellulose. Plant Cell Environ. 32:1071–90 [Google Scholar]
  95. Ogle K, Pacala SW. 95.  2009. A modeling framework for inferring tree growth and allocation from physiological, morphological and allometric traits. Tree Physiol. 29:587–605 [Google Scholar]
  96. Palacio S, Hernández R, Maestro-Martínez M, Camarero JJ. 96.  2012. Fast replenishment of initial carbon stores after defoliation by the pine processionary moth and its relationship to the re-growth ability of trees. Trees 26:1627–40 [Google Scholar]
  97. Paynter VA, Reardon JC, Schelburne VB. 97.  1992. Changing carbohydrate profiles in shortleaf pine (Pinus echinata) after prolonged exposure to acid rain and ozone. Can. J. For. Res. 22:1556–61 [Google Scholar]
  98. Piispanen R, Saranpää P. 98.  2001. Variation of non-structural carbohydrates in silver birch (Betula rendula Roth) wood. Trees 15:444–51 [Google Scholar]
  99. Piper FI. 99.  2011. Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen nothofagus species of differential drought resistance. Ann. For. Sci. 68:415–24 [Google Scholar]
  100. Piper FI, Reyes-Díaz M, Corcuera LJ, Lusk CH. 100.  2009. Carbohydrate storage, survival, and growth of two evergreen nothofagus species in two contrasting light environments. Ecol. Res. 24:1233–41 [Google Scholar]
  101. Poorter L, Kitajima K. 101.  2007. Carbohydrate storage and light requirements of tropical moist and dry forest tree species. Ecology 88:1000–11 [Google Scholar]
  102. Regier N, Streb S, Cocozza C, Schaub M, Cherubini P. 102.  et al. 2009. Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. Plant Cell Environ. 32:1724–36 [Google Scholar]
  103. Reich PB. 103.  1987. Quantifying plant response to ozone: a unifying theory. Tree Physiol. 3:63–91 [Google Scholar]
  104. Rennie EA, Turgeon R. 104.  2009. A comprehensive picture of phloem loading strategies. Proc. Natl. Acad. Sci. USA 106:14162–67 [Google Scholar]
  105. Retzlaff WA, Weinstein DA, Laurence JA, Gollands B. 105.  1996. Simulated root dynamics of a 160-year-old sugar maple (Acer saccharum Marsh) tree with and without ozone exposure using the TREGRO model. Tree Physiol. 16:915–21 [Google Scholar]
  106. Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY. 106.  et al. 2013. Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol. 197:850–61 [Google Scholar]
  107. Ruehr NK, Offermann CA, Gessler A, Winkler JB, Ferrio JP. 107.  et al. 2009. Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux. New Phytol. 184950–61 [Google Scholar]
  108. Ruelland E, Vaultier MN, Zachowski A, Hurry V. 108.  2009. Cold signalling and cold acclimation in plants. Advances in Botanical Research 49 J-C Kader, M Delseny 35–150 San Diego, CA: Academic [Google Scholar]
  109. Ryan MG. 109.  2011. Tree responses to drought. Tree Physiol. 31:237–39 [Google Scholar]
  110. Ryan MG, Phillips N, Bond BJ. 110.  2006. The hydraulic limitation hypothesis revisited. Plant Cell Environ. 29:367–81 [Google Scholar]
  111. Sala A, Hoch G. 111.  2009. Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant Cell Environ. 32:22–30 [Google Scholar]
  112. Sala A, Piper FI, Hoch G. 112.  2010. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol. 186:274–81 [Google Scholar]
  113. Sala A, Woodruff DR, Meinzer FC. 113.  2012. Carbon dynamics in trees: feast or famine?. Tree Physiol. 32:764–75 [Google Scholar]
  114. Sampson DA, Johnsen KH, Ludovici KH, Albaugh TJ, Maier CA. 114.  2001. Stand-scale correspondence in empirical and simulated labile carbohydrates in loblolly pine. For. Sci. 47:60–68 [Google Scholar]
  115. Samuelson LJ, Kelly JM. 115.  1996. Carbon partitioning and allocation in northern red oak seedlings and mature trees in response to ozone. Tree Physiol. 16:853–58 [Google Scholar]
  116. Schaefer K, Collatz GJ, Tans P, Denning AS, Baker I. 116.  et al. 2008. Combined Simple Biosphere/Carnegie-Ames-Stanford Approach terrestrial carbon cycle model. J. Geophys. Res. 113:G03034 [Google Scholar]
  117. Schutz AEN, Bond WJ, Cramer MD. 117.  2009. Juggling carbon: allocation patterns of a dominant tree in a fire-prone savanna. Oecologia 160:235–46 [Google Scholar]
  118. Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT. 118.  2014. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 37153–61 [Google Scholar]
  119. Shigihara A, Matsumoto K, Sakurai N, Igawa M. 119.  2008. Growth and physiological responses of beech seedlings to long-term exposure of acid fog. Sci. Total Environ. 391:124–31 [Google Scholar]
  120. Shumejko P, Ossipov V, Neuvonen S. 120.  1996. The effect of simulated acid rain on the biochemical composition of Scots pine (Pinus sylvestris L.) needles. Environ. Pollut. 92:315–21 [Google Scholar]
  121. Sloan JL, Jacobs DF. 121.  2012. Leaf physiology and sugar concentrations of transplanted Quercus rubra seedlings in relation to nutrient and water availability. New For. 43:779–90 [Google Scholar]
  122. Smith AM, Zeeman SC, Smith SM. 122.  2005. Starch degradation. Annu. Rev. Plant Biol. 56:73–98 [Google Scholar]
  123. Smith NG, Dukes JS. 123.  2012. Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO2. Glob. Change Biol. 19:45–63 [Google Scholar]
  124. Sterner RW, Elser JJ. 124.  2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere Princeton, NJ: Princeton Univ. Press [Google Scholar]
  125. Stitt M, Zeeman SC. 125.  2012. Starch turnover: pathways, regulation and role in growth. Curr. Opin. Plant Biol. 15:282–92 [Google Scholar]
  126. Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M. 126.  et al. 2009. Starch as a major integrator in the regulation of plant growth. Proc. Natl. Acad. Sci. USA 106:10348–53 [Google Scholar]
  127. Sveinbjörnsson B. 127.  2000. North American and European treelines: external forces and internal processes controlling position. Ambio 29:388–95 [Google Scholar]
  128. Terziev N, Boutelje J, Larsson K. 128.  1997. Seasonal fluctuations of low-molecular-weight sugars, starch and nitrogen in sapwood of Pinus sylvestris L. Scand. J. For. Res. 12:216–24 [Google Scholar]
  129. Thomas VFD, Braun S, Flückiger W. 129.  2005. Effects of simultaneous ozone exposure and nitrogen loads on carbohydrate concentrations, biomass, and growth of young spruce trees (Picea abies). Environ. Pollut. 137:507–16 [Google Scholar]
  130. Thornley JHM. 130.  1991. A transport-resistance model of forest growth and partitioning. Ann. Bot. 68:211–26 [Google Scholar]
  131. Thornley JHM, Cannell MGR. 131.  2000. Modelling the components of plant respiration: representation and realism. Ann. Bot. 85:55–67 [Google Scholar]
  132. Tomlinson GH. 132.  2003. Acidic deposition, nutrient leaching and forest growth. Biogeochemistry 65:51–81 [Google Scholar]
  133. Turgeon R. 133.  2006. Phloem loading: how leaves gain their independence. BioScience 56:15–24 [Google Scholar]
  134. Turgeon R. 134.  2010. The puzzle of phloem pressure. Plant Physiol. 154:578–81 [Google Scholar]
  135. Vanderklein D, Reich P. 135.  1999. The effect of defoliation intensity and history on photosynthesis, growth and carbon reserves of two conifers with contrasting leaf lifespans and growth habits. New Phytol. 144:121–32 [Google Scholar]
  136. Vargas R. 136.  2012. How a hurricane disturbance influences extreme CO2 fluxes and variance in a tropical forest.. Environ. Res. Lett. 7:035704 [Google Scholar]
  137. Vargas R, Baldocchi DD, Bahn M, Hanson PJ, Hosman KP. 137.  et al. 2011. On the multi-temporal correlation between photosynthesis and soil CO2 efflux: reconciling lags and observations. New Phytol. 191:1006–17 [Google Scholar]
  138. Vargas R, Hasselquist N, Allen EB, Allen MF. 138.  2010. Effects of a hurricane disturbance on aboveground forest structure, arbuscular mycorrhizae and belowground carbon in a restored tropical forest. Ecosystems 13:118–28 [Google Scholar]
  139. Vargas R, Trumbore SE, Allen MF. 139.  2009. Evidence of old carbon used to grow new fine roots in a tropical forest. New Phytol. 182:710–18 [Google Scholar]
  140. Verdaguer D, Ojeda F. 140.  2002. Root starch storage and allocation patterns in seeder and resprouter seedlings of two Cape Erica (Ericaceae) species. Am. J. Bot. 89:1189–96 [Google Scholar]
  141. Vingarzan R. 141.  2004. A review of surface ozone background levels and trends. Atmos. Environ. 38:3431–42 [Google Scholar]
  142. Warren JM, Iversen CM, Garten CT, Norby RJ, Childs J. 142.  et al. 2012. Timing and magnitude of C partitioning through a young loblolly pine (Pinus taeda L.) stand using 13C labeling and shade treatments. Tree Physiol. 32:799–813 [Google Scholar]
  143. Weinstein DA, Beloin RM, Yanai RD. 143.  1991. Modeling changes in red spruce carbon balance and allocation in response to interacting ozone and nutrient stresses. Tree Physiol. 9:127–46 [Google Scholar]
  144. Wigley BJ, Cramer MD, Bond WJ. 144.  2009. Sapling survival in a frequently burnt savanna: mobilisation of carbon reserves in Acacia karroo. Plant Ecol. 203:1–11 [Google Scholar]
  145. Wiley E, Helliker B. 145.  2012. A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol. 195:285–89 [Google Scholar]
  146. Wittig VE, Ainsworth EA, Long SP. 146.  2007. To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments. Plant Cell Environ. 30:1150–62 [Google Scholar]
  147. Wittig VE, Ainsworth EA, Naidu SL, Karnosky DF, Long SP. 147.  2009. Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta-analysis. Glob. Change Biol. 15:396–424 [Google Scholar]
  148. Woodruff DR, Meinzer FC. 148.  2011. Water stress, shoot growth and storage of non-structural carbohydrates along a tree height gradient in a tall conifer. Plant Cell Environ. 34:1920–30 [Google Scholar]
  149. Würth M, Pelaez-Riedl S, Wright S, Körner C. 149.  2005. Non-structural carbohydrate pools in a tropical forest. Oecologia 143:11–24 [Google Scholar]
  150. Zeeman SC, Kossmann J, Smith AM. 150.  2010. Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61:209–34 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error