Chin J Plant Ecol ›› 2019, Vol. 43 ›› Issue (12): 1036-1047.doi: 10.17521/cjpe.2019.0104

• Reviews • Previous Articles     Next Articles

Mechanisms of carbon source-sink limitations to tree growth

WANG Zhao-Guo,WANG Chuan-Kuan()   

  1. Center for Ecological Research, Northeast Forestry University, Harbin 150040, China; and Key Laboratory of Sustainable Forest Ecosystem Management- Ministry of Education, Northeast Forestry University, Harbin 150040, China
  • Received:2019-05-09 Accepted:2019-11-08 Online:2020-02-24 Published:2019-12-20
  • Contact: WANG Chuan-Kuan ORCID:0000-0003-3513-5426 E-mail:Wangck-cf@nefu.edu.cn
  • Supported by:
    National Key R&D Program of China(2016YFD0600201);Program for Changjiang Scholars and Innovative Research Team of Ministry of Education of China(IRT_15R09)

Abstract:

Forests are large and persistent carbon (C) sink mainly through the C sequestration of tree growth, which can mitigate the rising rate of CO2 concentration in the atmosphere. According to C availability in trees, two mechanisms involved in controlling tree growth are attributed to limitations to C input and C utilities. Since many environmental factors influence the activities of C-source and C-sink of trees interdependently, it is difficult to quantify how the sensitivity of C-source or C-sink activity to environmental changes affects tree growth. Therefore, it is of significance to understand physiological mechanisms underlying potential limitations to tree growth in order to predict tree growth and forest C sink under global change scenarios. In this review, the debates on the C-source and C-sink limitations to tree growth were firstly introduced. Second, we discussed responses of tree growth to biotic and abiotic stresses, such as defoliation, drought and low temperature from the perspective of C-source/sink limitations. Finally, we proposed three priorities for future studies in this field: (1) to explore the regulating mechanisms on the allocation of non-structural carbohydrates (NSC) in trees, and to determine what conditions and what extent trees actively allocate the photosynthates to NSC storage at the expense of growth; (2) to strengthen studies on the tree C-sink, and determine the photosynthates allocated to all components of tree C-sink, especially the missing C-sinks such as the activities of roots and related microorganisms; and (3) to implement studies on interactions among C metabolism, mineral nutrition and hydraulics physiology, and fully understand the C-water-nutrient coupling and its effects on tree growth.

Key words: carbon sink, carbon source, non-structural carbohydrates, stress, tree growth

Fig. 1

A conceptual framework of the mechanisms of carbon source-sink limitations to tree growth. From a-b-c pathway, carbon assimilation is reduced by biotic and abiotic stresses (such as defoliation, drought and low temperature), hence tree growth is limited by available carbon (i.e. carbon source limitation). From d-e-c pathway, the storage of non-structural carbohydrates (NSC) is an active process, which decreases available carbon for tree growth (carbon source limitation). From f-h-i pathway, tree growth is constrained by biotic and abiotic stresses directly, leading to NSC accumulation and thus limitation to photosynthesis (i.e. carbon sink limitation). Solid lines represent direct effects, and dotted lines represent feedbacks. + and - represent positive and negative effects, respectively."

[1] Aber J, Neilson RP, McNulty S, Lenihan JM, Bachelet D, Drapek RJ ( 2001). Forest processes and global environmental change: Predicting the effects of individual and multiple stressors. BioScience, 51, 735-751.
doi: 10.1641/0006-3568(2001)051[0735:FPAGEC]2.0.CO;2
[2] Ågren GI ( 2008). Stoichiometry and nutrition of plant growth in natural communities. Annual Review of Ecology, Evolution, and Systematics, 39, 153-170.
doi: 10.1146/annurev.ecolsys.39.110707.173515
[3] Ainsworth EA, Rogers A ( 2007). The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant, Cell & Environment, 30, 258-270.
doi: 10.1111/j.1365-3040.2007.01641.x pmid: 17263773
[4] Alvarez-Uria P, Körner C ( 2007). Low temperature limits of root growth in deciduous and evergreen temperate tree species. Functional Ecology, 21, 211-218.
doi: 10.1111/fec.2007.21.issue-2
[5] Bader MKF, Leuzinger S, Keel SG, Siegwolf RTW, Hagedorn F, Schleppi P, Körner C ( 2013). Central European hardwood trees in a high-CO2 future: Synthesis of an 8-year forest canopy CO2 enrichment project. Journal of Ecology, 101, 1509-1519.
doi: 10.1111/1365-2745.12149
[6] Bader MKF, Siegwolf R, Körner C ( 2010). Sustained enhancement of photosynthesis in mature deciduous forest trees after 8 years of free air CO2 enrichment. Planta, 232, 1115-1125.
doi: 10.1007/s00425-010-1240-8 pmid: 20700744
[7] Barry KM, Pinkard EA ( 2013). Growth and photosynthetic responses following defoliation and bud removal in eucalypts. Forest Ecology and Management, 293, 9-16.
doi: 10.1016/j.foreco.2012.12.012
[8] Bauerle WL, Hinckley TM, Cermak J, Kucera J, Bible K ( 1999). The canopy water relations of old-growth Douglas-‌‌fir trees. Trees, 13, 211-217.
doi: 10.3897/CompCytogen.v13i3.35346 pmid: 31428293
[9] Beer C, Reichstein M, Tomelleri E, Ciais P, Jung M, Carvalhais N, Rodenbeck C, Arain MA, Baldocchi D, Bonan GB, Bondeau A, Cescatti A, Lasslop G, Lindroth A, Lomas M, Luyssaert S, Margolis H, Oleson KW, Roupsard O, Veenendaal E, Viovy N, Williams C, Woodward FI, Papale D ( 2010). Terrestrial gross carbon dioxide uptake: Global distribution and covariation with climate. Science, 329, 834-838.
doi: 10.1126/science.1184984 pmid: 20603496
[10] Berdanier AB, Clark JS ( 2016). Multi-year drought-induced morbidity preceding tree death in Southeastern US forests. Ecological Applications, 26, 17-23.
doi: 10.1890/15-0274 pmid: 27039506
[11] Bond BJ, Czarnomski NM, Cooper C, Day ME, Greenwood MS ( 2007). Developmental decline in height growth in Douglas-fir. Tree Physiology, 27, 441-453.
doi: 10.1093/treephys/27.3.441 pmid: 17241986
[12] Bréda N, Huc R, Granier A, Dreyer E ( 2006). Temperate forest trees and stands under severe drought: A review of ecophysiological responses, adaptation processes and long-‌term consequences. Annals of Forest Science, 63, 625-644.
doi: 10.1051/forest:2006042
[13] Burnett AC, Rogers A, Rees M, Osborne CP ( 2016). Carbon source-sink limitations differ between two species with contrasting growth strategies. Plant, Cell & Environment, 39, 2460-2472.
doi: 10.1111/pce.12801 pmid: 27422294
[14] Cavieres LA, Rada F, Azócar A, García-Núñez C, Cabrera HM ( 2000). Gas exchange and low temperature resistance in two tropical high mountain tree species from the Venezuelan Andes. Acta Oecologica, 21, 203-211.
doi: 10.3109/02841868209134006 pmid: 6293262
[15] Chapin III FS, Schulze E, Mooney HA ( 1990). The ecology and economics of storage in plants. Annual Review of Ecology and Systematics, 21, 423-447.
doi: 10.1146/annurev.es.21.110190.002231
[16] Chapin III FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz S ( 2000). Consequences of changing biodiversity. Nature, 405, 234-242.
doi: 10.1038/35012241 pmid: 10821284
[17] Chaves MM, Flexas J, Pinheiro C ( 2009). Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Annals of Botany, 103, 551-560.
doi: 10.1093/aob/mcn125 pmid: 18662937
[18] Collett NG, Neumann FG ( 2002). Effects of simulated chronic defoliation in summer on growth and survival of blue gum (Eucalyptus globulus Labill.) within young plantations in northern Victoria. Australian Forestry, 65, 99-106.
doi: 10.1080/00049158.2002.10674860
[19] Dannoura M, Epron D, Desalme D, Massonnet C, Tsuji S, Plain C, Priault P, Gérant D ( 2019). The impact of prolonged drought on phloem anatomy and phloem transport in young beech trees. Tree Physiology, 39, 201-210.
doi: 10.1093/treephys/tpy070 pmid: 29931112
[20] Dawes MA, Hagedorn F, Handa IT, Streit K, Ekblad A, Rixen C, Körner C, Hättenschwiler S ( 2013). An alpine treeline in a carbon dioxide-rich world: Synthesis of a nine-year free-air carbon dioxide enrichment study. Oecologia, 171, 623-637.
doi: 10.1007/s00442-012-2576-5 pmid: 23340765
[21] Dawes MA, Hättenschwiler S, Bebi P, Hagedorn F, Handa IT, Körner C, Rixen C ( 2011). Species-specific tree growth responses to 9 years of CO2 enrichment at the alpine treeline. Journal of Ecology, 99, 383-394.
doi: 10.1111/j.1365-2745.2010.01764.x
[22] Deppong DO, Cline MG ( 2000). Do leaves control episodic shoot growth in woodyplants? The Ohio Journal of Science, 100, 19-23.
[23] Deslauriers A, Huang JG, Balducci L, Beaulieu M, Rossi S ( 2016). The contribution of carbon and water in modulating wood formation in black spruce saplings. Plant Physiology, 170, 2072-2084.
doi: 10.1104/pp.15.01525 pmid: 26850274
[24] Dietze MC, Sala AN, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R ( 2014). Nonstructural carbon in woody plants. Annual Review of Plant Biology, 65, 667-687.
doi: 10.1146/annurev-arplant-050213-040054 pmid: 24274032
[25] Dolezal J, Kopecky M, Dvorsky M, Macek M, Rehakova K, Capkova K, Borovec J, Schweingruber F, Liancourt P, Altman J ( 2019). Sink limitation of plant growth determines tree line in the arid Himalayas. Functional Ecology, 33, 553-565.
doi: 10.1111/fec.2019.33.issue-4
[26] Duan H, Amthor JS, Duursma RA, O’Grady AP, Choat B, Tissue DT ( 2013). Carbon dynamics of eucalypt seedlings exposed to progressive drought in elevated [CO2] and elevated temperature. Tree Physiology, 33, 779-792.
doi: 10.1093/treephys/tpt061 pmid: 23963410
[27] Dymond CC, Beukema S, Nitschke CR, Coates KD, Scheller RM ( 2016). Carbon sequestration in managed temperate coniferous forests under climate change. Biogeosciences, 13, 1933-1947.
doi: 10.5194/bg-13-1933-2016
[28] Epron D, Cabral OMR, Laclau JP, Dannoura M, Packer AP, Plain C, Battie-Laclau P, Moreira MZ, Trivelin PCO, Bouillet JP, Gérant D, Nouvellon Y ( 2016). In situ 13CO2 pulse labelling of field-grown eucalypt trees revealed the effects of potassium nutrition and throughfall exclusion on phloem transport of photosynthetic carbon. Tree Physiology, 36, 6-21.
doi: 10.1093/treephys/tpv090 pmid: 26423335
[29] Evans CG ( 1972). The Quantitative Analysis of Plant Growth. Blackwell Scientific, Oxford.
[30] Fajardo A, Piper FI ( 2014). An experimental approach to explain the southern Andes elevational treeline. American Journal of Botany, 101, 788-795.
doi: 10.3732/ajb.1400166 pmid: 24812110
[31] Fajardo A, Piper FI ( 2017). An assessment of carbon and nutrient limitations in the formation of the southern Andes tree line. Journal of Ecology, 105, 517-527.
doi: 10.1111/jec.2017.105.issue-2
[32] Farquhar GD, von Caemmerer S, Berry JA ( 1980). A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 149, 78-90.
doi: 10.1007/BF00386231 pmid: 24306196
[33] Fatichi S, Leuzinger S, Körner C ( 2014). Moving beyond photosynthesis: From carbon source to sink-driven vegetation modeling. New Phytologist, 201, 1086-1095.
doi: 10.1111/nph.12614 pmid: 24261587
[34] Fatichi S, Pappas C, Zscheischler J, Leuzinger S ( 2019). Modelling carbon sources and sinks in terrestrial vegetation. New Phytologist, 221, 652-668.
doi: 10.1111/nph.15451 pmid: 30339280
[35] Feild TS, Brodribb T ( 2001). Stem water transport and freeze-thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath. Oecologia, 127, 314-320.
doi: 10.1007/s004420000603 pmid: 28547101
[36] Friend AD, Eckes-Shephard AH, Fonti P, Rademacher TT, Rathgeber CBK, Richardson AD, Turton RH ( 2019). On the need to consider wood formation processes in global vegetation models and a suggested approach. Annals of Forest Science, 76, 49.
doi: 10.1007/s13595-019-0819-x
[37] Galiano L, Martínez-Vilalta J, Lloret F ( 2011). Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytologist, 190, 750-759.
doi: 10.1111/j.1469-8137.2010.03628.x pmid: 21261625
[38] Galiano L, Timofeeva G, Saurer M, Siegwolf R, Martínez-‌Vilalta J, Hommel R, Gessler A ( 2017). The fate of recently fixed carbon after drought release: Towards unravelling C storage regulation in Tilia platyphyllos and Pinus sylvestris. Plant, Cell & Environment, 40, 1711-1724.
doi: 10.1111/pce.12972 pmid: 28432768
[39] Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M ( 2009). 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. Plant, Cell & Environment, 32, 859-874.
doi: 10.1111/j.1365-3040.2009.01965.x pmid: 19236606
[40] Greenwood MS, Ward MH, Day ME, Adams SL, Bond BJ ( 2008). Age-related trends in red spruce foliar plasticity in relation to declining productivity. Tree Physiology, 28, 225-232.
doi: 10.1093/treephys/28.2.225 pmid: 18055433
[41] Gričar J, Zavadlav S, Jyske T, Lavrič M, Laakso T, Hafner P, Eler K, Vodnik D ( 2019). Effect of soil water availability on intra-annual xylem and phloem formation and non-structural carbohydrate pools in stem of Quercus pubescens. Tree Physiology, 39, 222-233.
doi: 10.1093/treephys/tpy101 pmid: 30239939
[42] Hagedorn F, Joseph J, Peter M, Luster J, Pritsch K, Geppert U, Kerner R, Molinier V, Egli S, Schaub M, Liu JF, Li MH, Sever K, Weiler M, Siegwolf RTW, Gessler A, Arend M ( 2016). Recovery of trees from drought depends on belowground sink control. Nature Plants, 2, 1-5.
doi: 10.1038/nplants.2016.111 pmid: 27428669
[43] Handa IT, Körner C, Hättenschwiler S ( 2005). A test of the treeline carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology, 86, 1288-1300.
doi: 10.1890/04-0711
[44] Hararuk O, Campbell EM, Antos JA, Parish R ( 2019). Tree rings provide no evidence of a CO2 fertilization effect in old-growth subalpine forests of western Canada. Global Change Biology, 25, 1222-1234.
doi: 10.1111/gcb.2019.25.issue-4
[45] Hartmann H, Adams HD, Hammond WM, Hoch G, Landhäusser SM, Wiley E, Zaehle S ( 2018). Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environmental and Experimental Botany, 152, 7-18.
doi: 10.1016/j.envexpbot.2018.03.011
[46] Hartmann H, McDowell NG, Trumbore S ( 2015). Allocation to carbon storage pools in Norway spruce saplings under drought and low CO2. Tree Physiology, 35, 243-252.
doi: 10.1093/treephys/tpv019 pmid: 25769339
[47] 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 Phytologist, 211, 386-403.
doi: 10.1111/nph.13955 pmid: 27061438
[48] Hesse BD, Goisser M, Hartmann H, Grams TEE ( 2019). Repeated summer drought delays sugar export from the leaf and impairs phloem transport in mature beech. Tree Physiology, 39, 192-200.
doi: 10.1093/treephys/tpy122 pmid: 30388272
[49] Hillabrand RM, Hacke UG, Lieffers VJ ( 2019). Defoliation constrains xylem and phloem functionality. Tree Physiology, 39, 1099-1108.
doi: 10.1093/treephys/tpz029 pmid: 30901057
[50] Hoch G, Körner C ( 2009). Growth and carbon relations of tree line forming conifers at constant vs. variable low temperatures. Journal of Ecology, 97, 57-66.
doi: 10.1111/jec.2009.97.issue-1
[51] Hoch G, Popp M, Körner C ( 2002). Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos, 98, 361-374.
doi: 10.1034/j.1600-0706.2002.980301.x
[52] Hoch G, Richter A, Körner C ( 2003). Non-structural carbon compounds in temperate forest trees. Plant, Cell and Environment, 26, 1067-1081.
doi: 10.1007/s00442-002-1154-7 pmid: 12647099
[53] Hsiao TC, Acevedo E, Fereres E, Henderson DW ( 1976). Water stress, growth, and osmotic adjustment. Philosophical Transactions of the Royal Society B: Biological Sciences, 273, 479-500.
[54] Huang JB, Hammerbacher A, Weinhold A, Reichelt M, Gleixner G, Behrendt T, Dam NM, Sala AN, Gershenzon J, Trumbore S, Hartmann H ( 2019). Eyes on the future—Evidence for trade-offs between growth, storage and defense in Norway spruce. New Phytologist, 222, 144-158.
doi: 10.1111/nph.15522 pmid: 30289558
[55] Huang JG, Guo XL, Rossi S, Zhai LH, Yu BY, Zhang SK, Zhang MF ( 2018). Intra-annual wood formation of subtropical Chinese red pine shows better growth in dry season than wet season. Tree Physiology, 38, 1225-1236.
doi: 10.1093/treephys/tpy046 pmid: 29757427
[56] Ishii HT, Jennings GM, Sillett SC, Koch GW ( 2008). Hydrostatic constraints on morphological exploitation of light in tall Sequoia sempervirens trees. Oecologia, 156, 751-763.
doi: 10.1007/s00442-008-1032-z pmid: 18392856
[57] Jacquet JS, Bosc A, O’Grady A, Jactel H ( 2014). Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiology, 34, 367-376.
doi: 10.1093/treephys/tpu018 pmid: 24736390
[58] Jensen KH, Rio E, Hansen R, Clanet C, Bohr T ( 2009). Osmotically driven pipe flows and their relation to sugar transport in plants. Journal of Fluid Mechanics, 636, 371-396.
doi: 10.1017/S002211200900799X
[59] Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC ( 2012). Hydraulic safety margins and embolism reversal in stems and leaves: Why are conifers and angiosperms so different? Plant Science, 195, 48-53.
doi: 10.1016/j.plantsci.2012.06.010
[60] Kiorapostolou N, Petit G ( 2019). Similarities and differences in the balances between leaf, xylem and phloem structures in Fraxinus ornus along an environmental gradient. Tree Physiology, 39, 234-242.
doi: 10.1093/treephys/tpy095 pmid: 30189046
[61] Kirschbaum MUF ( 2011). Does enhanced photosynthesis enhance growth? lessons learned from CO2 enrichment studies. Plant Physiology, 155, 117-124.
doi: 10.1104/pp.110.166819 pmid: 21088226
[62] Klein T, Bader MKF, Leuzinger S, Mildner M, Schleppi P, Siegwolf RTW, Körner C ( 2016). Growth and carbon relations of mature Picea abies trees under 5 years of free-air CO2 enrichment. Journal of Ecology, 104, 1720-1733.
doi: 10.1111/jec.2016.104.issue-6
[63] Körner C ( 2003). Carbon limitation in trees. Journal of Ecology, 91, 4-17.
doi: 10.1046/j.1365-2745.2003.00742.x
[64] Körner C ( 2006). Plant CO2 responses: An issue of definition, time and resource supply. New Phytologist, 172, 393-411.
doi: 10.1111/j.1469-8137.2006.01886.x pmid: 17083672
[65] Körner C ( 2012). Alpine Treelines: Functional Ecology of the Global High Elevation Tree Limits. Springer, Berlin.
[66] Körner C ( 2015). Paradigm shift in plant growth control. Current Opinion in Plant Biology, 25, 107-114.
doi: 10.1016/j.pbi.2015.05.003 pmid: 26037389
[67] Landhäusser SM, Lieffers VJ ( 2012). Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees, 26, 653-661.
doi: 10.1007/s00468-011-0633-z
[68] Li MH, Jiang Y, Wang A, Li XB, Zhu WZ, Yan CF, Du Z, Shi Z, Lei JP, Schönbeck L, He P, Yu FH, Wang X ( 2018). Active summer carbon storage for winter persistence in trees at the cold alpine treeline. Tree Physiology, 38, 1345-1355.
doi: 10.1093/treephys/tpy020 pmid: 29538773
[69] Li MH, Xiao WF, Wang SG, Cheng GW, Cherubini P, Cai XH, Liu XL, Wang XD, Zhu WZ ( 2008). Mobile carbohydrates in Himalayan treeline trees I. Evidence for carbon gain limitation but not for growth limitation. Tree Physiology, 28, 1287-1296.
doi: 10.1093/treephys/28.8.1287 pmid: 18519260
[70] Li MH, Yang J ( 2004). Effects of microsite on growth of Pinus cembra in the subalpine zone of the Austrian Alps. Annals of Forest Science, 61, 319-325.
doi: 10.1051/forest:2004025
[71] Litton CM, Giardina CP ( 2008). Below-ground carbon flux and partitioning: Global patterns and response to temperature. Functional Ecology, 22, 941-954.
[72] Litton CM, Raich JW, Ryan MG ( 2007). Carbon allocation in forest ecosystems. Global Change Biology, 13, 2089-2109.
[73] Liu YY, Wang AY, An YN, Lian PY, Wu DD, Zhu JJ, Meinzer FC, Hao GY ( 2018). Hydraulics play an important role in causing low growth rate and dieback of aging Pinus sylvestris var. mongolica trees in plantations of Northeast China. Plant, Cell & Environment, 41, 1500-1511.
[74] Luo YQ, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, Mc Murtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB ( 2004). Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience, 54, 731.
[75] MacNeill GJ, Mehrpouyan S, Minow MAA, Patterson JA, Tetlow IJ, Emes MJ ( 2017). Starch as a source, starch as a sink: The bifunctional role of starch in carbon allocation. Journal of Experimental Botany, 68, 4433-4453.
[76] Maherali H, Pockman WT, Jackson RB ( 2004). Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology, 85, 2184-2199.
[77] Martínez-Vilalta J, Sala AN, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F ( 2016). Dynamics of non-structural carbohydrates in terrestrial plants: A global synthesis. Ecological Monographs, 86, 495-516.
[78] McCarthy HR, Oren R, Johnsen KH, Gallet-Budynek A, Pritchard SG, Cook CW, LaDeau SL, Jackson RB, Finzi AC ( 2010). Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: Interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytologist, 185, 514-528.
[79] Meinzer FC, Bond BJ, Karanian JA ( 2008). Biophysical constraints on leaf expansion in a tall conifer. Tree Physiology, 28, 197-206.
[80] Michelot A, Simard S, Rathgeber C, Dufrêne E, Damesin C ( 2012). Comparing the intra-annual wood formation of three European species (Fagus sylvatica, Quercus petraea and Pinus sylvestris) as related to leaf phenology and non-structural carbohydrate dynamics. Tree Physiology, 32, 1033-1045.
[81] Millard P, Sommerkorn M, Grelet GA ( 2007). Environmental change and carbon limitation in trees: A biochemical, ecophysiological and ecosystem appraisal. New Phytologist, 175, 11-28.
[82] Minchin PEH (2007). Mechanistic modelling of carbon partitioning. In: Vos J, Marcelis LFM, de Visser PHB, Struik PC, Evers JB eds. Functional-Structural Plant Modelling in Crop Production. Springer, Dordrecht. 113-122.
[83] Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y ( 2011). Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany, 62, 1715-1729.
[84] Nardini A, Lo Gullo MA, Salleo S ( 2011). Refilling embolized xylem conduits: Is it a matter of phloem unloading? Plant Science, 180, 604-611.
[85] Nikinmaa E, Hölttä T, Hari P, Kolari P, Mäkelä A, Sevanto S, Vesala T ( 2013). Assimilate transport in phloem sets conditions for leaf gas exchange. Plant, Cell & Environment, 36, 655-669.
[86] Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE ( 2010). CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proceedings of the National Academy of Sciences of the United States of America, 107, 19368-19373.
[87] Palacio S, Camarero JJ, Maestro M, Alla AQ, Lahoz E, Monserrat-Martí G ( 2018). Are storage and tree growth related? Seasonal nutrient and carbohydrate dynamics in evergreen and deciduous Mediterranean oaks. Trees, 32, 777-790.
[88] Palacio S, Hoch G, Sala AN, Körner C, Millard P ( 2014). Does carbon storage limit tree growth? New Phytologist, 201, 1096-1100.
[89] Paul MJ, Foyer CH ( 2001). Sink regulation of photosynthesis. Journal of Experimental Botany, 52, 1383-1400.
[90] Pinkard EA, Eyles A, O’Grady AP ( 2011). Are gas exchange responses to resource limitation and defoliation linked to source:sink relationships? Plant, Cell & Environment, 34, 1652-1665.
[91] Piper FI, Fajardo A ( 2011). No evidence of carbon limitation with tree age and height in Nothofagus pumilio under Mediterranean and temperate climate conditions. Annals of Botany, 108, 907-917.
[92] Piper FI, Fajardo A ( 2014). Foliar habit, tolerance to defoliation and their link to carbon and nitrogen storage. Journal of Ecology, 102, 1101-1111.
[93] Piper FI, Fajardo A, Hoch G ( 2017). Single-provenance mature conifers show higher non-structural carbohydrate storage and reduced growth in a drier location. Tree Physiology, 37, 1001-1010.
[94] Power SA ( 1994). Temporal trends in twig growth of Fagus sylvatica L. and their relationships with environmental factors. Forestry, 67, 13-30.
[95] Poyatos R, Aguadé D, Galiano L, Mencuccini M, Martínez-‌Vilalta J ( 2013). Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytologist, 200, 388-401.
[96] Puri E, Hoch G, Körner C ( 2015). Defoliation reduces growth but not carbon reserves in Mediterranean Pinus pinaster trees. Trees, 29, 1187-1196.
[97] Quentin AG, O’Grady AP, Beadle CL, Mohammed C, Pinkard EA ( 2012). Interactive effects of water supply and defoliation on photosynthesis, plant water status and growth of Eucalyptus globulus Labill. Tree Physiology, 32, 958-967.
[98] Rosati A, Paoletti A, Al Hariri R, Morelli A, Famiani F ( 2018). Resource investments in reproductive growth proportionately limit investments in whole-tree vegetative growth in young olive trees with varying crop loads. Tree Physiology, 38, 1267-1277.
[99] Rossi S, Deslauriers A, Anfodillo T, Carraro V ( 2007). Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia, 152, 1-12.
[100] Rossi S, Deslauriers A, Gričar J, Seo JW, Rathgeber CB, Anfodillo T, Morin H, Levanic T, Oven P, Jalkanen R ( 2008). Critical temperatures for xylogenesis in conifers of cold climates. Global Ecology and Biogeography, 17, 696-707.
[101] Ryan MG, Oren R, Waring RH ( 2018). Fruiting and sink competition. Tree Physiology, 38, 1261-1266.
[102] Ryan MG, Phillips N, Bond BJ ( 2006). The hydraulic limitation hypothesis revisited. Plant, Cell & Environment, 29, 367-381.
[103] Ryan MG, Yoder BJ ( 1997). Hydraulic limits to tree height and tree growth. BioScience, 47, 235-242.
[104] Sala AN, Hoch G ( 2009). Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant, Cell & Environment, 32, 22-30.
[105] Sala AN, Piper F, Hoch G ( 2010). Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist, 186, 274-281.
[106] Sala AN, Woodruff DR, Meinzer FC ( 2012). Carbon dynamics in trees: Feast or famine? Tree Physiology, 32, 764-775.
[107] Salmon Y, Dietrich L, Sevanto S, Hölttä T, Dannoura M, Epron D ( 2019). Drought impacts on tree phloem: From cell-level responses to ecological significance. Tree Physiology, 39, 173-191.
[108] Schmid S, Palacio S, Hoch G ( 2017). Growth reduction after defoliation is independent of CO2 supply in deciduous and evergreen young oaks. New Phytologist, 214, 1479-1490.
[109] Sevanto S ( 2014). Phloem transport and drought. Journal of Experimental Botany, 65, 1751-1759.
[110] Sigurdsson BD, Medhurst JL, Wallin G, Eggertsson O, Linder S ( 2013). Growth of mature boreal Norway spruce was not affected by elevated [CO2] and/or air temperature unless nutrient availability was improved. Tree Physiology, 33, 1192-1205.
[111] 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 Physiology, 33, 913-923.
[112] Smith AM, Stitt M ( 2007). Coordination of carbon supply and plant growth. Plant, Cell & Environment, 30, 1126-1149.
[113] Steppe K, Sterck F, Deslauriers A ( 2015). Diel growth dynamics in tree stems: Linking anatomy and ecophysiology. Trends in Plant Science, 20, 335-343.
[114] Stevens GC, Fox JF ( 1991). The causes of treeline. Annual Review of Ecology and Systematics, 22, 177-191.
[115] Stribley GH, Ashmore MR ( 2002). Quantitative changes in twig growth pattern of young woodland beech (Fagus sylvatica L.) in relation to climate and ozone pollution over 10 years. Forest Ecology and Management, 157, 191-204.
[116] Susiluoto S, Hilasvuori E, Berninger F ( 2010). Testing the growth limitation hypothesis for subarctic Scots pine. Journal of Ecology, 98, 1186-1195.
[117] Tardieu F, Granier C, Muller B ( 2011). Water deficit and growth. Co-ordinating processes without an orchestrator? Current Opinion in Plant Biology, 14, 283-289.
[118] Trugman AT, Detto M, Bartlett MK, Medvigy D, Anderegg WRL, Schwalm C, Schaffer B, Pacala SW ( 2018). Tree carbon allocation explains forest drought-kill and recovery patterns. Ecology Letters, 21, 1552-1560.
[119] van der Sleen P, Groenendijk P, Vlam M, Anten NPR, Boom A, Bongers F, Pons TL, Terburg G, Zuidema PA ( 2015). No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nature Geoscience, 8, 24-28.
[120] von 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. Functional Ecology, 31, 1371-1382.
[121] Wang H, Prentice IC, Davis TW, Keenan TF, Wright IJ, Peng CH ( 2017). Photosynthetic responses to altitude: An explanation based on optimality principles. New Phytologist, 213, 976-982.
[122] Wardlaw IF ( 1990). The control of carbon partitioning in plants. New Phytologist, 116, 341-381.
[123] Weber R, Gessler A, Hoch G ( 2019). High carbon storage in carbon-limited trees. New Phytologist, 222, 171-182.
[124] White AC, Rogers A, Rees M, Osborne CP ( 2016). How can we make plants grow faster? A source-sink perspective on growth rate. Journal of Experimental Botany, 67, 31-45.
[125] Wiley E, Casper BB, Helliker BR ( 2017). Recovery following defoliation involves shifts in allocation that favour storage and reproduction over radial growth in black oak. Journal of Ecology, 105, 412-424.
[126] Wiley E, Helliker B ( 2012). A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytologist, 195, 285-289.
[127] Yan JH, Zhang YP, Yu GR, Zhou GY, Zhang LM, Li K, Tan ZH, Sha LQ ( 2013). Seasonal and inter-annual variations in net ecosystem exchange of two old-growth forests in southern China. Agricultural and Forest Meteorology, 182- 183, 257-265.
[128] Zimmermann MH, Brown CL ( 1974). Trees, Structure and Function. Springer, New York.
[1] Liang ZHANG Zhilei Wang Tingting Xue Xiaoyun Hao Chenlou Yang Feifei gao Ying Wang Xing Han Hua Li Hua Wang. Review of carbon source/sink and emission reduction strategies in vineyard ecosystem [J]. Chin J Plant Ecol, 2020, 44(预发表): 0-0.
[2] . Response of Arabidopsis AtR8 lncRNA to Salt Stress and Its Regulation on Seed Germination [J]. Chin Bull Bot, 2020, 55(4): 0-0.
[3] Lei -Yang. Advances in AP2/ERF transcription factors regulating plant abiotic stress response [J]. Chin Bull Bot, 2020, 55(4): 0-0.
[4] qi yijunyijun. Small RNA, No Small Feat - Plants deploy 22 nt siRNAs to combat environmental stresses [J]. Chin Bull Bot, 2020, 55(3): 0-0.
[5] Zhang Yang,Liu Huajie,Xue Ruili,Li Haixia,Li Hua. Cloning of Wheat TaLCD Gene and Its Regulation on Osmotic Stress [J]. Chin Bull Bot, 2020, 55(2): 137-146.
[6] Xinting Wang,Jing Chai,Chao Jiang,Yang Tai,Yanyan Chi,Weihua Zhang,Fang Liu,Suying Li. Population spatial pattern of Stipa grandis and its response to long-term overgrazing [J]. Biodiv Sci, 2020, 28(2): 128-134.
[7] Yang Xiaoqing,Huang Xiaoqin,Han Xiaoyang,Liu Tengfei,Yue Xiaowei,Yi Ran. Effect of Exogenous Substances on Cold Tolerance and Key Sucrose Metabolic Gene Expression in Camellia sinensis [J]. Chin Bull Bot, 2020, 55(1): 21-30.
[8] Wang Menglong,Peng Xiaoqun,Chen Zhufeng,Tang Xiaoyan. Research Advances on Lectin Receptor-like Kinases in Plants [J]. Chin Bull Bot, 2020, 55(1): 96-105.
[9] Cao Dongdong,Chen Shanyu,Qin Yebo,Wu Huaping,Ruan Guanhai,Huang Yutao. Regulatory Mechanism of Salicylic Acid on Seed Germination Under Salt Stress in Kale [J]. Chin Bull Bot, 2020, 55(1): 49-61.
[10] ZOU An-Long,LI Xiu-Ping,NI Xiao-Feng,JI Cheng-Jun. Responses of tree growth to nitrogen addition in Quercus wutaishanica forests in Mount Dongling, Beijing, China [J]. Chin J Plant Ecol, 2019, 43(9): 783-792.
[11] Zhang Tong,Guo Yalu,Chen Yue,Ma Jinjiao,Lan Jinping,Yan Gaowei,Liu Yuqing,Xu Shan,Li Liyun,Liu Guozhen,Dou Shijuan. Expression Characterization of Rice OsPR10A and Its Function in Response to Drought Stress [J]. Chin Bull Bot, 2019, 54(6): 711-722.
[12] Chen Wei,Yang Yingzeng,Chen Feng,Zhou Wenguan,Shu Kai. Stress Memory Mediated by Epigenetic Modification in Plants [J]. Chin Bull Bot, 2019, 54(6): 779-785.
[13] Guo Qianqian, Zhou Wenbin. Advances in the Mechanism Underlying Plant Response to Stress Combination [J]. Chin Bull Bot, 2019, 54(5): 662-673.
[14] Zhang Xun, Yu Juanjuan, Wang Sizhu, Li Ying, Dai Shaojun. Research Advances in DREPP Gene Family in Plants [J]. Chin Bull Bot, 2019, 54(5): 582-595.
[15] Wang Xiaolong, Liu Fengzhi, Shi Xiangbin, Wang Xiaodi, Ji Xiaohao, Wang Zhiqiang, Wang Baoliang, Zheng Xiaocui, Wang Haibo. Evolution and Expression of NCED Family Genes in Vitis vinifera [J]. Chin Bull Bot, 2019, 54(4): 474-485.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Yang Ying-gen;Zhang Li-jun and Li yu. Studies on the Postharvest Physiology properties of Peach Fruits[J]. Chin Bull Bot, 1995, 12(04): 47 -49 .
[2] Zhou Shi-gong. Applications of Lanthanum in Botanical Research[J]. Chin Bull Bot, 1992, 9(02): 26 -29 .
[3] . [J]. Chin Bull Bot, 1996, 13(专辑): 105 .
[4] 杜维广 王彬如 谭克辉 郝迺斌. An Approach to the Breeding of Soybean with High Photosynthetic Efficiency[J]. Chin Bull Bot, 1984, 2(23): 7 -11 .
[5] ZHAO Yun-Yun ZHOU Xiao-Mei YANG Cai. Production of Hybrid F1 Between Avena magna and Avena nuda and It''s Identification[J]. Chin Bull Bot, 2003, 20(03): 302 -306 .
[6] . Professor Jiayang Li, a Plant Molecular Genetist[J]. Chin Bull Bot, 2003, 20(03): 370 -372 .
[7] . [J]. Chin Bull Bot, 1996, 13(专辑): 100 -101 .
[8] Qiong Jiang, Youning Wang, Lixiang Wang, Zhengxi Sun, Xia Li. Validation of Reference Genes for Quantitative RT-PCR Analysis in Soybean Root Tissue under Salt Stress[J]. Chin Bull Bot, 2015, 50(6): 754 -764 .
[9] MA Ke-Ming. Advances of the Study on Species Abundance Pattern[J]. Chin J Plan Ecolo, 2003, 27(3): 412 -426 .
[10] ZHANG Zhi-Meng, WAN Shu-Bo, NING Tang-Yuan, DAI Liang-Xiang. EFFECTS OF NITROGEN LEVEL ON NITROGEN METABOLISM AND CORRELATING ENZYME ACTIVITY IN PEANUT[J]. Chin J Plan Ecolo, 2008, 32(6): 1407 -1416 .