Skip to main content
SpringerLink
Log in

Variation in the functional traits of fine roots is linked to phylogenetics in the common tree species of Chinese subtropical forests

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

The phylogenetic variations of fine root traits, which are related to plant growth and development as well as to physiological and ecological processes, are not fully understood. This study aimed to: (1) examine how tree species and sampling methodology affect the anatomical, morphological and nutrient traits of fine roots; and (2) determine whether phylogenetic signals affect fine root trait relationships and influence comparison of root traits between the branch order-based and diameter-based cut-off sampling categories.

Methods

Fine root samples of 16 subtropical forest tree species were obtained and their anatomical, morphological and nutrient traits were studied. The phylogenetic signals of trait variations were calculated to determine trait relationships.

Results

Tree species and sampling methodology significantly affected fine root traits (p < 0.05). Mean root diameters, root tissue density (RTD) and carbon-to-nitrogen ratio were the lowest in the first-order category and highest in the ≤2 mm category. The reverse pattern was found for specific root length, specific root area and nitrogen concentration. Morphological traits showed significant phylogenetic signals; however, nutrient traits did not reflect phylogenetic conservatism. Phylogenetic factors influenced correlations between traits for the first-order root economics spectrum. Root traits were multidimensional and RTD was loaded on a novel phylogenetic principal component analysis.

Conclusions

Functional traits of fine roots are multidimensional for subtropical tree species and closely linked to phylogeny. Morphological traits of first order roots showed a much stronger phylogenetic signal than those of roots ≤2 mm (traditionally defined fine roots). The findings improve understanding of root trait strategies in response to environmental changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alexander L, Miroslava L, Jun A, Morita S (2004) Root cortex: structural and functional variability and responses to environmental stress. Root Res 13(3):117–131

  • Baraloto C, Hardy OJ, Paine CE, Dexter KG, Cruaud C, Dunning LT, Gonzalez MA, Molino JF, Sabatier D, Savolainen V, Chave J (2012) Using functional traits and phylogenetic trees to examine the assembly of tropical tree communities. J Ecol 100(3):690–701

    Article  Google Scholar 

  • Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29(12):692–699

    Article  PubMed  Google Scholar 

  • Baylis GTS (1975) The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In: Sanders FE, Mosse B, Tinker PB (eds) Endomycorrhizas. Academic Press, London, pp 373–389

    Google Scholar 

  • Beerling DJ, Woodward FI (2001) Vegetation and the terrestrial carbon cycle: modelling the first 400 million years. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Beyer F, Hertel D, Leuschner C (2013) Fine root morphological and functional traits in Fagus sylvatica and Fraxinus excelsior saplings as dependent on species, root order and competition. Plant Soil 373(1):143–156

    Article  CAS  Google Scholar 

  • Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745

    Article  PubMed  Google Scholar 

  • Chandler JN, Bartels D (2008) Drought: “avoidance and adaptation”. In: Trimble SW, Stewart BA, Howel TA (eds) Encyclopedia of water science. Taylor and Francis Group, London, pp 222–224

    Google Scholar 

  • Chen WL, Zeng H, Eissenstat DM, Guo DL (2013) Variation of first-order root traits across climatic gradients and evolutionary trends in geological time. Glob Ecol Biogeogr 22(7):846–856

    Article  Google Scholar 

  • Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339(6127):1615–1618

    Article  CAS  PubMed  Google Scholar 

  • Collins CG, Wright SJ, Wurzburger N (2016) Root and leaf traits reflect distinct resource acquisition strategies in tropical lianas and trees. Oecologia 180(4):1037–1047

    Article  PubMed  Google Scholar 

  • Comas LH, Eissenstat DM (2009) Patterns in root trait variation among 25 co-existing north American forest species. New Phytol 182(4):919–928

    Article  CAS  PubMed  Google Scholar 

  • Comas LH, Bouma TJ, Eissenstat DM (2002) Linking root traits to potential growth rate in six temperate tree species. Oecologia 132(1):34–43

    Article  CAS  PubMed  Google Scholar 

  • Comas LH, Mueller KE, Taylor LL, Midford PE, Callahan HS, Beerlingz DJ (2012) Evolutionary patterns and biogeochemical significance of angiosperm root traits. Int J Plant Sci 57(6):584–595

    Article  Google Scholar 

  • de la Riva EG, Marañón T, Pérez-Ramos I, Navarro-Fernández CM, Olmo M, Villar R (2018) Root traits across environmental gradients in Mediterranean woody communities: are they aligned along the root economics spectrum? Plant Soil 424(1–2):35–48

    Article  CAS  Google Scholar 

  • Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14(6):927–930

    Article  Google Scholar 

  • Dong XY, Wang HF, Gu JC, Wang Y, Wang ZQ (2015) Root morphology, histology and chemistry of nine fern species (pteridophyta) in a temperate forest. Plant Soil 393(1):215–227

    Article  CAS  Google Scholar 

  • Doyle JA, Hickey LJ (1976) Pollen and leaves from the mid-cretaceous and their bearing on early angiosperm evolution. In: Beck CB (ed) Origin and early evolution of angiosperms. Columbia University Press, New York, pp 139–206

    Google Scholar 

  • Eissenstat DM, Achor DS (1999) Anatomical characteristics of roots of citrus rootstocks that vary in specific root length. New Phytol 141(2):309–321

    Article  PubMed  Google Scholar 

  • Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60

    Article  Google Scholar 

  • Eissenstat DM, Yanai RD (2002) Root life span, efficiency, and turnover. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots, the hidden half, 3rd edn. Marcel Dekker Inc, New York, pp 221–238

    Google Scholar 

  • Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications carbon isotope patterns in Pinus sylvestris. New Phytol 147(1):33–42

    Article  CAS  Google Scholar 

  • Erktan A, McCormack ML, Roumet C (2018) Frontiers in root ecology: recent advances and future challenges. Plant Soil 424(1–2):1–9

    Article  CAS  Google Scholar 

  • Esau K (1965) Plant anatomy. Wiley, New York

    Google Scholar 

  • Espeleta JF, Donovan LA (2002) Fine root demography and morphology in response to soil resources availability among xeric and mesics and hill tree species. Funct Ecol 16(1):113–121

    Article  Google Scholar 

  • Fan P, Jiang Y (2010) Nitrogen dynamics differed among the first six root branch orders of Fraxinus mandshurica and Larix gmelinii during short-term decomposition. J Plant Res 123(4):433–438

    Article  CAS  PubMed  Google Scholar 

  • Feild TS, Chatelet DS, Brodribb TJ (2009) Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7(2):237–264

    Article  CAS  PubMed  Google Scholar 

  • Fitter AH, Stickland TR, Harvey ML, Wilson GW (1991) Architectural analysis of plant root systems. I. Architectural correlates of exploitation efficiency. New Phytol 118(3):375–382

    Article  Google Scholar 

  • Fletcher BJ, Brentnall SJ, Anderson CW, Berner RA, Beerling DJ (2008) Atmospheric carbon dioxide linked Mesozoic and early Cenozoic climatic change. Nat Geosci 1(1):43–48

    Article  CAS  Google Scholar 

  • Flores O, Garnier E, Wright IJ, Reich PB, Pierce S, Diaz S, Pakeman RJ, Rusch GM, Bernard-Verdier M, Testi B, Bakker JP, Bekker RM, Cerabolini BEL, Ceriani RM, Cornu G, Cruz P, Delcamp M, Dolezal J, Eriksson O, Fayolle A, Freitas H, Golodets C, Gourlet-Fleury S, Hodgson JG, Brusa G, Kleyer M, Kunzmann D, Lavorel S, Papanastasis VP, Pérez-Harguindeguy N, Vendramini F, Weiher E (2014) An evolutionary perspective on leaf economics: phylogenetics of leaf mass per area in vascular plants. Ecol Evol 4(14):2799–2811

    Article  PubMed  PubMed Central  Google Scholar 

  • Fort F, Cruz P, Lecloux E, Bittencourt de Oliveira L, Stroia C, Theau JP, Jouany C (2016) Grassland root functional parameters vary according to a community-level resource acquisition – conservation trade-off. J Veg Sci 27(4):749–758

    Article  Google Scholar 

  • Freschet GT, Roumet C (2017) Sampling roots to capture plant and soil functions. Funct Ecol 8(31):1506–1518

    Article  Google Scholar 

  • Friedman J, Bohonak AJ, Levine RA (2013) When are two pieces better than one: fitting and testing OLS and RMA regressions. Environmetrics 24(5):306–316

    Article  Google Scholar 

  • Gu JC, Xu Y, Dong XY, Wang HF, Wang ZQ (2014) Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species. Tree Physiol 34(4):415–425

    Article  PubMed  Google Scholar 

  • Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140(3):450–457

    Article  PubMed  Google Scholar 

  • Guo DL, Li H, Mitchell RJ, Han W, Hendricks JJ, Fahey TJ, Hendrick RL (2008a) Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytol 177(2):443–456

    PubMed  Google Scholar 

  • Guo DL, Xia MX, Wei X, Liu Y, Wang ZQ (2008b) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180(3):673–683

    Article  PubMed  Google Scholar 

  • Hernández EI, Vilagrosa A, Pausas JG, Bellot J (2009) Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecol 207(2):233–244

    Article  Google Scholar 

  • Hickey LJ, Doyle JA (1977) Early cretaceous fossil evidence for angiosperm evolution. Bot Rev 43(1):3–104

    Article  Google Scholar 

  • Hishi T (2007) Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions. J For Res 12(2):126–133

    Article  Google Scholar 

  • Hishi T, Takeda H (2005) Dynamics of heterorhizic root systems: protoxylem groups within the fine-root system of Chamaecyparis obtusa. New Phytol 167(2):509–521

    Article  PubMed  Google Scholar 

  • Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB (2010) Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162(2):505–513

    Article  PubMed  Google Scholar 

  • Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162(1):9–24

    Article  Google Scholar 

  • Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120000-year soil chronosequence in temperate rain forest. J Ecol 99(4):954–963

    Article  Google Scholar 

  • Hummel I, Vile D, Violle C, Devaux J, Ricci B, Blanchard A, Garnier É, Roumet C (2007) Relating root structure and anatomy to whole-plant functioning in 14 herbaceous Mediterranean species. New Phytol 173(2):313–321

    Article  PubMed  Google Scholar 

  • IUSS Working Group WRB (2006) World Reference Base for soil resource 2006. In: world soil resources reports no. 103. 2nd ed. FAO, Rome

  • Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci. USA 94(14):7362–7366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia SX, McLaughlin NB, Gu JC, Li XP, Wang ZQ (2013) Relationships between root respiration rate and root morphology, chemistry and anatomy in Larix gmelinii and Fraxinus mandshurica. Tree Physiol 33(6):579–589

    Article  CAS  PubMed  Google Scholar 

  • Kembel SW, De Kroon H, Cahill JF Jr, Mommer L (2008) Improving the scale and precision of hypotheses to explain root foraging ability. Ann Bot 101(9):1295–1301

    Article  PubMed  PubMed Central  Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11):1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kong DL, Ma CN, Zhang Q, Li L, Chen XY, Zeng H, Guo DL (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol 203(3):863–872

    Article  PubMed  Google Scholar 

  • Kong DL, Wang JJ, Kardol P, Wu HF, Zeng H, Deng XB, Deng Y (2016) Economic strategies of plant absorptive roots vary with root diameter. Biogeosciences 13(2):415–424

    Article  Google Scholar 

  • Kong DL, Wang JJ, Zeng H, Liu MZ, Miao Y, Wu HF, Kardol P (2017) The nutrient absorption–transportation hypothesis: optimizing structural traits in absorptive roots. New Phytol 213(4):1569–1572

    Article  PubMed  Google Scholar 

  • Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104(5):1299–1310

    Article  Google Scholar 

  • Kress WJ, Erickson DL, Jones FA, Swenson NG, Perez R, Sanjur O, Bermingham E (2009) Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proc Natl Acad Sci. USA 106(44):18621–18626

    Article  PubMed  PubMed Central  Google Scholar 

  • Laliberté E (2017) Below-ground frontiers in trait-based plant ecology. New Phytol 213(4):1597–1603

    Article  PubMed  Google Scholar 

  • Laughlin DC (2014) The intrinsic dimensionality of plant traits and its relevance to community assembly. J Ecol 102(1):186–193

    Article  Google Scholar 

  • Lavorel S, Díaz S, Cornelissen J, Garnier E, Harrison SP, McIntyre S, Pausas JG, Pérez-Harguindeguy N, Roumet C, Urcelay C (2007) Plant functional types: are we getting any closer to the holy grail?  In: Canadell JG, Pataki DE, Pitelka LF (eds) Terrestrial Ecosystems in a Changing World. Global Change-The IGBP Series. Springer, Berlin, Heidelberg, pp. 149–164

  • Li A, Guo DL, Wang ZQ, Liu HY (2010) Nitrogen and phosphorus allocation in leaves, twigs, and fine roots across 49 temperate, subtropical and tropical tree species: a hierarchical pattern. Funct Ecol 24(1):224–232

    Article  Google Scholar 

  • Liao Y, McCormack ML, Fan H, Wang H, Wu J, Tu J, Liu W, Guo D (2014) Relation of fine root distribution to soil C in a Cunninghamia lanceolata plantation in subtropical China. Plant Soil 381(1–2):225–234

    Article  CAS  Google Scholar 

  • Liu GF, Freschet GT, Pan X, Cornelissen JHC, Li Y, Dong M (2010a) Coordinated variation in leaf and root traits across multiple spatial scales in Chinese semi-arid and arid ecosystems. New Phytol 188(2):543–553

    Article  PubMed  Google Scholar 

  • Liu J, Xiang WH, Xu X, Chen R, Tian DL, Peng CH, Fang X (2010b) Analysis of architecture and functions of fine roots of five subtropical tree species in Huitong, Hunan Province, China. Chin J Plant Ecology 34(8):938–945 (in Chinese, with English abstract)

    Google Scholar 

  • Liu C, Xiang WH, Lei PF, Deng XW, Tian DL, Fang X, Peng CH (2014) Standing fine root mass and production in four Chinese subtropical forests along a succession and species diversity gradient. Plant Soil 376(1):445–459

    Article  CAS  Google Scholar 

  • Ma ZQ, Guo DL, Xu XL, Lu MZ, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97

    Article  CAS  PubMed  Google Scholar 

  • McCormack ML, Adams TS, Smithwick EH, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195(4):823–831

    Article  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo DL, Helmisaari H, 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 below-ground contributions to terrestrial biosphere processes. New Phytol 207(3):505–518

    Article  PubMed  Google Scholar 

  • Mckenzie BE, Peterson CA (2015) Root browning in pinus banksiana lamb. And eucalyptus pilularis sm. 1. Anatomy and permeability of the white and tannin zones. Plant Biol 108(2):127–137

    Google Scholar 

  • Meier IC, Leuschner C (2008) Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Glob Chang Biol 14(9):2081–2095

    Article  Google Scholar 

  • Milla R, Reich PB (2011) Multi-trait interactions, not phylogeny, fine-tune leaf size reduction with increasing altitude. Ann Bot 107(3):455–465

    Article  PubMed  PubMed Central  Google Scholar 

  • Montagnoli A, Terzaghi M, Giussani B, Scippa GS, Chiatante D (2018) An integrated method for high-resolution definition of new diameter-based fine root sub-classes of Fagus sylvatica L. Ann For Sci 75(3):76

    Article  Google Scholar 

  • Norby RJ, Jackson RB (2000) Root dynamics and global change: seeking an ecosystem perspective. New Phytol 147(1):3–12

    Article  CAS  Google Scholar 

  • Osnas JLD, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science 340(6133):741–744

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290

    Article  CAS  PubMed  Google Scholar 

  • Pei NC, Lian JY, Erickson DL, Swenson NG, Kress WJ, Ye WH, Ge XJ (2011) Exploring tree-habitat associations in a Chinese subtropical forest plot using a molecular phylogeny generated from DNA barcode loci. PLoS One 6(6):e21273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson CA, Enstone DE, Taylor JH (1999) Pine root structure and its potential significance for root function. Plant Soil 217(1–2):205–213

    Article  Google Scholar 

  • Picon-Cochard C, Pilon R, Tarroux E, Pages L, Robertson J, Dawson L (2012) Effect of species, root branching order and season on the root traits of 13 perennial grass species. Plant Soil 353(1):47–57

    Article  CAS  Google Scholar 

  • Pregitzer KS (2002) Fine roots of trees – a new perspective. New Phytol 154(2):267–273

    Article  PubMed  Google Scholar 

  • Pregitzer KS, Kubiske ME, Yu CK, Hendrick RL (1997) Relationships among root branch order, carbon, and nitrogen in four temperate species. Oecologia 111(3):302–308

    Article  PubMed  Google Scholar 

  • Pregitzer KS, DeForest JA, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north American trees. Ecol Monogr 72(2):293–309

    Article  Google Scholar 

  • Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght JL, Mao Z, Pierret A, Portillo N, Roupsard O, Thammahacksa C, Stokes A (2015) Root functional parameters along a land-use gradient: evidence of a community-level economics spectrum. J Ecol 103(2):361–373

    Article  Google Scholar 

  • Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102(2):275–301

    Article  Google Scholar 

  • Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164(3):143–164

    Article  Google Scholar 

  • Retallack GJ (2001) A 300-million-year record of atmospheric carbon dioxide from fossil plant cuticles. Nature 411(6835):287–290

    Article  CAS  PubMed  Google Scholar 

  • Revell LJ (2009) Size-correction and principal components for specific comparative studies. Evolution 63(12):3258–3268

    Article  PubMed  Google Scholar 

  • Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3(2):217–223

    Article  Google Scholar 

  • Roumet C, Urcelay C, Díaz S (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytol 170(2):357–368

    Article  PubMed  Google Scholar 

  • Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S, Cao KF, Stokes A (2016) Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol 210(3):815–826

    Article  PubMed  Google Scholar 

  • Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19(2):301–302

    Article  CAS  PubMed  Google Scholar 

  • Savin SM (1977) The history of the Earth's surface temperature during the past 100 million years. Annu Rev Earth Planet Sci 5(1):319–355

    Article  CAS  Google Scholar 

  • Solari LI, Pernice F, DeJong TM (2006) The relationship of hydraulic conductance to root system characteristics of peach (Prunus persica) rootstocks. Physiol Plant 128(2):324–333

    Article  CAS  Google Scholar 

  • Stamatakis A (2006) RA×ML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Swenson NG, Erickson DL, Mi XC, Bourg NA, Forero-Montaña J, Ge XJ, Howe R, Lake JK, Liu XJ, KP MA, Pei NC, Thompson J, Uriarte M, Wolf A, Wright SJ, Ye WH, Zhang JL, Zimmerman JK, Kress WJ (2012) Phylogenetic and functional alpha and beta diversity in temperate and tropical tree communities. Ecology 93(8):S112–S125

    Article  Google Scholar 

  • Valenzuela-Estrada LR, Vera-Caraballo V, Ruth LE, Eissenstat DM (2008) Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae). Am J Bot 95(12):1506–1514

    Article  PubMed  Google Scholar 

  • Valverde-Barrantes OJ, Smemo KA, Feinstein LM, Kershner MW, Blackwood CB (2013) The distribution of below-ground traits is explained by intrinsic species differences and intraspecific plasticity in response to root neighbours. J Ecol 101(4):933–942

    Article  Google Scholar 

  • Valverde-Barrantes OJ, Smemo KA, Blackwood CB (2015) Fine root morphology is phylogenetically structured but nitrogen is related to the plant economics spectrum in temperate trees. Funct Ecol 29(6):796–807

    Article  Google Scholar 

  • Valverde-Barrantes OJ, Freschet GT, Roumet C, Blackwood CB (2017) A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants. New Phytol 215(4):1562–1573

    Article  PubMed  Google Scholar 

  • Wahl S, Ryser P (2000) Root tissue structure is linked to ecological strategies of grasses. New Phytol 148(3):459–471

    Article  PubMed  Google Scholar 

  • Wang R, Wang Q, Zhao N, Xu Z, Zhu X, Jiao C, Yu G, He N (2018) Different phylogenetic and environmental controls of first-order root morphological and nutrient traits: evidence of multidimensional root traits. Funct Ecol 32:29–39

    Article  Google Scholar 

  • Warton DI, Duursma RA, Falster DS, Taskinen S (2012) Smatr 3–an R package for estimation and inference about allometric lines. Methods Ecol Evol 3(2):257–259

    Article  Google Scholar 

  • Weemstra M, Mommer L, Visser EJ, Ruijven J, Kuyper TW, Mohren GM, Sterck FJ (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211(4):1159–1169

    Article  CAS  PubMed  Google Scholar 

  • Wells CE, Eissenstat DM (2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82(3):882–892

    Article  Google Scholar 

  • Wells CE, Eissenstat DM (2003) Beyond the roots of young seedlings: the influence of age and order on fine root physiology. J Plant Growth Regul 21(4):324–334

    Article  CAS  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428(6985):821–827

    Article  CAS  PubMed  Google Scholar 

  • Xiang WH, Fan GW, Lei PF, Zeng YL, Tong J, Fang X, Deng XW, Peng CH (2015) Fine root interactions in subtropical mixed forests in China depend on tree species composition. Plant Soil 395(1–2):335–349

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the National Natural Science Foundation of China (31570447 and 31870431) and the Huitong Forest Ecological Station funded by the State Forestry Administration of the People’s Republic of China. Cong Liu would like to acknowledge the China Scholarship Council for supporting her joint Ph.D. program grant (201708430137).

Author information

Authors and Affiliations

  1. Faculty of Life Science and Technology, Central South University of Forestry and Technology, Changsha, 410004, Hunan Province, China

    Cong Liu, Wenhua Xiang, Limei Zou, Pifeng Lei, Yelin Zeng, Shuai Ouyang, Xiangwen Deng & Xi Fang

  2. Huitong National Station for Scientific Observation and Research of Chinese Fir Plantation Ecosystems in Hunan Province, Huitong, 438107, China

    Cong Liu, Wenhua Xiang, Limei Zou, Pifeng Lei, Yelin Zeng, Shuai Ouyang, Xiangwen Deng & Xi Fang

  3. Institute of Environment Sciences, Department of Biological Sciences, University of Quebec at Montreal, Montreal, QC, H3C 3P8, Canada

    Cong Liu, Zelin Liu & Changhui Peng

Authors
  1. Cong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenhua Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Limei Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pifeng Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yelin Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shuai Ouyang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiangwen Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xi Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zelin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Changhui Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Idea and study design: WX; data collection and analysis: CL, LZ, PL, YZ and ZL, with support from SO, XD, and XF; manuscript writing: CL, WX and CP.

Corresponding author

Correspondence to Wenhua Xiang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Zhun Mao.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOC 79367 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Xiang, W., Zou, L. et al. Variation in the functional traits of fine roots is linked to phylogenetics in the common tree species of Chinese subtropical forests. Plant Soil 436, 347–364 (2019). https://doi.org/10.1007/s11104-019-03934-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-03934-0

Keywords

Search

Navigation