Skip to main content
SpringerLink
Log in

Differences in the relationship between metabolomic and ionomic traits of Quercus variabilis growing at contrasting geologic-phosphorus sites in subtropics

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

Abstract

Aims

Subtropical ecosystems are generally characterized by phosphorus (P)-deficient soils; however, extreme P-rich soils develop on phosphate rocks. We aimed to integrate metabolomic and ionomic analyses to survey how in situ trees adaptively respond to such contrasting P soils.

Methods

Gas (GC-MS) or liquid (LC-MS) chromatography-mass spectrometry and inductively coupled plasma-optical emission spectrometer (ICP-OES) were used to analyze leaf metabolome and ionome of Quercus variabilis, which grew at two geologic P-rich and P-deficient sites in subtropical China.

Results

Two Q. variabilis populations were significantly discriminated in terms of metabolome and ionome, with major contributions from 25 identified metabolites (e.g. sugars and P-containing compounds) and P and four other chemical elements. And of these 25 metabolites, orthophosphate was predominant in influencing the variation in the metabolomes of Q. variabilis between the two P-type sites. Moreover, orthophosphate was correlated with leaf P (r = 0.85, p < 0.001), while leaf P was significantly influenced only by soil resident P at the P-rich site. Furthermore, the metabolic pathway analysis indicated four critical metabolic pathways: galactose metabolism, amino sugar and nucleotide sugar metabolism, glyoxylate and dicarboxylate metabolism, fructose and mannose metabolism.

Conclusions

These findings suggested that there were distinct ionome-metabolome interactions in Q. variabilis populations, between P-rich and P-deficient sites, which contributed to novel insights into how plants interactively adapt to P-limiting soils.

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
Fig. 4

Similar content being viewed by others

References

  • Amtmann A, Armengaud P (2009) Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis. Curr Opin Plant Biol 12:275–283

    Article  CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Attiwill PM, Adams MA (1993) Nutrient cycling in forests. New Phytol 124:561–582

    Article  CAS  PubMed  Google Scholar 

  • Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nutr 12:547–562

    Article  Google Scholar 

  • Brosché M, Vinocur B, Alatalo ER, Lamminmäki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot M-B, Altman A (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6:R101

    Article  PubMed  PubMed Central  Google Scholar 

  • Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Funct Plant Biol 35:412–426

    Article  CAS  PubMed  Google Scholar 

  • Cernusak LA, Winter K, Turner BL (2010) Leaf nitrogen to phosphorus ratios of tropical trees: experimental assessment of physiological and environmental controls. New Phytol 185:770–779

    Article  CAS  PubMed  Google Scholar 

  • Chen D, Zhang X, Kang H, Sun X, Yin S, Du H, Yamanaka N, Gapare W, Wu HX, Liu C (2012) Phylogeography of Quercus variabilis based on chloroplast DNA sequence in East Asia: multiple glacial refugia and mainland-migrated island populations. PLoS One 7:e47268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cleveland CC, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante M, Chuyong G, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:939–947

    Article  PubMed  Google Scholar 

  • Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombois D, Vitousek PM (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424

    Article  Google Scholar 

  • Cronan CS, Grigal DF (1995) Use of calcium/aluminum ratios as indicators of stress in forest ecosystems. J Environ Qual 24:209–226

    Article  CAS  Google Scholar 

  • Davey MP, Burrell MM, Woodward FI, Quick WP (2008) Population-specific metabolic phenotypes of Arabidopsis lyrata ssp. petraea. New Phytol 177:380–388

    CAS  PubMed  Google Scholar 

  • De Vos RCH, Moco S, Lommen A, Keurentjes JJB, Bino RJ, Hall RD (2007) Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry. Nat Protoc 2:778–791

    Article  CAS  PubMed  Google Scholar 

  • Di Martino C, Delfine S, Pizzuto R, Loreto F, Fuggi A (2003) Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. New Phytol 158:455–463

    Article  CAS  Google Scholar 

  • Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608

    Article  CAS  PubMed  Google Scholar 

  • FAO I (1998) World reference base for soil resources. World soil resources reports

  • Fester T, Merbach I, Schulz E, Härtig C (2014) Metabolic response of Medicago sativa to severe nutrient imbalances and disturbances under field conditions. J Plant Nutr Soil Sci 177:245–259

    Article  CAS  Google Scholar 

  • Fonville JM, Richards SE, Barton RH, Boulange CL, Ebbels TMD, Nicholson JK, Holmes E, Dumas M-E (2010) The evolution of partial least squares models and related chemometric approaches in metabonomics and metabolic phenotyping. J Chemom 24:636–649

    Article  CAS  Google Scholar 

  • Gan H, Jiao Y, Jia J, Wang X, Li H, Shi W, Peng C, Polle A, Luo Z (2015) Phosphorus and nitrogen physiology of two contrasting poplar genotypes when exposed to phosphorus and/or nitrogen starvation. Tree Physiol 36:22–38

    Article  CAS  PubMed  Google Scholar 

  • Grattan SR, Grieve CM (1985) Betaine status in wheat in relation to nitrogen stress and to transient salinity stress. Plant Soil 85:3–9

    Article  CAS  Google Scholar 

  • Guo R, Shi L, Yang C, Yan C, Zhong X, Liu Q, Xia X, Li H (2016) Comparison of ionomic and metabolites response under alkali stress in old and young leaves of cotton (Gossypium hirsutum L.) seedlings. Front. Plant Sci 7:1785

    Google Scholar 

  • Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  PubMed  Google Scholar 

  • Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385

    Article  CAS  PubMed  Google Scholar 

  • Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (cu, Zn, Mn, Fe, Ni, Mo, B, cl). Curr Opin Plant Biol 12:259–266

    Article  CAS  PubMed  Google Scholar 

  • Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, Shirley N, Langridge P, Bacic A (2008) Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol 49:691–703

    Article  CAS  PubMed  Google Scholar 

  • Irakli L, Elser JJ (2011) The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. Ecol Lett 14:244–250

    Article  Google Scholar 

  • Ji H, Du B, Liu C (2017) Elemental stoichiometry and compositions of weevil larvae and two acorn hosts under natural phosphorus variation. Sci Rep 7:45810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kimmins JP (2004) Forest ecology. Benjamin-Cummings Publishing Company, Menlo Park, California

    Google Scholar 

  • Kind T, Wohlgemuth G, Lee DY, Lu Y, Palazoglu M, Shahbaz S, Fiehn O (2009) FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal Chem 81:10038–10048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450

    Article  Google Scholar 

  • Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry–based metabolite profiling in plants. Nat Protoc 1:387–396

    Article  CAS  PubMed  Google Scholar 

  • Lundstedt T, Seifert E, Abramo L, Thelin B, Nyström Å, Pettersen J, Bergman R (1998) Experimental design and optimization. Chemom Intell Lab Syst 42:3–40

    Article  CAS  Google Scholar 

  • Matzek V, Vitousek PM (2009) N: P stoichiometry and protein: RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett 12:765–771

    Article  PubMed  Google Scholar 

  • Monreal JA, Jimenez ET, Remesal E, Morillo-Velarde R, García-Mauriño S, Echevarría C (2007) Proline content of sugar beet storage roots: response to water deficit and nitrogen fertilization at field conditions. Environ Exp Bot 60:257–267

    Article  CAS  Google Scholar 

  • Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, BLÄSING O, Usadel B, Czechowski T, Udvardi MK, Stitt M (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    Article  CAS  PubMed  Google Scholar 

  • Mulholland MM, Otte ML (2000) Effects of varying sulphate and nitrogen supply on DMSP and glycine betaine levels in Spartina anglica. J Sea Res 43:199–207

    Article  CAS  Google Scholar 

  • Mulholland MM, Otte ML (2002) The effects of nitrogen supply and salinity on DMSP, glycine betaine and proline concentrations in leaves of Spartina anglica. Aquat Bot 72:193–200

    Article  Google Scholar 

  • Nanamori M, Shinano T, Wasaki J, Yamamura T, Rao IM, Osaki M (2004) Low phosphorus tolerance mechanisms: phosphorus recycling and photosynthate partitioning in the tropical forage grass, Brachiaria hybrid cultivar Mulato compared with rice. Plant Cell Physiol 45:460–469

    Article  CAS  PubMed  Google Scholar 

  • Plaxton WC, Carswell MC (1999) Metabolic aspects of the phosphate starvation response in plants. In: Lerner HR (ed) Plant responses to environmental stresses: from phytohormones to genome reorganization. Marcel Dekker, Inc., New York, pp 349–372

    Google Scholar 

  • Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693

    Article  CAS  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci U S A 101:11001–11006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro DM, Silva Júnior DD, Cardoso FB, Martins AO, Silva WA, Nascimento VL, Araújo WL (2016) Growth inhibition by selenium is associated with changes in primary metabolism and nutrient levels in Arabidopsis thaliana. Plant Cell Environ 39:2235–2246

    Article  CAS  PubMed  Google Scholar 

  • Rivas-Ubach A, Sardans J, Pérez-Trujillo M, Estiarte M, Peñuelas J (2012) Strong relationship between elemental stoichiometry and metabolome in plants. Proc Natl Acad Sci U S A 109:4181–4186

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanchez DH, Pieckenstain FL, Escaray F, Erban A, Kraemer U, Udvardi MK, Kopka J (2011) Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. Plant Cell Environ 34:605–617

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Calderón L, Chacon-López A, Pérez-Torres CA, Herrera-Estrella L (2010) Phosphorus: plant strategies to cope with its scarcity. In: Hell R, Mendel RR (eds) Cell biology of metals and nutrients. Springer, Berlin, Heidelberg, pp 173–198

    Chapter  Google Scholar 

  • Sardans J, Peñuelas J, Rivas-Ubach A (2011a) Ecological metabolomics: overview of current developments and future challenges. Chemoecology 21:191–225

    Article  CAS  Google Scholar 

  • Sardans J, Rivas-Ubach A, Peñuelas J (2011b) Factors affecting nutrient concentration and stoichiometry of forest trees in Catalonia (NE Spain). For Ecol Manage 262:2024–2034

    Article  Google Scholar 

  • Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst 38:595–619

    Article  Google Scholar 

  • Sawai Y, Yamaguchi Y, Miyama D, Yoshitomi H (2001) Cycling treatment of anaerobic and aerobic incubation increases the content of γ-aminobutyric acid in tea shoots. Amino Acids 20:331–334

    Article  CAS  PubMed  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serraj R, Shelp BJ, Sinclair TR (1998) Accumulation of γ-aminobutyric acid in nodulated soybean in response to drought stress. Physiol Plant 102:79–86

    Article  CAS  PubMed  Google Scholar 

  • Shaver GR, Chapin FSI, Billings WD (1979) Ecotypic differentiation in Carex aquatilis on ice-wedge polygons in the Alaskan coastal tundra. J Ecol 67:1025–1045

    Article  CAS  Google Scholar 

  • Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi C, Han R, Wu P, Fang M, Lai H, Shentu L (2011) Geochemistry and provenance of source rock for matoushan formation rocks (late cretaceous) in the Mouding area, Central Yunnan. Acta Sedimentol Sin 29:303–311

    CAS  Google Scholar 

  • Silberbush M, Waisel Y, Kafkafi U (1981) The role of soil phosphorus in differentiation of edaphic ecotypes in Aegilops peregrina. Oecologia 49:419–424

    Article  PubMed  Google Scholar 

  • Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78:779–787

    Article  CAS  PubMed  Google Scholar 

  • Snaydon RW, Bradshaw AD (1962) Differences between natural populations of Trifolium repens L. in response to mineral nutrients. J Exp Bot 13:422–434

    Article  CAS  Google Scholar 

  • Soetan KO, Olaiya CO, Oyewole OE (2010) The importance of mineral elements for humans, domestic animals and plants: a review. Afr J Food Sci 4:200–222

    CAS  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Sun X, Kang H, Du H, Hu H, Zhou J, Hou J, Zhou X, Liu C (2012) Stoichiometric traits of oriental oak (Quercus variabilis) acorns and their variations in relation to environmental variables across temperate to subtropical China. Ecol Res 27:765–773

    Article  Google Scholar 

  • Tao Y (2005) A proximate mathematical model of the content of main chemical constituents in an industrial phosphorus ore. Yunnan Geol 24:151–166

    Google Scholar 

  • Tawaraya K, Horie R, Shinano T, Wagatsuma T, Saito K, Oikawa A (2014) Metabolite profiling of soybean root exudates under phosphorus deficiency. Soil Sci Plant Nutr 60:679–694

    Article  CAS  Google Scholar 

  • Tiessen H (2008) Phosphorus in the global environment. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions. Springer, Dordrecht, pp 1–7

    Google Scholar 

  • Tillberg JE, Rowley JR (1989) Physiological and structural effects of phosphorus starvation on the unicellular green alga Scenedesmus. Physiol Plant 75:315–324

    Article  CAS  Google Scholar 

  • Tissue DT, Lewis JD, Niinemets Ü (2010) Photosynthetic responses of cottonwood seedlings grown in glacial through future atmospheric [CO2] vary with phosphorus supply. Tree Physiol 30:1361–1372

    Article  CAS  PubMed  Google Scholar 

  • Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131:1064–1079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  PubMed  Google Scholar 

  • Vitousek P (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  CAS  Google Scholar 

  • Warren CR (2011) How does P affect photosynthesis and metabolite profiles of Eucalyptus globulus? Tree Physiol 31:727–739

    Article  CAS  PubMed  Google Scholar 

  • Westheimer FH (1987) Why nature chose phosphates. Science 235:1173–1178

    Article  CAS  PubMed  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Zhu Y, Jiang H (1987) The vegetation of Yunnan. Science, Beijing

  • Wu D, Shen Q, Cai S, Chen Z, Dai F, Zhang G (2013) Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol 54:1976–1988

    Article  CAS  PubMed  Google Scholar 

  • Xia J, Wishart DS (2010) MSEA: a web-based tool to identify biologically meaningful patterns in quantitative metabolomic data. Nucleic Acids Res 38:W71–W77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Res 43:W251–W257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao G, Li T, Zhang X, Yu H, Huang H, Gupta DK (2009) Uptake and accumulation of phosphorus by dominant plant species growing in a phosphorus mining area. J Hazard Mater 171:542–550

    Article  CAS  PubMed  Google Scholar 

  • Yan X, Lynch JP, Beebe SE (1995) Genetic variation for phosphorus efficiency of common bean in contrasting soil types: I. Vegetative response. Crop Sci 35:1086–1093

    Article  Google Scholar 

  • Yan K, Fu D, He F, Duan C (2011) Leaf nutrient stoichiometry of plants in the phosphorus-enriched soils of the Lake Dianchi watershed, southwestern China. Chin J Plant Ecol 35:353–361

    Article  Google Scholar 

  • Yan K, Ranjitkar S, Zhai D, Li Y, Xu J, Li B, Lu Y (2017) Current re-vegetation patterns and restoration issues in degraded geological phosphorus-rich mountain areas: a synthetic analysis of Central Yunnan, SW China. Plant Diversity 39:140–148

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu Q, Wu H, He N, Lü X, Wang Z, Elser JJ, Wu J, Han X (2012) Testing the growth rate hypothesis in vascular plants with above-and below-ground biomass. PLoS One 7:e32162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Sun X, Du B, Yin S, Liu C (2015) Multielement stoichiometry in Quercus variabilis under natural phosphorus variation in subtropical China. Sci Rep 5:7839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu F, Lu X, Liu L, Mo J (2015) Phosphate addition enhanced soil inorganic nutrients to a large extent in three tropical forests. Sci Rep 5:7923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was funded by the National Natural Science Foundation of China (No. 31670626, No. 31270640, and No. 31070532) and the National Key R&D Program of China (2017YFC0505501). We thank the Instrumental Analysis Center of Shanghai Jiao Tong University for the support on chemical analysis.

Data accessibility

All data are included in the manuscript and the supplementary files, and all metabolites identified by GC-TOF-MS and UHPLC-QTOF-MS are included in the excel file named “ESM 2”.

Author information

Authors and Affiliations

  1. School of Agriculture and Biology and Research Centre for Low-Carbon Agriculture, Shanghai Jiao Tong University, Dongchuan Rd. 800, Shanghai, 200240, China

    Huawei Ji, Baoming Du, Jiahao Wen & Chunjiang Liu

  2. Shanghai Urban Forest Research Station, State Forestry Administration, Beijing, China

    Huawei Ji, Baoming Du, Jiahao Wen & Chunjiang Liu

  3. Natural Chemistry Research Group, Department of Chemistry, University of Turku, Turku, Finland

    Vladimir Ossipov

  4. Laboratory of Metabolomics, All-Russian Institute of Medicinal and Aromatic Plants, Moscow, Russia

    Vladimir Ossipov

  5. Key Laboratory of Urban Agriculture, Ministry of Agriculture, Beijing, China

    Chunjiang Liu

Authors
  1. Huawei Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vladimir Ossipov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baoming Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiahao Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunjiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C. Liu designed the study, H. Ji, B. Du and J. Wen collected field samples and data, H. Ji performed the experiments, and H. Ji, V. Ossipov and C. Liu analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Chunjiang Liu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: John Hammond.

Publisher’s note

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

Electronic supplementary material

ESM 1

(PDF 1336 kb)

ESM 2

(XLSX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ji, H., Ossipov, V., Du, B. et al. Differences in the relationship between metabolomic and ionomic traits of Quercus variabilis growing at contrasting geologic-phosphorus sites in subtropics. Plant Soil 439, 339–355 (2019). https://doi.org/10.1007/s11104-019-04020-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04020-1

Keywords

Search

Navigation