Ecological Research

, Volume 33, Issue 1, pp 261–269 | Cite as

Growth responses of Canada goldenrod (Solidago canadensis L.) to increased nitrogen supply correlate with bioavailability of insoluble phosphorus source

  • Ling-Yun Wan
  • Shan-Shan Qi
  • Zhi-Cong Dai
  • Chris B. Zou
  • Yi-Ge Song
  • Zhi-Yuan Hu
  • Bin Zhu
  • Dao-Lin Du
Original Article


Anthropogenic nitrogen (N) inputs lead to the increase of phosphorus (P) demand for plants and plant species competition in a N enriched environment may hinge on its ability to utilize soil P sources. In soils, P mostly exists as insoluble phosphate compounds with three mineral elements: iron (Fe), aluminum (Al) or calcium (Ca), and it remains largely unknown whether invasive plant species are able to access such insoluble P sources and its interaction with N enrichment to gain competitive advantage. We determined the morphological traits, growth and nutrient status of an invasive plant Canada goldenrod (Solidago canadensis L.) cultured in soluble phosphate KH2PO4 (Ortho-P), and insoluble inorganic phosphate AlPO4 (Al–P), FePO4 (Fe–P), Ca5(OH)(PO4)3 (Ca–P) at three N supply levels. Results showed that S. canadensis was able to selectively utilize P from Al–P but not from Fe–P or Ca–P by increasing root number and length under N additions. The increasing growth in S. canadensis was closely correlated with the increasing foliar P. Ability to utilize insoluble P sources under enriched N environment serves as a competitive advantage for S. canadensis in Al rich soils. Effective control of S. canadensis invasion may need to consider soil P management in the context of atmospheric N deposition as well.


Canada goldenrod (Solidago canadensis L.) Insoluble phosphorus Nitrogen addition Growth 



This work was supported by the State Key Research Development Program of China (2017YFC1200103). the National Natural Science Foundation of China (31570414, 31770446), the Natural Science Foundation of Jiangsu (BK20150503, BK20150504), the Research and Innovation Project for College Graduates of Jiangsu Province (KYLX15_1088, 15A316, 15A318), the China Postdoctoral Science Foundation (2016M590416, 2017T100329), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). This work was also supported by the USDA National Institute of Food and Agriculture through McIntire-Stennis project to C.B. Zou and the Division of Agricultural Sciences and Natural Resources at Oklahoma State University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Behera BC, Singdevsachan SK, Mishra RR, Dutta SK, Thatoi HN (2013) Diversity, mechanism and biotechnology of phosphate solubilising microorganism in mangrove—a review. Biocatal Agric Biotechnol 3:97–110. Google Scholar
  2. Bhadoria PS, Steingrobe B, Claassen N (2002) Phosphorus efficiency of wheat and sugar beet seedlings grown in soils with mainly calcium, or iron and aluminum phosphate. Plant Soil 246:41–52. CrossRefGoogle Scholar
  3. Brooks ML (2003) Effects of increased soil nitrogen on the dominance of alien annual plants in the Mojave Desert. J Appl Ecol 40:344–353. CrossRefGoogle Scholar
  4. Butcko VM, Jensen RJ (2009) Evidence of tissue-specific allelopathic activity in Euthamia graminifolia and Solidago canadensis (Asteraceae). Am Midl Nat 148: 253–262.[0253:eotsaa];2Google Scholar
  5. Dong M, Lu BR, Zhang HB, Chen JK, Li B (2006a) Role of sexual reproduction in the spread of an invasive clonal plant Solidago canadensis revealed using intersimple sequence repeat markers. Plant Spec Biol 21:13–18. CrossRefGoogle Scholar
  6. Dong M, Lu JZ, Zhang WJ, Chen JK, Li B (2006b) Canada goldenrod (Solidago canadensis): an invasive alien weed rapidly spreading in China. Acta Phytotaxon Sin 44:72–85 (In Chinese) CrossRefGoogle Scholar
  7. Elser JJ (2012) Phosphorus: a limiting nutrient for humanity? Curr Opin Biotechnol 23:833–838. CrossRefPubMedGoogle Scholar
  8. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Högberg P, Linder S, Mackenzie FT, Moore B III, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 290:291–296. CrossRefPubMedGoogle Scholar
  9. Foley JA, Defries R, Asner G, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574. CrossRefPubMedGoogle Scholar
  10. Fujita Y, Robroek BJM, de Ruiter PC, Heil GW, Wassen MJ (2010) Increased N affects P uptake of eight grassland species: the role of root surface phosphatase activity. Oikos 119:1665–1673. CrossRefGoogle Scholar
  11. Gahoonia TS, Claassen N, Jungk A (1992) Mobilization of phosphate in different soils by ryegrass supplied with ammonium or nitrate. Plant Soil 140:241–248. CrossRefGoogle Scholar
  12. Gress SE, Nichols TD, Northcraft CC, Peterjohn WT (2007) Nutrient limitation in soils exhibiting differing nitrogen availabilities: What lies beyond nitrogen saturation? Ecology 88:119–130.[119:nlised];2Google Scholar
  13. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Plant Ecol Evol Syst 5:37–61. CrossRefGoogle Scholar
  14. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195. CrossRefGoogle Scholar
  15. Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape. Plant Soil 113:155–160. CrossRefGoogle Scholar
  16. Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239. CrossRefGoogle Scholar
  17. Hu Y, Ye X, Shi L, Duan H, Xu F (2010) Genotypic differences in root morphology and phosphorus uptake kinetics in Brassica napus under low phosphorus supply. J Plant Nutr 33:889–901. CrossRefGoogle Scholar
  18. Huang WJ, Zhou GY, Liu JX (2012) Nitrogen and phosphorus status and their influence on aboveground production under increasing nitrogen deposition in three successional forests. Acta Oecol 44:20–27. CrossRefGoogle Scholar
  19. Jin L, Gu YJ, Xiao M, Chen JK, Li B (2004) The history of Solidago canadensis invasion and the development of its mycorrhizal associations in newly-reclaimed land. Funct Plant Biol 31:979–986. CrossRefGoogle Scholar
  20. 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. CrossRefGoogle Scholar
  21. Li B, Hsu PS, Chen JK (2001) Perspectives on general trends of plant invasions with special reference to alien weed flora of Shanghai. Chin Biodivers Sci 9:446–457 (In Chinese) Google Scholar
  22. Li H, Shen J, Zhang F, Marschner P, Cawthray G, Rengel Z (2010) Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil. Biol Fertil Soils 46:79–91. CrossRefGoogle Scholar
  23. Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462. CrossRefPubMedGoogle Scholar
  24. Lu JZ, Weng ES, Wu XW, Weber E, Zhao B, Li B (2007) Potential distribution of Solidago canadensis in China. Acta Phytotaxon Sin 45:670–674 (In Chinese) CrossRefGoogle Scholar
  25. Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R, Gojon A et al (2015) AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat Commun 27(6):6274. CrossRefGoogle Scholar
  27. Mohren GMJ, Vandenburg J, Burger FW (1986) Phosphorus deficiency induced by nitrogen input in Douglas-fir in the Netherlands. Plant Soil 95:191–200. CrossRefGoogle Scholar
  28. Otani T, Ae N (1996) Phosphorus (P) uptake mechanisms of crops grown in soils with low P status: I. Screening of crops for efficient P uptake. Soil Sci Plant Nutr 42:155–163. CrossRefGoogle Scholar
  29. Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MD, Lambers H (2006) Triticum aestivum shows a greater biomass response to a supply of aluminum phosphate than Lupinus albus despite releasing fewer carboxylates into the rhizosphere. New Phytol 169:515–524. CrossRefPubMedGoogle Scholar
  30. Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2007) Carboxylate composition of root exudates does not relate consistently to a crop species’ ability to use phosphorus from aluminum, iron or calcium phosphate sources. New Phytol 173:181–190. CrossRefGoogle Scholar
  31. Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2008) Rhizosphere processes do not explain variation in P acquisition from sparingly soluble forms among Lupinus albus accessions. Aust J Agric Res 59:616–623. CrossRefGoogle Scholar
  32. Perez Corona ME, Van der Klundert I, Verhoeven JTA (1996) Availability of organic and inorganic phosphorus compounds as phosphorus sources for Carex species. New Phytol 133:225–231. CrossRefGoogle Scholar
  33. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Physiol Plant Mol Biol 52:527–560. CrossRefGoogle Scholar
  34. Satyavir SS, Phour M, Choudhary SR, Chaudhary D (2014) Phosphorus cycling: prospects of using rhizosphere microorganisms for improving phosphorus nutrition of plants. Geomicrobiol Biogeochem 39:199–237. CrossRefGoogle Scholar
  35. Shen J, Rengel Z, Tang C, Zhang F (2003) Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus. Plant Soil 248:199–206. CrossRefGoogle Scholar
  36. Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Struthers PH, Sieling DH (1950) Effect of organic anions in phosphate precipitation by iron and aluminum as influenced by pH. Soil Sci 69:205–214CrossRefGoogle Scholar
  38. Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534. CrossRefGoogle Scholar
  39. Tomassen H, Smolders AJ, Limpens J, Lamers LP, Roelofs JG (2004) Expansion of invasive species on ombrotrophic bogs: desiccation or high N deposition? J Appl Ecol 41:139–150. CrossRefGoogle Scholar
  40. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115. CrossRefGoogle Scholar
  41. Wang X, Tang C, Guppy CN, Sale PWG (2010) Cotton, wheat and white lupin differ in phosphorus acquisition from sparingly soluble sources. Environ Exp Bot 69:267–272. CrossRefGoogle Scholar
  42. Wang X, Guppy CN, Watson L, Sale PWG, Tang C (2011) Availability of sparingly soluble phosphorus sources to cotton (Gossypium hirsutum L.), wheat (Triticum aestivum L.) and white lupin (Lupinus albus L.) with different forms of nitrogen as evaluated by a 32P isotopic dilution technique. Plant Soil 348:85–98. CrossRefGoogle Scholar
  43. Weand MP, Arthur MA, Lovett GM, Sikora F, Weathers KC (2010) The phosphorus status of northern hardwoods differs by species but is unaffected by nitrogen fertilization. Biogeochemistry 97:159–181. CrossRefGoogle Scholar
  44. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wissuwa M, Gamat G, Ismail AM (2005) Is root growth under phosphorus deficiency affected by source or sink limitations? J Exp Bot 56:1943–1950. CrossRefPubMedGoogle Scholar
  46. Yang RY, Mei LX, Tang JJ, Chen X, An M, Wu H, Pratley J (2007) Allelopathic effects of invasive Solidago canadensis L. on germination and growth of native Chinese plant species. Allelopathy J 19:241–248Google Scholar
  47. Yang RY, Zhou G, Zan ST, Guo FY, Su NN, Li J (2014) Arbuscular mycorrhizal fungi facilitate the invasion of Solidago canadensis L. in southeastern China. Acta Oecol 61:71–77 (In Chinese) CrossRefGoogle Scholar
  48. Zaidi A, Khan MS, Ahemad M, Oves M, Wani PA (2009) Recent advances in plant growth promotion by phosphate-solubilizing microbes. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer, Berlin, pp 23–50. CrossRefGoogle Scholar
  49. Zhang R, Zhou ZC, Luo WJ, Wang Y, Feng ZP (2013) Effects of nitrogen deposition on growth and phosphate efficiency of Schima superba of different provenances grown in phosphorus-barren soil. Plant Soil 370:435–445. CrossRefGoogle Scholar
  50. Zhao Q, Liu XY, Hu YL, Zeng DH (2010) Effects of nitrogen addition on nutrient allocation and nutrient resorption efficiency in Larix gmelinii. Sci Silvae Sin 46:14–19 (in Chinese) Google Scholar
  51. Zhao FJ, Ma Y, Zhu YG, Tang Z, Mcgrath SP (2015) Soil contamination in China: current status and mitigation strategies. Environ Sci Technol 49:750. CrossRefPubMedGoogle Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  • Ling-Yun Wan
    • 1
    • 3
  • Shan-Shan Qi
    • 1
  • Zhi-Cong Dai
    • 1
    • 2
  • Chris B. Zou
    • 3
    • 4
  • Yi-Ge Song
    • 1
  • Zhi-Yuan Hu
    • 1
  • Bin Zhu
    • 5
  • Dao-Lin Du
    • 1
    • 2
  1. 1.Institute of Environment and Ecology, Academy of Environmental Health and Ecological Security, School of the Environment and Safety EngineeringJiangsu UniversityZhenjiangChina
  2. 2.Institute of Agricultural EngineeringJiangsu UniversityZhenjiangChina
  3. 3.Department of Natural Resource Ecology and ManagementOklahoma State UniversityStillwaterUSA
  4. 4.Ecohydrology Research Institute, The University of Tokyo Forests, Graduate School of Agricultural and Life SciencesThe University of TokyoSetoJapan
  5. 5.Department of BiologyUniversity of HartfordWest HartfordUSA

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