Abstract
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.
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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. https://doi.org/10.1016/j.bcab.2013.09.008
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. https://doi.org/10.1023/A:1021567331637
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. https://doi.org/10.1046/j.1365-2664.2003.00789.x
Butcko VM, Jensen RJ (2009) Evidence of tissue-specific allelopathic activity in Euthamia graminifolia and Solidago canadensis (Asteraceae). Am Midl Nat 148: 253–262. https://doi.org/10.1674/0003-0031(2002)148[0253:eotsaa]2.0.co;2
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. https://doi.org/10.1111/j.1442-1984.2006.00146.x
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)
Elser JJ (2012) Phosphorus: a limiting nutrient for humanity? Curr Opin Biotechnol 23:833–838. https://doi.org/10.1016/j.copbio.2012.03.001
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. https://doi.org/10.1126/science.290.5490.291
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. https://doi.org/10.1126/science.1111772
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. https://doi.org/10.1111/j.1600-0706.2010.18427.x
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. https://doi.org/10.1007/BF00010600
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. https://doi.org/10.1890/0012-9658(2007)88[119:nlised]2.0.co;2
Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Plant Ecol Evol Syst 5:37–61. https://doi.org/10.1078/1433-8319-0000022
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. https://doi.org/10.1023/A:1013351617532
Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape. Plant Soil 113:155–160. https://doi.org/10.1007/BF02280175
Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239. https://doi.org/10.1071/S96047
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. https://doi.org/10.1080/01904161003658239
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. https://doi.org/10.1016/j.actao.2011.06.005
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. https://doi.org/10.1071/FP04061
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. https://doi.org/10.2307/2404783
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)
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. https://doi.org/10.1007/s00374-009-0411-x
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. https://doi.org/10.1038/nature11917
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)
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. https://doi.org/10.1104/pp.111.175414
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. https://doi.org/10.1038/ncomms7274
Mohren GMJ, Vandenburg J, Burger FW (1986) Phosphorus deficiency induced by nitrogen input in Douglas-fir in the Netherlands. Plant Soil 95:191–200. https://doi.org/10.1007/BF02375071
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. https://doi.org/10.1080/00380768.1996.10414699
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. https://doi.org/10.1111/j.1469-8137.2005.01614.x
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. https://doi.org/10.1111/j.1469-8137.2006.01897.x
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. https://doi.org/10.1071/AR07404
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. https://doi.org/10.1111/j.1469-8137.1996.tb01889.x
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. https://doi.org/10.1146/annurev.arplant.52.1.527
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. https://doi.org/10.1007/978-3-642-41837-2_11
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. https://doi.org/10.1023/A:1022375229625
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. https://doi.org/10.1104/pp.111.174581
Struthers PH, Sieling DH (1950) Effect of organic anions in phosphate precipitation by iron and aluminum as influenced by pH. Soil Sci 69:205–214
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. https://doi.org/10.1046/j.1365-2664.2003.00820.x
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. https://doi.org/10.1111/j.1365-2664.2004.00870.x
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115. https://doi.org/10.1007/BF00002772
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. https://doi.org/10.1016/j.envexpbot.2010.04.007
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. https://doi.org/10.1007/s11104-011-0901-0
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. https://doi.org/10.1007/s10533-009-9364-2
Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882. https://doi.org/10.1104/pp.126.2.875
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. https://doi.org/10.1093/jxb/eri189
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 19:241–248
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)
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. https://doi.org/10.1007/978-3-642-01979-1_2
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. https://doi.org/10.1007/s11104-013-1644-x
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)
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. https://doi.org/10.1021/es5047099
Acknowledgements
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.
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Wan, LY., Qi, SS., Dai, ZC. et al. Growth responses of Canada goldenrod (Solidago canadensis L.) to increased nitrogen supply correlate with bioavailability of insoluble phosphorus source. Ecol Res 33, 261–269 (2018). https://doi.org/10.1007/s11284-017-1552-2
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DOI: https://doi.org/10.1007/s11284-017-1552-2