Skip to main content
Log in

Nitrogen enrichment intensifies legume reliance on root phosphatase activity but weakens inter-specific correlations between N2 fixation and mycorrhizal colonization

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

Abstract

Aims

The relationships between nitrogen (N) and phosphorus (P) acquisition strategies among herbaceous legume species remain poorly understood, particularly in relation to how they are altered by N availability. This study aimed to investigate the relationships between N2 fixation, plant N concentration and P acquisition through two main strategies in temperate herbaceous legumes, and to demonstrate the influences of soil N availability on these relationships.

Methods

In a field pot experiment, eight temperate herbaceous legumes were grown with or without N addition. Plant growth, plant N and P concentrations, N2 fixation, arbuscular mycorrhizal (AM) fungal colonization and root phosphatase activity (RPA) were measured, and the relationships between N2 fixation, plant N concentration and each P acquisition strategy were assessed under contrasting N availability.

Results

N addition increased RPA. However, AM fungal colonization showed species-specific responses to N addition, and the ratio of AM fungal colonization to root phosphatase activity was decreased by N addition. Among eight legume species, AM fungal colonization increased with N2 fixation rate in the absence of N addition, but no relationship was observed with N addition. RPA increased with plant N concentration among legume species, regardless of N addition.

Conclusions

As two key P acquisition strategies, neither RPA nor AM fungal colonization of temperate herbaceous legumes were species-specific traits, since both were positively correlated with N2 fixation rate and plant N concentration. In addition, the correlation between N2 fixation and AM fungal colonization was regulated by N availability. While N enrichment intensifies the legume reliance on RPA for acquiring more P, it weakens the association of N2 fixation in driving across species AM colonization.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams MA, Turnbull TL, Sprent JI, Buchmann N (2016) Legumes are different: leaf nitrogen, photosynthesis, and water use efficiency. Proc Natl Acad Sci U S A 113:4098–4103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Augusto L, Delerue F, Gallet-Budynek A, Achat DL (2013) Global assessment of limitation to symbiotic nitrogen fixation by phosphorus availability in terrestrial ecosystems using a meta-analysis approach. Glob Biogeochem Cycles 27:804–815

    Article  CAS  Google Scholar 

  • Barron AR, Purves DW, Hedin LO (2011) Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165:511–520

    Article  PubMed  Google Scholar 

  • Batterman SA, Hall JS, Turner BL, Hedin LO, Walter JKL, Sheldon P, Breugel MV (2018) Phosphatase activity and nitrogen fixation reflect species differences, not nutrient trading or nutrient balance, across tropical rainforest trees. Ecol Lett 21:1486–1495

    Article  PubMed  Google Scholar 

  • Batterman SA, Wurzburger N, Hedin LO (2013) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J Ecol 101:1400–1408

    Article  CAS  Google Scholar 

  • Denton MD, Veneklaas EJ, Freimoser FM, Lambers H (2007) Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilisation of phosphorus. Plant Cell Environ 30:1557–1565

    Article  CAS  PubMed  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  PubMed  Google Scholar 

  • Fisher JB, Sitch S, Malhi Y, Huntingford C, Tan SY (2010) Carbon cost of plant nitrogen acquisition: a mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation. Glob Biogeochem Cycles 24:GB1014

    Article  CAS  Google Scholar 

  • Guilbeault-Mayers X, Turner BL, Laliberté E (2020) Greater root phosphatase activity of tropical trees at low phosphorus despite strong variation among species. Ecology:e03090

  • Hedin LO, Brookshire ENJ, Menge DNL, Barron AR (2009) The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Evol S 40:613–635

    Article  Google Scholar 

  • Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB (2003) Nitrogen enrichment alters mycorrhizal allocation at five Mesic to semiarid grasslands. Ecology 84:1895–1908

    Article  Google Scholar 

  • Kafle A, Garcia K, Wang XR, Pfeffer PE, Strahan GD, Bücking H (2019) Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula. Plant Cell Environ 42:270–284

    Article  CAS  PubMed  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    Article  PubMed  Google Scholar 

  • Li Q, Song YT, Li GD, Yu PJ, Wang P, Zhou DW (2015) Grass-legume mixtures impact soil N, species recruitment, and productivity in temperate steppe grassland. Plant Soil 394:271–285

    Article  CAS  Google Scholar 

  • Li Q, Yu PJ, Li GD, Zhou DW (2016) Grass-legume ratio can change soil carbon and nitrogen storage in a temperate steppe grassland. Soil Till Res 157:23–31

    Article  Google Scholar 

  • Liang X, Zhang T, Lu X, Ellsworth DS, BassiriRad H, You CM, Wang D, He PC, Deng Q, Liu H, Mo JM, Ye Q (2020) Global response patterns of plant photosynthesis to nitrogen addition: a meta-analysis. Glob Chang Biol 26:3585–3600

    Article  PubMed  Google Scholar 

  • Lu Y, Liu X, Chen F, Zhou SR (2020) Shifts in plant community composition weaken the negative effect of nitrogen addition on community-level arbuscular mycorrhizal fungi colonization. P Roy Soc B: Biol Sci 287:20200483

    CAS  Google Scholar 

  • Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704

    Article  CAS  PubMed  Google Scholar 

  • McKey D (1994) Legumes and nitrogen-the evolutionary ecology of a nitrogen demanding lifestyle. In: Sprent JI, McKey D (eds) Advances in legume systematics, part 5: the nitrogen factor. Kew, UK, Royal Botanic Gardens, pp 211–228

    Google Scholar 

  • Montesinos-Navarro A, Segarra-Moragues JG, Valiente-Banuet A, Verdú M (2012) The network structure of plant-arbuscular mycorrhizal fungi. New Phytol 194:536–547

    Article  CAS  PubMed  Google Scholar 

  • Nasto MK, Alvarez-Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC (2014) Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol Lett 17:1282–1289

    Article  PubMed  Google Scholar 

  • Nasto MK, Osborne BB, Lekberg Y, Asner GP, Balzotti CS, Porder S, Taylor PG, Townsend AR, Cleveland CC (2017) Nutrient acquisition, soil phosphorus partitioning and competition among trees in a lowland tropical rain forest. New Phytol 214:1506–1517

    Article  CAS  PubMed  Google Scholar 

  • Nasto MK, Winter K, Turner BL, Cleveland CC (2019) Nutrient acquisition strategies augment growth in tropical N2-fixing trees in nutrient-poor soil and under elevated CO2. Ecology 100:e02646

    Article  PubMed  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochem 49:175–190

    Article  CAS  Google Scholar 

  • Olde Venterink H (2011) Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply. Plant Soil 347:137–146

    Article  CAS  Google Scholar 

  • Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263

    Article  CAS  PubMed  Google Scholar 

  • Page AL (1982) Methods of soil analysis, part 2. Chemical and Microbiological Properties. American Society of Agronomy, Soil Science Society of America, Masison, WI

  • Pang J, Ruchi B, Zhao R, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KHM (2018) The carboxylate-releasing phosphorus-mobilising strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529

    Article  CAS  PubMed  Google Scholar 

  • Png GK, Turner BL, Albornoz FE, Hayes PE, Lambers H, Laliberté E (2017) Greater root phosphatase activity in nitrogen-fixing rhizobial but not actinorhizal plants with declining phosphorus availability. J Ecol 105:1246–1255

    Article  CAS  Google Scholar 

  • Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2007) Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant Soil 296:65–75

    Article  CAS  Google Scholar 

  • Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J (2017) Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp through improved phosphorus acquisition. Front Plant Sci 8:390

    Article  PubMed  PubMed Central  Google Scholar 

  • Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101

    Article  Google Scholar 

  • Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London, UK

    Google Scholar 

  • Soper FM, Nasto MK, Osborne BB, Cleveland CC (2019) Nitrogen fixation and foliar nitrogen do not predict phosphorus acquisition strategies in tropical trees. J Ecol 107:118–126

    Article  CAS  Google Scholar 

  • Sparks DL, Page A, Helmke P, Loeppert R, Soltanpour P, Tabatabai M, Johnston C, Sumner M (1996) Methods of soil analysis. Part 3-chemical methods. Soil science Society of America, Masison, WI

  • Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879

    Article  CAS  PubMed  Google Scholar 

  • Sulieman S, Tran LSP (2015) Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci 239:36–43

    Article  CAS  PubMed  Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Article  PubMed  Google Scholar 

  • Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:1–9

    Article  Google Scholar 

  • Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370

    Article  CAS  PubMed  Google Scholar 

  • Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. Australian Centre for International Agricultural Research (ACIAR)

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750

    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 

  • Wen Z, Li H, Shen Q, Tang XM, Xiong CY, Li HG, Pang JY, Ryan MH, Lambers H, Shen JB (2019) Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol 223:882–895

    Article  CAS  PubMed  Google Scholar 

  • West JB, HilleRisLambers J, Lee TD, Hobbie SE, Reich PB (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530

    Article  CAS  PubMed  Google Scholar 

  • Wolf AA, Funk JL, Menge DN (2017) The symbionts made me do it: legumes are not hardwired for high nitrogen concentrations but incorporate more nitrogen when inoculated. New Phytol 213:690–699

    Article  CAS  PubMed  Google Scholar 

  • Wu N, Li Z, Liu H, Tang M (2015) Influence of arbuscular mycorrhiza on photosynthesis and water status of Populus cathayana Rehder males and females under salt stress. Acta Physiol Plant 37:183

    Article  CAS  Google Scholar 

  • Wurzburger N, Hedin LO (2015) Taxonomic identity determines N2 fixation by canopy trees across lowland forests. Ecol Lett 19:62–70

    Article  PubMed  Google Scholar 

  • Zhan S, Wang Y, Zhu Z, Li W, Bai Y (2017) Nitrogen enrichment alters plant N: P stoichiometry and intensifies phosphorus limitation in a steppe ecosystem. Environ Exp Bot 134:21–32

    Article  CAS  Google Scholar 

  • Zheng M, Zhou Z, Luo Y, Zhao P, Mo J (2019) Global pattern and controls of biological nitrogen fixation under nutrient enrichment: a meta-analysis. Glob Change Biol 25:3018–3030

    Article  Google Scholar 

  • Zheng Y, Kim YC, Tian XF, Chen L, Yang W, Gao C, Song MH, Xu XL, Guo LD (2014) Differential responses of arbuscular mycorrhizal fungi to nitrogen addition in a near pristine Tibetan alpine meadow. FEMS Microbiol Ecol 89:594–605

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by Strategic Science and Technology Guide Project of CAS (XDA23060403) and National Key Research and Development Program of China (2016YFC0500606) and Natural Science Foundation of China (31600318) and Jilin Province Science and Technology Development Plan (20190303066SF) and The grant of Youth Innovation Promotion Association of CAS (2016210).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Qiang Li, Matthew D. Denton or Yingxin Huang.

Additional information

Responsible Editor: Maarja Öpik.

Publisher’s note

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

Supplementary Information

Supplementary data consist of the following. Table S1: Available nitrogen (NH4++NO3) and available P concentrations and available N:P ratio in bulk soil.

ESM 1

(DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Q., Denton, M.D., Huang, Y. et al. Nitrogen enrichment intensifies legume reliance on root phosphatase activity but weakens inter-specific correlations between N2 fixation and mycorrhizal colonization. Plant Soil 465, 503–514 (2021). https://doi.org/10.1007/s11104-021-04989-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-04989-8

Keywords

Navigation