Soybean (Glycine max (L.) Merrill) intercropping with reduced nitrogen input influences rhizosphere phosphorus dynamics and phosphorus acquisition of sugarcane (Saccharum officinarum)

Abstract

Reducing nitrogen (N) input can improve crop productivity in cereal-legume intercrops, but the impact on phosphorus (P) acquisition is unclear. A 10-year (2009–2018) field experiment was conducted to quantify how P acquisition by sugarcane (Saccharum officinarum) was affected by intercropping with soybean (Glycine max (L.) Merrill at 1:1 and 1:2) with two N inputs (300 kg ha−1 [reduced], 525 kg ha−1 [conventional]). Nitrogen was supplied only to the sugarcane crop, and soybean received no N. There was a significantly higher land-equivalent ratio of sugarcane-soybean intercropping than of the sole cropping, and the intercropping advantage was more pronounced under reduced N input which can be associated with high degree of complementary N use. Furthermore, soybean intercropping with reduced N input stimulated acid phosphomonoesterase activity and depleted organic P in the rhizosphere of sugarcane, resulting in increased sugarcane stem P concentration and system P-use efficiency. The interspecific facilitation of P acquisition could be associated with the increased symbiotic N2 fixation in soybean, soil microbial biomass and activity under reduced N input. In conclusion, soybean intercropping with reduced N input to sugarcane enhanced rhizosphere enzymatic organic P transformation and sugarcane P acquisition, which may contribute to maintaining a sustainable sugarcane production under low N supply. The findings advance our understanding of interactions between N and P cycling and provide new evidence for the value of cereal-legume intercrops in reducing fertilizer input.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Bedoussac L, Justes E (2010) The efficiency of a durum wheat-winter pea intercrop to improve yield and wheat grain protein concentration depends on N availability during early growth. Plant Soil 330:19–35

    CAS  Google Scholar 

  2. Bedoussac L, Journet E-P, Hauggaard-Nielsen H, Naudin C, Corre-Hellou G, Jensen ES, Prieur L, Justes E (2015) Ecological principles underlying the increase of productivity achieved by cereal-grain legume intercrops in organic farming. A review. Agron Sustain Dev 35:911–935

    Google Scholar 

  3. Chen CR, Condron LM, Davis MR, Sherlock RR (2000) Effects of afforestation on phosphorus dynamics and biological properties in a New Zealand grassland soil. Plant Soil 220:151–163

    CAS  Google Scholar 

  4. Chen J, Arafat Y, Wu L, Xiao Z, Li Q, Khan MA, Khan MU, Lin S, Lin W (2018) Shifts in soil microbial community, soil enzymes and crop yield under peanut/maize intercropping with reduced nitrogen levels. Appl Soil Ecol 124:327–334

    Google Scholar 

  5. Condron LM, Newman S (2011) Revisiting the fundamentals of phosphorus fractionation of sediments and soils. J Soils Sediment 11:830–840

    CAS  Google Scholar 

  6. Condron LM, Tiessen H (2005) Interactions of organic phosphorus in terrestrial ecosystems. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CAB International, Wallingford, UK, pp 295–308

    Google Scholar 

  7. Cu STT, Hutson J, Schuller KA (2005) Mixed culture of wheat (Triticum aestivum L.) with white lupiu (Lupinus albus L.) improves the growth and phosphorus nutrition of the wheat. Plant Soil 272:143–151

    CAS  Google Scholar 

  8. Dai Z, Liu G, Chen H, Chen C, Wang J, Ai S, Wei D, Li D, Ma B, Tang C, Brookes PC, Xu J (2020) Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. ISME J 14:757–770

    CAS  PubMed  Google Scholar 

  9. Dissanayaka DMSB, Maruyama H, Masuda G, Wasaki J (2015) Interspecific facilitation of P acquisition in intercropping of maize with white lupin in two contrasting soils as influenced by different rates and forms of P supply. Plant Soil 390:223–236

    CAS  Google Scholar 

  10. Fan F, Zhang F, Song Y, Sun J, Bao X, Guo T, Li L (2006) Nitrogen fixation of faba bean (Vicia faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant Soil 283:275–286

    CAS  Google Scholar 

  11. Fraser TD, Lynch DH, Gaiero J, Khosla K, Dunfield KE (2017) Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Appl Soil Ecol 111:48–56

    Google Scholar 

  12. Garside A, Bell M, Singh V (1999) The potential for legumes in sugarcane cropping systems in Australia. Proc Aust Soc Sug Cane Technol, pp:100–106

  13. George TS, Turner BL, Gregory PJ, Cade-Menun BJ, Richardson AE (2006) Depletion of organic phosphorus from Oxisols in relation to phosphatase activities in the rhizosphere. Eur J Soil Sci 57:47–57

    CAS  Google Scholar 

  14. Gopalasundaram P, Bhaskaran A, Rakkiyappan P (2012) Integrated nutrient management in sugarcane. Sugar Tech 14:3–20

    CAS  Google Scholar 

  15. 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

    CAS  Google Scholar 

  16. Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156:1078–1086

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  18. Houngnandan P, Yemadje RGH, Oikeh SO, Djidohokpin CF, Boeckx P, Van Cleemput O (2008) Improved estimation of biological nitrogen fixation of soybean cultivars (Glycine max L. Merril) using 15N natural abundance technique. Biol Fert Soils 45:175–183

    CAS  Google Scholar 

  19. Inal A, Gunes A, Zhang F, Cakmak I (2007) Peanut/maize intercropping induced changes in rhizosphere and nutrient concentrations in shoots. Plant Physiol Bioch 45:350–356

    CAS  Google Scholar 

  20. Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEC value. Soil Biol Biochem 28:25–31

    CAS  Google Scholar 

  21. Kermah M, Franke AC, Adjei-Nsiah S, Ahiabor BDK, Abaidoo RC, Giller KE (2017) Maize-grain legume intercropping for enhanced resource use efficiency and crop productivity in the Guinea savanna of northern Ghana. Field Crop Res 213:38–50

    Google Scholar 

  22. Kuo S (1996) Phosphorus. In: Sparks, D.L. (Ed.), methods of soil analysis. Part 3: Chemical Methods. Soil Science Society of America, American Society of Agronomy, Madison, WI, pp. 869-919

  23. Li SM, Li L, Zhang FS, Tang C (2004) Acid phosphatase role in chickpea/maize intercropping. Ann Bot 94:297–303

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Li L, Li S-M, Sun J-H, Zhou L-L, Bao X-G, Zhang H-G, Zhang F-S (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. P Natl Acad Sci USA 104:11192–11196

    CAS  Google Scholar 

  25. Li X, Mu Y, Cheng Y, Liu X, Nian H (2013) Effects of intercropping sugarcane and soybean on growth, rhizosphere soil microbes, nitrogen and phosphorus availability. Acta Physiol Plant 35:1113–1119

    CAS  Google Scholar 

  26. Lian T, Mu Y, Jin J, Ma Q, Cheng Y, Cai Z, Nian H (2019) Impact of intercropping on the coupling between soil microbial community structure, activity, and nutrient-use efficiencies. Peerj 7:e6412

    PubMed  PubMed Central  Google Scholar 

  27. Luo S, Yu L, Liu Y, Zhang Y, Yang W, Li Z, Wang J (2016) Effects of reduced nitrogen input on productivity and N2O emissions in a sugarcane/soybean intercropping system. Eur J Agron 81:78–85

    Google Scholar 

  28. Nannipieri P, Johnson RL, Paul EA (1978) Criteria for measurement of microbial growth and activity in soil. Soil Biol Biochem 10:223–229

    CAS  Google Scholar 

  29. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action, Soil biology, vol 26. Springer Verlag, Berlin, pp 215–241

    Google Scholar 

  30. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fert Soils 54:11–19

  31. Oberson A, Besson JM, Maire N, Sticher H (1996) Microbiological processes in soil organic phosphorus transformations in conventional and biological cropping systems. Biol Fert Soils 21:138–148

    CAS  Google Scholar 

  32. 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

    CAS  Google Scholar 

  33. 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

    CAS  Google Scholar 

  34. Ramouthar PV, Rhodes R, Wettergreen T, Pillay U, Jones MR, Van Antwerpen R, Berry SD (2014) Intercropping in sugarcane a practice worth pursuing? Int Sugar J 116:46–53

    Google Scholar 

  35. Rao MR, Willey RW (1980) Evaluation of yield stability in intercropping: studies on sorghum/pigeonpea. Exp Agr 16:105–116

    Google Scholar 

  36. Santachiara G, Salvagiotti F, Rotundo JL (2019) Nutritional and environmental effects on biological nitrogen fixation in soybean: a meta-analysis. Field Crop Res 240:106–115

    Google Scholar 

  37. Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120

    CAS  Google Scholar 

  38. Solanki MK, Wang F-Y, Wang Z, Li C-N, Lan T-J, Singh RK, Singh P, Yang L-T, Li Y-R (2019) Rhizospheric and endospheric diazotrophs mediated soil fertility intensification in sugarcane-legume intercropping systems. J Soils Sediment 19:1911–1927

    CAS  Google Scholar 

  39. Streeter J, Wong PP (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23

    CAS  Google Scholar 

  40. Tabatabai MA (1994) Soil Enzymes. In: Bottomley PS, Angle JS, Weaver RW (eds) Methods of Soil Analysis: Part 2—Microbiological and Biochemical Properties. Soil Science Society of America, Madison, WI, pp 775–833

    Google Scholar 

  41. Tarafdar JC, Jungk A (1987) Phosphatase activity in the rhizosphere and its relation to the depletion of soil organic phosphorus. Biol Fert Soils 3:199–204

    CAS  Google Scholar 

  42. Tian J, Boitt G, Black A, Wakelin S, Condron LM, Chen L (2017) Accumulation and distribution of phosphorus in the soil profile under fertilized grazed pasture. Agric Ecosyst Environ 239:228–235

    CAS  Google Scholar 

  43. Wang X, Deng X, Pu T, Song C, Yong T, Yang F, Sun X, Liu W, Yan Y, Du J, Liu J, Su K, Yang W (2017) Contribution of interspecific interactions and phosphorus application to increasing soil phosphorus availability in relay intercropping systems. Field Crop Res 204:12–22

    Google Scholar 

  44. Willey RW, Rao MR (1980) A competitive ratio for quantifying competition between intercrops. Exp Agr 16:117–125

    Google Scholar 

  45. Zhou J, Guan D, Zhou B, Zhao B, Ma M, Qin J, Jiang X, Chen S, Cao F, Shen D, Li J (2015) Influence of 34-years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China. Soil Biol Biochem 90:42–51

Download references

Acknowledgments

We thank Dr. Jiang Tian, professor of South China Agricultural University, for valuable comments and suggestions to improve the original manuscript.

Funding

This study was financially supported by the Integrated Demonstration of Key Techniques for the Industrial Development of Featured Crops in Rocky Desertification Areas of Yunnan–Guangxi–Guizhou Provinces (SMH2019-2021), the National Natural Science Foundation of China (41807084), the Natural Science Foundation of Guangdong Province, China (2018A030310214), and the Science and Technology Project of Guangdong Province, China (2019B030301007).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jianwu Wang.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 1103 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tian, J., Tang, M., Xu, X. et al. Soybean (Glycine max (L.) Merrill) intercropping with reduced nitrogen input influences rhizosphere phosphorus dynamics and phosphorus acquisition of sugarcane (Saccharum officinarum). Biol Fertil Soils (2020). https://doi.org/10.1007/s00374-020-01484-7

Download citation

Keywords

  • Cereal-legume intercrop
  • Phosphorus fractionation
  • Acid phosphomonoesterase
  • Phosphorus-use efficiency
  • Low nitrogen application