Skip to main content

Advertisement

Log in

Effect of root exudates on beneficial microorganisms—evidence from a continuous soybean monoculture

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Soybean (Glycine max) agriculture is characterized by a high proportion of mono-cropping which results in reduced crop production in the Northeast China. Among all biotic and abiotic factors, changes in soil microbial communities induced by root activities, especially root exudates, might play an important role in these effects. The aim of the present study was to investigate response of microbial biomass and two major beneficial microbial functional groups, ammonia-oxidizing bacteria (AOB), and arbuscular mycorrhizal fungi (AMF), to root exudates in an experimental field under continuous soybean monoculture for 13 years. The results showed that microbial biomass carbon changed significantly with years of mono-cropping and correlated with concentrations of genistein (r = 0.4399, P < 0.001) and daidzein (r = 0.4082, P < 0.05) in the rhizosphere. However, root exudates had little effect on the nitrifier community, but reduced nitrification in the rhizosphere. In contrast, total AMF hyphal length was significantly stimulated by genistein (r = 0.5252, P < 0.01). There was a trend that AMF spore density increased in the rhizosphere with increasing years of mono-cropping, while AMF infection was constant over time, which might be attributed to competition between AMF and soil-borne fungal pathogens, as the results of stimulatory effect of flavonoids on fungal community, especially fungal pathogens. Our results suggested that the yield reduction in the beginning of continuous soybean monoculture could be partially attributed to nitrogen availability and yield stabilization after few years to stimulatory effects on AMF. These results imply that some of plant root exudates play a crucial role in changing the soil microbial community, and that underground ecosystem functioning is also affected by interactions among microbial functional groups.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816

    Article  PubMed  CAS  Google Scholar 

  • Avrahami S, Bohannan BJM (2007) Response of Nitrosospira sp. strain AF-like ammonia oxidizers to changes in temperature, soil moisture content, and fertilizer concentration. Appl Environ Microbiol 73:1166–1173

    Article  PubMed  CAS  Google Scholar 

  • Bever JD (2002) Host-specificity of AM fungal population growth rates can generate feedback on growth. Plant Soil 244:281–290

    Article  CAS  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473

    Article  Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  PubMed  CAS  Google Scholar 

  • Bünemann EK, Steinebrunner F, Smithson PC, Frossard E, Oberson A (2004) Phosphorus dynamics in a highly weathered soil as revealed by isotopic labeling techniques. Soil Sci Soc Am J 68:1645–1655

    Article  Google Scholar 

  • Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1–25

    Article  CAS  Google Scholar 

  • Chen HY, Li XM, Wang JG (2005) Changes of microflora in the rhizoplane and rhizosphere of different disease soybean cultivar. I. Changes of microflora in the rhizoplane and rhizosphere of soybean under normal rotation condition (In Chinese). Plant Nutr Fert Sci 11:804–809

    Google Scholar 

  • Chen HY, Li XM, Wang JG (2006) Changes of microflora in the rhizoplane and rhizosphere of different disease soybean cultivar. II. Changes of microflora in the rhizoplane and rhizosphere of soybean under continuous cropping condition (In Chinese). Plant Nutr Fert Sci 12:104–108

    Google Scholar 

  • Colpas FT, Ono EO, Rodrigues JD, de Souza Passos JR (2003) Effects of some phenolic compounds on soybean seed germination and on seed-borne fungi. Braz Arch Biol Technol 46:155–161

    Article  CAS  Google Scholar 

  • Daniels BA, Skipper HD (1982) Methods for the recovery and quantitative estimation of propagules from soil. In: Schenck NC (ed) Methods and principles of mycorrhizal research. American Phytopathological Society, St. Paul, pp 29–35

    Google Scholar 

  • de la Peña E, Echeverría SR, van der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840

    Article  PubMed  Google Scholar 

  • Franche C, Lindstrom K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59

    Article  CAS  Google Scholar 

  • Ge Y, Zhang JB, Zhang LM, Yang M, He JZ (2008) Long-term fertilization regimes affect bacterial community structure and diversity of an agricultural soil in Northern China. J Soil Sediment 8:43–50

    Article  CAS  Google Scholar 

  • Gil SV, Meriles JM, Haro R, Casini C, March GJ (2008) Crop rotation and tillage systems as a proactive strategy in the control of peanut fungal soilborne diseases. Biocontrol 53:685–698

    Article  Google Scholar 

  • Guo ZY, Kong CH, Wang JG, Wang YF (2011) Rhizosphere isoflavones (daidzein and genistein) levels and their relation to the microbial community structure of mono-cropped soybean soil in field and controlled conditions. Soil Biol Biochem 43:2242–2257

    Article  Google Scholar 

  • Han LM, Shen QR, Ju HY, Yan S, Yan F (2002) Allelopathy of the aqueous extracts of above ground parts of soybean and the identification of the allelochemicals (In Chinese). Acta Ecol Sin 22:1425–1432

    Google Scholar 

  • Hu JC, Xue DL, Wang SJ (1998) Obstacles of soybean continuous cropping II: mechanism of soybean yield decline and control strategies for toxin of Penicillium purouregenum in soils (In Chinese). Chin J Appl Ecol 9:429–434

    Google Scholar 

  • Jansa J, Mozafar A, Anken T, Voulgari OK, Mamolos AP, Alifragis DA, Veresoglou DS (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234

    Article  PubMed  CAS  Google Scholar 

  • Jia ZJ, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  PubMed  CAS  Google Scholar 

  • Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992

    Article  PubMed  Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115

    Article  CAS  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2005) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  Google Scholar 

  • Li CG, Li XM, Kong WD, Wu Y, Wang JG (2010) Effect of monoculture soybean on soil microbial community in the Northeast China. Plant Soil 330:423–433

    Article  CAS  Google Scholar 

  • Lin QM, Wu YG, Liu HL (1999) Modification of fumigation extraction methods for measuring soil microbial biomass carbon (In Chinese). Chin J Ecol 18:63–66

    Google Scholar 

  • Liu XB, Herbert SJ (2002) Fifteen years of research examining cultivation of continuous soybean in Northeast China: a review. Field Crops Res 79:1–7

    Article  Google Scholar 

  • Majumdar D, Dutta A, Kumar S, Pathak H, Jain MC (2001) Mitigation of N2O emission from an alluvial soil by application of karanjin. Biol Fert Soil 33:438–442

    Article  CAS  Google Scholar 

  • Masamune T, Anetai M, Takasugi M, Katsui N (1982) Isolation of a natural hatching stimulus, glycinoeclepin A, for the soybean cyst nematode. Nature 297:495–496

    Article  CAS  Google Scholar 

  • Michelson A, Rosendahl S (1990) The effect of VA mycorrhizal fungi, phosphorus and drought stress on the growth of Acacia nilotica and Leucaena leucocephala seedlings. Plant Soil 124:7–13

    Article  Google Scholar 

  • Miller MH, McGonigle TP, Addy HD (1995) Functional ecology of vesicular-arbuscular mycorrhizas as influenced by phosphate fertilization and tillage in an agricultural ecosystem. Crit Rev Biotechnol 15:241–255

    Article  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mader P, Boller T, Wiemken A (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microbiol 69:2816–2824

    Article  PubMed  CAS  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mader P, Boller T, Wiemken A, Dubois D (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583

    Article  PubMed  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Ris EA, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283

    Article  PubMed  Google Scholar 

  • Pankhurst CE, Ophel-Keller K, Doube BM, Gupta VVSR (1996) Biodiversity of soil microbial communities in agricultural systems. Biodiv Conserv 5:197–209

    Article  Google Scholar 

  • Qu XH, Wang JG (2008) Effect of amendments with different phenolic acids on soil microbial biomass, activity, and community diversity. Appl Soil Ecol 39:172–179

    Article  Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    PubMed  CAS  Google Scholar 

  • Ruan WB, Wang JG, Zhang FS (2003) The effect of continuous cropping factors on soybean seedling growth and nitrogen fixation (In Chinese). Acta Ecol Sin 23:22–29

    Google Scholar 

  • Sieverding E (1990) Ecology of VAM fungi in tropical agrosystems. Agri Ecosyst Environ 29:369–390

    Article  Google Scholar 

  • Skiba MW, George TS, Baggs EM, Daniell TJ (2011) Plant influence on nitrification. Biochem Soc Trans 39:851–856

    Article  Google Scholar 

  • Smithson PC, Giller KE (2002) Appropriate farm management practices for alleviating N and P deficiencies in low-nutrient soils of the tropics. Plant Soil 245:169–180

    Article  CAS  Google Scholar 

  • Smits NAC, Bobbink R, Laanbroek HJ, Paalman AJ, Hefting MM (2011) Repression of potential nitrification activities by matgrass sward species. Plant Soil 337:435–445

    Article  Google Scholar 

  • Song YN, Zhang FS, Marschner P, Fan FL, Gao HM, Bao XG, Sun JH, Li L (2007) Effect of intercropping on crop yield and chemical and microbiological properties in rhizosphere of wheat (Triticum aestivum L.), maize (Zea mays L.), and faba bean (Vicia faba L.). Biol Fert Soils 43:565–574

    Article  CAS  Google Scholar 

  • Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Molecules, flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306

    Article  PubMed  CAS  Google Scholar 

  • Suarez-Ojeda ME, Guisasola A, Carrera J (2010) Inhibitory impact of quinone-like compounds over partial nitrification. Chemosphere 80:474–480

    Article  PubMed  CAS  Google Scholar 

  • Subbarao GV, Nakahara K, Hurtado MP, Ono H, Moreta DE, Salcedo AF, Yoshihashi AT, Ishikawa T, Ishitani M, Ohnishi-Kameyama M, Yoshida M, Rondon M, Rao IM, Lascano CE, Berry WL, Ito O (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. Proc Natl Acad Sci USA 106:17302–17307

    Article  PubMed  CAS  Google Scholar 

  • Tanaka JP, Nardi P, Wissuwa M (2011) Nitrification inhibition activity, a novel trait in root exudates of rice. AoB plants plq014. doi: 10.1093/aobpla/plq014

  • Taylor AE, Zeglin LH, Dooley S, Myrold DD, Bottomley PJ (2010) Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse Oregon Soils. Appl Environ Microbiol 76:7691–7698

    Article  PubMed  CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un systeme radiculaire. Recherche des methodes d’estimation ayant une signification functionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221

    Google Scholar 

  • Tyler BM, Wu MH, Wang JM, Cheung W, Morris PF (1996) Chemotactic preferences and strain variation in the response of Phytophthora sojae zoospores to host isoflavones. Appl Environ Microbiol 62:2811–2817

    PubMed  CAS  Google Scholar 

  • Utkhede RS (2006) Soil sickness, replant problem or replant disease and its integrated control. Allelopathy J 18:23–38

    Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  Google Scholar 

  • Vigo C, Norman JR, Hooker JE (2000) Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol 49:509–514

    Article  Google Scholar 

  • Westover KM, Kennedy AC, Kelley SE (1997) Patterns of rhizosphere microbial community structure associated with co-occurring plant species. J Ecol 85:863–873

    Article  Google Scholar 

  • Xu YL, Chen YL, Si ZS, Li ZL, Li CJ, Wen GY (2004) The effects of the root diffusate of different crops from different rotation systems on the egg hatch of soybean cyst nematode Heterodera glycines (In Chinese). Acta Phytopathol Sin 34:481–486

    Google Scholar 

  • Zeglin LH, Taylor AE, Myrold DD, Bottomley PJ (2011) Bacterial and archaeal amoA gene distribution covaries with soil nitrification properties across a range of land uses. Environ Microbiol Rep 3:717–726

    Article  CAS  Google Scholar 

  • Zhang SX, Gao ZQ, Liu HL (2000) Continuous cropping obstacle and rhizospheric microecology III. Soil phenolic acids and their biological effect (In Chinese). Chin J Appl Ecol 11:741–744

    CAS  Google Scholar 

  • Zhang JY, Wang JG, Xu YL, Li HG (2007) Effect of nitrogen on the species and content of organic acids in root exudates of different soybean cultivars (In Chinese). Plant Nutr Fert Sci 13:398–403

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (NSFC) (40871121) and the innovative group grant of Natural Science Foundation of China (31121062).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Junling Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, J., Li, X., Zhang, J. et al. Effect of root exudates on beneficial microorganisms—evidence from a continuous soybean monoculture. Plant Ecol 213, 1883–1892 (2012). https://doi.org/10.1007/s11258-012-0088-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-012-0088-3

Keywords

Navigation