Skip to main content
SpringerLink
Log in

Formononetin stimulates mycorrhizal fungi colonization on the surface of active root nodules in soybean

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

The symbiosis of Leguminosae with arbuscular mycorrhizal fungi (AMF) and N2-fixing nodulating bacteria (NFNB) can occur simultaneously, forming a tripartite symbiosis. In particular, AMF can colonize root nodules, although this interaction is not yet well elucidated, especially with regard to nodule activity and to the influence of external factors, such as biostimulants. In this study, we hypothesized that the application of the flavonoid formononetin, used to stimulate root colonization by native AMF, increases the AMF colonization of soybean (Glycine max) root nodules, especially under low availability of phosphorus (P). To test this hypothesis, we performed a field experiment in randomized blocks in a 4 × 3 factorial design, with 4 treatments of formononetin (0, 0.46, 0.92 and 1.84 g per kg seed) and 3 of P (0, 60 and 120 kg ha−1) with 5 replicates. Nodules and roots were collected during the R2 stage (full flowering) and evaluated with respect to AMF colonization. Formononetin stimulated mycorrhizal fungi colonization of active nodules, especially when no P was applied, as also observed for AMF root colonization; however, it had no effect with 60 and 120 kg P ha−1. Thus, the application of formononetin increases surface AMF colonization of active nodules and roots, but its effect disappears with an increase in P and the inactivity of the nodule.

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

Access this article

Log in via an institution

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

  • Ahmad MH (1995) Compatibility and coselection of vesicular-arbuscular mycorrhizal fungi and Rhizobia for tropical legumes. Crit Rev Biotechnol 15:229–239. doi:10.3109/07388559509147410

    Article  Google Scholar 

  • Antunes PM, Rajcan I, Goss MJ (2006) Specific flavonoids as interconnecting signals in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium japonicum (Kirchner) Jordan and soybean (Glycine max [L.] Merr.). Soil Biol Biochem 38:533–543. doi:10.1016/j.soilbio.2005.06.008

    Article  CAS  Google Scholar 

  • Azcón R, Rubio R, Barea JM (1991) Selective interactions between different species of mycorrhizal fungi and Rhizobium meliloti strains, and their effects on growth, N2-fixation (15N) and nutrition of Medicago sativa L. New Phytol 117:399–404. doi:10.1111/j.1469-8137.1991.tb00003.x

    Article  Google Scholar 

  • Baird LM, Caruso KJ (1994) Development of root nodules in Phaseolus vulgaris inoculated with Rhizobium and mycorrhizal fungi. Int J Plant Sci 155:633–639. doi:10.1086/297203

    Article  Google Scholar 

  • Bouyoucos GJ (1951) A recalibration of the hydrometer method for making analysis of soils. Agric J 43:433–437. doi:10.2134/agronj1951.00021962004300090005x

    Google Scholar 

  • Catford JG, Staehelin C, Lerat S, Piche Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonisation and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with nod factors. J Exp Bot 54:1481–1487. doi:10.1093/jxb/erg156

    Article  CAS  PubMed  Google Scholar 

  • Catford JG, Staehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isofavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266. doi:10.1007/s11104-006-9012-8

    Article  CAS  Google Scholar 

  • Davies JFT, Calderón CM, Huaman Z, Gómez R (2005a) Influence of a flavonoid (formononetin) on mycorrhizal activity and potato crop productivity in the highlands of Peru. Sci Hortic 106:318–329. doi:10.1016/j.scienta.2005.04.013

    Article  CAS  Google Scholar 

  • Davies JFT, Calderón CM, Huaman Z (2005b) Influence of Arbuscular Mycorrhizae indigenous to Peru and a flavonoid on growth, yield, and leaf elemental concentration of ‘Yungay’ potatoes. Hortscience 40:381–385

    Google Scholar 

  • Douds DD Jr., Nagahashi G, Pfeffer PE, Reider C, Kayser WM (2006) On-farm production of AM fungus inoculum in mixtures of compost and vermiculite. Bioresour Technol 97:809–818. doi:10.1016/j.biortech.2005.04.015

    Article  CAS  PubMed  Google Scholar 

  • Franzini VI, Azcón R, Latanze-Mendes F, Aroca R (2010) Interaction between Glomus species and rhizobium strains affect the nutritional physiology of drought stressed legume hosts. J Plant Physiol. doi:10.1016/j.jplph.2009.11.010

    PubMed  Google Scholar 

  • Fries LLM, Pacovsky RS, Safir GR (1998) Influence of phosphorus and formononetin on isozyme expression in the Zea mays–Glomus intraradices symbiosis. Physiol Plant 103:172–180. doi:10.1034/j.1399-3054.1998.1030204.x

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. doi:10.1111/j.1469-8137.1980.tb04556.x

    Article  Google Scholar 

  • Giovannetti M, Avio L, Sbrana C, Citernesi AS (1993) Factors affecting appressorium development in the vesicular arbuscular mycorrhizal fungus Glomus mosseae (Nicol & Gerd.) Gerd. and Trappe. New Phytol 123:114–122

    Google Scholar 

  • Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244. doi:10.1016/j.soilbio.2009.03.005

    Article  CAS  Google Scholar 

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488. doi:10.1016/S0953-7562(89)80195-9

    Article  Google Scholar 

  • Lambais MR, Ríos-Ruiz WF, Andrade RM (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytol 160:421–428. doi:10.1046/j.1469-8137.2003.00881.x

    Article  CAS  Google Scholar 

  • Mehlich A (1953) Determination of P, Ca, Mg, K, Na and NH4. North Carolina Soil Testing Laboratories, Raleigh

    Google Scholar 

  • Minchin FR, James EK, Becana M (2008) Oxygen diffusion, production of reactive oxygen and nitrogen species, and antioxidants in legume nodules. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Nitrogen-fixing leguminous symbioses. Springer, Dordrecht, pp. 321–353

    Google Scholar 

  • Moreira FMS, Siqueira JO (2006) Microbiologia e bioquímica do solo. Editora UFLA, Lavras

    Google Scholar 

  • Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019–1027. doi:10.1016/j.soilbio.2007.11.014

    Article  CAS  Google Scholar 

  • Nair MG, Safir GR, Siqueira JO (1991) Isolation and identification of vesicular-arbuscular mycorrhiza-stimulatory compounds from clover (Trifolium repens) roots. Appl Environ Microbiol 57:434–439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nogueira MA, Cardoso EJBN (2006) Plant growth and phosphorus uptake in mycorrhizal rangpur lime seedlings under different levels of phosphorus. Pesq Agrop Brasileira 41:93–99. doi:10.1590/S0100-204X2006000100013

    Article  Google Scholar 

  • Nogueira MA, Cardoso EJBN (2007) Phosphorus availability changes the internal and external endomycorrhizal colonization and affects symbiotic effectivenes. Sci Agric 64:295–300. doi:10.1590/S0103-90162007000300013

    Article  CAS  Google Scholar 

  • Novais CB, Siqueira JO (2009) Formononetin application on colonization and sporulation of arbuscular mycorrhizal fungi in Brachiaria. Pesq Agropec Brasileira 44:496–502. doi:10.1590/S0100-204X2009000500009

    Article  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Powell CL, Bagyaraj DJ (1984) VA mycorrhiza. CRC Press, Boca Raton

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Rodríguez NF, Gómez R (2011) Asociación simbiótica entre hongos micorrízicos arbusculares y el sistema radicular de plántulas de cacao (Theobroma cacao L.): efecto de la formononetina y la disponibilidad de fósforo en el suelo. Rev Corpoica Cienc Tecnol Agropec 12:77–85

    Google Scholar 

  • Scheublin TR, van der Heijden MGA (2006) Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species. New Phytol 172:732–738. doi:10.1111/j.1469-8137.2006.01858.x

    Article  PubMed  Google Scholar 

  • Scheublin TR, Karyn PR, Young JPW, van der Heijden MGA (2004) Non-legumes, legumes, and root nodules harbour different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246. doi:10.1128/AEM.70.10.6240-6246.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sena JOA, Labate CA, Cardoso EJBN (2004) Caracterização fisiológica da redução de crescimento de mudas de citros micorrizadas em altas doses de fósforo. Rev Bras Ciênc Solo 28:827–832. doi:10.1590/S0100-06832004000500005

    Article  Google Scholar 

  • Sheng M, Lalande R, Hamel C, Ziadi N, Shi Y (2012) Growth of corn roots and associated arbuscular mycorrhizae are affected by long-term tillage and phosphorus fertilization. Agron J 104:1672–1678. doi:10.2134/agronj2012.0153

    Article  Google Scholar 

  • Siqueira JO, Colozzi-Filho A (1986) Micorrizas vesículo-arbusculares em mudas de cafeeiro. II. Efeito do fósforo no estabelecimento e funcionamento da simbiose. Rev Bras Ciênc Solo 10:207–211

    CAS  Google Scholar 

  • Siqueira JO, Hubbell DH, Valle RR (1984) Effect of phosphorus on formation of the vesicular-arbuscular mycorrhizal symbiosis. Pesq Agrop Brasileira 19:1465–1474

    Google Scholar 

  • Siqueira JO, Safir GR, Nair MG (1991) Stimulation of vesicular-arbuscular mycorrhiza formation and growth of white clover by flavonoid compounds. New Phytol 118:87–93. doi:10.1111/j.1469-8137.1991.tb00568.x

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, Amsterdam

    Google Scholar 

  • Steinberg PD, Rillig MC (2003) Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol Biochem 35:191–194. doi:10.1016/S0038-0717(02)00249-3

    Article  CAS  Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805. doi:10.1146/annurev-arplant-050312-120235

    Article  CAS  PubMed  Google Scholar 

  • Vadez V, Beck DP, Lasso JH, Drevon J-J (1997) Utilization of the acetylene reduction assay to screen for tolerance of symbiotic N2 fixation to limiting P nutrition in common bean. Physiol Plant 99:227–232

    Article  CAS  Google Scholar 

  • Vidal-Dominguez MT, Azcón-Aguilar C, Barea JM (1994) Preferential sporulation of Glomus fasciculatum in the root nodules of herbaceous legumes. Symbiosis 16:65–73

    Google Scholar 

  • Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

    Article  CAS  Google Scholar 

  • Xavier LJC, Germida JJ (2002) Response of lentil under controlled conditions to co-inoculation with arbuscular mycorrhizal fungi and rhizobia varying in efficacy. Soil Biol Biochem 34:181–188. doi:10.1016/S0038-0717(01)00165-1

    Article  CAS  Google Scholar 

  • Xiao TJ, Yang QS, Ran W, Xu GH, Shen QR (2010) Effect of inoculation with arbuscular mycorrhizal fungus on nitrogen and phosphorus utilization in upland rice-mungbean intercropping system. Agric Sci 9:528–535. doi:10.1016/S1671-2927(09)60126-7

    Google Scholar 

  • Xie ZP, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Brough-Ton WJ, Ègeli-Lange VR, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiol 108:1519–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. doi:10.1111/j.2041-210X.2009.00001.x

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and the Ministry of Science and Technology (Ministério de Ciência e Tecnologia) (MCT/CNPq/Ct-AGRO N° 69/2009) for financial support and for a scientific initiation fellowship to Jacqueline Savana da Silva and Teotonio Soares de Carvalho, a doctoral fellowship to Jessé Valentim dos Santos, and a research productivity fellowship to Fatima Maria de Souza Moreira. We also acknowledge the Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Capes) for a doctoral fellowship to Paula Rose de Almeida Ribeiro.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ciência do Solo, Departamento de Ciência do Solo, Universidade Federal de Lavras, Cx Postal 3037, Lavras, MG, CEP 37200-000, Brazil

    Jacqueline Savana da Silva, Teotonio Soares de Carvalho, Jessé Valentim dos Santos, Paula Rose de Almeida Ribeiro & Fatima Maria de Souza Moreira

Authors
  1. Jacqueline Savana da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teotonio Soares de Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jessé Valentim dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paula Rose de Almeida Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fatima Maria de Souza Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fatima Maria de Souza Moreira.

Electronic supplementary material

Table S1

(DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Savana da Silva, J., Soares de Carvalho, T., Valentim dos Santos, J. et al. Formononetin stimulates mycorrhizal fungi colonization on the surface of active root nodules in soybean. Symbiosis 71, 27–34 (2017). https://doi.org/10.1007/s13199-016-0408-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-016-0408-9

Keywords

Search

Navigation