Skip to main content

Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P

Abstract

Soybean plants can form tripartite symbiotic associations with rhizobia and arbuscular mycorrhizal (AM) fungi, but little is known about effects of co-inoculation with rhizobia and AM fungi on plant growth, or their relationships to root architecture as well as nitrogen (N) and phosphorus (P) availability. In the present study, two soybean genotypes contrasting in root architecture were grown in a field experiment to evaluate relationships among soybean root architecture, AMF colonization, and nodulation under natural conditions. Additionally, a soil pot experiment in greenhouse was conducted to investigate the effects of co-inoculation with rhizobia and AM fungi on soybean growth, and uptake of N and P. Our results indicated that there was a complementary relationship between root architecture and AMF colonization in the field. The deep root soybean genotype had greater AMF colonization at low P, but better nodulation with high P supply than the shallow root genotype. A synergistic relationship dependent on N and P status exists between rhizobia and AM fungi on soybean growth. Co-inoculation with rhizobia and AM fungi significantly increased soybean growth under low P and/or low N conditions as indicated by increased shoot dry weight, along with plant N and P content. There were no significant effects of inoculation under adequate N and P conditions. Furthermore, the effects of co-inoculation were related to root architecture. The deep root genotype, HN112, benefited more from co-inoculation than the shallow root genotype, HN89. Our results elucidate new insights into the relationship between rhizobia, AM fungi, and plant growth under limitation of multiple nutrients, and thereby provides a theoretical basis for application of co-inoculation in field-grown soybean.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Adesemoye AO, Kloeppe JW (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12

    PubMed  Article  CAS  Google Scholar 

  • Ao J, Fu J, Tian J, Yan X, Liao H (2010) Genetic variability for root morph-architecture traits and root growth dynamics as related to phosphorus efficiency in soybean. Func Plant Biol 37:304–312

    Article  Google Scholar 

  • Barea JM, Azcon-Aguilar C (1983) Mycorrhizas and their significance in nodulation, nitrogen fixing plants. Adv Agron 36:1–54

    Article  Google Scholar 

  • Berta G, Fusconi A, Trotta A, Scannerini S (1990) Morphogenetic modifications induced by the mycorrhizal fungus Glomus strain E3 in the root system of Allium porrum L. New Phytol 114:207–215

    Article  Google Scholar 

  • Bethlenfalvay GJ, Brown MS, Stafford AE (1985) The Glycine-Glomus-Rhizobium symbiosis II. Antagonistic effects between mycorrhizal colonization and nodulation. Plant Physiol 79:1054–1058

    PubMed  Article  CAS  Google Scholar 

  • Blilou J, Ocampo J, Garcia-Garrido J (1999) Resistance of pea roots to endomycorrhiza fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid. J Exp Bot 50:1663–1668

    Article  CAS  Google Scholar 

  • Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological N fixation for sustainable agriculture: a perspective. Plant Soil 141:1–11

    Article  CAS  Google Scholar 

  • Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:187–207

    Article  Google Scholar 

  • Cao GQ (2007) Screening of effective rhizobial strains for soybean and characterization of their biological nitrogen fixation efficiency on acid red soils. Master dissertation, South China Agricultural University

  • Cheng F, Cao G, Wang X, Zhao J, Yan X, Liao H (2009) Identification and application of effective rhizobial strains for soybean on acid laterite soils in South China. Chinese Sci Bull 54:412–420

    Article  CAS  Google Scholar 

  • Cluett HC, Boucher DH (1983) Indirect mutualism in the legume Rhizobium-mycorrhizal fungus interaction. Oecologia 59:405–408

    Article  Google Scholar 

  • Cruz C, Green JJ, Watson GC, Wilson F, Martins-Loução MA (2004) Functional aspects of root architecture and mycorrhizal inoculation with respect to nutrient uptake capacity. Mycorrhiza 14:177–184

    PubMed  Article  CAS  Google Scholar 

  • FAO (Food and Agriculture Organization) (2003) http://apps.fao.org

  • Fitter AH (2006) What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytol 172:3–6

    PubMed  Article  CAS  Google Scholar 

  • Garnett T, Conn V, Kaiser B (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283

    PubMed  Article  CAS  Google Scholar 

  • Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crop Res 65:93–106

    Article  Google Scholar 

  • Graham PH, Viteri SE, Mackie F, Vargas AT, Palacios A (1982) Variation in acid soil tolerance among strains of Rhizobium phaseoli. Field Crop Res 5:121–128

    Article  Google Scholar 

  • Hardarson G, Atkins C (2003) Optimising biological N2 fixation by legumes in farming systems. Plant Soil 252:41–54

    Article  CAS  Google Scholar 

  • Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soybean-Rhizobium-Glomus associations. New Phytol 101:427–440

    Article  CAS  Google Scholar 

  • Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187

    Article  CAS  Google Scholar 

  • Huang HC (2007) Studies on mycorrhizae and AMF diversity of plant communities on Nankunshan and Tonggufeng of Guangdong province. Doctoral dissertation, South China Agricultural University

  • Jakobsen I (1995) Transport of phosphorus and carbon in VA mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer-Verlag, Berlin, pp 297–324

    Google Scholar 

  • Kuang R, Liao H, Yan X, Dong Y (2005) Phosphorus and nitrogen interactions in field-grown soybean as related to genetic attributes of root morphological and nodular traits. J Integr Plant Biol 47:549–559

    Article  CAS  Google Scholar 

  • Li SM, Li L, Zhang FS (2004) Enhancing phosphorus and nitrogen uptake of faba bean by inoculating arbuscular mycorrhizal fungus and Rhizobium leguminosarum. J China Agri Uni 9:11–15

    CAS  Google Scholar 

  • Li YY, Yu CB, Cheng X, Li CJ, Sun JH, Zhang FS, Lambers H, Li L (2009) Intercropping alleviates the inhibitory effect of N fertilization on nodulation and symbiotic N2 fixation of faba bean. Plant Soil 323:295–308

    Article  CAS  Google Scholar 

  • Liao H, Yan X, Rubio G, Beebe S, Blair M, Lynch JP (2004) Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct Plant Biol 31:959–970

    Article  CAS  Google Scholar 

  • Lisette J, Xavier C, Germida JJ (2003) Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol Fertil Soils 37:261–267

    Google Scholar 

  • Liu L, Liao H, Wang X, Yan X (2008) Regulation effect of soil P availability on mycorrhizal infection in relation to root architecture and P efficiency of Glycine max. Chinese J Appl Ecol 19:564–568

    CAS  Google Scholar 

  • Lynch JP (1998) The role of nutrient-efficient crops in modern agriculture. J Crop Prod 1:241–264

    Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plant, 2nd edn. Academic, New York, p 889

    Google Scholar 

  • Marshchner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    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

    Article  CAS  Google Scholar 

  • Oláh B, Brière C, Bécard G, Dénarié J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207

    PubMed  Article  Google Scholar 

  • Pacovsky RS (1986) Micronutrient uptake and distribution in mycorrhizal and phosphorus fertilized soybeans. Plant Soil 95:379–385

    Article  CAS  Google Scholar 

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693

    Article  CAS  Google Scholar 

  • Salvagiotti F, Specht JE, Cassman KG, Walters DT, Weiss A, Dobermann A (2009) Growth and nitrogen fixation in high-yielding soybean: impact of nitrogen fertilization. Agron J 101:958–970

    Article  CAS  Google Scholar 

  • Saxena AK, Rathi SK, Tilak KVBR (1997) Differential effect of various endomycorrhizal fungi on nodulating ability of green gram by Bradyrhizobium sp. (Vigna) strain S24. Biol Fert Soils 24:175–178

    Article  CAS  Google Scholar 

  • Schellenbaum L, Berta G, Ravolanirina F, Tisserant B, Gianinazzi S, Fitter AH (1991) Influence of endomycorrhizal infection on root morphology in a micropropagated woody plant species (Vitis vinifera L.). Ann Bot (Lond) 67:135–141

    Google Scholar 

  • Smith SE (2002) Soil microbes and plants—raising interest, mutual gains. New Phytol 156:142–144

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego, p 605

    Google Scholar 

  • Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

    PubMed  Article  CAS  Google Scholar 

  • Tang J, Mborehal I, She L, Liao H, Chen H, Sun Z, Yan X (2005) Nutritional effects of soybean root architecture in a soybean/maize intercropping system. Sci Agri Sin 38:1196–1203

    Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    PubMed  Article  CAS  Google Scholar 

  • Vance CP (1997) Enhanced agricultural sustainability through biological nitrogen fixation. In: Legocki A, Bothe H, Puhle A (eds) Biological fixation of nitrogen for ecology and sustainable agriculture. Springer, Berlin, pp 179–186

    Google Scholar 

  • Vance CP, Uhde-stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microb 64:5004–5007

    CAS  Google Scholar 

  • Wang X, Wang Y, Tian J, Lim B, Yan X, Liao H (2009) Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiol 151:233–240

    PubMed  Article  CAS  Google Scholar 

  • Xie Z, Staehelin C, Vierheili H, Wiemken A, Jabbouri S, Broughton WJ, Vogeli-Lange R, Boller T, Xie ZP (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of undulating and non-nodulating soybeans. Plant Physiol 108:1519–1525

    PubMed  CAS  Google Scholar 

  • Yao Q, Wang L, Zhu H, Chen J (2009) Effect of arbuscular mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Sci Hortic 121:458–461

    Article  Google Scholar 

  • Zhao J, Fu J, Liao H, He Y, Nian H, Hu Y, Qiu L, Dong Y, Yan X (2004) Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chinese Sci Bull 49:1611–1620

    CAS  Google Scholar 

Download references

Acknowledgments

This research was in part financially supported by grants from the National Natural Science Foundation of China (Grant no. 30890132) and the National Key Basic Research Special Funds of China (Grant no. 2005CB120902). We are grateful to Dr. Xiaolin Li for the generous gift of mycorrhizal fungus Glomus mosseae, Dr. Tom Walk and Mr. Larry York for English writing. The authors would also like to thank Dr. Andrew Smith for the technical assistance in the AM work and valuable and critical comments on an earlier version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hong Liao.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wang, X., Pan, Q., Chen, F. et al. Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21, 173–181 (2011). https://doi.org/10.1007/s00572-010-0319-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-010-0319-1

Keywords

  • Soybean
  • Arbuscular mycorrhizal fungi
  • Rhizobia
  • Co-inoculation