Exploiting Arbuscular Mycorrhizal Fungi-Rhizobia-Legume Symbiosis to Increase Smallholder Farmers’ Crop Production and Resilience Under a Changing Climate

  • Ezekiel Mugendi Njeru
  • Morris Muthini
  • Mercy Martha Muindi
  • Omwoyo Ombori
  • Shem Bonuke Nchore
  • Steve Runo
  • John M. Maingi


Beneficial soil microbiota, such as arbuscular mycorrhizal fungi (AMF) and rhizobia, provide essential agroecosystem services in smallholder farming systems. Such microorganisms have great potential to promote crop production and resilience under a changing climate in sub-Saharan Africa. However, their function is affected by agronomic management practices, crop genotype and soil quality, among other factors. In this work, we sought to determine the effect of soil quality and crop genotype on nodulation, percentage mycorrhizal colonization and growth of maize and cowpea crops. Soil samples were obtained from ten smallholder farms with known management history in Embu and Kitui counties of Kenya and analysed for physicochemical parameters. Greenhouse bioassays were then carried out, where the samples were put in sterilized pots in four replicates and maintained in a completely randomized design. Four cowpea and maize genotypes (locally grown landraces and recommended genotypes from Kenya Agricultural and Livestock Research Organization) were grown in pots for 40 days. After harvesting, nodulation in the case of cowpea, shoot dry weights and mycorrhizal root colonization were determined. Remarkably, cowpea genotypes differed significantly (p < 0.0001) in nodule number. The locally cultivated landrace (C2) recorded the lowest nodulation with 30.4 nodules plant−1, compared to the open pollinated varieties (OPVs): C1, 39.15; C3, 43.70; and C4, 40.6 nodules plant−1. Among the maize genotypes, the locally cultivated landrace (M3) recorded a significantly (p = 0.008) higher percentage of mycorrhizal root colonization (68.9%) compared to the OPVs: M1 58.1% and M2 65.3%, while the hybrid (M4) had the lowest root colonization of 57.8%. Soil characteristics influenced nodulation and mycorrhizal colonization, where soil P was positively correlated to cowpea nodulation. Soil organic matter, nitrogen, pH and calcium positively correlated with AMF maize root colonization. Our results demonstrate the strong effect of soil quality and crop genotype on AMF-rhizobia-legume symbiosis, which affects overall crop growth and production. These factors should therefore be critically considered during the development of efficient low-cost inocula for enhanced smallholder farmers’ crop production.


Arbuscular mycorrhizal fungi Cowpea Crop genotype Maize Rhizobia Smallholder agro-ecosystems 



This work was funded by The World Academy of Science (TWAS) and Kenyatta University. The authors wish to thank the farmers at Machang’a and Kitui West for their contributions and assistance during soil sampling.


  1. Agoyi EE, Odong TL, Tumuhairwe JB, Chigeza G, Diers BW, Tukamuhabwa P (2017) Genotype by environment effects on promiscuous nodulation in soybean (Glycine max L. Merrill). Agric Food Secur 6(1):29. Scholar
  2. Antunes PM, Goss MJ (2005) Communication in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, rhizobia and legume plants: a review. In: Zobel R, Wright S (eds), Roots and soil management: interactions between roots and the soil. Agron Monogr 48. ASA, CSSA and SSSA, Madison, WI, pp 199–222Google Scholar
  3. Aquino S, Scabora MH, Antonio J, Maria S, Maltoni KL, Maria A, Cassiolato R (2015) Mycorrhizal colonization and diversity and corn genotype yield in soils of the Cerrado region, Brazil. Colonização e diversidade micorrízica e produtividade de genótipos de milho, em solo de Cerrado:4107–4118.
  4. Argaw A (2013) Evaluation of symbiotic effectiveness and size of resident Rhizobium leguminosarum var. viciae nodulating lentil (Lens culinaris medic) in some Ethiopian soils. Arch Agron Soil Sci 59(7):929–945. Scholar
  5. Argaw A, Muleta D (2018) Effect of genotypes-Rhizobium-environment interaction on nodulation and productivity of common bean (Phaseolus vulgaris L.) in Eastern Ethiopia. Environ Syst Res 6(1):14. Scholar
  6. Bargaz A, Faghire M, Abdi N, Farissi M, Sifi B, Drevon J, Ghoulam C (2012) Low soil phosphorus availability increases acid phosphatases activities and affects P partitioning in nodules, seeds and rhizosphere of Phaseolus vulgaris. Agriculture 2:139–153. Scholar
  7. Battini F, Grønlund M, Agnolucci M, Giovannetti M, Jakobsen I (2017) Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria article. Sci Rep 7(1):1–11.
  8. Berta G, Copetta A, Gamalero E, Bona E, Cesaro P, Scarafoni A, D’Agostino G (2013) Maize development and grain quality are differentially affected by mycorrhizal fungi and a growth promoting pseudomonad in the field. Mycorrhiza 24(3):161–170. Scholar
  9. Boon E, Zimmerman E, Lang BF, Hijri M, Cozzolino V, Di Meo V, Chen H (2013) Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. PLoS One 129(3):40–44. Scholar
  10. Castellane L, Maria A, Bueno M (2015) Characterization of exopolysaccharides produced by rhizobia species. Rev Bras Ciênc Solo 39(6):1566–1575. Scholar
  11. Cerozi S, Fitzsimmons K (2016) The effect of pH on phosphorus availability and speciation in an aquaponics nutrient solution. Bioresour Technol 219:778–781. Scholar
  12. Chen M, Graedel TE (2016) A half-century of global phosphorus flows, stocks, production, consumption, recycling, and environmental impacts. Glob Environ Chang 36:139–152. Scholar
  13. Chu Q, Wang X, Yang Y, Chen F, Zhang F, Feng G (2013) Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza 23(6):497–505. Scholar
  14. Clair SBS, Lynch JP (2010) The opening of Pandora’s Box: climate change impacts on soil fertility and crop nutrition in developing countries. Plant Soil 335:101–115. Scholar
  15. Cozzolino V, Di Meo V, Piccolo A (2013) Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. J Geochem Explor 129:40–44. Scholar
  16. Erbas BC (2017) In the presence of climate change, the use of fertilizers and the effect of income on agricultural emissions. Sustainability 9(11):1–17. Scholar
  17. Garg N, Geetanjali (2007) Symbiotic nitrogen fixation in legume nodules: process and signaling. A review. Agron Sustain Dev 27(1):59–68. Scholar
  18. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20(8):519–530. Scholar
  19. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring arbuscular mycorrhiza infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  20. Gomes EA, Oliveira CA, Lana UGP, Noda RW, Marriel IE, De Souza FA, Lagoas S (2015) Arbuscular mycorrhizal fungal communities in the roots of maize lines contrasting for Al tolerance grown in limed and non-limed Brazilian Oxisoil. J Microbiol Biotechnol 25(7):978–987CrossRefGoogle Scholar
  21. Jida M, Assefa F (2011) Phenotypic and plant growth promoting characteristics of Rhizobium leguminosarum bv. viciae from lentil growing areas of Ethiopia. Afr J Biotechnol 5(24):4133–4142. Scholar
  22. Jordan-meille AL, Pellerin S (2018) Shoot and root growth of hydroponic maize (Zea mays L.) as influenced by K deficiency. Plant Soil 304(1):157–168. Scholar
  23. Leghari SJ, Wahocho NA, Laghari GM, Hafeez Laghari A, Mustafa Bhabhan G, Hussain Talpur K, Bhutto TA, Wahocho SA, Lashari AA (2016) Role of nitrogen for plant growth and development: a review. Adv Environ Biol 10(9):2019–2219Google Scholar
  24. Lindstrom K, Murwira M, Willems A, Altier N (2010) The biodiversity of beneficial microbe-host mutualism: the case of rhizobia. Res Microbiol 161:453–463. Scholar
  25. Liu W, Zhang Y, Jiang S, Deng Y, Christie P, Murray PJ, Zhang J (2016) Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil. Sci Rep 6(1):24902. Scholar
  26. Motaroki EM, Njeru EM, Koskey G, Maingi J (2018) Rhizobial inoculation methods affect the nodulation and plant growth traits of host plant genotypes: a case study of Common bean Phaseolus vulgaris L. germplasms cultivated by smallholder farmers in Eastern Kenya. Advances in Agricultural. Science 6(3):77–94Google Scholar
  27. Mothapo NV, Grossman JM, Sooksa-nguan T, Maul J, Bräuer SL, Shi W (2013) Cropping history affects nodulation and symbiotic efficiency of distinct hairy vetch (Vicia villosa Roth.) genotypes with resident soil rhizobia. Biol Fertil Soils 49(7):871–879. Scholar
  28. Mwendwa P, Giliba RA (2012) Climate change impacts and adaptation strategies in Kenya. Chin J Popul Resour and Environ 10(4):22–29. Scholar
  29. Njeru EM (2018) Exploiting diversity to promote arbuscular mycorrhizal symbiosis and crop productivity in organic farming systems. AIMS Agric Food 3(3):280–294CrossRefGoogle Scholar
  30. Njeru E, Avio L, Sbrana C, Turrini A, Bocci G, Bàrberi P, Giovannetti M (2013) First evidence for a major cover crop effect on arbuscular mycorrhizal fungi and organic maize growth. Agron Sustain Dev 34(4):841–848. Scholar
  31. Okalebo RJ, Gathua KW, Woomer PL (2002) Laboratory methods of soil and plant analysis: a working manual, 2nd edn. TSBF-CIAT and Sacred Africa, Nairobi, KenyaGoogle Scholar
  32. Oliveira JP, Galli-Terasawa LV, Enke CG, Cordeiro VK, Armstrong LCT, Hungria M (2010) Genetic diversity of rhizobia in a Brazilian oxisol nodulating Mesoamerican and Andean genotypes of common bean (Phaseolus vulgaris L.). World J Microbiol Biotechnol 27(3):643–650CrossRefGoogle Scholar
  33. Ondieki DK, Nyaboga EN, Wagacha JM, Mwaura FB (2017) Morphological and genetic diversity of rhizobia nodulating cowpea (Vigna unguiculata L.) from agricultural soils of lower Eastern Kenya. Int J Microbiol 2017(8684921):9. Scholar
  34. Onono PA, Wawire NWH, Ombuki C (2013) The response of maize production in Kenya to economic incentives. Int J Dev Sustain 2(2):530–543Google Scholar
  35. Oruru MB, Njeru EM (2016) Upscaling arbuscular mycorrhizal symbiosis and related agroecosystems services in smallholder farming systems. Biomed Res Int 2016:1–12. Scholar
  36. Oruru MB, Njeru EM, Pasquet R, Runo S (2018) Response of a wild-type and modern cowpea cultivars to arbuscular mycorrhizal fungi inoculation in sterilized and non-sterilized soil. J Plant Nutr 48(1):90–101. Scholar
  37. Otieno PE, Muthomi JW, Chemining’wa GN, Nderitu JH (2009) Effect of rhizobia inoculation, farmyard manure, nitrogen fertilizer on nodulation and yield of food grain legumes. J Biol Sci 9:326–332CrossRefGoogle Scholar
  38. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11(11):789–799. Scholar
  39. Razaq M, Zhang P, Shen H, Salahuddin (2017) Influence of nitrogen and phosphorous on the growth and root morphology of Acer mono. PLOS ONE 12(2):e0171321. Scholar
  40. Rondon MA, Lehmann J, Ramírez J, Hurtado M (2006) Biological nitrogen fixation by common beans (Phaseolus vulgaris L.) increases with bio-char additions. Biol Fertil Soils 43(6):699–708. Scholar
  41. Slattery J, Pearce P (2002) Development of elite inoculant Rhizobium strains in South Eastern Australia. In: Herridge D (ed) Inoculants and Nitrogen Fixation of Legumes in Vietnam, ACIAR Proceedings, pp 86–94Google Scholar
  42. Smith SE, Read DJ (2008) Mycorrhiza Symbioses. Elsevier, LondonGoogle Scholar
  43. Ulzen J, Abaidoo RC, Mensah NE, Masso C, AbdelGadir AH (2016) Bradyrhizobium inoculants enhance grain yields of soybean and cowpea in Northern Ghana. Front Plant Sci 7:1770. Scholar
  44. van Tuinen D, Bouffaud M, Bernaud E, Colombet A, Tuinen D, Van Wipf D, Redecker D (2016) Regional-scale analysis of arbuscular mycorrhizal fungi: the case of Burgundy vineyards, International Molecular Mycorrhiza Meeting, Sept 2015, Cambridge, UKGoogle Scholar
  45. Wambugu PW, Mathenge PW, Auma EO, van Rheenen HA, Wambugu PW, Mathenge PW, van Rheenen HA (2012) Constraints to on-farm maize (Zea mays L.) seed production in Western Kenya: plant growth and yield. ISRN Agron 2012:1–7. Scholar
  46. Yang Y, Liang Y, Han X, Chiu T, Ghosh A, Chen H, Tang M (2016) The roles of arbuscular mycorrhizal fungi (AMF) in phytoremediation and tree-herb interactions in Pb contaminated soil. Sci Rep 6(February):1–14.

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Ezekiel Mugendi Njeru
    • 1
  • Morris Muthini
    • 1
  • Mercy Martha Muindi
    • 1
  • Omwoyo Ombori
    • 2
  • Shem Bonuke Nchore
    • 2
  • Steve Runo
    • 1
  • John M. Maingi
    • 1
  1. 1.Department of Biochemistry, Microbiology and BiotechnologyKenyatta UniversityNairobiKenya
  2. 2.Department of Plant SciencesKenyatta UniversityNairobiKenya

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