Dual inoculation of soybean with <i>Rhizophagus irregularis</i> and commercial <i>Bradyrhizobium japonicum</i> increases nitrogen fixation and growth in organic and conventional soils

Nicholas Mawira Gitonga; Gilbert Koskey; Ezekiel Mugendi Njeru; John M. Maingi; Richard Cheruiyot; Nicholas Mawira Gitonga; Gilbert Koskey; Ezekiel Mugendi Njeru; John M. Maingi; Richard Cheruiyot

doi:10.3934/agrfood.2021028

AIMS Agriculture and Food

2021, Volume 6, Issue 2: 478-495. doi: 10.3934/agrfood.2021028

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Dual inoculation of soybean with Rhizophagus irregularis and commercial Bradyrhizobium japonicum increases nitrogen fixation and growth in organic and conventional soils

1.
Department of Biochemistry, Microbiology and Biotechnology, Kenyatta University, Nairobi, Kenya
2.
Department of Biological and Physical Sciences, Karatina University, Karatina, Kenya
3.
Institute of Life Sciences, Sant'Anna School of Advanced Studies, Pisa, Italy
4.
Department of Plant Sciences, Kenyatta University, Nairobi, Kenya

Received: 17 December 2020 Accepted: 04 March 2021 Published: 12 March 2021

Soil amendment with beneficial microorganisms is gaining popularity among farmers to alleviate the decline of soil fertility and to increase food production and maintain environmental quality. However, farm management greatly influence soil microbial abundance and function, which overly affects crop growth and development. In this work, greenhouse experiments involving soybeans were conducted to evaluate the effects of bradyrhizobia and arbuscular mycorrhizal fungi (AMF) dual inoculation on nodulation, AMF root colonization, growth and nutrient acquisition under contrasting farming systems. The experimental treatments were AMF and/or bradyrhizobia inoculation and dual inoculation on SC squire soybean variety. The exotic AMF inoculants used were Funneliformis mosseae (BEG 12) and Rhizophagus irregularis (BEG 44) while bacteria were commercial Bradyrhizobium japonicum (USDA110) and native bradyrhizobia isolates. Experiments with soil samples from organic and conventional farms were set out using a completely randomized design with three replicates. The results demonstrated that bradyrhizobia and AMF dual inoculation consistently and significantly enhanced soybean nodule dry weight (NDW), shoot dry weight (SDW) and AMF root colonization compared with individual bradyrhizobia, AMF and non-inoculated control. Moreover, organic soil significantly (p = 0.001) increased soybean SDW, NDW and AMF root colonization compared to conventional soil. Remarkably, shoot nutrients content differed in organic and conventional farming where, shoot nitrogen, phosphorus, potassium and organic carbon were higher in organic farming than the latter. Among individual inoculants, Rhizophagus irregularis out-performed Funneliformis mosseae, while commercial Bradyrhizobium japonicum showed higher performance than native bradyrhizobia. Our results demonstrated the importance of organic farming, AMF and bradyrhizobia dual inoculation in enhancing soybean growth and nutrient acquisition. However, field trials should be assessed to determine the good performance of bradyrhizobia and AMF dual inoculation in organic farming before being popularized and adopted by farmers as a sustainable agronomical management strategy to increase soil fertility and food productivity.
- dual inoculation,
- soybean,
- bradyrhizobia,
- arbuscular mycorrhizal fungi,
- organic,
- conventional farming
Citation: Nicholas Mawira Gitonga, Gilbert Koskey, Ezekiel Mugendi Njeru, John M. Maingi, Richard Cheruiyot. Dual inoculation of soybean with Rhizophagus irregularis and commercial Bradyrhizobium japonicum increases nitrogen fixation and growth in organic and conventional soils[J]. AIMS Agriculture and Food, 2021, 6(2): 478-495. doi: 10.3934/agrfood.2021028

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Abstract

Soil amendment with beneficial microorganisms is gaining popularity among farmers to alleviate the decline of soil fertility and to increase food production and maintain environmental quality. However, farm management greatly influence soil microbial abundance and function, which overly affects crop growth and development. In this work, greenhouse experiments involving soybeans were conducted to evaluate the effects of bradyrhizobia and arbuscular mycorrhizal fungi (AMF) dual inoculation on nodulation, AMF root colonization, growth and nutrient acquisition under contrasting farming systems. The experimental treatments were AMF and/or bradyrhizobia inoculation and dual inoculation on SC squire soybean variety. The exotic AMF inoculants used were Funneliformis mosseae (BEG 12) and Rhizophagus irregularis (BEG 44) while bacteria were commercial Bradyrhizobium japonicum (USDA110) and native bradyrhizobia isolates. Experiments with soil samples from organic and conventional farms were set out using a completely randomized design with three replicates. The results demonstrated that bradyrhizobia and AMF dual inoculation consistently and significantly enhanced soybean nodule dry weight (NDW), shoot dry weight (SDW) and AMF root colonization compared with individual bradyrhizobia, AMF and non-inoculated control. Moreover, organic soil significantly (p = 0.001) increased soybean SDW, NDW and AMF root colonization compared to conventional soil. Remarkably, shoot nutrients content differed in organic and conventional farming where, shoot nitrogen, phosphorus, potassium and organic carbon were higher in organic farming than the latter. Among individual inoculants, Rhizophagus irregularis out-performed Funneliformis mosseae, while commercial Bradyrhizobium japonicum showed higher performance than native bradyrhizobia. Our results demonstrated the importance of organic farming, AMF and bradyrhizobia dual inoculation in enhancing soybean growth and nutrient acquisition. However, field trials should be assessed to determine the good performance of bradyrhizobia and AMF dual inoculation in organic farming before being popularized and adopted by farmers as a sustainable agronomical management strategy to increase soil fertility and food productivity.

References

[1]	Masciarelli O, Llanes A, Luna V (2014) A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol Res 169: 609-615. doi: 10.1016/j.micres.2013.10.001
[2]	Maphosa Y, Jideani VA (2017) The role of legumes in human nutrition. Functional Food-Improve Health through Adequate Food. Intech.
[3]	Medic J, Atkinson C, Hurburgh CR (2014) Current knowledge in soybean composition. J Am Oil Chem Soc 91: 363-384. doi: 10.1007/s11746-013-2407-9
[4]	Da Silva Júnior EB, Favero VO, Xavier GR, et al. (2018) Rhizobium inoculation of cowpea in Brazilian cerrado increases yields and nitrogen fixation. Agron J 110: 722-727. doi: 10.2134/agronj2017.04.0231
[5]	Jackson AS (2016) A brief history of soybean production in Kenya. Res J Agric Environ Manage 5: 58-64.
[6]	Muniu FK (2017) Characterization and evaluation of local cowpea accessions and their response to organic and inorganic nitrogen fertilizers in coastal Kenya. Doctoral dissertation, University of Nairobi.
[7]	Njeru EM, Maingi JM, Cheruiyot R, et al. (2013) Managing soybean for enhanced food production and soil bio-fertility in smallholder systems through maximized fertilizer use efficiency. Int J Agric For 3: 191-197.
[8]	Ndungu SM, Messmer MM, Ziegler D, et al. (2018) Cowpea (Vigna unguiculata L. Walp) hosts several widespread bradyrhizobial root nodule symbionts across contrasting agro-ecological production areas in Kenya. Agr Ecosyst Environ 261: 161-171.
[9]	Lobell DB, Field CB (2007) Global scale climate-crop yield relationships and the impacts of recent warming. Environ Res Lett 2: 014002. doi: 10.1088/1748-9326/2/1/014002
[10]	Ku YS, Au-Yeung WK, Yung YL, et al. (2013) Drought stress and tolerance in soybean. A Comprehensive Survey of Internaitonal Soybean Research-Genetics, Physiology, Agronomy and Nitrogen Relationships, 209-237.
[11]	Caliskan S, Ozkaya I, Caliskan ME, et al. (2008) The effects of nitrogen and iron fertilization on growth, yield and fertilizer use efficiency of soybean in a Mediterranean-type soil. Field Crop Res 108: 126-132. doi: 10.1016/j.fcr.2008.04.005
[12]	Brahim S, Niess A, Pflipsen M, et al. (2017) Effect of combined fertilization with rock phosphate and elemental sulphur on yield and nutrient uptake of soybean. Plant Soil Environ 63: 89-95. doi: 10.17221/22/2017-PSE
[13]	Samson ME, Menasseri-Aubry S, Chantigny MH, et al. (2019) Crop response to soil management practices is driven by interactions among practices, crop species and soil type. Field Crop Res 243: 107623. doi: 10.1016/j.fcr.2019.107623
[14]	Chibeba AM, Kyei-Boahen S, de Fátima Guimarã es M, et al. (2017) Isolation, characterization and selection of indigenous Bradyrhizobium strains with outstanding symbiotic performance to increase soybean yields in Mozambique. Agric Ecosyst Environ 246: 291-305. doi: 10.1016/j.agee.2017.06.017
[15]	Butler SJ, Vickery JA, Norris K (2007) Farmland biodiversity and the footprint of agriculture. Science 315: 381-384. doi: 10.1126/science.1136607
[16]	Wezel A, Casagrande M, Celette F, et al. (2014) Agroecological practices for sustainable agriculture. A review. Agron Sustain Dev 34: 1-20.
[17]	Altieri MA, Farrell JG, Hecht SB, et al. (2018) The Agroecosystem: Determinants, Resources, Processes, and Sustainability. Agroecology. CRC Press, 41-68.
[18]	Adesemoye AO, Kloepper JW (2009) Plant-Microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85: 1-12. doi: 10.1007/s00253-009-2196-0
[19]	Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32: 1272-1283. doi: 10.1111/j.1365-3040.2009.02011.x
[20]	Reddy CA, Saravanan RS (2013) Polymicrobial multi-functional approach for enhancement of crop productivity. Adv Appl Microbiol 82: 53-113. doi: 10.1016/B978-0-12-407679-2.00003-X
[21]	Mwenda GM (2010) Diversity and symbiotic efficiency of rhizobia isolated from Embu, Kenya. Soil Sci Soc Am J 78: 1643.
[22]	Parr MC (2014) Promiscuous soybean: Impacts on Rhizobia diversity and smallholder Malawian agriculture. Available from: http://www.lib.ncsu.edu/resolver/1840.16/9425.
[23]	Meena RS, Yadav RS, Meena H, et al. (2015) Towards the current need to enhance legume productivity and soil sustainability worldwide: A book review. J Clean Prod 104: 513-515.
[24]	Xiao TJ, Yang QS, Ran W, et al. (2010) Effect of inoculation with arbuscularmycorrhizal fungus on nitrogen and phosphorus utilization in upland rice-mungbean intercropping system. Agr Sci China 9: 528-535. doi: 10.1016/S1671-2927(09)60126-7
[25]	Perez-Jaramillo JE, Mendes R, Raaijmakers JM (2016) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol 90: 635-644. doi: 10.1007/s11103-015-0337-7
[26]	Abd-Alla MH, El-Enany AWE, Nafady NA, et al. (2014) Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiol Res 169: 49-58.
[27]	Ruiz-Lozano JM, Collados C, Barea JM, et al. (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean mplants. New Phytol 151: 493-502. doi: 10.1046/j.0028-646x.2001.00196.x
[28]	Okalebo JR, Gathua KW, Woomer PL (2002) Laboratory methods of soil and plant analysis: A working manual. Second Edition. TSBF-CIAT and Sacred Africa, Nairobi, Kenya.
[29]	Ashworth AJ, Allen FL, Wight JP, et al. (2014) Soil organic carbon sequestration rates under crop sequence diversity, bio-covers, and no-tillage. SSSAJ 78: 1726-1733. doi: 10.2136/sssaj2013.09.0422
[30]	Sáez-Plaza P, Navas MJ, Wybraniec S (2013) An overview of the kjeldahl method of nitrogen determination. Part Ⅱ. Sample preparation, working scale, instrumental finish, and quality control, Crit Rev Anal Chemi 43: 224-272.
[31]	Furseth BJ, Conley SP, Ané JM (2012) Soybean response to soil rhizobia and seed-applied rhizobia inoculants in Wisconsin. Crop Sci 52: 339-344. doi: 10.2135/cropsci2011.01.0041
[32]	Jaetzol R, Schimdt H, Hornetz B, et al. (2006) Farm management handbook of Kenya. Vol Ⅱ, Natural conditions and farm information. East Kenya, Ministry of Agriculture, Nairobi.
[33]	Woomer PL, Huising J, Giller K, et al. (2014) N2Africa final report of the first phase: 2009-2013.
[34]	Khalil S, Loynachan TE, Tabatabai MA (1994) Mycorrhizal dependency and nutrient uptake by improved and unimproved corn and soybean cultivars. Agron. J 86: 949-958.
[35]	Somasegaran P, Hoben HJ (1985) Available from: https: //www.ctahr.hawaii.edu/bnf/Downloads/Training/Rhizobium%20technology/Title%20Page.PDF.
[36]	Takács T, Cseresnyés I, Kovács R, et al. (2018) Symbiotic Effectivity of Dual and Tripartite Associations on Soybean (Glycine max L. Merr.) Cultivars Inoculated with Bradyrhizobium japonicum and AM Fungi. Front Plant Sci 9: 1631.
[37]	Xie MM, Zou YN, Wu QS, et al. (2020) Single or dual inoculation of arbuscular mycorrhizal fungi and rhizobia regulates plant growth and nitrogen acquisition in white clover. Plant Soil Environ 66: 287-294. doi: 10.17221/234/2020-PSE
[38]	Jaiswal SK, Anand A, Dhar B, et al. (2011) Genotypic characterization of phage-typed indigenous soybean bradyrhizobia and their host range symbiotic effectiveness. Microb Ecol 63: 116-126. doi: 10.1007/s00248-011-9950-4
[39]	Muthini M, Maingi JM, Muoma JO, et al. (2014) Morphological assessment and effectiveness of indigenous rhizobia isolates that nodulate P. vulgaris in water hyacinth compost testing field in Lake Victoria basin. Br J Appl Sci Technol 4: 718-738.
[40]	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. doi: 10.1016/S0007-1536(70)80110-3
[41]	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
[42]	Hassink J (1995) Density fractions of soil macroorganic matter and microbial biomass as predictors of C and N mineralization. Soil Biol Biochem 27: 1099-1108. doi: 10.1016/0038-0717(95)00027-C
[43]	Gajda AM, Martyniuk S, Stachyra A, et al. (2000) Relations between microbiological and biochemical properties of soil under different agrotechnical conditions and its productivity. Polish J Soil Sci 33: 55-60.
[44]	Mishra V, Ellouze W, Howard RJ (2018) Utility of arbuscular mycorrhizal fungi for improved production and disease mitigation in organic and hydroponic greenhouse crops. J Hortic 5: 1000537. doi: 10.4172/2376-0354.1000237
[45]	Karunasinghe TG, Fernando WC, Jayasekera LR (2009) The effect of poultry manure and inorganic fertilizer on the arbuscular mycorrhiza in coconut. J Natn Sci Foundation Sri Lanka 37: 277-279. doi: 10.4038/jnsfsr.v37i4.1476
[46]	Hunt ND, Hill JD, Liebman M (2019) Cropping system diversity effects on nutrient discharge, soil erosion, and agronomic performance. Environ Sci Technol 53: 1344-1352.
[47]	Liu XD, Feng ZW, Zhao ZY, et al. (2020) Acidic soil inhibits the functionality of arbuscular mycorrhizal fungi by reducing arbuscule formation in tomato roots. Soil Sci Plant Nutr 66: 275-284. doi: 10.1080/00380768.2020.1721320
[48]	Ye GP, Lin YX, Luo JF, et al. (2020) Responses of soil fungal diversity and community composition to long-term fertilization: Field experiment in an acidic Ultisol and literature synthesis. Appl Soil Ecol 145: 103305. doi: 10.1016/j.apsoil.2019.06.008
[49]	Sarr PS, Yamakawa T, Saeki Y, et al. (2011) Phylogenetic diversity of indigenous cowpea bradyrhizobia from soils in Japan based on sequence analysis of the 16S-23S rRNA internal transcribed spacer (ITS) region. Syst Appl Microbiol 34: 285-292. doi: 10.1016/j.syapm.2010.11.021
[50]	Koskey G, Mburu SW, Njeru EM, et al. (2017) Potential of native rhizobia in enhancing nitrogen fixation and yields of climbing beans (Phaseolus vulgaris L.) in contrasting environments of Eastern Kenya. Front Plant Sci 8: 443.
[51]	Simbine MG, Baijukya FP, Onwonga RN (2018) Intermediate maturing soybean produce multiple benefits at 1: 2 maize: soybean planting density. J Agric Sci 10: 29-46.
[52]	Njeru EM, Muthini M, Muindi MM, et al. (2020) Exploiting Arbuscular Mycorrhizal Fungi-Rhizobia-Legume Symbiosis to Increase Smallholder Farmers' Crop Production and Resilience Under a Changing Climate. Climate impacts on agricultural and natural resource sustainability in Africa. Springer, Cham, 471-488.
[53]	Lodwig EM, Poole PS (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22: 37-38. doi: 10.1080/713610850
[54]	Antunes PM (2004) Determination on nutritional and signalling factors involved in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium and soybean. Doctoral dissertation, University of Guelph.
[55]	Mirdhe RM, Lakshman HC (2014) Synergistic interaction between arbuscular mycorrhizal fungi, Rhizobium and phosphate solubilising bacteria on Vigna Unguiculata (L) Verdc. Int J Bioassays 3: 2096-2099.
[56]	Antunes PM, Goss MJ (2005) Communication in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, rhizobia and legume plants: a review. In: Zobel RW, Wright SF. (Eds), Roots and soil management: Interactions between roots and the soil. American Society of Agronomy, 48: 199-222.
[57]	Schneider KD, Lynch DK, Dunfielda K, et al. (2015) Farm system management affects community structure of arbuscular mycorrhizal fungi. Appl Soil Ecol 96: 192-200. doi: 10.1016/j.apsoil.2015.07.015
[58]	Abbott L, Robson A, Jasper DA, et al. (1992) What is the role of VA mycorrhizal hyphae in soil? In: Read DJ. (Ed), Mycorrhizas in ecosystems. Wallingford: CAB International, 37-41.
[59]	Thonar C, Frossard E, Smilauer P, et al. (2014) Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi. Mol Ecol 23: 733-746. doi: 10.1111/mec.12625
[60]	Tabassum B, Khan A, Tariq M, et al. (2017) Bottlenecks in commercialisation and future prospects of PGPR. Appl soil Ecol 121: 102-117. doi: 10.1016/j.apsoil.2017.09.030
[61]	de Paiva Barbosa L, Costa PF, Ribeiro PRA, et al. (2017) Symbiotic efficiency and genotypic characterization of variants of Bradyrhizobium spp. in commercial inoculants for soybeans. Rev Bras Ciênc Do Solo 41.
[62]	Oruru MB, Njeru EM, Pasquet R, et al. (2018) Response of a wild-type and modern cowpea cultivars to arbuscular mycorrhizal inoculation in sterilized and non-sterilized soil. J Plant Nutr 41: 90-101. doi: 10.1080/01904167.2017.1381728
[63]	Ouma EW, Asango AM, Maingi J, et al. (2016) Elucidating the potential of native rhizobial isolates to improve biological nitrogen fixation and growth of common bean and soybean in smallholder farming systems of Kenya. Int J Agron 2016: 4569241.
[64]	Miransari M (2011) Arbuscular mycorrhizal fungi and nitrogen uptake. Arch Microbiol 193: 77-81.
[65]	Upadhayay VK, Singh J, Khan A, et al. (2019) Mycorrhizal mediated micronutrients transportation in food based plants: A biofortification strategy. Mycorrhizosphere and pedogenesis. Singapore: Springer, 1-24.
[66]	Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: With special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59: 1115-1126. doi: 10.1093/jxb/ern059
[67]	Sofi MN, Bhat RA, Rashid A, et al. (2017) Rhizosphere Mycorrhizae communities an input for organic agriculture. Mycorrhiza-Nutrient Uptake, Biocontrol, Ecorestoration. DOI: 10.1007/978-3-319-68867-1.

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