Hostname: page-component-848d4c4894-nr4z6 Total loading time: 0 Render date: 2024-05-27T16:25:39.828Z Has data issue: false hasContentIssue false

Does coinoculation with bradyrhizobia and cyanobacteria improve groundnut growth and yield?

Published online by Cambridge University Press:  11 March 2024

Diva Souza Andrade*
Affiliation:
Soil Science department, Instituto de Desenvolvimento Rural do Paraná – IAPAR-EMATER, Rod Celso Garcia Cid, km 375, Londrina, Paraná 86.047-902, Brazil
Gisele Milani Lovato
Affiliation:
Soil Science department, Instituto de Desenvolvimento Rural do Paraná – IAPAR-EMATER, Rod Celso Garcia Cid, km 375, Londrina, Paraná 86.047-902, Brazil
Glaciela Kaschuk
Affiliation:
Post-Graduation in Soil Science, Federal University of Paraná, Rua dos Funcionários, 1540, Curitiba, Paraná CEP 80035-050, Brazil
Mariangela Hungria
Affiliation:
Soil Biotechnology Laboratory, Embrapa Soja, C.P. 231, Londrina, Paraná 86001-970, Brazil
*
Corresponding author: Diva Souza Andrade; Emails: diva@idr.pr.gov.br; 2013divaandrade@gmail.com

Summary

Groundnut plants can obtain N from N2 fixation via symbiosis with rhizobia, and inoculation with selected strains can improve grain yields. We report the results of four field experiments carried out under subtropical conditions to confirm whether microbial inoculants can improve groundnut performance through the effects of single inoculation with Bradyrhizobium arachidis (SEMIA6144), coinoculation with Arthrospira platensis (IPR7059) or Synechocystis sp. (IPR7061), or N fertilization with 100 kg ha-1 N on plant growth, nodulation, N accumulation in tissues, grain protein concentration (GPC), and grain yield. There were no effects of inoculation treatment or N fertilizer on shoot or root dry weight. In clayey soil, coinoculation with B. arachidis and cyanobacteria increased grain productivity by an average of 19% compared to that in the noninoculated control. In this clayey soil with a higher P content, regardless of whether coinoculated with B. arachidis or cyanobacteria or single inoculated, grain productivity was 16% greater on average than that resulting from N fertilizer addition. In conclusion, the success of rhizobial inoculation in groundnuts is dependent on the soil, probably due to P limitation and weather conditions.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahemad, M and Kibret, M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. Journal of King Saud University, Science 26, 120.CrossRefGoogle Scholar
Amatussi, JO, Mógor, Á.F, Cordeiroi, ECN, Mógor, G, Marques, HMC and de Larai, GB (2023) Synergic combination of calcareous algae and cyanobacteria stimulate metabolic alterations improving plant growth and yield. Journal of Applied Phycology 35, 483493.CrossRefGoogle Scholar
Andrade, D.S., Colozzi Filho, A. and Gatti, I. (2014). Microalgas de Águas Continentais: Coleção Ipr de Microalgas. Londrina: IAPAR.Google Scholar
Andrade, DS, Leal, AC, Ramos, ALM and de Goes, KCGP (2015) Growth of Casuarina cunninghamiana inoculated with arbuscular mycorrhizal fungi and Frankia actinomycetes. Symbiosis 66, 6573. https://doi.org/10.1007/s13199-015-0335-1.CrossRefGoogle Scholar
Andrade, DS, Machineski, GS, Lovato, GM, Colozzi, AF, de Goes, KCGP (2014) Inoculação de microalgas em leguminosas e gramíneas. In Andrade, D.S. and Colozzi, F.A. (eds). Microalgas de águas continentais: desafios e potencialidades do cultivo, Londrina: IAPAR, pp. 413438 Google Scholar
Araujo, GS, Santiago, CS, Moreira, RT, Dantas Neto, MP and Fernandes, FAN (2021) Nutrient removal by Arthrospira platensis cyanobacteria in cassava processing wastewater. Journal of Water Process Engineering 40, 101826.CrossRefGoogle Scholar
Asante, M, Ahiabor, BDK and Atakora, WK (2020) Growth, nodulation, and yield responses of groundnut (Arachis hypogaea L.) as influenced by combined application of Rhizobium inoculant and phosphorus in the Guinea Savanna Zone of Ghana. Int. J Agron 2020, 8691757.CrossRefGoogle Scholar
Badawi, FSF, Biomy, AMM and Desoky, AH (2011) Peanut plant growth and yield as influenced by co-inoculation with Bradyrhizobium and some rhizo-microorganisms under sandy loam soil conditions. Ann Agric Sci 56, 1725.CrossRefGoogle Scholar
Bhowmik, D, Dubey, J and Mehra, S (2010) Evaluating potential of Spirulina as innoculant for pulses. Acad J Plant Sci 3, 161164.Google Scholar
Bogino, P, Banchio, E, Rinaudi, L, Cerioni, G, Bonfiglio, C and Giordano, W (2006) Peanut (Arachis hypogaea) response to inoculation with Bradyrhizobium sp. in soils of Argentina. Annals of Applied Biology 148, 207212.CrossRefGoogle Scholar
Bouznif, B, Guefrachi, I, Rodríguez de la Vega, RC, Hungria, M, Mars, M, Alunni, B and Shykoff, JA (2019) Phylogeography of the Bradyrhizobium spp. associated with peanut, Arachis hypogaea: fellow travelers or new associations?. Frontiers in Microbiology 10, 2041.CrossRefGoogle ScholarPubMed
Bremner, J and Keeney, D (1966) Steam distillation methods for determination of ammonium, nitrate and nitrite. Analytica Chimica Acta 32, 482485.Google Scholar
Cardoso, JD, Gomes, DF, Goes, KGP, Fonseca-Junior, NS, Dorigo, OF, Hungria, M and Andrade, DS (2009) Relationship between total nodulation and nodulation at the root crown of peanut, soybean and common bean plants. Soil Biology and Biochemistry 41, 17601763.CrossRefGoogle Scholar
Castro, S, Permigiani, M, Vinocur, M and Fabra, A (1999) Nodulation in peanut (Arachis hypogaea L.) roots in the presence of native and inoculated rhizobia strains. Applied Soil Ecology 13, 3944.CrossRefGoogle Scholar
CONAB (2023) Acompanhamento da Safra Brasileira de Grãos – Safra 2022/23 - Décimo Segundo Levantamento. Brasília, DF: CONAB.Google Scholar
Dineshkumar, R, Kumaravel, R, Gopalsamy, J, Sikder, MNA and Sampathkumar, P (2018) Microalgae as bio-fertilizers for rice growth and seed yield productivity. Waste and Biomass Valorization 9, 793800.CrossRefGoogle Scholar
FAO (2021). “FAO-Food and Agriculture Organization of the United Nations.” FAOSTAT- Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#data/QC (accessed 20 September 2023).Google Scholar
Ferreira, DF (2011) Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia 35, 10391042.CrossRefGoogle Scholar
Figueredo, M, Tonelli, ML, Taurian, T, Angelini, J, Ibanez, F, Valetti, L, Munoz, V, Anzuay, MS, Ludueña, L and Fabra, A (2014) Interrelationships between Bacillus sp. CHEP5 and Bradyrhizobium sp. SEMIA6144 in the induced systemic resistance against Sclerotium rolfsii and symbiosis on peanut plants. J Biosci 39, 877885.CrossRefGoogle ScholarPubMed
Gavilanes, FZ, Amaral, HF, García, MC, Araujo-Junior, CF, Zanão Júnior, LA, Nomura, RBG and Andrade, DS (2021) Interactions between edaphoclimatic conditions and plant–microbial inoculants and their impacts on plant growth, nutrient uptake, and yields. In Maddela, N.R., García Cruzatty, L.C. and Chakraborty, S., (eds). Advances in the Domain of Environmental Biotechnology: Microbiological Developments in Industries, Wastewater Treatment and Agriculture. Singapore: Springer Singapore.Google Scholar
Gavilanes, FZ, Andrade, DS, Zucareli, C, Horácio, EH, Yunes, JS, Barbosa, AP, Ribeiro Alves, LA, Cruzatti, LG, Maddela, NR and de Fátima Guimarães, M (2020) Co-inoculation of anabaena cylindrica with Azospirillum brasilense increases maize grain yield. Rhizosphere 15, 100224.CrossRefGoogle Scholar
Gericó, TG, Tavanti, RFR, de Oliveira, SC, Lourenzani, AEBS, de Lima, JP, Ribeiro, RP, dos Santos, LCC and dos Reis, AR (2020) Bradyrhizobium sp. enhance ureide metabolism increasing peanuts yield. Archives of Microbiology 202, 645656.CrossRefGoogle ScholarPubMed
Horácio, EH, Zucareli, C, Gavilanes, FZ, Yunes, JS, Sanzov, o AW.d.S and Andrade, DS (2020) Co-inoculation of rhizobia, azospirilla and cyanobacteria for increasing common bean production. Semin Cienc Agrar 41, 20152028.CrossRefGoogle Scholar
Jones, DB (1931) Factors for Converting Percentages of Nitrogen in Foods and Feeds into Percentages of Proteins. Washington, D. C.: U.S. Department of Agriculture.Google Scholar
Jovino, RS, da Silva, TR, Rodrigues, RT, de Sá Carvalho, JR, Cunh, a JB.d.A, de Lima, LM, dos Santos, RC, Santos, CE.d.R.e.S, Ribeiro, PR.d.A, de Freitas, ADS, Martins, LMV and Fernandes-Júnior, PI (2022) Elite bradyrhizobium strains boost biological nitrogen fixation and peanut yield in tropical drylands. Brazilian Journal of Microbiology 53, 16231632.CrossRefGoogle ScholarPubMed
Jowkar, A, Bashiri, K and Golmakani, MT (2017) The effect of soil fertilization and foliar spray of semperflorens begonia (Begonia semperflorens) by Spirulina cyanobacterium biomass. J Sci Techn Greenhouse Culture 8, 6574.Google Scholar
Kaschuk, G, Auler, AC, Vieira, CE, Dakora, FD, Jaiswal, SK and da Cruz, SP (2022) Coinoculation impact on plant growth promotion: a review and meta-analysis on coinoculation of rhizobia and plant growth-promoting bacilli in grain legumes. Brazilian Journal of Microbiology 53, 20272037.CrossRefGoogle ScholarPubMed
Kaschuk, G, Nogueira, MA, de Luca, MJ and Hungria, M (2016) Response of determinate and indeterminate soybean cultivars to basal and topdressing N fertilization compared to sole inoculation with Bradyrhizobium . Field Crops Res 195, 2127.CrossRefGoogle Scholar
Kermah, M, Franke, AC, Adjei-Nsiah, S, Ahiabor, BDK, Abaidoo, RC and Giller, KE (2018) N2-fixation and N contribution by grain legumes under different soil fertility status and cropping systems in the Guinea savanna of northern Ghana. Agriculture Ecosystems and Environment 261, 201210.CrossRefGoogle Scholar
Khurshid, S, Zahid, C and Husnain, S (2017) Indoleacetic acid production and chromium reduction by cyanobacteria Synechocystis sp. P2A (chroococcales) immobilized in alginate beads. Biosci j 33, 15921600.CrossRefGoogle Scholar
Lanier, JE, Jordan, DL, Spears, JF, Wells, R and Johnson, PD (2005) Peanut response to inoculation and nitrogen fertilizer. J Agron 97, 7984.CrossRefGoogle Scholar
Li, YH, Wang, R, Zhang, XX, Young, JPW, Wang, ET, Sui, XH and Chen, WX (2015) Bradyrhizobium guangdongense sp. nov. and Bradyrhizobium guangxiense sp. nov., isolated from effective nodules of peanut. Int J Syst Evol 65, 46554661.CrossRefGoogle ScholarPubMed
Melo, JM, Telles, TS, Ribeiro, MR, de Carvalho Junior, O and Andrade, DS (2022) Chlorella sorokiniana as bioremediator of wastewater: nutrient removal, biomass production, and potential profit. Bioresource Technology Reports 17, 100933.CrossRefGoogle Scholar
Moda-Cirino, V, Ribeiro, GP, Buratto, JS, Sou, za SNMD and Jr, NDSF (2015) Oil content and phenotypic stability for grain yield in peanut cultivars. Científica 43, 378387.CrossRefGoogle Scholar
Muñoz, V, Ibañez, F, Tonelli, ML, Valetti, L, Anzuay, MS and Fabra, A (2011) Phenotypic and phylogenetic characterization of native peanut Bradyrhizobium isolates obtained from Córdoba, Argentina. Systematic and Applied Microbiology 34, 446452.CrossRefGoogle ScholarPubMed
Muñoz, V, Ibáñez, F, Tordable, M, Megías, M and Fabra, A (2015) Role of reactive oxygen species generation and Nod factors during the early symbiotic interaction between bradyrhizobia and peanut, a legume infected by crack entry. Journal of Applied Microbiology 118, 182192.CrossRefGoogle ScholarPubMed
Palmero, F, Fernandez, JA, Garcia, FO, Haro, RJ, Prasad, PVV, Salvagiotti, F and Ciampitti, IA (2022) A quantitative review into the contributions of biological nitrogen fixation to agricultural systems by grain legumes. European Journal of Agronomy 136, 126514.CrossRefGoogle Scholar
Pavan, MA, Bloch, MFD, Zempulski, HCD, Miyazawa, M, Zocoler, DC (1992) Manual de Análise Quimica de Solo e Controle de Qualidade. Londrina: IAPAR.Google Scholar
Peoples, MB, Giller, KE, Jensen, ES and Herridge, DF (2021) Quantifying country-to-global scale nitrogen fixation for grain legumes: I. Reliance on nitrogen fixation of soybean, groundnut and pulses. Plant and Soil 469, 114.CrossRefGoogle Scholar
Preyanga, R, Anandham, R, Krishnamoorthy, R, Senthilkumar, M, Gopal, NO, Vellaikumar, A and Meena, S (2021) Groundnut (Arachis hypogaea) nodule Rhizobium and passenger endophytic bacterial cultivable diversity and their impact on plant growth promotion. Rhizosphere 17, 100309.CrossRefGoogle Scholar
Rippka, R, Deruelles, J, Waterbury, JB, Herdman, M and Stanier, RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111, 161.Google Scholar
Santo, s CE.d.R.e.S, da Silva, AF, Silva, VSG.d, Freitas, ADS.d, da Silva, AF, Bezerra, R.d.V, de Lyra, M.d.CCP and Ferreira, J.d.S (2017) Prospecting of efficient rhizobia for peanut inoculation in a Planosol under different vegetation covers. Afr J Microbiol Res 11, 123131.Google Scholar
Singh, R, Parihar, P, Singh, M, Bajguz, A, Kumar, J, Singh, S, Singh, VP and Prasad, SM (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Frontiers in Microbiology 8, 515.CrossRefGoogle ScholarPubMed
Sivalingam, KM (2020) Isolation, identification and evaluation of Spirulina platensis for its effect on seed germination of groundnut (Arachis hypogaea L.), Wolaita Sodo, Southern Ethiopia. J Algal Biomass Util 11, 3442.Google Scholar
Snedecor, GW, Cochran, W (1980) Statistical Methods. Ames: Iowa State University Press.Google Scholar
Soil Survey Staff, US (2014) Keys to Soil Taxonomy. Washington, DC: United States Department of Agriculture Natural Resources Conservation Service.Google Scholar
Supraja, KV, Behera, B and Balasubramanian, P (2020) Performance evaluation of hydroponic system for co-cultivation of microalgae and tomato plant. J Clean Prod 272, 122823.CrossRefGoogle Scholar
Sutherland, DL, McCauley, J, Labeeuw, L, Ray, P, Kuzhiumparambil, U, Hall, C, Doblin, M, Nguyen, LN and Ralph, PJ (2021) How microalgal biotechnology can assist with the UN sustainable development goals for natural resource management. Curr Opin Environ Sustain 3, 100050.CrossRefGoogle Scholar
Taira, H, Baba, J, Togashi, S, Berdiyar, J, Yashima, M and Inubushi, K (2021) Chemical characteristics of degraded soils in Uzbekistan and remediation by cyanobacteria. Nutrient Cycling in Agroecosystems 120, 193203.CrossRefGoogle Scholar
Taurian, T, Anzuay, MS, Ludueña, LM, Angelini, JG, Muñoz, V, Valetti, L and Fabra, A (2013) Effects of single and co-inoculation with native phosphate solubilising strain Pantoea sp J49 and the symbiotic nitrogen fixing bacterium Bradyrhizobium sp SEMIA 6144 on peanut (Arachis hypogaea L.) growth. Symbiosis 59, 7785.CrossRefGoogle Scholar
Torres-Júnior, CV, Leite, J, Santos, CRS, Fernandes Junior, PI, Zilli, JE, Rumjanek, NG and Xavier, GR (2014) Diversity and symbiotic performance of peanut rhizobia from Southeast region of Brazil. Afr J Microbiol Res 8, 566577.Google Scholar
Yaro, RN, Mahama, AR, Kugbe, JX and Berdjour, A (2021) Response of peanut varieties to phosphorus and Rhizobium inoculant rates on Haplic Lixisols of Guinea Savanna Zone of Ghana. Front sustain food syst 5, 616033.CrossRefGoogle Scholar
Supplementary material: File

Andrade et al. supplementary material

Andrade et al. supplementary material
Download Andrade et al. supplementary material(File)
File 386.9 KB