Characterisation of nodulation capacity with native rhizobia in germplasm of the under-utilised forage species Macroptilium
Juan Marcelo Zabala
A B * , Lorena Marinoni A B , Nicolas Zuber B C , Laura Viviana Fornasero B and José Pensiero A B
A
B
C
Abstract
The Gran Chaco is a livestock producing region of Argentina with several under-utilised legume forage genetic resources, including species from the genus Macroptilium.
We aimed to generate reliable characterisation and selection schemes in germplasm of Macroptilium for biological nitrogen fixation with native rhizobia, and evaluate the germplasm variability for initial growth and nodulation capacity with native soil of subtropical environment.
The trial evaluated 20 accessions of four Macroptilium species with or without added nitrogen. The variables were analysed through a nested ANOVA with the factor species, accessions nested within species, nitrogen level, and the corresponding interactions. Relationships between variables and accessions were examined using principal component analysis.
There was variability in the symbiotic response and initial growth, and most of the variance was explained by differences between species. Nodulation capacity was related with biological nitrogen fixation, since the accessions with higher nodule number and nodule weight showed higher initial growth and higher crude protein content in shoot.
We found variability for nodulation capacity associated with biological nitrogen fixation within the evaluated germplasm of Macroptilium. In relation to effectiveness, five of 20 accessions evaluated were classified as effective.
Our breeding approach could contribute to develop native legume forage cultivars with better symbiosis with native rhizobia, which would reduce implantation costs and reduce the use of chemical nitrogen fertilisers.
Keywords: forage legume, nitrogen fixation, plant breeding, plant genetic resources, subtropical cattle pastures.
References
Armstrong RD, McCosker K, Johnson SB, et al. (1999) Legume and opportunity cropping systems in central Queensland. 1. Legume growth, nitrogen fixation, and water use. Australian Journal of Agricultural Research 50, 909-924.
| Crossref | Google Scholar |
Batello C, Brinkman R, Mannetje L, Martinez A, Suttie J (2008) Plant genetic resources of forage crops, pasture and Rangelands. Thematic background study. FAO report. Available at https://www.fao.org/fileadmin/templates/agphome/documents/PGR/SoW2/thematicstudy_forage.pdf [Accessed 16 January 2024]
Bell LW, Lawrence J, Johnson B, Peoples MB (2017) New ley legumes increase nitrogen fixation and availability and grain crop yields in subtropical cropping systems. Crop & Pasture Science 68, 11-26.
| Crossref | Google Scholar |
Bianco L (2020) Principales aspectos de la nodulación y fijación biológica de nitrógeno en Fabáceas [Main aspects of the nodulation and biological fixation of nitrogen in Fabáceas]. Idesia 38, 21-29.
| Crossref | Google Scholar |
Borges RO, Antonio RP, da Silva Neto JL, Lira ICSA (2019) Intra- and interspecific genetic divergence in Macroptilium (Benth.) Urb.: a forage option for Brazilian semiarid. Genetic Resources and Crop Evolution 66, 363-382.
| Crossref | Google Scholar |
Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Science 59, 39-46.
| Crossref | Google Scholar |
Bray RA, Woodroffe TD (1994) Macroptilium atropurpureum (DC.) Urban (atro) cv. Aztec. Australian Journal of Experimental Agriculture 34, 121.
| Google Scholar |
Brito KA, Rocha SMB, Antunes JEL, de Araujo Pereira AP, do Nascimento Costa G, de Oliveira Sousa J, Brito da Silva V, Matos Filho CHA, Ferreira Gomes RL, de Almeida Lopes ÂC, Araujo ASF (2023) The lima bean breeding decreases the ability of segregating generations to nodulate with indigenous rhizobia. Rhizosphere 27, 100732.
| Crossref | Google Scholar |
Bromfield ESP, Barran LR (1990) Promiscuous nodulation of Phaseolus vulgaris, Macroptilium atropurpureum, and Leucaena leucocephala by indigenous Rhizobium meliloti. Canadian Journal of Microbiology 36, 369-372.
| Crossref | Google Scholar |
Brummer EC, Barber WT, Collier SM, Cox TS, Johnson R, Murray SC, Olsen RT, Pratt RC, Thro AM (2011) Plant breeding for harmony between agriculture and the environment. Frontiers in Ecology and the Environment 9, 561-568.
| Crossref | Google Scholar |
Byun J, Sheaffer CC, Russelle MP, Ehlke NJ, Wyse DL, Graham PH (2004) Dinitrogen fixation in Illinois bundleflower. Crop Science 44, 493-500.
| Crossref | Google Scholar |
Cameron DG (1985a) Tropical and subtropical legumes 8: Phasey bean (Macroptilium lathyroides). The predecessor of Siratro. Queensland Agricultural Journal 111, 211-214.
| Google Scholar |
Cameron DG (1985b) Tropical and subtropical pasture legumes 5. Siratro (Macroptilium atropurpureum): the most widely planted subtropical legume. Queensland Agricultural Journal 111, 45-49.
| Google Scholar |
CIAT (1988) ‘Legume-rhizobium symbiosis: methods manual for evaluation, selection, and agronomic management.’ p. 178. (CIAT: Cali, Colombia). Available at http://ciat-library.ciat.cgiar.org/articulos_ciat/Digital/SB203.S541_Simbiosis_leguminosa-rizobio_Manual_de_m%C3%A9todos_de_evaluaci%C3%B3n,_selecci%C3%B3n_y_manejo.pdf [Accessed 16 January 2024]
Cooper CS (1977) Growth of the legume seedling. Advances in Agronomy 29, 119-139.
| Crossref | Google Scholar |
Covas G (1978) Forrajeras indígenas: Especies que requieren un plan de conservación de germoplasma [Native forage: species that require a germplasm conservation plan]. Ciencia e Investigación 34, 209-213.
| Google Scholar |
Crews TE, Peoples MB (2004) Legume versus fertilizer sources of nitrogen: ecological tradeoffs and human needs. Agriculture, Ecosystems & Environment 102, 279-297.
| Crossref | Google Scholar |
Crews TE, Carton W, Olsson L (2018) Is the future of agriculture perennial? Imperatives and opportunities to reinvent agriculture by shifting from annual monocultures to perennial polycultures. Global Sustainability 1, e11.
| Crossref | Google Scholar |
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2020) InfoStat versión 2020. Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available at http://www.infostat.com.ar
Durcan R (2023) Investigating soil carbon dynamic along land use change gradients in subtropicaland tropical grazing lands. Doctoral Dissertation, Lancaster University, UK. Available at https://eprints.lancs.ac.uk/id/eprint/185992/ [Accessed 16 January 2024]
FAO (2020) FAOSTAT statistics database. Food and Agriculture Organization of the United Nations, Rome. Available at http://www.fao.org/faostat/en/ [Accessed 16 January 2024]
Fornasero LV, Toniutti MA, Zuber NE (2018) Caracterización fenotípica y genotípica de rizobios simbiontes de Macroptilium erythroloma recuperados de suelos de las provincias de Corrientes y Santa Fe [Phenotypic and genotypic characterization of rhizobia symbionts of Macroptilium erythroloma recovered from soils in the provinces of Corrientes and Santa Fe]. Ciencia del suelo 36, 64-73.
| Google Scholar |
Freitas Costa P, Oliveira Silva A, Azarias Guimarães A, Resende de Assis LL, Rufni M, de Paiva Barbosa L, Soares de Carvalho T, de Souza Moreira FM (2023) Diversity and efficiency of rhizobia from a revegetated area and hotspot-phytophysiognomies affected by iron mining as indicators of rehabilitation and biotechnological potential. Current Microbiology 80, 40.
| Crossref | Google Scholar |
Golluscio R, Faigón A, Tanke M (2006) Spatial distribution of roots and nodules, and δ15N evidence of nitrogen fixation in Adesmia volckmanni, a Patagonian leguminous shrub. Journal of Arid Environments 67, 328-335.
| Crossref | Google Scholar |
Gwata ET, Wofford DS, Pfahler PL, Boot KJ (2004) Genetics of promiscuous nodulation in soybean: nodule dry weight and leaf color score. Journal of Heredity 95, 154-157.
| Crossref | Google Scholar | PubMed |
Hacker JB, Glatzle A, Vanni R (1996) Paraguay – a potential source of new pasture legumes for the subtropics. Tropical Grasslands 30, 273-281.
| Google Scholar |
Hawkins HS, Donald CM (1963) Pasture development in the beef cattle regions of Argentina. Part II. Grass and Forage Science 18, 56-61.
| Crossref | Google Scholar |
Helgadóttir Á, Østrem L, Collins RP, Humphreys M, Marshall A, Julier B, Gastal F, Barre P, Louarn G (2016) Breeding forages to cope with environmental challenges in the light of climate change and resource limitations. In ‘Breeding in a world of scarcity’. (Eds I Roldán-Ruiz, J Baert, D Reheul) pp. 3–13. (Springer Nature: Switzerland)
Hernández-Oaxaca D, Claro-Mendoza KL, Rogel MA, Rosenblueth M, Velasco-Trejo JA, Alarcón-Gutiérrez E, García-Pérez JA, Martínez-Romero J, James EK, Martínez-Romero E (2022) Genomic diversity of Bradyrhizobium from the tree legumes Inga and Lysiloma (Caesalpinioideae-Mimosoid Clade). Diversity 14, 518.
| Crossref | Google Scholar |
Herridge D, Rose I (2000) Breeding for enhanced nitrogen fixation in crop legumes. Field Crops Research 65, 229-248.
| Crossref | Google Scholar |
Jones RM, Rees MC (1997) Evaluation of tropical legumes on clay soils at four sites in southern inland Queensland. Tropical Grasslands 31, 95-106.
| Google Scholar |
Kinyua M, Diogo RVC, Sibomana J, Bolo PO, Gbedjissokpa G, Mukiri J, Mukalama J, Paul B, Sommer R, Kihara J (2019) Green manure cover crops in Benin and Western Kenya - A review. CIAT Publication No. 481. International Center for Tropical Agriculture (CIAT), Nairobi, Kenya. 41 p. Available at https://hdl.handle.net/10568/105923 [Accessed 16 January 2024]
Liu J, Yu X, Qin Q, Dinkins RD, Zhu H (2020) The impacts of domestication and breeding on nitrogen fixation symbiosis in legumes. Frontiers in Genetics 11, 00973.
| Crossref | Google Scholar |
Milford R (1967) Nutritive values and chemical composition of seven tropical legumes and lucerne grown in subtropical south-eastern Queensland. Australian Journal of Experimental Agriculture and Animal Husbandry 7, 540-545.
| Crossref | Google Scholar |
Millar N, Piovia-Scott J, Porter SS (2023) Impacts of domestication on the rhizobial mutualism of five legumes across a gradient of nitrogen-fertilisation. Plant and Soil 491, 479-499.
| Crossref | Google Scholar |
Morales M, Oakley L, Sartori ALB, Mogni VY, Atahuachi M, Vanni RO, Fortunato RH, Prado DE (2019) Diversity and conservation of legumes in the Gran Chaco and biogeograpical inferences. PLoS ONE 14, e0220151.
| Crossref | Google Scholar |
Mosciaro MJ, Calamari NC, Peri PL, Montes NF, Seghezzo L, Ortiz E, Rejalaga L, Barral P, Villarino S, Mastrangelo M, Volante J (2022) Future scenarios of land use change in the Gran Chaco: how far is zero-deforestation? Regional Environmental Change 22, 115.
| Crossref | Google Scholar |
Mpepereki S, Javaheri F, Davis P, Giller KE (2000) Soyabeans and sustainable agriculture: promiscuous soyabeans in southern Africa. Field Crop Research 65, 137-149.
| Crossref | Google Scholar |
Muir JP, Dubeux JCB, Jr, dos Santos MVF, Maposse IC, Pitman WD, Butler TJ (2014) Challenges to domesticating native forage legumes. Tropical Grasslands-Forrajes Tropicales 2, 94-96.
| Crossref | Google Scholar |
Muller KE, Guinness J, Hecking M, Drinkwater LE (2021) Estimating agronomically relevant symbiotic nitrogen fixation in green manure breeding programs. Crop Science 61, 3314-3330.
| Crossref | Google Scholar |
Neves MCP, Hungria M, Sprent JI (1987) The physiology of nitrogen fixation in tropical grain legumes. Critical Reviews in Plant Sciences 6, 267-321.
| Crossref | Google Scholar |
Nichols PGH, Loi A, Nutt BJ, Evans PM, Craig AD, Pengelly BC, Dear BS, Lloyd DL, Revell CK, Nair RM, Ewing MA, Howieson JG, Auricht GA, Howie JH, Sandral GA, Carr SJ, de Koning CT, Hackney BF, Crocker GJ, Snowball R, Hughes SJ, Hall EJ, Foster KJ, Skinner PW, Barbetti MJ, You MP (2007) New annual and short-lived perennial pasture legumes for Australian agriculture—15 years of revolution. Field Crop Research 104, 10-23.
| Crossref | Google Scholar |
Othman MW, Asher CJ (1987) The effects of height and frequency of previous defoliation on nodulation, nitrogen fixation and regrowth of phasey bean [Macroptilium lathyroides]. Pertanika 10, 1-10.
| Google Scholar |
Pensiero JF, Zabala JM, Marinoni LDR, Richard GA (2021) Native and naturalized forage plant genetic resources for saline environments of the southernmost portion of the American Chaco. In ‘Saline and alkaline soils in latin america: natural resources, management and productive alternatives’. (Eds E Taleisnik, R Lavado) pp. 339–380. (Springer: Singapore)
Peoples MB, Herridge DF (1990) Nitrogen fixation by legumes in tropical and subtropical agriculture. Advances in Agronomy 44, 155-223.
| Crossref | Google Scholar |
Pulver EL, Kueneman EA, Ranga-Rao V (1985) Identification of promiscuous nodulating soybean efficient in N2 fixation. Crop Science 25, 660-663.
| Crossref | Google Scholar |
Rebetzke GJ, Jimenez-Berni J, Fischer RA, Deery DM, Smith DJ (2019) Review: High-throughput phenotyping to enhance the use of crop genetic resources. Plant Science 282, 40-48.
| Crossref | Google Scholar | PubMed |
Reiss ER, Drinkwater LE (2022) Promoting enhanced ecosystem services from cover crops using intra-and interspecific diversity. Agriculture, Ecosystems & Environment 323, 107586.
| Crossref | Google Scholar |
Rodríguez-Rodríguez RM, Guimarães AA, de Castro JL, Siqueira JO, Carneiro MAC, de Souza Moreira FM (2021) Rhizobia and endophytic bacteria isolated from rainforest fragments within an iron ore mining site of the Eastern Brazilian Amazon. Brazilian Journal of Microbiology 52, 1461-1474.
| Crossref | Google Scholar | PubMed |
Rose TJ, Kearney LJ, Erler DV, Rose MT, Van Zwieten L, Raymond CA (2018) Influence of growth stage and seed nitrogen on B values and potential contributions to error in estimating biological N2 fixation using the 15N natural abundance method. Plant and Soil 425, 389-399.
| Crossref | Google Scholar |
Rubiales D (2023) Plant breeding is needed to meet agroecological requirements: legume crops as a case study. Outlook on Agriculture 52, 294-302.
| Crossref | Google Scholar |
Santana MA, Pihakaski-Maunsbach K, Sandal N, Marcker KA, Smith AG (1998) Evidence that the plant host synthesizes the heme moiety of leghemoglobin in root nodules. Plant Physiology 116, 1259-1269.
| Crossref | Google Scholar | PubMed |
Schultze-Kraft R, Rao IM, Peters M, Clements RJ, Bai C, Liu G (2018) Tropical forage legumes for environmental benefits: an overview. Tropical Grasslands-Forrajes Tropicales 6, 1-14.
| Crossref | Google Scholar |
Senaratne R, Ratnasinghe DS (1993) Ontogenic variation in nitrogen fixation and accumulation of nitrogen in mungbean, blackgram, cowpea, and groundnut. Biology and Fertility of Soils 16, 125-130.
| Crossref | Google Scholar |
Shelton HM, Franzel S, Peters M (2005) Adoption of tropical legume technology around the world: analysis of success. Tropical Grasslands 39, 198-209.
| Google Scholar |
Stuber CW, Hancock J (2008) Sustaining plant breeding–national workshop. Crop Science 48, 25-29.
| Crossref | Google Scholar |
Thrall PH, Millsom DA, Jeavons AC, Waayers M, Harvey GR, Bagnall DJ, Brockwell J (2005) Seed inoculation with effective root-nodule bacteria enhances revegetation success. Journal of Applied Ecology 42, 740-751.
| Crossref | Google Scholar |
Tobisa M, Nakano Y (2019) Effects of sowing methods and seeding rates on growth and yield characteristics of phasey bean (Macroptilium lathyroides). Grass and Forage Science 74, 696-707.
| Crossref | Google Scholar |
Toniutti MA, Fornasero LV, Trod BS, Zuber NE, Córdoba MS (2015) Caracterización fenotípica y funcional de rizobios noduladores de dos especies del género Macroptilium [Phenotypic and functional characterization of nodulating rhizobia of two Macroptilium species]. FAVE Sección Ciencias Agrarias 14, 107-119.
| Crossref | Google Scholar |
Unkovich MJ, Pate JS (2000) An appraisal of recent field measurements of symbiotic N2 fixation by annual legumes. Field Crops Research 65, 211-228.
| Crossref | Google Scholar |
Vanlauwe B, Hungria M, Kanampiu F, Giller KE (2019) The role of legumes in the sustainable intensification of African smallholder agriculture: lessons learnt and challenges for the future. Agriculture, Ecosystems & Environment 284, 106583.
| Crossref | Google Scholar |
Yuhashi KI, Ichikawa N, Ezura H, et al. (2000) Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Applied and Environmental Microbiology 66, 2658-2663.
| Crossref | Google Scholar |
