Early nitrogen supplementation stimulates the nodulation and growth of common bean plants inoculated with rhizobium
Resumo
The initial development of common bean plants (Phaseolus vulgaris L.) relying on symbiotic nitrogen (N) can be limited by delayed active N2 fixation, requiring supplemental N which in turn may inhibit the symbiosis. Five experiments were carried out in hydroponics to identify the initiation of nodulation and nitrogenase activity in common bean cultivars, and the effects of additions of mineral N on plant nodulation and growth. Three experiments evaluated the initial growth of five inoculated bean cultivars in the absence or presence of mineral N, and two experiments evaluated the effect of the moment of mineral N addition until the beginning of reproductive stage. The first root nodules appeared 10 days after plant transplant (DAT) and nitrogenase activity initiated 11 DAT. Cultivars of large seeds had lower initial nodulation and nitrogenase activity than those of small seeds. Inoculated plants showed limited shoot growth that lasted until 21-25 DAT as compared to inoculated plants receiving mineral N. Addition of mineral N reduced nodule mass more intensively than nodule number and more strongly nitrogenase activity. Nitrogen applied until 15 DAT enhanced nodulation and nitrogenase activity without limiting shoot growth, as compared to plants receiving N throughout their growth. Otherwise, plants that received N after 15 DAT had lower nodule mass and nitrogenase activity than plants only inoculated. The results indicate that symbiotic N did not suffice to an adequate growth of common beans and some supplemental N is necessary. This N should be added in the beginning of growth cycle to stimulate plant growth without inhibiting further nodulation and N fixation.
Downloads
Referências
Araújo, A. P., Plassard, C., & Drevon, J. J. (2008). Phosphatase and phytase activities in nodules of common bean genotypes at different levels of phosphorus supply. Plant and Soil, 312(1), 129-138. DOI: 10.1007/s11104-008-9595-3
Atkins, C. A., Pate, J. S., Sanford, P. J., Dakora, F. D., & Matthews, I. (1989). Nitrogen nutrition of nodules in relation to ‘N-hunger’ in cowpea (Vigna unguiculata L. Walp). Plant Physiology, 90(4), 1644-1649. DOI: 10.1104/pp.90.4.1644
Barros, R. L. N., Oliveira, L. B., Magalhães, W. B., Médici, O., & Pimentel, C. (2013). Interação entre inoculação com rizóbio e adubação nitrogenada de plantio na produtividade do feijoeiro nas épocas da seca e das águas. Semina: Ciências Agrárias, 34(4), 1443-1450. DOI: 10.5433/1679-0359.2013v34n4p1443
Bitocchi, E., Bellucci, E., Giardini, A., Rau, D., Rodriguez, M., Biagetti, E., ... Papa, R. (2013). Molecular analysis of the parallel domestication of the common bean (Phaseolus vulgaris L.) in Mesoamerica and the Andes. New Phytologist, 197(1), 300-313. DOI: 10.1111/j.1469-8137.2012.04377.x
Bliss, F. A. (1993). Breeding common bean for improved biological nitrogen fixation. Plant and Soil, 152(1), 71-79. DOI: 10.1007/BF00016334
Brito, L. F., Pacheco, R. S., Souza Filho, B. F., Ferreira, E. P. B., Straliotto, R., & Araújo, A. P. (2015). Resposta do feijoeiro comum à inoculação com rizóbio e suplementação com nitrogênio mineral em DOIs biomas brasileiros. Revista Brasileira de Ciência do Solo, 39, 981-992. DOI: 10.1590/01000683rbcs20140322
George, T., & Singleton, P. W. (1992). Nitrogen assimilation traits and dinitrogen fixation in soybean and common bean. Agronomy Journal, 84(6), 1020-1028. DOI: 10.2134/agronj1992.00021962008400060022x
Graham, P. H., Rosas, J. C., Jensen, C. E., Peralta, E., Tlusty, B., Acosta-Gallegos, J., & Pereira, P. A. A. (2003). Addressing edaphic constraints to bean production: the Bean/Cowpea CRSP project in perspective. Field Crops Research, 82(2-3), 179-192.
Guo, R. Q., Silsbury, J. H., & Graham, R. D. (1992) Effect of four nitrogen compounds on nodulation and nitrogen fixation in faba bean, white lupin and medic plants. Australian Journal of Plant Physiology, 19(5), 501-508. DOI: 10.1071/PP9920501
Hardarson, G., Bliss, F. A., Cigales-Rivero, M. R., Henson, R. A., Kipe-Nolt, J. A., Longeri L., … Tsai, S. M. (1993). Genotypic variation in biological nitrogen fixation by common bean. Plant and Soil, 152(1), 59-70.
Hungria, M., Barradas, C. A. A., & Wallsgrove, R. M. (1991). Nitrogen fixation, assimilation and transport during the initial growth stages of Phaseolus vulgaris L. Journal of Experimental Botany, 42, 839-844. DOI: 10.1093/jxb/42.7.839
Hungria, M., Campo, R. J., & Mendes, I. C. (2003). Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biology and Fertility of Soils, 39, 88-93. DOI: 10.1007/s00374-003-0682-6
Imsande, J. (1986). Inhibition of nodule development in soybean by nitrate or reduced nitrogen. Journal of Experimental Botany, 37(3), 348-355. DOI: 10.1093/jxb/37.3.348
Knupp, A. M., Ferreira, E. P. B., & Araújo, A. P. (2017). Variability of nodulation traits in Andean and Mesoamerican common bean gene pools. Pesquisa Agropecuária Brasileira, 52(4), 252-260. DOI: 10.1590/s0100-204x2017000400005
Kumarasinghe, K. S., Danso, S. K. A., & Zapata, F. (1992). Field evaluation of N2 fixation and N partitioning in climbing bean (Phaseolus vulgaris L.) using 15N. Biology and Fertility of Soils, 13, 142-146. DOI: 10.1007/BF00336269
Müller, S. H., & Pereira, P. A. A. (1995). Nitrogen fixation of common bean (Phaseolus vulgaris L.) as affected by mineral nitrogen supply at different growth stages. Plant and Soil, 177, 55-61. DOI: 10.1007/BF00010337
Murray, J. D. (2011). Invasion by invitation: rhizobial infection in legumes. Molecular Plant-Microbe Interactions, 24(6), 631-639. DOI: 10.1094/MPMI-08-10-0181
Nanjareddy, K., Blanco, L., Arthikala, M. K., Affantrange, X. A., Sanchez, F., & Lara, M. (2014). Nitrate regulates rhizobial and mycorrhizal symbiosis in common bean (Phaseolus vulgaris L.). Journal of Integrative Plant Biology, 56(3), 281-298. DOI: 10.1111/jipb.12156
Nova-Franco, B., Íñiguez, L. P., Valdés-López, O., Alvarado-Affantranger, X., Leija, A., Fuentes, S. I., ... Hernández, G. (2015). The Micro-RNA172c-APETALA2-1 node as a key regulator of the common bean-Rhizobium etli nitrogen fixation symbiosis. Plant Physiology, 168, 273-291. DOI: 10.1104/pp.114.255547
Pacheco, R. S., Boddey, R. M., Alves, B. J. R., Ferreira, E. P. B., Straliotto, R., & Araújo, A. P. (2020) Differences in contribution of biological nitrogen fixation to yield performance of common bean cultivars as assessed by the 15N natural abundance technique. Plant and Soil, 454(1-2), 327-341. DOI: 10.1007/s11104-020-04654-6
Pelegrin, R., Mercante, F. M., Otsubo, I. M. N., & Otsubo, A. A. (2009). Resposta da cultura do feijoeiro à adubação nitrogenada e à inoculação com rizóbio. Revista Brasileira de Ciência do Solo, 33(1), 219-226. DOI: 10.1590/S0100-06832009000100023
Ramaekers, L., Galeano, C. H., Garzón, N., Vanderleyden, J., & Blair, M. W. (2013). Identifying quantitative trait loci for symbiotic nitrogen fixation capacity and related traits in common bean. Molecular Breeding, 31(1), 163-180. DOI: 10.1007/s11032-012-9780-1
Reid, D. E., Ferguson, B. J., Hayashi, S., Lin, Y.-H., & Gresshoff, P. M. (2011). Molecular mechanisms controlling legume autoregulation of nodulation. Annals of Botany, 108, 789-795. DOI: 10.1093/aob/mcr205
Rennie, R. J., & Kemp, G. A. (1983). N2-fixation in field beans quantified by 15N isotope dilution. II. Effect of cultivars of beans. Agronomy Journal, 75(4), 645-649. DOI: 10.2134/agronj1983.00021962007500040016x
Saito, A., Tanabata, S., Tanabata, T., Tajima, S., Ueno, M., Ishikawa, S., ... Ohyama, T. (2014). Effect of nitrate on nodule and root growth of soybean (Glycine max (L.) Merr.). International Journal of Molecular Sciences, 15(3), 4464-4480. DOI: 10.3390/ijms15034464
Sexton, P. J., Boote, K. J., White, J. W., & Peterson, C. M. (1997). Seed size and seed growth rate in relation to cotyledon cell volume and number in common bean. Field Crops Research, 54(2-3), 163-172. DOI: 10.1016/S0378-4290(97)00046-4
Singh, S. P., Gepts, P., & Debouck, D. G. (1991). Races of common bean (Phaseolus vulgaris, Fabaceae). Economic Botany, 45, 379-396. DOI: 10.1007/BF02887079
Sprent, J. I., & Thomas, R. J. (1984). Nitrogen utilization of seedling grain legumes: some taxonomic, morphological and physiological constraints. Plant, Cell and Environment, 7(9), 637-645. DOI: 10.1111/1365-3040.ep11571523
Streeter, J. G., & Wong, P. P. (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Critical Reviews in Plant Sciences, 7(1), 1-23. DOI: 10.1080/07352688809382257
Unkovich, M. J., & Pate, J. S. (2000). An appraisal of recent field measurements of symbiotic N2 fixation by annual legumes. Field Crops Research, 65(1-2), 211-228. DOI: 10.1016/S0378-4290(99)00088-X
Vadez, V., Beck, D. P., Lasso, J. H., & Drevon, J. J. (1997). Utilization of the acetylene reduction assay to screen for tolerance of symbiotic N2 fixation to limiting P nutrition in common bean. Physiologia Plantarum, 99(2), 227-232. DOI: 10.1111/j.1399-3054.1997.tb05406.x
Wilker, J., Navabi, A., Rajcan, I., Marsolais, F., Hill, B., Torkamaneh, D., & Pauls, K. P. (2019). Agronomic performance and nitrogen fixation of heirloom and conventional dry bean varieties under low-nitrogen field conditions. Frontiers in Plant Science, 10, 952. DOI: 10.3389/fpls.2019.00952
Witte, C- P. (2011). Urea metabolism in plants. Plant Science, 180(3), 431-438. DOI: 10.1016/j.plantsci.2010.11.01
DECLARAÇÃO DE ORIGINALIDADE E DIREITOS AUTORAIS
Declaro que o presente artigo é original, não tendo sido submetido à publicação em qualquer outro periódico nacional ou internacional, quer seja em parte ou em sua totalidade.
Os direitos autorais pertencem exclusivamente aos autores. Os direitos de licenciamento utilizados pelo periódico é a licença Creative Commons Attribution 4.0 (CC BY 4.0): são permitidos o compartilhamento (cópia e distribuição do material em qualqer meio ou formato) e adaptação (remix, transformação e criação de material a partir do conteúdo assim licenciado para quaisquer fins, inclusive comerciais.
Recomenda-se a leitura desse link para maiores informações sobre o tema: fornecimento de créditos e referências de forma correta, entre outros detalhes cruciais para uso adequado do material licenciado.