FACTORS AFFECTING THE NITROGEN FIXATION IN THE Inga spp.-RHIZOBIA SYSTEM IN SHADE COFFEE PLANTATIONS

Jorge Alejandro Velasco-Trejo, Enrique Alarcón-Gutiérrez, José Antonio García-Pérez, María del Rosario Pineda-López, Norma Flores-Estévez

Abstract


Background. The results of a review on the factors that affect nitrogen fixation in the Inga-café system are presented. The nitrogen contribution that the Inga Miller tree genus provides to shade coffee plantations and the factors that affect its stability in biological nitrogen fixation are scarcely recognized. This work delves into the ecological factors and glyphosate herbicides that can affect the symbiosis of Inga spp. with diazotrophic bacteria in their roots (rhizobia), which form nodules and carry out biological nitrogen fixation. Methodology. Different information sources such as EBSCO, Scopus and Google Schoolar were reviewed, with logical or Boolean data search. 183 papers were used to address the factors that affect the symbiosis between trees of the Inga genus and rhizobia. The findings were organized in: Inga Miller taxonomy, shade coffee plantations with Inga spp., symbiosis between Inga spp. and Bradyrhizobium spp., ecological factors that affect the functioning of the Inga spp.-rhizobia symbiosis and the agrochemical factor: glyphosate herbicide. Results. The genus Inga is recognized as a clade Mimosoideae nested in the subfamily Caesalpinioideae. Shade coffee plantations with Inga are established below 23º N and 30º S, up to 3,100 m.a.s.l. and the symbiont genus is predominantly Bradyrhizobium spp. whose ecological limits of Inga spp-rhizobia were: altitude [988.7-1,381.5 m.a.s.l.], annual precipitation [2,048.4-2,064.36 mm], temperature [20.39-21.93 ºC] and soil pH [4.88-5.42 pH]. Glyphosated herbicides, as an external stimulus, can reduce the benefit of biological nitrogen fixation and erode the soil by keeping it devoid of vegetation. Additionally, some Bradyrhizobium spp. (thiO gene), which oxidizes glyphosate to aminomethylphosphonic acid (AMPA), could be a potential glyphosate degrader in the soil. Implications. Shade coffee plantations with 205-250 trees per hectare of Inga spp. allow fixing around 45 kg of N ha-1 year-1. This review may allow the adoption of new observational or experimental studies of the Inga spp.-rhizobia symbiosis, to approach the performance that favors the biological fixation of nitrogen in shade coffee plantations. Conclusions. The review indicates that there is a specific association between Inga spp. and Bradyrhizobium spp., that ecological factors, including the agronomic management with glyphosated herbicides can decrease nitrogen fixation performance during the symbiosis between Inga spp. and rhizobia. No systematic studies of the symbiosis-environment-agrochemical interaction in shade coffee plantations were found.

Keywords


Fixation of nitrogen; diazotrophs; glyphosate; Ingeae.

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References


Abdel-Wahab, S., 1985. Potassium nitrution and nitrogen fixation by nodulated legumes. Fertilizer Research, 8, pp. 9–20. https://doi.org/10.1007/BF01048903.

Adams, M.A., Simon and J. and Pfautsch, S., 2010. Woody legumes: a (re)view from the South. Tree Physiology, 30, pp. 1072–1082. https://doi.org/10.1093/treephys/tpq061.

Aigang, L., Tianming, W., Shichang and K. and Deqian, P., 2009. On the Relationship between Latitude and Altitude Temperature Effects, in: 2009 International Conference on Environmental Science and Information Application Technology. Presented at the 2009 International Conference on Environmental Science and Information Application Technology, pp. 55–58. https://doi.org/10.1109/ESIAT.2009.335.

Akeel, A. and Jahan, A., 2020. Role of Cobalt in Plants: Its Stress and Alleviation, in: Naeem, M., Ansari, A.A., Gill, S.S. (Eds.), Contaminants in Agriculture: Sources, Impacts and Management. Springer International Publishing, Cham, pp. 339–357. https://doi.org/10.1007/978-3-030-41552-5_17.

Alam, F., Kim, T.Y., Kim, S.Y., Alam, S.S., Pramanik, P., Kim, P.J. and Lee, Y.B., 2015. Effect of molybdenum on nodulation, plant yield and nitrogen uptake in hairy vetch (Vicia villosa Roth). Soil Science and Plant Nutrition, 61, pp. 664–675. https://doi.org/10.1080/00380768.2015.1030690.

Alcantara-de la Cruz, R., Cruz-Hipolito, H., Domíguez-Valenzuela, J. and de Prado, R., 2021. Glyphosate ban in Mexico: potential impacts on agriculture and weed management. Pest Management Science, 77, pp. 3820–3831. https://doi.org/10.1002/ps.6362.

Ali, B., Hayat, S., Hayat, Q. and Ahmad, A., 2010. Cobalt stress affects nitrogen metabolism, photosynthesis and antioxidant system in chickpea (Cicer arietinum L.). Journal of Plant Interactions, 5, pp. 223–231. https://doi.org/10.1080/17429140903370584.

Al-Saedi, S. and Razaq, I., Ali, N., 2016. Effect of Soil Textural Classes on the Biological Nitrogen Fixation by Bradyrhizobium Measured by 15N Dilution Analysis. Baghdad Science Journal, 13, 4, pp. 734-744. https://doi.org/10.21123/bsj.2016.13.4.0734.

Andrews, M. and Andrews, M.E., 2017. Specificity in Legume-Rhizobia Symbioses. International Journal of Molecular Sciences, 18, 705, pp. 1-39. https://doi.org/10.3390/ijms18040705.

Aranjuelo, I., Irigoyen, J.J. and Sánchez-Díaz, M., 2007. Effect of elevated temperature and water availability on CO2 exchange and nitrogen fixation of nodulated alfalfa plants. Environmental and Experimental Botany 59, pp. 99–108. https://doi.org/10.1016/j.envexpbot.2005.10.008.

Ardley, J. and Sprent, J., 2021. Evolution and biogeography of actinorhizal plants and legumes: A comparison. Journal of Ecology, 109, pp. 1098–1121. https://doi.org/10.1111/1365-2745.13600.

Attar, H.A., Blavet, D., Selim, E.M., Abdelhamid, M.T. and Drevon, J.J., 2012. Relationship between phosphorus status and nitrogen fixation by common beans (Phaseolus vulgaris L.) under drip irrigation. International Journal Environment Science and Technology, 9, pp. 1–13. https://doi.org/10.1007/s13762-011-0001-y.

Ávila Bello, C.H. and Zamora Moreno, P., 2010. Producción de hojarasca y materia orgánica en agroecosistemas cafetaleros marginales de Ocotal Chico, Veracruz, México. Polibotánica, pp. 69–87.

Aynalem, B. and Assefa, F., 2017. Effect of Glyphosate and Mancozeb on the Rhizobia Isolated from Nodules of Vicia faba L. and on Their N Fixation, North Showa, Amhara Regional State, Ethiopia. Advances in Biology, 2017, pp. 1–7. https://doi.org/10.1155/2017/5864598.

Babiker, N.N., Babiker, H.M. and Mukhtar, N.O., 2005. Effect of Temperature on in vitro Survival of some Bradyrhizobium Strains. Gezira Journal of Agricultural Science, 3, pp. 117–122.

Bala, A., Murphy, P. and Giller, K.E., 2003a. Distribution and diversity of rhizobia nodulating agroforestry legumes in soils from three continents in the tropics. Molecular Ecology, 12, pp. 917–929. https://doi.org/10.1046/j.1365-294X.2003.01754.x.

Bala, A., Murphy, P., Osunde, A.O. and Giller, K.E., 2003b. Nodulation of tree legumes and the ecology of their native rhizobial populations in tropical soils. Applied Soil Ecology, 22, pp. 211–223. https://doi.org/10.1016/S0929-1393(02)00157-9.

Banks, M.L., Kennedy, A.C., Kremer, R.J. and Eivazi, F., 2014. Soil microbial community response to surfactants and herbicides in two soils. Applied Soil Ecology, 74, pp. 12–20. https://doi.org/10.1016/j.apsoil.2013.08.018.

Barrera-Cataño, J.I. and Valdés-López, C., 2007. Herramientas para la restauración ecológica de áreas disturbadas en Colombia. Universitas Scientiarum, 12, 15, pp. 11-24.

Barron, A.R., Purves, D.W. and Hedin, L.O., 2011. Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia, 165, pp. 511–520. https://doi.org/10.1007/s00442-010-1838-3.

Bellamy, A.S., 2011. Weed control practices on Costa Rican coffee farms: is herbicide use necessary for small-scale producers? Agriculture and Human Values, 28, pp. 167–177. https://doi.org/10.1007/s10460-010-9261-2.

Benbrook, C.M., 2016. Trends in glyphosate herbicide use in the United States and globally. Enviromental Sciencie Europe, 28, pp. 2–15.

Bianco, L., 2020. Principales aspectos de la nodulación y fijación biológica de nitrógeno en Fabáceas. Idesia, 38, pp. 21–29. https://doi.org/10.4067/S0718-34292020000200021.

Blanco, S.R. and Aguilar-Carrillo, A., 2015. Soil erosion and erosion thresholds in an agroforestry system of coffee (Coffea arabica) and mixed shade trees (Inga spp and Musa spp) in Northern Nicaragua. Agriculture, Ecosystems and Environment, 210, pp. 25–35. https://doi.org/10.1016/j.agee.2015.04.032.

Bolanos, L., Brewin, N.J. and Bonilla, I., 1996. Effects of Boron on Rhizobium-Legume Cell-Surface Interactions and Nodule Development. Plant Physiology, 110, pp. 1249–1256. https://doi.org/10.1104/pp,110.4.1249.

Boumahdi, M., Mary, P. and Hornez, J.-P., 1999. Influence of growth phases and desiccation on the degrees of unsaturation of fatty acids and the survival rates of rhizobia. Journal of Applied Microbiology, 87, pp. 611–619. https://doi.org/10.1046/j.1365-2672.1999.00860.x.

Brewbaker, J.L., 1987. Leucaena: a multipurpose tree genus for tropical agroforestry, in: Nair, P.K.R., Steppler, H.A. (Eds.), Agroforestry, a Decade of Development. International Council for Research in Agroforestry, Nairobi, pp. 289–323.

Caltran, M.E., 2012. Potencial de fixação de nitrogênio por leguminosas noduladas e cianobactérias terrestres na mata atlântica, sp. Universidade Estadual de Campinas, Campinas, Brasil. 85 p.

Cannavo, P., Sansoulet, J., Harmand, J.-M., Siles, P., Dreyer, E. and Vaast, P., 2011. Agroforestry associating coffee and Inga densiflora results in complementarity for water uptake and decreases deep drainage in Costa Rica. Agriculture, Ecosystems & Environment, 140, pp. 1–13. https://doi.org/10.1016/j.agee.2010.11.005

Capitán, G.C., Ávila-Bello, C.H.´and González, F.D.L., 2014. Structure and tree diversity in traditional Popoluca coffee agroecosystems in the los Tuxtlas Biosphere Reserve, Mexico. Interciencia, 39, 9, pp. 608-619.

Cardoso, E.J.B.N., Gonçalves, J.L. de M., Balieiro, F. de C. and Franco, A.A. (Eds.), 2020. Mixed Plantations of Eucalyptus and Leguminous Trees: Soil, Microbiology and Ecosystem Services. Springer International Publishing, Cham. 269 p. https://doi.org/10.1007/978-3-030-32365-3.

Castañeda Camacho, A.C., 2014. Diseño de una metodología para evaluar el estado de los servicios ecosistémico. Universidad Militar Nueva Granada: Especialización en Planeación ambiental y gestión Integral de los Recursos Naturales, pp. 1-19.

Catoira, R., Galera, C., de Billy, F., Penmetsa, R.V., Journet, E.-P., Maillet, F., Rosenberg, C., Cook, D., Gough, C. and Dénarié, J., 2000. Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway. The Plant Cell, 12, pp. 1647–1665. https://doi.org/10.1105/tpc.12.9.1647

Cerda, R., Allinne, C., Gary, C., Tixier, P., Harvey, C.A., Krolczyk, L., Mathiot, C., Clément, E., Aubertot, J.-N. and Avelino, J., 2017. Effects of shade, altitude and management on multiple ecosystem services in coffee agroecosystems. European Journal of Agronomy, 82, pp. 308–319. https://doi.org/10.1016/j.eja.2016.09.019.

Cerdán, C.R., Rebolledo, M.C., Soto, G., Rapidel, B. and Sinclair, F.L., 2012. Local knowledge of impacts of tree cover on ecosystem services in smallholder coffee production systems. Agricultural Systems, 110, pp. 119–130. https://doi.org/10.1016/j.agsy.2012.03.014.

Ceroni Stuva, A., 2003. Distribución de las leguminosas de la parte alta de la cuenca La Gallega. Morropón. Piura. Ecología Aplicada, 2, pp. 9–13.

Charbonnier, F., Roupsard, O., le Maire, G., Guillemot, J., Casanoves, F., Lacointe, A., Vaast, P., Allinne, C., Audebert, L., Cambou, A., Clément-Vidal, A., Defrenet, E., Duursma, R.A., Jarri, L., Jourdan, C., Khac, E., Leandro, P., Medlyn, B.E., Saint-André, L., Thaler, P., Van Den Meersche, K., Barquero Aguilar, A., Lehner, P. and Dreyer, E., 2017. Increased light-use efficiency sustains net primary productivity of shaded coffee plants in agroforestry system. Plant, Cell & Environment 40, pp. 1592–1608. https://doi.org/10.1111/pce.12964.

Corby, H.D.L., 1988. Types of rhizobial nodules and their distribution among the leguminosae. Kirkia, 13, pp. 53–123. http://www.jstor.org/stable/23502364.

da Silva, A., Franzini, V.I., Piccolla, C.D. and Muraoka, T., 2017. Molybdenum supply and biological fixation of nitrogen by two Brazilian common bean cultivars. Revista Brasileira de Ciência do Solo, 21, pp. 100–105. https://doi.org/10.1590/1807-1929/agriambi.v21n2p100-105.

de Almeida, C. and Viani, R.A.G., 2019. Selection of shade trees in forest restoration plantings should not be based on crown tree architecture alone: Shade trees for tropical forest restoration. Restoration Ecology, 27, pp. 832–839. https://doi.org/10.1111/rec.12930.

de Silva, K., De Meyer, S.E., Rouws, L.F.M., Farias, E.N.C., dos Santos, M.A.O., O’Hara, G., Ardley, J.K., Willems, A., Pitard, R.M. and Zilli, J.E., 2014. Bradyrhizobium ingae sp. nov., isolated from effective nodules of Inga laurina grown in Cerrado soil. International Journal of Systematic and Evolutionary Microbiology, 64, pp. 3395–3401. https://doi.org/10.1099/ijs.0.063727-0.

de Sousa, K., Zonneveld, M., Casanoves, F., Kindt and R., Ordonez, J.C., 2017. Suitability of key Central American agroforestry species under future climates: an Atlas. ICRAF. 257 p.

dos Santos, E.R.M., 2010. Diversidade de bactérias em nódulos de Inga vera willd. (leguminosae- mimosoideae) do sul da Bahia. (M .Sc.). UNIVERSIDA DE ESTADUAL DE SANTA CRUZ, Ilhéus, Bahía, Brasil. 269 p.

dos Santos, P.C., Fang, Z., Mason, S.W., Setubal, J.C., Dixon, R., 2012. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics, 13, pp. 162. https://doi.org/10.1186/1471-2164-13-162.

Downie, J.A., 2014. Legume nodulation. Current Biology, 24, pp. 184–190. https://doi.org/10.1016/j.cub.2014.01.028.

Du, M., Gao, Z., Li, X., Liao, H., 2020. Excess nitrate induces nodule greening and reduces transcript and protein expression levels of soybean leghaemoglobins. Annals of Botany, pp. 1-12. https://doi.org/10.1093/aob/mcaa002.

Dupont, L., Alloing, G., Pierre, O., El, S., Hopkins, J., Hrouart, D., Frendo, P., 2012. The Legume Root Nodule: From Symbiotic Nitrogen Fixation to Senescence, in: Nagata, T. (Ed.), Senescence. InTech. 850 p https://doi.org/10.5772/34438.

Durand-Bessart, C., Tixier, P., Quinteros, A., Andreotti, F., Rapidel, B., Tauvel, C. and Allinne, C., 2020. Analysis of interactions amongst shade trees, coffee foliar diseases and coffee yield in multistrata agroforestry systems. Crop Protection, 133, pp.105137. https://doi.org/10.1016/j.cropro.2020.105137

Escamilla, P.E., Licona Vargas, A., Díaz Cardenas, S., Santoyo Cortés, H., Sosa, R. and Rodríguez Ramírez, L., 1994. Los Sistemas de Producción de Café en el Centro de Veracruz, México. Un Análisis Tecnológico. Revista de Historia, 30, pp. 41–67.

Farfan-Valencia, F., 2014. Agroforestería y sistemas agroforestales con café. Manizales (Colombia). Cenicafé. 342 p. https://biblioteca.cenicafe.org/handle/10778/4213.

Faria, S.M. de, Diedhiou, A., de Lima, H.C., Ribeiro, R.D., Galiana, A., Castilho and A.F. and Henriques, J.C., 2010. Evaluating the Nodulation Status of Leguminous Species from the Amazonian Forest of Brazil. Journal of Experimental Botany, 61, pp. 3119–3127. https://doi.org/10.1093/jxb/erq142.

Faria, S.M. de, Lewis, G.P., Sprent, J.I. and Sutherland, J.M., 1989. Occurrence of nodulation in the Leguminosae. New Phytologist 111, pp. 607–619. https://doi.org/10.1111/j.1469-8137.1989.tb02354.x.

Faria, S.M. de and Silva, U.E. de, 2007. Indicação de estirpes de rizóbio eficientes na fixação biológica de nitrogênio para espécies de uso múltiplo, atualização ano base 2006. Embrapa Agrobiologia 228, pp. 10–16.

Fauth, J.E., 1997. Working toward Operational Definitions in Ecology: Putting the System Back into Ecosystem. Bulletin of the Ecological Society of America, 78, pp. 295–297.

Ferguson, B.J., Lin, M.-H. and Gresshoff, P.M., 2013. Regulation of legume nodulation by acidic growth conditions. Plant Signaling & Behavior, 8, pp. e23426-1-e23426-5. https://doi.org/10.4161/psb.23426.

Fernández-Pascual, M., 2002. Fijación biológica de nitrógeno: factores limitantes. Ciencia y Medio Ambiente, pp. 195–202.

Ferreira González, I., Urrútia, G. and Alonso-Coello, P., 2011. Revisiones sistemáticas y meta-análisis: bases conceptuales e interpretación. Revista Española de Cardiología. 64, pp. 688–696. https://doi.org/10.1016/j.recesp.2011.03.029.

Ferreira, T.C., Aguilar, J.V., Souza, L.A., Justino, G.C., Aguiar, L.F. and Camargos, L.S., 2016. pH effects on nodulation and biological nitrogen fixation in Calopogonium mucunoides. Brazilian Journal and Botany 39, 1015–1020. https://doi.org/10.1007/s40415-016-0300-0.

Fonseca, M.B., Peix, A., Faria, S.M.D., Mateos, P.F., Rivera, L.P., Simões-araujo, J.L., Giovanni, M., Mary, R., Isaias, S., Cruz, C., Scotti, M.R., Sprent, J.I. and James, E.K., 2012. Nodulation in Dimorphandra wilsonii Rizz. (Caesalpinioideae), a Threatened Species Native to the Brazilian Cerrado. Plos One, 7, pp. e495 20. http://doi.org/10.1371/journal.pone.0049520 .

Fonseca, S.A., 2006. El café de sombra: un ejemplo de pago de servicios ambientales para proteger la biodiversidad. Gaceta Ecológica, pp. 19–31. http://www.redalyc.org/articulo.oa?id=53908002.

Franco, A.A. and De Faria, S.M., 1997. The contribution of N2-fixing tree legumes to land reclamation and sustainability in the tropics. Soil Biology and Biochemistry, International Symposium - Sustainable Agriculture for the Tropics: The Role of Biological Nitrogen Fixation, 29, pp. 897–903. https://doi.org/10.1016/S0038-0717(96)00229-5.

Friis, I., Balslev, H. and Selskab, K.D. 2005. Plant Diversity and Complexity Patterns: Local, Regional and Global Dimensions: Proceedings of an International Symposium Held at the Royal Danish Academy of Sciences and Letters in Copenhagen, Denmark, 25-28 May, 2003. Kgl. Danske Videnskabernes Selskab. 622 p.

Fujita, K., Ofosu-Budu, K.G. and Ogata, S., 1992. Biological nitrogen fixation in mixed legume-cereal cropping systems. Plant Soil, 141, pp. 155–175. https://doi.org/10.1007/BF00011315.

Gage, D.J., 2004. Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes. Microbiology and Molecular Biology Reviews, 68, pp. 280–300. https://doi.org/10.1128/MMBR.68.2.280-300.2004.

García-Pérez, J.A., Alarcón-Gutiérrez, E., Perroni, Y. and Barois, I., 2014. Earthworm communities and soil properties in shaded coffee plantations with and without application of glyphosate. Applied Soil Ecology 83, pp. 230–237. https://doi.org/10.1016/j.apsoil.2013.09.006.

Garza-Lau, R., Maldonado-Torres, R., Álvarez-Sánchez, M.E. and Torres-Rivera, J.A., 2020. Caracterización de especies arbóreas asociadas al cultivo de café. Remexca, 11, pp. 25–32. https://doi.org/10.29312/remexca.v11i1.2210.

Geurts, R. and Franssen, H., 1996. Signal Transduction in Rhizobium-lnduced Nodule Formation. Plant Physiology, 112, pp. 447–453.

Góes, G.S., Gross, E., Brito-Rocha, E. and Mielke, M.S., 2015. Efeitos da inoculação com bactérias diazotróficas e da adubação nitrogenada no crescimento e na qualidade de mudas de Inga laurina (SW.) Willd. (Fabaceae). Revista Árvore, 39, pp. 1031–1038. https://doi.org/10.1590/0100-67622015000600005.

Gómez-Martínez, M.J., Diaz-Padilla, G., Charbonnier, F., Sánchez-Viveros, G. and Cerdán-Cabrera, C.R., 2018. Ensambles arbóreos en sistemas agroforestales cafetaleros con diferente intensidad de manejo en Veracruz, México. Revista de Ciencias Ambientales, 52, 16, pp. 16-38. https://doi.org/10.15359/rca.52-2.2.

Graham, P.H., 1992. Stress tolerance in Rhizobium and Bradyrhizobium and nodulation under adverse soil conditions. Canadian Journal of Microbiology, 38, pp. 475–484. https://doi.org/10.1139/m92-079.

Graham, P.H., Draeger, K.J., Ferrey, M.L., Conroy, M.J., Hammer, B.E., Martinez, E., Aarons, S.R. and Quinto, C., 1994. Acid pH tolerance in strains of Rhizobium and Bradyrhizobium and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Canadian Journal of Microbiology, 40, pp. 198–207. https://doi.org/10.1139/m94-033.

Gross, J. and Bhattacharya, D., 2009. Mitochondrial and plastid evolution in eukaryotes: an outsiders’ perspective. Nature Reviews Genetics, 10, pp. 495–505. https://doi.org/10.1038/nrg2610.

Grossman, J.M., Sheaffer, C., Wyse, D., Bucciarelli, B., Vance, C. and Graham, P.H., 2006. An assessment of nodulation and nitrogen fixation in inoculated Inga oerstediana, a nitrogen-fixing tree shading organically grown coffee in Chiapas, Mexico. Soil Biology and Biochemistry, 38, pp. 769–784. https://doi.org/10.1016/j.soilbio.2005.07.009.

Guijarro, K.H., Aparicio, V., De Gerónimo, E., Castellote, M., Figuerola, E.L., Costa, J.L. and Erijman, L., 2018. Soil microbial communities and glyphosate decay in soils with different herbicide application history. Science of The Total Environment, 634, pp. 974–982. https://doi.org/10.1016/j.scitotenv.2018.03.393.

Gyaneshwar, P., Hirsch, A.M., Moulin, L., Chen, W.-M., Elliott, G.N., Bontemps, C., Estrada-de los Santos, P., Gross, E., dos Reis, F.B., Sprent, J.I., Young, J.P.W. and James, E.K., 2011. Legume-Nodulating Betaproteobacteria: Diversity, Host Range and Future Prospects. Molecular Plant-Microbe Interactions, 24, pp. 1276–1288. https://doi.org/10.1094/MPMI-06-11-0172.

Hafeez, F.Y., Shah, N.H. and Malik, K.A., 2000. Field evaluation of lentil cultivars inoculated with Rhizobium leguminosarum bv. viciae strains for nitrogen fixation using nitrogen-15 isotope dilution. Biology and Fertility of Soils, 31, pp. 65–69. https://doi.org/10.1007/s003740050625.

Haggar, J., Medina, B., Aguilar, R.M. and Munoz, C., 2013. Land Use Change on Coffee Farms in Southern Guatemala and its Environmental Consequences. Environmental Management, 51, pp. 811–823. https://doi.org/10.1007/s00267-013-0019-7.

Hala, K., Gad, N. and Abdelhamid, M., 2013. Effects of Different Rates of Phosphorus and Molybdenum Application on Two Varieties Common Bean of (Phaseolus vulgaris L.). Journal of Agriculture and Food Technology, 3, pp. 8–16.

Hedin, L.O., Brookshire, E.N.J., Menge, D.N.L. and Barron, A.R., 2009. The Nitrogen Paradox in Tropical Forest Ecosystems. Annual Review of Ecology, Evolution and Systematics, 40, pp. 613–635. https://doi.org/10.1146/annurev.ecolsys.37.091305.110246.

Hergoualc’h, K., Blanchart, E., Skiba, U., Hénault, C. and Harmand, J.-M., 2012. Changes in carbon stock and greenhouse gas balance in a coffee (Coffea arabica) monoculture versus an agroforestry system with Inga densiflora, in Costa Rica. Agriculture, Ecosystems and Environment, 148, pp. 102–110. https://doi.org/10.1016/j.agee.2011.11.018.

Hernández, G., De Gerónimo, E. and Erijman, L., 2021. Glyphosate Biodegradation Potential in Soil Based on Glycine Oxidase Gene (thiO) from Bradyrhizobium. Current Microbiology, 78, pp. 1991–2000. https://doi.org/10.1007/s00284-021-02467-z.

Hernandez, V.E., Campos, A.G., Enriquez, del V.J., Rodriguez-Ortiz, G. and Velasco, A., 2012. Captura de carbono por Inga jinicuil Schltdl: En un sistema agroforestal de café bajo sombra. Revista Mexicana de Ciencias Forestales, 3, pp. 11–21.

Hernández-Sanchez, M.I. and Nava-Tablada, M.E., 2018. Cafeticultura en áreas naturales protegidas. el caso del sitio RAMSAR “Cascadas de Texolo y su entorno” en Veracruz, México. Agro Productividad, Innovaciones Tecnológicas en la Producción de Planta de Café, 11, pp. 3–8.

Herridge, D.F., Peoples, M.B. and Boddey, R.M., 2008. Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil, 311, pp. 1–18. https://doi.org/10.1007/s11104-008-9668-3.

Hobbie, S.E., 1992. Effects of plant species on nutrient cycling. Trends in Ecology & Evolution 7, pp. 336–339. https://doi.org/10.1016/0169-5347(92)90126-V.

Hungria, M. and Franco, A.A., 1993. Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant Soil, 149, pp. 95–102. https://doi.org/10.1007/BF00010766.

Hungria, M. and Stacey, G., 1997. Molecular signals exchanged between host plants and rhizobia: Basic aspects and potential application in agriculture. Soil Biology and Biochemistry, International Symposium - Sustainable Agriculture for the Tropics: The Role of Biological Nitrogen Fixation, 29, pp. 819–830. https://doi.org/10.1016/S0038-0717(96)00239-8.

Hussain, K., Islam, M., Siddique, M.T., Hayat, R. and Mohsan, S., 2011. Soybean Growth and Nitrogen Fixation as Affected by Sulfur Fertilization and Inoculation under Rainfed Conditions in Pakistan. International Journal of Agriculture & Biology, 13, pp. 951–955.

INIFAP, 2017. Agenda Técnica Agrícola Veracruz. INIFAP, Ciudad de México. 191 p.

Innan, H. and Kim, Y., 2004. Pattern of polymorphism after strong artificial selection in a domestication event. Proceedings of the National Academy of Sciences 101, pp. 10667–10672. https://doi.org/10.1073/pnas.0401720101.

Islam, M., Mohsan, S. and Ali, S., 2012. Effect of different phosphorus and sulfur levels on nitrogen fixation and uptake by chickpea (Cicer arietinum L.). Agrociencia 46, pp. 1–12.

Izaguirre, M.L., 2005. Distribución geográfica, nodulación y comportamiento agronómico de tres especies de Sesbania nativas de zonas inundables en Venezuela. Agronomía Tropical, 55, 1, pp. 63-82. http://ve.scielo.org/scielo.php?script=sci_abstract&pid=S0002-192X2005000100004&lng=es&nrm=iso&tlng=es

Justino, G., Omena-Garcia, R., dos Santos, A., de Camargos, L., Sodek, L. and Gonçalves, J., 2017. Nitrogen used strategies of nodulated amazonian legume: Inga edulis. Journal of Tropical Forest Science 29, pp. 1–9.

Kanmegne, J., Bayomock, L.A., Degrande, A., Asaah, E. and Duguma, B., 2003. Establishment of Inga edulis and Calliandra calothyrsus in improved fallow systems in southern Cameroon. Agroforestry Systems, 58, pp. 119–124. https://doi.org/10.1023/A:1026088303184.

Karanja, N.K. and Wood, M., 1988. Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya: Tolerance of high temperature and antibiotic resistance. Plant Soil, 112, pp. 15–22. https://doi.org/10.1007/BF02181747.

Kemppinen, J., Niittynen, P., Riihimäki, H. and Luoto, M., 2018. Modelling soil moisture in a high-latitude landscape using LiDAR and soil data. Earth Surface Processes and Landforms, 43, pp. 1019–1031. https://doi.org/10.1002/esp.430.

Kessel, C.V., Roskoski, J.P., Wood, T. and Montano, J., 1983. 15N2 Fixation and H2 Evolution by Six Species of Tropical Legumious Trees. Plant Physiology, 72, pp. 909–910.

Kiss, S.A., Stefanovits-Bányai, E. and Takács-Hájos, M., 2004. Magnesium-Content of Rhizobium Nodules in Different Plants: The Importance of Magnesium in Nitrogen-Fixation of Nodules. Journal of the American College of Nutrition, 23, pp. 751S-753S. https://doi.org/10.1080/07315724.2004.10719422.

Klinger, C.R., Lau, J.A. and Heath, K.D., 2016. Ecological genomics of mutualism decline in nitrogen-fixing bacteria. Proceedings of the Royal Society B: Biological Sciences, 283, pp. 20152563-1-20152563-9. https://doi.org/10.1098/rspb.2015.2563.

Kobe, R., 1999. Light Gradient Partitioning among Tropical Tree Species through Differential Seedling Mortality and Growth. Ecology, 80, pp. 187–201. https://doi.org/10.1890/0012-9658(1999)080[0187:LGPATT]2.0.CO;2.

Krouma, A., Drevon, J.-J. and Abdelly, C., 2006. Genotypic variation of N2-fixing common bean (Phaseolus vulgaris L.) in response to iron deficiency. Journal of Plant Physiology 163, pp. 1094–1100. https://doi.org/10.1016/j.jplph.2005.08.013.

Lawrence, A., Pennington, T.D., Toby, D., Hands, M.R., Michel, R. and Zuñiga, A., 1994. Inga: high diversity in the neotropics; Nitrogen fixing trees for acid soils; proceedings. Presented at the Workshop on Nitrogen Fixing Trees for Acid Soils, Morrilton, Ark. (EUA). 1995., Turrialba, C.R., pp. 130-141.

Lawson, I.Y.D., Muramatsu, K. and Nioh, I., 1995. Effect of organic matter on the growth, nodulation and nitrogen fixation of soybean grown under acid and saline conditions. Soil Science and Plant Nutrition, 41, pp. 721–728. https://doi.org/10.1080/00380768.1995.10417022.

Leblanc, H.A., McGraw, R.L. and Nygren, P., 2007. Dinitrogen-fixation by three neotropical agroforestry tree species under semi-controlled field conditions. Plant Soil, 291, pp. 199–209. https://doi.org/10.1007/s11104-006-9186-0.

Leblanc, H.A., McGraw, R.L., Nygren, P. and Roux, C.L., 2005. Neotropical Legume Tree Inga edulis Forms N2-fixing Symbiosis with Fast-growing Bradyrhizobium Strains. Plant Soil, 275, pp. 123–133. https://doi.org/10.1007/s11104-005-0808-8.

Leblanc, H.A., Nygren, P. and McGraw, R.L., 2006. Green mulch decomposition and nitrogen release from leaves of two Inga spp. in an organic alley-cropping practice in the humid tropics. Soil Biology and Biochemistry, 38, pp. 349–358. https://doi.org/10.1016/j.soilbio.2005.05.012.

Liu, C.-W. and Murray, J.D., 2016. The Role of Flavonoids in Nodulation Host-Range Specificity: An Update. Plants, 5, pp. 33. https://doi.org/10.3390/plants5030033.

López, L.F.A. and Mora, J.M., 2006. Factores estructurales, bioquímicos y moleculares de la simbiosis Bradyrhizobium sp. (Lupinus)-Lupinus. Anual de Revista Academica Nacional Farmaceutica, 72, pp. 423–442.

López-Gómez, A.M., Williams-Linera, G. and Manson, R.H., 2008. Tree species diversity and vegetation structure in shade coffee farms in Veracruz, Mexico. Agriculture, Ecosystems & Environment, 124, pp. 160–172. https://doi.org/10.1016/j.agee.2007.09.008.

López-Rodríguez, G., Sotomayor-Ramírez, D., Amador, J.A. and Schröder, E.C., 2015. Contribution of nitrogen from litter and soil mineralization to shade and sun coffee (Coffea arabica L.) agroecosystems. Tropical Ecology, 56, pp. 155–167.

LPWG, 2017. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny – The Legume Phylogeny Working Group (LPWG). Phylogeny and classification of the Leguminosae 66, pp. 44–77. https://doi.org/10.12705/661.3.

Mamani-Pati, F., Clay, D.E., Clay, S.A., Smeltekop, H. and Yujra-Callata, M.A., 2012. The Influence of Strata on the Nutrient Recycling within a Tropical Certified Organic Coffee Production System. International Scholarly Research Network Agronomy, 2012, pp. e389290-1- e389290-8. https://doi.org/10.5402/2012/389290.

Manson, R.H., 2008. Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación. Instituto Nacional de Ecología. 349 p.

Maqueda, C., Undabeytia, T., Villaverde, J. and Morillo, E., 2017. Behaviour of glyphosate in a reservoir and the surrounding agricultural soils. Science of The Total Environment, 593–594, pp. 787–795. https://doi.org/10.1016/j.scitotenv.2017.03.202.

Marchetti, M.M., Pires Santos, J.C. and Baratto, C.M., 2017. Caracterização de bactérias em nódulos de leguminosas arbóreas de fragmentos da floresta ombrófila mista. Scientia Agraria, 18, pp. 50. https://doi.org/10.5380/rsa.v18i4.51383.

María de las Heras, N. de, 2006. Efecto del glifosato sobre la simbiosis “lupinus albus-bradyrhizobium” SP. (“lupinus”). [Universidad Complutense], Servicio de Publicaciones, Madrid. 199 p.

Martínez-Romero, E. and Caballero-Mellado, J., 1996. Rhizobium Phylogenies and Bacterial Genetic Diversity. Critical Reviews in Plant Sciences, 15, pp. 113–140. https://doi.org/10.1080/07352689.1996.10393183.

Martins da Costa, E., Azarias Guimarães, A., Soares de Carvalho, T., Louzada Rodrigues, T., de Almeida Ribeiro, P.R., Lebbe, L., Willems, A. and de Souza Moreira, F.M., 2018. Bradyrhizobium forestalis sp. nov., an efficient nitrogen-fixing bacterium isolated from nodules of forest legume species in the Amazon. Archives of Microbiology, 200, pp. 743–752. https://doi.org/10.1007/s00203-018-1486-2.

Martins da Costa, E., de Lima, W., de Almeida Ribeiro, P.R. and de Souza Moreira, F.M., 2021. Acid and high-temperature tolerant Bradyrhizobium spp. strains from Brazilian soils are able to promote Acacia mangium and Stizolobium aterrimum growth. Symbiosis, 83, pp. 65–78. https://doi.org/10.1007/s13199-020-00732-6.

Mary, P., Ochin, D. and Tailliez, R., 1985. Rates of Drying and Survival of Rhizobium meliloti Strains During Storage at Different Relative Humidities. Applied and Environmental Microbiology, 50, pp. 207–211. https://doi.org/10.1128/AEM.50.2.207-211.1985.

Massot, F., Gkorezis, P., Van Hamme, J., Marino, D., Trifunovic, B.S., Vukovic, G., d’Haen, J., Pintelon, I., Giulietti, A.M., Merini, L., Vangronsveld, J. and Thijs, S., 2021. Isolation, Biochemical and Genomic Characterization of Glyphosate Tolerant Bacteria to Perform Microbe-Assisted Phytoremediation. Frontiers in Microbiology 11, pp. 598507-1-598507-19. https://doi.org/10.3389/fmicb.2020.598507

Melgarejo, V., Bautista, S. and Camargo, M., 2020. Challenges and trends in the valuation of ecosystem services in agro-ecosystems: a systematic revision. Tropical and Subtropical Agroecosystems, 23, 3, pp. 1-32.

Menge, D.N.L. and Crews, T.E., 2016. Can evolutionary constraints explain the rarity of nitrogen-fixing trees in high-latitude forests? New Phytologist, 211, pp. 1195–1201. https://doi.org/10.1111/nph.14080.

Menge, D.N.L., Lichstein, J.W. and Ángeles-Pérez, G., 2014. Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. Ecology, 95, pp. 2236–2245. https://doi.org/10.1890/13-2124.1.

Mengel, K. and Viro, M., 1974. Effect of Potassium Supply on the Transport of Photosynthates to the Fruits of Tomatoes (Lycopersicon esculentum). Physiology Plant, 30, pp. 295–300. https://doi.org/10.1111/j.1399-3054.1974.tb03660.x.

Menna, P. and Hungria, M., 2011. Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin and spread and maintenance by both horizontal and vertical transfer. International Journal of Systematic and Evolutionary Microbiology, 61, pp. 3052–3067. https://doi.org/10.1099/ijs.0.028803-0.

Menza, H.D. and Salazar, L.F., 2007. Alternativas de control químico para la prevención y manejo de la resistencia de arvenses al glifosato. CENICAFÉ, 58, pp. 91–98.

Michel, D.C., Passos, S.R., Simões-Araujo, J.L., Baraúna, A.C., da Silva, K., Parma, M.M., Melo, I.S., De Meyer, S.E., O’Hara, G. and Zilli, J.E., 2017. Bradyrhizobium centrolobii and Bradyrhizobium macuxiense sp. nov. isolated from Centrolobium paraense grown in soil of Amazonia, Brazil. Archives of Microbiology, 199, pp. 657–664. https://doi.org/10.1007/s00203-017-1340-y.

Miransari, M. and Smith, D., 2008. Using signal molecule genistein to alleviate the stress of suboptimal root zone temperature on soybean-Bradyrhizobium symbiosis under different soil textures. Journal of Plant Interactions, 3, pp. 287–295. https://doi.org/10.1080/17429140802160136.

Moguel, P. and Toledo, V.M., 1999. Biodiversity Conservation in Traditional Coffee Systems of Mexico. Conservation Biology 13, pp. 11–21. https://doi.org/10.1046/j.1523-1739.1999.97153.x.

Mohammadi, K., 2012. Effective factors on biological nitrogen fixation. African Journal of Agricultural Research, 7. 12, pp. 1782-1788. https://doi.org/10.5897/AJARX11.034.

Moorman, T.B., 1989. A Review of Pesticide Effects on Microorganisms and Microbial Processes Related to Soil Fertility. Journal of Production Agriculture, 2, pp. 14–23. https://doi.org/10.2134/jpa1989.0014.

Myster, R.W., 2011. Light and nutrient effects on growth and allocation of Inga vera (Leguminosae), a successional tree of Puerto Rico. Canadian Journal of Forest Research, 36, pp. 1121-1128. https://doi.org/10.1139/x06-006.

Nelson, S., 2008. Glyphosate Herbicide Injury to Coffee. Published by the College of Tropical Agriculture and Human Resources (CTAHR) and issued in furtherance of Cooperative Extension work, Acts of May 8 and June 30, 1914. Cooperative Extension Service/CTAHR, University of Hawai‘i at Mänoa. Honolulu, Hawai‘i. 56, pp. 1-5.

Nguyen, H.P., Miwa, H., Obirih-Opareh, J., Suzaki, T., Yasuda, M. and Okazaki, S., 2020. Novel rhizobia exhibit superior nodulation and biological nitrogen fixation even under high nitrate concentrations. FEMS Microbiology Ecology, 96, 2, pp. 1-13 https://doi.org/10.1093/femsec/fiz184.

Nolasco, M., Downing, T.E., Toledo, A. and Fuentes, R., 1985. Café y sociedad en México, México, Centro de Ecodesarrollo. ed. D.F. 273 p.

Nygren, P., Fernández, M.P., Harmand, J.-M. and Leblanc, H.A., 2012. Symbiotic dinitrogen fixation by trees: an underestimated resource in agroforestry systems? Nutrient Cycling in Agroecosystems, 94, pp. 123–160. https://doi.org/10.1007/s10705-012-9542-9.

Ohyama, T., Fujikake, H., Yashima, H., Tanabata, S., Ishikawa, S., Sato, T., Nishiwaky, T., Ohtake, N., Sueyoshi, K., Ishii, S. and Fujimaki, S., 2011. Effect of Nitrate on Nodulation and Nitrogen Fixation of Soybean, in: H. El-Shemy, ed. Soybean Physiology and Biochemistry, London: IntechOpen, pp. 333-364.

Oldroyd, G.E.D. and Downie, J.A., 2008. Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes. Annual Review of Plant Biology, 59, pp. 519–546. https://doi.org/10.1146/annurev.arplant.59.032607.092839.

Omena-Garcia, R.P., Justino, G.C. and Sodek, L., 2011. Mineral nitrogen affects nodulation and amino acid xylem transport in the Amazonian legume Inga edulis Mart. Plant Physiology and Biochemistry, 3, pp. 215–218.

Ormeño-Orrillo, E., Hungria, M. and Martínez-Romero, E., 2013. Dinitrogen-fixing prokaryotes. The prokaryotes, pp. 427–451. https://doi.org/10.1007/978-3-642-30141-4_72.

Palow, D.T., Nolting, K. and Kitajima, K., 2012. Functional trait divergence of juveniles and adults of nine Inga species with contrasting soil preference in a tropical rain forest. Functional Ecology, 26, pp. 1144–1152. https://doi.org/10.1111/j.1365-2435.2012.02019.x.

Pankhurst, C.E. and Sprent, J.I., 1976. Effects of Temperature and Oxygen Tension on the Nitrogenase and Respiratory Activities of Turgid and Water-stressed Soybean and French Bean Root Nodules. Journal of Experimental Botany, 27, pp. 1–9. https://doi.org/10.1093/jxb/27.1.1-a.

Paolini Gomez, J.E., 2018. Actividad microbiológica y biomasa microbiana en suelos cafetaleros de los Andes venezolanos. Revista Terra Latinoamericana, 36, pp. 13-22. https://doi.org/10.28940/terra.v36i1.257.

Parker, M.A., 2015. The Spread of Bradyrhizobium Lineages Across Host Legume Clades: from Abarema to Zygia. Microbial Ecology, 69, pp. 630–640. https://doi.org/10.1007/s00248-014-0503-5.

Peck, M.C., Fisher, R.F. and Long, S.R., 2006. Diverse Flavonoids Stimulate NodD1 Binding to nod Gene Promoters in Sinorhizobium meliloti. Journal of Bacteriology,188, pp. 5417–5427. https://doi.org/10.1128/JB.00376-06.

Peeters, L.Y.K., Soto-Pinto, L., Perales, H., Montoya, G. and Ishiki, M., 2003. Coffee production, timber and firewood in traditional and Inga-shaded plantations in Southern Mexico. Agriculture, Ecosystems & Environment 95, pp. 481–493. https://doi.org/10.1016/S0167-8809(02)00204-9.

Pereira-Gómez, M., Ríos, C., Zabaleta, M., Lagurara, P., Galvalisi, U., Iccardi, P., Azziz, G., Battistoni, F., Platero, R. and Fabiano, E., 2020. Native legumes of the Farrapos protected area in Uruguay establish selective associations with rhizobia in their natural habitat. Soil Biology and Biochemistry, 148, pp. 107854. https://doi.org/10.1016/j.soilbio.2020.107854.

Porto, D.S., Farias, E. do N.C., Chaves, J. da S., Souza, B.F., Medeiros, R.D. de, Zilli, J.É. and Silva, K. da, 2017. Symbiotic effectiveness of Bradyrhizobium ingae in promoting growth of Inga edulis Mart. seedlings. Revista Brasileira de Ciência do Solo, 41, pp. e0160222-1- e0160222-15. https://doi.org/10.1590/18069657rbcs20160222.

Possette, R.F. da S. and Rodrigues, W.A., 2010. O gênero Inga Mill. (Leguminosae - Mimosoideae) no estado do Paraná, Brasil. Acta Botanica Brasilica, 24, pp. 354–368. https://doi.org/10.1590/S0102-33062010000200006.

Prezeworski, M., Coop, G. and Wall, J.D., 2005. The Signature of Positive Selection on Standing Genetic Variation. Evolution, 59, pp. 2312–2323. https://doi.org/10.1111/j.0014-3820.2005.tb00941.x.

Purcell, L.C., King, C.A. and Ball, R.A., 2000. Soybean Cultivar Differences in Ureides and the Relationship to Drought Tolerant Nitrogen Fixation and Manganese Nutrition. Crop Science 40, pp. 1062–1070. https://doi.org/10.2135/cropsci2000.4041062x.

Ratnadass, A., Fernandes, P., Avelino, J. and Habib, R., 2012. Plant species diversity for sustainable management of crop pests and diseases in agroecosystems: a review. Agronomy for Sustainable Development, 32, pp. 273–303. https://doi.org/10.1007/s13593-011-0022-4.

Reich, P.B. and Oleksyn, J., 2004. Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences, 101, pp. 11001–11006. https://doi.org/10.1073/pnas.0403588101.

Reyes, S.R., Olvera, M.A.P., Palma, G.I., Rodríguez, J.A.C., Vibrans, H. and Sánchez, D.F., 2020. Diversidad y uso tradicional de árboles de sombra en cafetales agroecológicos. Revista de Geografía Agrícola, pp. 259–273. https://doi.org/10.5154/r.rga.2020.64.12.

Rhem, M.F.K., Silva, V.C., dos Santos, J.M.F., Zilli, J.É., James, E.K., Fragomeni Simon, M. and Gross, E., 2021. The large mimosoid genus Inga Mill. (tribe Ingeae, Caesalpinioideae) is nodulated by diverse Bradyrhizobium strains in its main centers of diversity in Brazil. Systematic and Applied Microbiology, 44, pp. 126268. https://doi.org/10.1016/j.syapm.2021.126268

Rice, W.A., Penney, D.C. and Nyborg, M., 1977. Effects of soil acidity on rhizobia numbers, nodulation and nitrogen fixation by alfalfa and red clover. Canadian Journal of Soil Science, 57, pp. 197–203. https://doi.org/10.4141/cjss77-024.

Rodríguez, C., 1990. Inga vera Willd. Guaba, in: Familia de las Leguminosas. Subfamilia Mimosas. Department of Agriculture, Forest Service, Southern Forest Experiment Station., New Orleans, LA: U.S., pp. 288–291.

Rodríguez-Haas, B., Finney, L., Vogt, S., González-Melendi, P., Imperial, J. and González-Guerrero, M., 2013. Iron distribution through the developmental stages of Medicago truncatula nodules. Metallomics 5, pp. 1247. https://doi.org/10.1039/c3mt00060e.

Romero-Alvarado, Y., Soto-Pinto, L., García-Barrios, L. and Barrera-Gaytán, J.F., 2002. Coffee yields and soil nutrients under the shades of Inga sp. vs. multiple species in Chiapas, Mexico. Agroforestry Systems 54, pp. 215–224.

Roskoski, J.P., 1982. Nitrogen fixation in a Mexican coffee plantation. Plant and Soil, 67, pp. 283–291.

Roskoski, J.P. and van Kessel, C., 1985. Annual, Seasonal and Diel Variation in Nitrogen Fixing Activity by Inga jinicuil, a Tropical Leguminous Tree. Oikos, 44, pp. 306. https://doi.org/10.2307/3544704.

Ruiz-García, P., Gómez-Díaz, J.D., Valdes-Velarde, E., Tinoco-Rueda, J.A., Flores-Ordoñez, M. and Monterroso-Rivas, A.I., 2020. Biophysical and structural composition characterization in agroforestry systems of organic coffee from Veracruz. Tropical and Subtropical Agroecosystems, 23(37), pp. 1-17.

Salazar G., L.F. and Hincapie G., E., 2013. Arvenses de mayor interferencia en los cafetales (Technical Report). Centro Nacional de Investigaciones de Café (Cenicafé), 5, pp 101-130. https://biblioteca.cenicafe.org/handle/10778/406.

Salgado, B.G., Macedo, R.L.G., Venturin, N. and de Carvalho, V.L., 2004. Produtividade de cafeeiros arborizados com ingazeiro e com grevílea em Lavras-MG. Agrossilvicultura, 1, 8, pp. 155-162.

Sauvadet, M., den Meersche, K.V., Allinne, C., Gay, F., de Melo Virginio Filho, E., Chauvat, M., Becquer, T., Tixier, P. and Harmand, J.-M., 2019. Shade trees have higher impact on soil nutrient availability and food web in organic than conventional coffee agroforestry. Science of The Total Environment, 649, pp. 1065–1074. https://doi.org/10.1016/j.scitotenv.2018.08.291.

SEMARNAT, 2019. Niega Semarnat importación de mil toneladas de glifosato, bajo el principio precautorio para la prevención de riesgos [WWW Document]. Gobierno de México. URL http://www.gob.mx/semarnat/prensa/niega-semarnat-importacion-de-mil-toneladas-de-glifosato-bajo-el-principio-precautorio-para-la-prevencion-de-riesgos [accessed 9.15.20].

Sheldon, K.S., 2019. Climate Change in the Tropics: Ecological and Evolutionary Responses at Low Latitudes. Annual Review of Ecology, Evolution, and Systematics, 50, pp. 303–333. https://doi.org/10.1146/annurev-ecolsys-110218-025005.

Shrivastava, N., Mahajan, S. and Varma, A. (Eds.), 2020. Symbiotic Soil Microorganisms: Biology and Applications, Soil Biology. Springer International Publishing, Cham. 482 p. https://doi.org/10.1007/978-3-030-51916-2.

Siles, P., Harmand, J.-M. and Vaast, P., 2010. Effects of Inga densiflora on the microclimate of coffee (Coffea arabica L.) and overall biomass under optimal growing conditions in Costa Rica | Kopernio. Agroforestry Systems, 78, pp. 269–286. https://doi.org/10.1007/s10457-009-9241-y.

Smith, D., Muscatine, L. and Lewis, D., 1969. Carbohydrate movement from autotrophs to heterotrophs in parasitic and mutualistic symbiosis. Biological Reviews, 44, pp. 17–85. https://doi.org/10.1111/j.1469-185X.1969.tb00821.x

Somarriba, E., Beer, J., Alegre-Orihuela, J. Andrade, H.J., Cerda, R., DeClerck, F., Detlefsen, G., Escalante, M., Giraldo, L.A., Ibrahim, M., Krishnamurthy, L., Mena-Mosquera, V.E., Mora-Degado, J.R., Orozco, L., Scheelje, M. and Campos, J.J., 2012. Mainstreaming Agroforestry in Latin America, in: Nair, P.K.R., Garrity, D. (Eds.), Agroforestry - The Future of Global Land Use, Advances in Agroforestry. Springer Netherlands, Dordrecht, pp. 429–453. https://doi.org/10.1007/978-94-007-4676-3_21.

Soto-Pinto, L., Perfecto, I., Castillo-Hernandez, J. and Caballero-Nieto, J., 2000. Shade effect on coffee production at the northern Tzeltal zone of the state of Chiapas, Mexico. Agriculture, Ecosystems & Environment, 80, pp. 61–69. https://doi.org/10.1016/S0167-8809(00)00134-1.

Sousa, M., 1993. El Genero Inga (Leguminosae: Mimosoideae) del Sur de México y Centroamérica, Estudio Previo Para la Flora Mesoamericana. Annals of the Missouri Botanical Garden, 80, pp. 223. https://doi.org/10.2307/2399826.

Sprent, J.I., 2007. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation: Tansley review. New Phytologist, 174, pp. 11–25. https://doi.org/10.1111/j.1469-8137.2007.02015.x.

Sprent, J.I., 1995. Legume Trees and Shrubs in the Tropics: N2 Fixation in Perspective. Soil Biology and Biochemestry, 27, pp. 401–407.

Sprent, J.I., Ardley, J. and James, E.K., 2017. Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytologist 215, pp. 40–56. https://doi.org/10.1111/nph.14474.

Sprent, J.I., Ardley, J.K. and James, E.K., 2013. From North to South: A latitudinal look at legume nodulation processes. South African Journal of Botany, 89, pp. 31–41. https://doi.org/10.1016/j.sajb.2013.06.011

Sprent, J.I. and Sprent, P., 1990. Nitrogen fixing organisms: pure and applied aspects. London: Chapman and Hall, 256 p.

Staver, C., Juventia, S., Navarrete, E., Navarrete, L., Sepulveda, N. and Barrios, M., 2020. Long-term response of groundcover components to organic and conventional weed control in shaded and open-sun coffee in Nicaragua. Crop Protection, 133, pp. 105150. https://doi.org/10.1016/j.cropro.2020.105150

Streeter, J.G., 1985. Nitrate Inhibition of Legume Nodule Growth and Activity. Plant Physiology, 77, pp. 321–324.

Székács, A. and Darvas, B., 2018. Re-registration Challenges of Glyphosate in the European Union. Frontiers in Environmental Science, 6, pp. 78-1-78-35.

Taiz, L. and Zeiger, E., 2006. Fisiología vegetal. Universitat Jaume I. 1338 p.

Tajima, R., Lee, O.N., Abe, J., Lux, A. and Morita, S., 2007. Nitrogen-Fixing Activity of Root Nodules in Relation to Their Size in Peanut ( Arachis hypogaea L.). Plant Production Science, 10, pp. 423–429. https://doi.org/10.1626/pps.10.423.

Taylor, B.N. and Menge, D.N.L., 2018. Light regulates tropical symbiotic nitrogen fixation more strongly than soil nitrogen. Nature Plants, 4, pp. 655–661. https://doi.org/10.1038/s41477-018-0231-9.

Thomas, R.B., Bashkin, M.A. and Richter, D.D., 2000. Nitrogen inhibition of nodulation and N2 fixation of a tropical N2-fixing tree (Gliricidia sepium) grown in elevated atmospheric CO2. New Phytologist, 145, pp. 233–243. https://doi.org/10.1046/j.1469-8137.2000.00577.x.

Tindwa, H., Semu, E. and Msumali, G., 2014. Effects of elevated copper levels on biological nitrogen fixation and occurrence of rhizobia in a Tanzanian coffee-cropped soil. Journal of Agricultural Science and Applications, 3, pp. 13-19. https://doi.org/10.14511/jasa.2014.030103.

Traveset, A., 2015. Impacto de especies no-nativas sobre las comunidades mediado por interacciones mutualistas. Ecosistemas, 24, pp. 67–75. https://doi.org/10.7818/ECOS.2015.24-1.11.

Tselioudis, G., Rossow, W.B. and Rind, D., 1992. Global Patterns of Cloud Optical Thickness Variation with Temperature. Journal of Climate, 5, pp. 1484–1495. https://doi.org/10.1175/1520-0442(1992)005<1484:GPOCOT>2.0.CO;2.

Tully, K.L., Lawrence, D. and Scanlon, T.M., 2012. More trees less loss: Nitrogen leaching losses decrease with increasing biomass in coffee agroforests. Agriculture, Ecosystems & Environment, 161, pp. 137–144. https://doi.org/10.1016/j.agee.2012.08.002.

Van Bruggen, A.H.C., He, M.M., Shin, K., Mai, V., Jeong, K.C., Finckh, M.R. and Morris, J.G., 2018. Environmental and health effects of the herbicide glyphosate. Science of The Total Environment, 616–617, pp. 255–268. https://doi.org/10.1016/j.scitotenv.2017.10.309.

Van de Peer, T., Verheyen, K., Kint, V., Van Cleemput, E. and Muys, B., 2017. Plasticity of tree architecture through interspecific and intraspecific competition in a young experimental plantation. Forest Ecology and Management, 385, pp. 1–9. https://doi.org/10.1016/j.foreco.2016.11.015.

Vera, D. and Lina, K., 2016. Taxonomía y distribución altitudinal de Inga Mill. (Leguminosae) en el parque nacional Yanachaga-Chemillén, Oxapampa-Pasco. Universidad Nacional de San Agustín de Arequipa. Perú. 158 p.

Vikman, P-$. and Vessey, J.K., 1993. Ontogenetic Changes in Root Nodule Subpopulations of Common Bean (Phaseolus vulgaris L.) I. nitrogenase activity and respiration during pod-filling. Journal of Experimental Botany, 44, pp. 563–569. https://doi.org/10.1093/jxb/44.3.563.

Villalobos, N.Z. and Pennington, T.D., 2001. Guabas y cuajiniquiles de Costa Rica (Inga spp.). Editorial INBio, 197 p.

Vincent, J.M., 1970. A manual for the practical study of the root-nodule bacteria. A manual for the practical study of the root-nodule bacteria. Editorial: IBP Handbk 15 Oxford y Edimburgo: Blackwell Scientific Publications, 164 p.

Wang, J., Andersen, S.U. and Ratet, P., 2018. Editorial: Molecular and Cellular Mechanisms of the Legume-Rhizobia Symbiosis. Frontiers in Plant Science, 9, pp. 1839-1-1839-3. https://doi.org/10.3389/fpls.2018.01839.

Weber, D.F. and Miller, V.L., 1972. Effect of Soil Temperature on Rhizobium japonicum Serogroup Distribution in Soybean Nodules1. Agronomy Journal 64, pp. 796–798. https://doi.org/10.2134/agronj1972.00021962006400060027x

Weston, L.A. and Putnam, A.R., 1985. Inhibition of Growth, Nodulation and Nitrogen Fixation of Legumes by Quackgrass1. Crop Science, 25, pp. 561-565. https://doi.org/10.2135/cropsci1985.0011183X002500030031x.

Willson, C., 1985. Mineral Nutrition and Fertiliser Needs, in: Clifford, M.N., Willson, K.C. (Eds.), Coffee. Springer US, Boston, MA, pp. 135–156. https://doi.org/10.1007/978-1-4615-6657-1_6

Yamagishi, M. and Yamamoto, Y., 1994. Effects of boron on nodule development and symbiotic nitrogen fixation in soybean plants. Soil Science and Plant Nutrition 40, pp. 265–274. https://doi.org/10.1080/00380768.1994.10413300

Yépez, C., Muschler, R., Benjamín, T. and Musálem, M., 2002. Selección de especies para sombra en cafetales diversificados en Chiapas, México. Agroforestaría de las Américas, Avances de Investigación, 9, pp. 35–36.

Zablotowicz, R.M. and Reddy, K.N., 2004. Impact of Glyphosate on the Bradyrhizobium japonicum Symbiosis with Glyphosate-Resistant Transgenic Soybean: A Minireview. Journal Enviromental Quality, 33, pp. 825-831.

Zaidi, A., Saghir Khan, Md. and Qamar Rizvi, P., 2005. Effect of herbicides on growth, nodulation and nitrogen content of greengram. Agronomy for Sustainable Development, 25, pp. 497–504.

Zhalnina, K., de Quadros, P., Gano, K., Davis-Richardson, A., Fagen, J., Brown, C., Giongo, A., Drew, J., Sayavedra-Soto, L., Arp, D., Camargo, F., Daroub, S., Clark, I., McGrath, S., Hirsch, P. and Triplett, E., 2013. Ca. Nitrososphaera and Bradyrhizobium are inversely correlated and related to agricultural practices in long-term field experiments. Frontiers in Microbiology, 4, pp. 104-4-104-13. https://doi.org/10.3389/fmicb.2013.00104.

Zhang, F., Lynch, D.H. and Smith, D.L., 1995. Impact of low root temperatures in soybean [Glycine max. (L.) Merr.] on nodulation and nitrogen fixation. Environmental and Experimental Botany, 35, pp. 279–285. https://doi.org/10.1016/0098-8472(95)00017-7.

Zhang, F. and Smith, D.L., 1997. Application of genistein to inocula and soil to overcome low spring soil temperature inhibition of soybean nodulation and nitrogen fixation. Plant and Soil, 192, pp. 141–151. https://doi.org/10.1023/A:1004284727885.

Zhang, Z.Q., Wong, M.H., Nie, X.P. and Lan, C.Y., 1998. Effects of zinc (zinc sulfate) on Rhizobia-earleaf acacia (Acacia auriculaeformis) symbiotic association. Bioresource Technology, 64, pp. 97–104. https://doi.org/10.1016/S0960-8524(97)00183-1.

Zobiole, L.H.S., Kremer, R.J., Oliveira, R.S. and Constantin, J., 2011. Glyphosate affects micro-organisms in rhizospheres of glyphosate-resistant soybeans. Journal of Applied Microbiology, 110, pp. 118–127. https://doi.org/10.1111/j.1365-2672.2010.04864.x.

Zobiole, L.H.S., Oliveira, R.S., Kremer, R.J., Constantin, J., Yamada, T., Castro, C., Oliveira, F.A. and Oliveira, A., 2010. Effect of glyphosate on symbiotic N2 fixation and nickel concentration in glyphosate-resistant soybeans. Applied Soil Ecology 44, pp. 176–180. https://doi.org/10.1016/j.apsoil.2009.12.003.




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v26i1.43176

DOI: http://dx.doi.org/10.56369/tsaes.4317

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