Skip to main navigation menu Skip to main content Skip to site footer

Combined application of humic substances and PGPR inoculated and co-inoculated in plants of Phaseolus lunatus (L.) and Leucaena leucocephala (Lam.) de Wit

Lima bean greenhouse experiment. Photo: J.G. Cubillos-Hinojosa

Abstract

The objective of this research was to evaluate the effect of inoculation and co-inoculation of rhizobia and Azospirillum brasilense combined with humic substances (HS) in growth promotion of Phaseolus lunatus (lima bean) and Leucaena leucocephala (leucaena). For this, experiments in a greenhouse with the cultivation of each plant species were carried out. A randomized complete block experimental design with five repetitions was followed. Plant seeds were sown and then inoculated with rhizobia and co-inoculated with A. brasilense. Subsequently, HS were added at the dose recommended by the manufacturer. In the experiments with both plants, control treatments with the addition of nitrogen (N) with or without HS were used. After 45 days, the shoot dry mass (SDM), root dry mass (RDM), shoot-accumulated N (Nac) and relative efficiency index (REI) were determined. In addition, the mass of dry nodules (MDN) in the lima bean plants and the number of nodules (NN) in leucaena plants were determined. The results showed that in the lima bean and leucaena plants there was a greater increase in SDM, RDM and Nac in treatments that received HS and co-inoculation with rhizobia and A. brasilense than in treatments that were inoculated only with rhizobia and HS and in treatments that received N and HS compared to addition of N and isolated inoculation of rhizobia. The combined application of HS and rhizobia in co-inoculation with A. brasilense had a greater effect on the increase of MDN in lima bean and NN in leucaena, than in treatments where only rhizobia with HS were added. These results indicate the existence of potential interaction of the use of HS with the co-inoculation of rhizobia and A. brasilense, showing promise for the production of sustainable agricultural crops.

Keywords

Humic substances, Co-inoculation, Rhizobia, Azospirillum, Biostimulants, Sustainability

PDF

References

  • Aguirre, E., D. Leménager, E. Bacaicoa, M. Fuentes, R. Baigorri, A.M. Zamarreño, and J.M. García-Mina. 2009. The root application of a purified leonardite humic acid modifies the transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol. Biochem. 47(3), 215-223. Doi: https://doi.org/10.1016/j.plaphy.2008.11.013
  • Aguirre-Medina, J.F., A. Ley-De Coss, M.E. Velazco-Zebadúa, and J.F. Aguirre-Cadena. 2015. Crecimiento de Leucaena leucocephala (Lam.) De Wit inoculada con hongo micorrízico y bacteria fijadora de nitrógeno en vivero. Quehacer Científico en Chiapas 10(1), 15-22.
  • Ahmad, M., Z.A. Zahir, H.N. Asghar, and M. Arshad. 2012. The combined application of rhizobial strains and plant growth promoting rhizobacteria improves growth and productivity of mung bean (Vigna radiata L.) under salt-stressed conditions. Ann. Microbiol. 62, 1321-1330. Doi: https://doi.org/10.1007/s13213-011-0380-9
  • Antunes, J.E.L., R.L.F. Gomes, A.C.A. Lopes, A.S.F. Araújo, M.C.C.P. Lyra, and M.V.B. Figueiredo. 2011. Eficiência simbiótica de isolados de rizóbio noduladores de feijão-fava (Phaseolus lunatus L.). Rev. Bras. Ciênc. Solo 35(3), 751-757. Doi: https://doi.org/10.1590/S0100-06832011000300011
  • Araujo, A.S.F., A.C.A. Lopes, R.L.F. Gomes, J.E.A. Beserra Junior, J.E.L. Antunes, M.C.C.P. Lyra, and M.V.B. Figueiredo. 2015. Diversity of native rhizobia-nodulating Phaseolus lunatus in Brazil. Legume Res. 38(5), 653-657. Doi: https://doi.org/10.18805/lr.v38i5.5946
  • Arshad, M. and W.T. Frankenberger Jr. 1992. Microbial biosynthesis of ethylene and its influence on plant growth. pp. 69-111. In: Marshall, K.C. (ed.). Advances in microbial ecology. Advances in microbial ecology. Vol. 12. Springer, Boston, MA. Doi: https://doi.org/10.1007/978-1-4684-7609-5_2
  • Aydin, A., C. Kant, and M. Turan. 2012. Humic acid application alleviates salinity stress of bean (Phaseolus vulgaris L.) plants decreasing membrane leakage. Afr. J. Agric. Res. 7, 1073-1086. Doi: https://doi.org/10.5897/AJAR10.274
  • Barreto, M.L.J., D.M. Lima Junior, J.P.F. Oliveira, A.H.N. Rangel, and E.M. Aguiar. 2010. Utilização da leucena (Leucaena leucocephala) na alimentação ruminantes. Rev. Verde 1, 7-16.
  • Brockwell, J., F.W. Hely, and C.A. Neal-Smith. 1966. Some symbiotic characteristics of rhizobia responsible for spontaneous, effective field nodulation of Lotus hispidus. Aust. J. Exp. Agric. Anim. Husb. 6(23), 365-370. Doi: https://doi.org/10.1071/EA9660365
  • Bueno, L. and J.C. Camargo. 2015. Nitrógeno edáfico y nodulación de Leucaena leucocephala (Lam.) de Wit en sistemas silvopastoriles. Acta Agron. 64(4), 349-354. Doi: https://doi.org/10.15446/acag.v64n4.45362
  • Burdman, S., J. Kigel, and Y. Okon. 1997. Effects of Azospirillum brasilense on nodulation and growth of common bean (Phaseolus vulgaris L). Soil Biol. Biochem. 29(5-6), 923-929. Doi: https://doi.org/10.1016/S0038-0717(96)00222-2
  • Canellas, L.P., D.M. Balmori, L.O. Médici, N.O. Aguiar, E. Campostrini, R.C.C. Rosa, A.R. Façanha, and F.L. Olivares. 2013. A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.). Plant Soil 366, 119-132. Doi: https://doi.org/10.1007/s11104-012-1382-5
  • Canellas, L.P., D.J. Dantas, N.O. Aguiar, L.E.P. Peres, A. Zsögön, F.L. Olivares, L.B. Dobbss, A.R. Façanha, A. Nebbioso, and A. Piccolo. 2011. Probing the hormonal activity of fractionated molecular humic components in tomato auxin mutants. Annal. Appl. Biol. 159(2), 202-211. Doi: https://doi.org/10.1111/j.1744-7348.2011.00487.x
  • Canellas, L.P. and A.R. Façanha. 2004. Chemical natures of soil humified fractions and their bioactivity. Pesq. Agropec. Bras. 39(3), 233-240. Doi: https://doi.org/10.1590/S0100-204X2004000300005
  • Canellas, L.P. and F.L. Olivares. 2014. Physiological responses to humic substances as plant growth promoter. Chem. Biol. Technol. Agric. 1, 3. Doi: https://doi.org/10.1186/2196-5641-1-3
  • Canellas, L.P., G.A. Santos, A.A. Moraes, V.M. Rumjanek, and F.L. Olivares. 2000. Avaliação de características de ácidos húmicos de resíduos de origem urbana: I. métodos espectroscópicos (UV-Vis, IV, RMN 13C-CP/MAS) e microscopia eletrônica de varredura. Rev. Bras. Ciênc. Solo 24(4), 741-750. Doi: https://doi.org/10.1590/S0100-06832000000400006
  • Canellas, L.P., S.F. Silva, D.C. Olk, and F.L. Olivares. 2015. Foliar application of of plant growth-promoting bacteria and humic acid increase maize yields. J. Food Agric. Environ. 13(1), 146-153.
  • Chassapis, K. and M. Roulia. 2008. Evaluation of low-rank coals as raw material for Fe and Ca organomineral fertilizer using a new EDXRF method. Int. J. Coal Geol. 75(3), 185-188. Doi: https://doi.org/10.1016/j.coal.2008.04.006
  • Chen, Y. and T. Aviad. 1990. Effects of humic substances on plant growth. pp. 161-186. In: Maccarthy, P., C.E. Clapp, R.L. Malcolm, and P.R. Bloom (eds.). Humic substances in soils and crop science: selected readings. Soil Science Society of America, Madison, WI.
  • Chen, Y., C.E. Clapp, and H. Magen. 2004. Mechanisms of plant growth stimulation by humic substances: the role of organo-iron complexes. Soil Sci. Plant Nutr. 50(7), 1089-1095. Doi: https://doi.org/10.1080/00380768.2004.10408579
  • Costa, J.N.M.N. and G. Durigan. 2010. Leucaena leucocephala (Lam.) de Wit (Fabaceae): invasora ou ruderal? Rev. Árvore 34(5), 825-833. Doi: https://doi.org/10.1590/S0100-67622010000500008
  • Cubillos-Hinojosa, J.G., F.S. Araujo, and E.L.S. Sá. 2020. Rizóbios nativos eficientes en la fijación de nitrógeno en Leucaena leucocephala en Rio Grande do Sul, Brasil. Biotecnol. Sector Agropec. Agroind. 19(1), 128-138. Doi: https://doi.org/10.18684/bsaa.v19.n1.2021.1482
  • Cubillos-Hinojosa, J.G., P.E. Milian, J.L. Hernández, and A.J. Peralta. 2019. Biological fixation of nitrogen by native isolates of Rhizobium sp. symbionts of Leucaena leucocephala (Lam.) De Wit. Acta Agron. 68(2), 75-83. Doi: https://doi.org/10.15446/acag.v68n2.69322
  • Cubillos-Hinojosa, J.G., E.L.S. Sá, and F.A. Silva. 2021. Efficiency of rhizobia selection in Rio Grande do Sul, Brazil using biological nitrogen fixation in Phaseolus lunatus. Afr. J. Agric. Res. 17(2), 229-237. Doi: https://doi.org/10.5897/AJAR2020.15066
  • Cubillos-Hinojosa, J.G., A.P. Tofiño, E.C. Suarez-Fragozo, L. Aguirre, and L.F. Gómez. 2023. Selección de rizobios eficientes en líneas de frijol común (Phaseolus vulgaris L.) tolerantes a sequía. Biotecnol. Sector Agropec. Agroind. 21(2), 32-49. Doi: https://doi.org/10.18684/rbsaa.v21.n2.2023.2188
  • Cubillos-Hinojosa, J.G., N.O. Valero, and L.M. Melgarejo. 2015. Assessment of a low rank coal inoculated with coal solubilizing bacteria as an organic amendment for a saline-sodic soil. Chem. Biol. Technol. Agric. 2, 21. Doi: https://doi.org/10.1186/s40538-015-0048-y
  • Dobbss, L.B., L.P. Canellas, F.L. Olivares, N.O. Aguiar, L.E.P. Peres, M. Azevedo, R. Spaccini, A. Piccolo, and A.R. Façanha. 2010. Bioactivity of chemically transformed humic matter from vermicompost on plant root growth. J. Agric. Food Chem. 58(6), 3681-3688. Doi: https://doi.org/10.1021/jf904385c
  • Duran, D., L. Rey, J. Mayo, D. Zúñiga-Dávila, J. Imperial, T. Ruiz-Argüeso, E. Martínez-Romero, and E. Ormeño-Orrillo. 2014. Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of lima bean (Phaseolus lunatus L.) in Peru. Int. J. Syst. Evol. Microbiol. 64(Pt 6), 2072-2078. Doi: https://doi.org/10.1099/ijs.0.060426-0
  • El-Ghamry, A.M., K.M.A. El-Hai, and K.M. Ghoneem. 2009. Amino and humic acids promote growth, yield and disease resistance of faba bean cultivated in clayey soil. Aust. J. Basic Appl. Sci. 3(2), 731-739.
  • Ekin, Z. 2019. Integrated use of humic acid and plant growth promoting rhizobacteria to ensure higher potato productivity in sustainable agriculture. Sustainability 11(12), 3417. Doi: https://doi.org/10.3390/su11123417
  • Façanha, A.R., A.L.O. Façanha, F.L. Olivares, F. Guridi, G.A. Santos, A.C.X. Velloso, V.M. Rumjanek, F. Brasil, J. Schripsema, R. Braz-Filho, M.A. Oliveira, and L.P. Canellas. 2002. Bioatividade de ácidos húmicos: efeitos sobre o desenvolvimento radicular e sobre a bomba de prótons da membrana plasmática. Pesq. Agropec. Bras. 37(9), 1301-1310. Doi: https://doi.org/10.1590/S0100-204X2002000900014
  • Franco, M.C., S.T.A. Cassini, V.R. Oliveira, C. Vieira, and S.M. Tsai. 2002. Nodulação em cultivares de feijão dos conjuntos gênicos andino e meso-americano. Pesq. Agropec. Bras. 37(8), 1145-1150. Doi: https://doi.org/10.1590/S0100-204X2002000800012
  • Giannouli, A., S. Kalaitzidis, G. Siavalas, A. Chatziapostolou, K. Christanis, S. Papazisimou, C. Papanicolaou, and A. Foscolos. 2009. Evaluation of Greek low-rank coals as potential raw material for the production of soil amendments and organic fertilizers. Int. J. Coal Geol. 77(3-4), 383-393. Doi: https://doi.org/10.1016/j.coal.2008.07.008
  • Hoagland, D.R. and D.I. Arnon. 1950. The water-culture method of growing plants without soil. Circular 347. University of California, Berkeley, CA.
  • Hungria, M., D.S. Andrade, L.M.O. Chueire, A. Probanza, F.J. Guttierrez-Mañero, and M. Megías. 2000. Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biol. Biochem. 32(11-12), 1515-1528. Doi: https://doi.org/10.1016/S0038-0717(00)00063-8
  • Hungria, M., R.J. Campo, and I.C. Mendes. 2003. Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biol. Fertil. Soils 39, 88-93. Doi: https://doi.org/10.1007/s00374-003-0682-6
  • Hungria, M., M.A. Nogueira, and R.S. Araujo. 2013. Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol. Fertil. Soils 49(7), 791-801. Doi: https://doi.org/10.1007/s00374-012-0771-5
  • Iniguez, A.L., Y. Dong, and E.W. Triplett. 2004. Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol. Plant-Microbe Interact. 17(10), 1078-1085. Doi: https://doi.org/10.1094/MPMI.2004.17.10.1078
  • Kant, R., R. Bishist, and M. Kumar. 2019. Effect of supplementation of Leucaena leucocephala (Lam.) de Wit (Leucaena) leaves on growth profile of crossbred calves. Int. J. Livest. Res. 10. Doi: https://doi.org/10.5455/ijlr.20181212024424
  • Kloepper, J.W. and M.N. Schroth. 1978. Plant growth promoting rhizobacteria on radishes. pp. 879-882. In: Proc. 5th International Conference on Plant Pathogenic Bacteria. INRA, Tours, France.
  • Kumar, R. and R. Chandra. 2008. Influence of PGPR and PSB on Rhizobium leguminosarum Bv. viciae strain competition and symbiotic performance in lentil. World J. Agric. Sci. 4(3) 297-301.
  • Melo, A.P., F.L. Olivares, L.O. Médici, A. Torres-Neto, L.B. Dobbss, and L.P. Canellas 2017. Mixed rhizobia and Herbaspirillum seropedicae inoculations with humic acid-like substances improve water-stress recovery in common beans. Chem. Biol. Technol. Agric. 4, 6. Doi. https://doi.org/10.1186/s40538-017-0090-z
  • Montañez, A., C. Abreu, P.R. Gill, G. Hardarson, and M. Sicardi. 2009. Biological nitrogen fixation in maize (Zea mays L.) by 15N isotope-dilution and identification of associated culturable diazotrophs. Biol. Fertil. Soils 45(3), 253-263. Doi: https://doi.org/10.1007/s00374-008-0322-2
  • Murgas, E. and A. Falla. 2016. Influencia de ácidos húmicos y bacterias diazotróficas sobre la germinación de las semillas y crecimiento temprano de plantas forrajeras. MSc thesis. Universidad Popular del Cesar, Valledupar, Colombia.
  • Murgueitio, E., F. Uribe, C. Molina, E. Molina, W. Galindo, J. Chará, M. Flores, C. Giraldo, C. Cuartas, J. Naranjo, L. Solarte, and J. González. 2016. Establecimiento del SSPi con leucaena asociado a pastos seleccionados. pp. 55-106. Murgueitio, E., W. Galindo, J. Chará, and F. Uribe (eds.). Establecimiento y manejo de sistemas silvopastoriles intensivos con Leucaena. CIPAV, Santiago de Cali, Colombia.
  • Muscolo, A., M. Sidari, and S. Nardi. 2013. Humic substance: relationship between structure and activity. Deeper information suggests univocal findings. J. Geochem. Explor. 129, 57-63. Doi: https://doi.org/10.1016/j.gexplo.2012.10.012
  • Nardi, S., M. Tosoni, D. Pizzeghello, M.R. Provenzano, A. Cilenti, A. Sturaro, R. Rella, and A. Vianello. 2005. Chemical characteristics and biological activity of organic substances extracted from soils by root exudates. Soil Sci. Soc. Am. J. 69(6), 2012-2019. Doi: https://doi.org/10.2136/sssaj2004.0401
  • Nicodemo, M.L.F., A.R. Garcia, V. Porfirio-da-Silva, and D.S.C. Paciullo. 2018. Desempenho, saúde e conforto animal em sistemas silvipastoris no Brasil. Documentos 129 Embrapa, São Carlos, SP.
  • Ormeño, E., R. Torres, J. Mayo, R. Rivas, A. Peix, E. Velázquez, and D. Zúñiga. 2007. Phaseolus lunatus is nodulated by a phosphate solubilizing strain of Sinorhizobium meliloti in a Peruvian soil. pp. 143-147. In: Velázquez, E.l. and C. Rodríguez-Barrueco (eds.). 1st International Meeting on Microbial Phosphate Solubilization. Developments in Plant and Soil Sciences. Springer, Dordrecht, The Netherlands. Doi: https://doi.org/10.1007/978-1-4020-5765-6_21
  • Ormeño-Orrillo, E., L. Rey, D. Durán, C.A. Canchaya, M.A. Rogel, D. Zúñiga-Dávila, J. Imperial, T. Ruiz-Argüeso, and E. Martínez-Romero. 2017. Draft genome sequence of Bradyrhizobium paxllaeri LMTR 21T isolated from Lima bean (Phaseolus lunatus) in Peru. Genom. Data 13, 38-40. Doi: https://doi.org/10.1016/j.gdata.2017.06.008
  • Pieterse, C.M., C. Zamioudis, R.L. Berendsen, D.M. Weller, S.C. Van Wees, and P.A. Bakker. 2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347-375. Doi: https://doi.org/10.1146/annurev-phyto-082712-102340
  • Pinton, R., Z. Varanini, G. Vizzotto, and A. Maggioni. 1992. Soil humic substances affect transport properties of tonoplast vesicles isolated from oat roots. Plant Soil 142(2), 203-210. Doi: https://doi.org/10.1007/BF00010966
  • Rodda, M.R.C., L.P. Canellas, A.R. Façanha, D.B. Zandonadi, J.G.M. Guerra, D.L. Almeida, and G.A. Santos. 2006. Estímulo no crescimento e na hidrólise de ATP em raízes de alface tratadas com humatos de vermicomposto. I - efeito da concentração. Rev. Bras. Ciênc. Solo 30(4), 649-656. Doi: https://doi.org/10.1590/S0100-06832006000400005
  • Rosa, C.M., R.M.V. Castilhos, L.C. Vahl, D.D. Castilhos, L.F.S. Pinto, E.S. Oliveira, and O.A. Leal. 2009. Efeito de substâncias húmicas na cinética de absorção de potássio, crescimento de plantas e concentração de nutrientes em Phaseolus vulgaris L. Rev. Bras. Ciênc. Solo 33(4), 959-967. https://doi.org/10.1590/S0100-06832009000400020
  • Santos, J.O., J.E.L. Antunes, A.S.F. Araújo, M.C.C.P. Lyra, R.L.F. Gomes, A.C.A. Lopes, and M.V.B. Figueiredo. 2011. Genetic diversity among native isolates of rhizobia from Phaseolus lunatus. Ann. Microbiol. 61(3), 437-444. Doi: https://doi.org/10.1007/s13213-010-0156-7
  • Santos, J.O., A.S.F. Araújo, R.L.F. Gomes, Â.C.A. Lopes, and M.V.B., Figueiredo. 2009. Ontogenia da nodulação em feijão-fava (Phaseolus lunatus). Rev. Bras. Cienc. Agrar. 4(4), 426-429. Doi: https://doi.org/10.5039/agraria.v4i4a9
  • Sarruge, J.R. 1975. Soluções nutritivas. Summa Phytopathol. 1(3), 231-234.
  • Scher, F.M. and R. Baker. 1982. Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. Phytopathology 72, 1567-1573. Doi: https://doi.org/10.1094/Phyto-72-1567
  • Senesi, N., C. Plaza, G. Brunetti, and A. Polo. 2007. A comparative survey of recent results on humic-like fractions in organic amendments and effects on native soil humic substances. Soil Biol. Biochem. 39(6), 1244-1262. Doi: https://doi.org/10.1016/j.soilbio.2006.12.002
  • Servín-Garcidueñas, L.E., A. Zayas-Del Moral, E. Ormeño-Orrillo, M.A. Rogel, A. Delgado-Salinas, F. Sánchez, and E. Martínez-Romero. 2014. Symbiont shift towards Rhizobium nodulation in a group of phylogenetically related Phaseolus species. Mol. Phylogenet. Evol. 79, 1-11. Doi: https://doi.org/10.1016/j.ympev.2014.06.006
  • Sessitsch, A., J.G. Howieson, X. Perret, H. Antoun, and E. Martínez-Romero. 2002. Advances in rhizobium research. Crit. Rev. Plant Sci. 21(4), 323-378. Doi: https://doi.org/10.1080/0735-260291044278
  • Shah, Z.H., H.M. Rehman, T. Akhtar, H. Alsamadany, B.T. Hamooh, T. Mujtaba, I. Daur, Y. Al Zahrani, H.A.S. Alzahrani, S. Ali, S.H. Yang, and G. Chung. 2018. Humic substances: determining potential molecular regulatory processes in plants. Front. Plant Sci. 9, 263. Doi: https://doi.org/10.3389/fpls.2018.00263
  • Silva, R.M., A. Jablonski, L. Siewerdt, and P. Silveira Júnior. 2000. Desenvolvimento radicular e produção de aveia preta até o estágio de grão pastoso, cultivada em solução nutritiva completa com adição de substâncias húmicas. Rev. Bras. Agrociência 1, 53-58.
  • Silveira, J.A.G., J.C.S. Matos, V.M. Ceccato, A.H. Sampaio, and R.C.L. Costa. 1998. Induction of reductase nitrate activity and nitrogen fixation in two Phaseolus species in relation to exogenous nitrate level. Physiol. Mol. Biol. Plant. 4, 81-188.
  • Spaccini, R., V. Cozzolino, V. Di Meo, D. Savy, M. Drosos, and A. Piccolo. 2019. Bioactivity of humic substances and water extracts from compost made by ligno-cellulose wastes from biorefinery. Sci. Total Environ. 646, 792-800. Doi: https://doi.org/10.1016/j.scitotenv.2018.07.334
  • Sturz, A.V., B.R. Christie, and J. Nowak. 2000. Bacterial endophytes: Potential role in developing sustainable systems of crop production. Crit. Rev. Plant Sci. 19(1), 1-30. Doi: https://doi.org/10.1080/07352680091139169
  • Tedesco, M.J., C. Gianello, C.A. Bissani, H. Bohnem, and S.J. Volkweiss. 1995. Análises de solo, plantas e outros materiais. 2nd ed. Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
  • Tilba, V.A. and V.T. Sinegovskaya. 2012. Role of symbiotic nitrogen fixation in increasing photosynthetic productivity of soybean. Russ. Agric. Sci. 38, 361-363. Doi: https://doi.org/10.3103/S1068367412050199
  • Tittonell, P. 2014. Ecological intensification of agriculture - sustainable by nature. Curr. Opin. Environ. Sustain. 8, 53-61. Doi: https://doi.org/10.1016/j.cosust.2014.08.006
  • Trevisan, S., A. Botton, S. Vaccaro, A. Vezzaro, S. Quaggiotti, and S. Nardi. 2011. Humic substances affect Arabidopsis physiology by altering the expression of genes involved in primary metabolism, growth and development. Environ. Exp. Bot. 74, 45-55. Doi: https://doi.org/10.1016/j.envexpbot.2011.04.017
  • Trevisan, S., O. Francioso, S. Quaggiotti, and S. Nardi. 2010. Humic substances biological activity at the plant-soil interface. From environmental aspects to molecular factors. Plant Signal. Behav. 5, 635-643. Doi. https://doi.org/10.4161/psb.5.6.11211
  • Vaughan, D. and R.E. Malcolm. 1985. Influence of humic substances on growth and physiological processes. pp. 37-75 In: Vaughan, D. and R.E. Malcolm (eds.). Soil organic matter and biological activity. Vol. 16. Springer, Dordrecht, The Netherlands. Doi: https://doi.org/10.1007/978-94-009-5105-1_2
  • Vincent, J.M. 1970. A manual for the practical study of root nodule bacteria. IBP Handbook 15 Blackwell Scientific, Oxford, UK.
  • Yadegari, M., H.A. Rahmani, G. Noormohammadi, and A. Ayneband. 2008. Evaluation of bean (Phaseolus vulgaris) seeds inoculation with Rhizobium phaseoli and plant growth promoting rhizobacteria (PGPR) on yield and yield components. Pak. J. Biol. Sci. 11(15), 1935-1939. Doi: https://doi.org/10.3923/pjbs.2008.1935.1939
  • Yakhin, O.I., A.A. Lubyanov, I.A. Yakhin, and P.H. Brown. 2017. Biostimulants in plant science: a global perspective. Front. Plant Sci. 7, 2049. Doi: https://doi.org/10.3389/fpls.2016.02049
  • Zandonadi, D.B. and J.G. Busato. 2012. Vermicompost humic substances: technology for converting pollution into plant growth regulators. Int. J. Environ. Sci. Eng. Res. 3(2), 73-84.
  • Zandonadi, D.B., L.P. Canellas, and A.R. Façanha. 2007. Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta 225(6), 1583-1595. Doi: https://doi.org/10.1007/s00425-006-0454-2
  • Zandonadi, D.B., M.P. Santos, J.G. Busato, L.E.P. Peres, and A.R. Façanha. 2013. Plant physiology as affected by humified organic matter. Theor. Exp. Plant Physiol. 25(1), 13-25. Doi: https://doi.org/10.1590/S2197-00252013000100003
  • Zandonadi, D.B., M.P. Santos, L.O. Medici, and J. Silva. 2014. Ação da matéria orgânica e suas frações sobre a fisiologia de hortaliças. Hortic. Bras. 32(1), 14-20. Doi: https://doi.org/10.1590/S0102-05362014000100003

Downloads

Download data is not yet available.

Most read articles by the same author(s)