Abstract
The use of beneficial fungi and bacteria can improve growth, yield and food quality of plants. The electrical conductivity (EC) of a nutrient solution is closely linked to better nutrition of arugula plants in a hydroponic system. Therefore, objectives of current study were to evaluate isolated and combined effect of inoculation with Azospirillum brasilense and Trichoderma hazianum under two ECs on root-shoot biomass, nutrition and yield of arugula in hydroponic cultivation system. The experiment was designed in a strip-plot block with five replications in a 4 × 2 factorial scheme. The treatments were consisted of four microbial inoculations (without, A. brasilense, T. harzianum and co-inoculation of both) and two ECs (1.4 and 1.6 dS m−1). The higher EC with A. brasilense inoculation provided greater growth of arugula plants in a hydroponic system. Inoculation with A. brasilense has increased leaf area, shoot–root length, leaf chlorophyll index (LCI) and shoot ammonium accumulation while reduced root-shoot nitrate accumulation. The leaf nutrition or biofortification of arugula plants with K, S, Ca, Mg, Zn, Fe, and Mn was improved under both isolated and combined inoculations of A. brasilense and T. harzianum.
Similar content being viewed by others
References
Aguiar ATE, Gonçalves C, Paterniani MEAGZ, Tucci MLSA, Castro CEF (2014) Instruções agrícolas para as principais culturas econômicas Campinas: Instituto Agronômico. (Boletim 200)
Alvarez RCF, Benetão J, Barzotto GR, Andrade MGO, Lima SF (2019) Application methods of Azospirillum brasilense in first and second-crop corn. Revista Brasileira De Engenharia Agrícola e Ambiental 23:840–846. https://doi.org/10.1590/1807-1929/agriambi.v23n11p840-846
Ardakani MR, Mazaheri D, Mafakheri S, Moghaddam A (2011) Absorption efficiency of NPK through triple inoculation of wheat (Triticum aestivum L) by Azospirillum brasilense, Streptomyces sp, Glomus intaradices and manure application. Physiol Mol Biol Plant 17:181–192. https://doi.org/10.1007/s12298-011-0065-7
Arshad Z, Hanif MA, Qadri RWK, Khanm MM (2014) Role of essential oils in plant diseases protection: a review. Int J Chem Biochem Sci 6:11–17
Besen MR, Goes Neto AF, Esper Neto M, Zampar EJO, Costa EJO, Cordioli VR, Inoue TT, Batista MA (2020) Nitrogen fertilization and leaf spraying with Azospirillum brasilense in wheat: effects on mineral nutrition and yield. Revista De Ciências Agroveterinárias 19:483–493. https://doi.org/10.5965/223811711942020483
Bulegon LG, Guimarães VF, Laureth JCU (2016) Azospirillum brasilense affects the antioxidant activity and leaf pigment content of Urochloa ruziziensis under water stress. Pesquisa Agropecuária Trop 46:343–349. https://doi.org/10.1590/1983-40632016v4641489
Cataldo DA, Maroon ML, Schrader E, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 1975:71–80
Cavarianni RL, Cecílio Filho AB, Cazetta JO, May A, Corradi MM (2008) Concentrations of nitrogen in the nutritious solution are hourly of crop in the tenor of nitrate in rocket. Revista Caatinga 21:44–49
Dalastra C, Teixeira Filho MCM, Vargas PF (2020) Periodicity of exposure of hydroponic lettuce plants to nutrient solution. Revista Caatinga 33:81–89. https://doi.org/10.1590/1983-21252020v33n109rc
Domínguez S, Rubio MB, Cardoza RE, Gutiérrez S, Nicolás C, Bettiol W, Hermosa R, Monte E (2016) Nitrogen metabolism and growth enhancement in tomato plants challenged with Trichoderma harzianum expressing the Aspergillus nidulans Acetamidase amdS gene. Front Microbiol 7:1182. https://doi.org/10.3389/fmicb.2016.01182
Emmett BD, Youngblut ND, Buckley DH, Drinkwater LE (2017) Plant phylogeny and life history shape rhizosphere bacterial microbiome of summer annuals in an agricultural field. Front Micro-Biol 8:2414. https://doi.org/10.3389/fmicb.2017.02414
Fukami J, Nogueira MA, Araujo RS, Hungria M (2016) Accessing inoculation methods of maize and wheat with Azospirillum brasilense. AMB Exp 6:1–13. https://doi.org/10.1186/s13568-015-0171-y
Galindo FS, Rodrigues WL, Biagini ALC, Fernandes GC, Baratella EB, da Silva Junior CA, Buzetti S, Teixeira Filho MCM (2019) Assessing forms of application of Azospirillum brasilense associated with silicon use on wheat. Agronomy 9:678. https://doi.org/10.3390/agronomy9110678
Galindo FS, Buzetti S, Rodrigues WL, Boleta EHM, Silva VM, Tavanti RFR, Fernandes GC, Biagini ALC, Rosa PAL, Teixeira Filho MCM (2020b) Inoculation of Azospirillum brasilense associated with silicon as a liming source to improve nitrogen fertilization in wheat crops. Sci Rep 10:6160. https://doi.org/10.1038/s41598-020-63095-4
Galindo FS, Pagliari PH, Fernandes GC, Rodrigues WL, Boleta EHM, Jalal A, Céu EGO, Lima BHd, Lavres J, Teixeira Filho MCM (2022) Improving sustainable field-grown wheat production with Azospirillum brasilense under tropical conditions: a potential tool for improving nitrogen management. Front Environ Sci 10:821628. https://doi.org/10.3389/fenvs.2022.821628
Galindo FS, Teixeira Filho MCM, Silva EC, Buzetti S, Fernandes GC, Rodrigues WL (2020a) Technical and economic viability of cowpea co-inoculated with Azospirillum brasilense and Bradyrhizobium spp. and nitrogen doses. Revista Brasileira de Engenharia Agrícola e Ambiental, 24(5):304–311. Doi: https://doi.org/10.1590/1807-1929/agriambi.v24n5p304-311
Garnica-Vergara A, Barrera-Ortiz S, Muñoz-Parra E, Raya-González J, Méndez-Bravo A, Macías-Rodrigues L, Ruiz-Herrera LF, López-Bucio J (2015) The volatile 6-pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ETHYLEN INSENSITIVE 2 functioning. New Phytol 209:1496–1512. https://doi.org/10.1111/nph.13725
Halifu S, Deng X, Song X, Song R (2019) Effects of two Trichoderma strains on plant growth, rhizosphere soil nutrients, and fungal community of Pinus sylvestris var. mongolica annual seedlings. Forests 10(9):758. https://doi.org/10.3390/f10090758
Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AA (2015) Nutrient homeostasis within the plant circadian network. Front Plant Sci 6:1–6. https://doi.org/10.3389/fpls.2015.00299
Hou XY, Wang YF, Jiang CY, Zhai TT, Miao R, Yao ZH, Zhang RS (2022) Correction to: a native Trichoderma harzianum strain Th62 displays antagonistic activities against phytopathogenic fungi and promotes the growth of Celosia cristata. Hortic Environ Biotechnol 63:147. https://doi.org/10.1007/s13580-021-00409-z
Jákli B, Tavakol E, Tränkner M, Senbayram M, Dittert K (2017) Quantitative limitations to photosynthesis in K deficient sunflower and their implications on water use efficiency. J Plant Physiol 209:20–30. https://doi.org/10.1016/j.jplph.2016.11.010
Jalal A, Shah S, Teixeira Filho MCM, Khan A, Shah T, Ilyas M, Rosa PAL (2020) Agro-biofortification of zinc and iron in wheat grains. Gesunde Pflanzen 72:227–236. https://doi.org/10.1007/s10343-020-00505-7
Jalal A, Galindo FS, Boleta EHM, Oliveira CES, Reis AR, Nogueira TAR, Moretti Neto MJ, Mortinho ES, Fernandes GC, Teixeira Filho MCM (2021) Common bean yield and zinc use efficiency in association with diazotrophic bacteria co-inoculations. Agronomy 11:959. https://doi.org/10.3390/agronomy11050959
Jamal Uddin AFM, Ahmad H, Hasan MR, Mahbuba S, Roni MZK (2016) Effects of Trichoderma spp on growth and yield characters of BARI Tomato-14. Int J Bus Soc Sci Res 4:117–122
Jilani MI, Ali A, Rehman R, Sadique S, Nisar S (2015) Health benefits of Arugula: a review International. J Chem Biochem Sci 8:65–70
Kim-Shapiro DB, Gladwin MT, Patel RP, Hogg N (2005) The reaction between nitrite and hemoglobin: the role of nitrite in hemoglobin-mediated hypoxic vasodilation. J Inorg Biochem 99:237–246. https://doi.org/10.1016/j.jinorgbio.2004.10.034
Liu F, Xing S, Ma H, Du Z, Ma B (2013) Cytokinin producing, plant growth promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97:9155–9164. https://doi.org/10.1007/s00253-013-5193-2
Luz GL, Medeiros SLP, Manfron PA, Amaral AD, Müller L, Torres MG, Mentges L (2008) The nitrate issue in hydroponic lettuce and the human health. Ciência Rural 38:2388–2394. https://doi.org/10.1590/S0103-84782008000800049
Malavolta E, Vitti GC, Oliveira SA (1997) Assessment of the nutritional status of plants: principles and applications, 2nd edn. Brazilian Association for the Research of Potash and Phosphate, Piracicaba
Malmierca MG, Barua J, McCormick SP, Izquierdo-Bueno I, Cardoza RE, Alexander NJ, Hermosa R, Monte E, Gutiérrez S (2015) Novel aspinolide production by Trichoderma arundinaceum with a potential role in Botrytis cinerea antagonistic activity and plant defense priming. Environ Microbiol 17:1103–1118. https://doi.org/10.1111/1462-2920.12514
Mangmang JS, Deaker R, Rogers G (2015) Azospirillum brasilense enhances recycling of fish effluent to support growth of tomato seedlings. Horticulturae 1:14–26. https://doi.org/10.3390/horticulturae1010014
Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, Vanhaecke M, Cammue BP, Coninck B (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front Plant Sci 3:108. https://doi.org/10.3389/fpls.2012.00108
Meza B, Bashan LE, Bashan Y (2015) Involvement of indole-3-acetic acid produced by Azospirillum brasilense in accumulating intracellular ammonium in Chlorella vulgaris. Res Microbiol 166:72–83. https://doi.org/10.1016/j.resmic.2014.12.010
Moreno AL, Kusdra JF, Picazevicz AAC (2021) Rhizobacteria inoculation in maize associated with nitrogen and zinc fertilization at sowing. Revista Brasileira de Engenharia Agrícola e Ambiental, 25(2): 96–100. Doi: https://doi.org/10.1590/1807-1929/agriambi.v25n2p96-100
Neilands JB (1995) Siderophores - structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726
Nieto-Jacobo MF, Steyaert JM, Salazar-Badillo FB, Nguyen DV, Rostás M, Braithwaite M, De Souza JT, Jimenez-Bremont JF, Ohkura M, Stewart A, Mendoza-Mendoza A (2017) Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Front Plant Sci 8:102. https://doi.org/10.3389/fpls.2017.00102
Nozzi V, Graber A, Schmautz Z, Mathis A, Junge R (2018) Nutrient management in aquaponics: comparison of three approaches for cultivating lettuce, mint and mushroom herb. Agronomy 27:1–15. https://doi.org/10.3390/agronomy8030027
Oliveira LM, Suchismita D, Gress J, Rathinasabapathi B, Chen Y, Ma LQ (2017) Arsenic uptake by lettuce from As-contaminated soil remediated with Pteris vittata and organic amendment. Chemosphere 176:249–254. https://doi.org/10.1016/j.chemosphere.2017.02.124
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/
Reis Junior FB, Machado CTT, Machdo AT, Sodek L (2008) Inoculation of Azospirillum amazonense in two maize genotypes under different N treatments. Rev Bras Ciênc Solo 32:1139–1146. https://doi.org/10.1590/S0100-06832008000300022
Samolski I, Rincón AM, Pinzón LM, Viterbo A, Monte E (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158:129–138. https://doi.org/10.1099/mic.0.053140-0
Schmidt D, Gabriel VJ, Caron BO, Souza VQ, Boscaini R, Pinheiro RR, Cocco C (2017) Hydroponic rocket salad growth and production according to different color profiles. Hortic Bras 35(1):111–118. https://doi.org/10.1590/S0102-053620170117
Scott S, Housh A, Powell G, Anstaett A, Gerheart A, Benoit M, Wilder S, Schueller M, Ferrieri R (2020) Crop Yield, Ferritin and Fe (II) boosted by Azospirillum brasilense (HM053) in Corn. Agronomy 10:394. https://doi.org/10.3390/agronomy10030394
Signore A, Serio F, Santamaria P (2016) A targeted management of the nutrient solution in a soilless tomato crop according to plant needs. Front Plant Sci 7:1–15. https://doi.org/10.3389/fpls.2016.00391
Silva FC (2009) Manual of chemical analysis of soils, plants and fertilizers. 2. ed. rev. ampl. - Brasília, DF: Embrapa Informação Tecnológica
Singh SK, Reddy VR (2017) Potassium starvation limits soybean growth more than the photosynthetic processes across CO2 levels. Front Plant Sci 8:991. https://doi.org/10.3389/fpls.2017.00991
Taiz L, Zeiger E, Moller IM, Murphy A (2017) Plant physiology and development, 6th edn. Sinauer Associates, Sunderland
Tassi EMM, Duarte RMT, Amaya-Farfan J (2018) Partial nutrient characterization of arugula (rocket - Eruca sativa L) and the effect of heat treatment on its lipoxidase activity. Braz J Food Technol 21:1–7. https://doi.org/10.1590/1981-6723.02417
Teixeira Filho MCM, Galindo FS, Buzetti S, Santini JMK (2017) Inoculation with Azospirillum brasilense improves nutrition and increases wheat yield in association with nitrogen fertilization. In: Wanyera R, Owuoche J (eds) wheat improvement, management and utilization. Intech Open, London
Vacheron J, Renoud S, Muller D, Babalola OO, Prigent-Combaret C (2015) Alleviation of abiotic and biotic stresses in plants by Azospirillum. In: Cassan FD, Okon Y, Creus C (eds) Handbook for Azospirillum: technical issues and protocols. Springer, Berlin, pp 333–365
Vilela NJ, Luengo RFA (2017) Produção de hortaliças folhosas no Brasil. Revista Campo & Negócios Available at <https://revistacampoenegocios.com.br/producao-de-hortalicas-folhosas-no-brasil/>. Accessed May 8, 2022
Viterbo A, Landau U, Kim S, Chernin L, Chet I (2010) Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 305:42–48. https://doi.org/10.1111/j.1574-6968.2010.01910.x
Winiarska-Mieczan A, Kowalczuk-Vasilev E, Kwiatkowska K, Kwiecień M, Baranowska-Wójcik E, Kiczorowska B, Klebaniuk R, Samolińska W (2019) Dietary Intake and Content of Cu, Mn, Fe, and Zn in selected cereal products marketed in Poland. Biol Trace Elem Res 187:568–578. https://doi.org/10.1007/s12011-018-1384-0
Wright MJ, Davison KL (1964) Nitrate accumulation in crops and nitrate poisoning in animals. Adv Agron 16:197–274
Xu X, Loke M, Leung P (2015) Is there a price premium for local food? The case of the fresh lettuce market in Hawaii. Agric Resour Econ Rev 44:110–123. https://doi.org/10.22004/ag.econ.200999
Zeffa DM, Perini LJ, Silva MB, de Sousa NV, Scapim CA, Oliveira ALM, Amaral AT, Gonçalves LSA (2019) Azospirillum brasilense promotes increases in growth and nitrogen use efficiency of maize genotypes. Plos One 14(4):0215332. https://doi.org/10.1371/journal.pone.0215332
Zhang JH, Huang J, Hussain S, Zhu LF, Cao XC, Zhu CQ, Jin QY, Zhang H (2021) Increased ammonification, nitrogenase, soil respiration and microbial biomass N in the rhizosphere of rice plants inoculated with rhizobacteria. J Integr Agric 20(10):2781–2796. https://doi.org/10.1016/S2095-3119(20)63454-2
Zhu X, Yang R, Han Y, Hao J, Liu C, Fan S (2020) Effects of different NO3−: NH4+ ratios on the photosynthesis and ultrastructure of lettuce seedlings. Hortic Environ Biotechnol 61:459–472. https://doi.org/10.1007/s13580-020-00242-w
Acknowledgements
This research was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP, Grant Number 2020/11621-0
Funding
This research ans second author was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP, Grant Number 2020/11621-0.
Author information
Authors and Affiliations
Contributions
For research articles with several authors, a short paragraph specifying their individual contributions must be provided. The following statements should be used “Conceptualization, CESO and MCMTF; methodology, CESO, TJSSO and PFV; soft-ware, BHL and AJ; validation, CESO, IMBG, VMG, and LSV; formal analysis, VAM, and LSV; investigation, CESO and PFV; resources, PFV and MCMTF; data curation, CESO; writing—original draft preparation, CESO and AJ; writing—review and editing, MCMTF and PFV; visualization, IMBG and BHL; supervision, MCMTF and CESO; project administration, CESO and MCMTF; funding acquisition, PFV and MCMTF. All authors have read and agreed to the published version of the manuscript.” Please turn to the CRediT taxonomy for the term explanation. Authorship must be limited to those who have con-tributed substantially to the work reported.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants as objects of research.
Additional information
Communicated by Myung-Min Oh.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gato, I.M.B., da Silva Oliveira, C.E., Oliveira, T.J.S.S. et al. Nutrition and yield of hydroponic arugula under inoculation of beneficial microorganisms. Hortic. Environ. Biotechnol. 64, 193–208 (2023). https://doi.org/10.1007/s13580-022-00476-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13580-022-00476-w