Skip to main content

Advertisement

SpringerLink
Log in

Inoculation with Trichoderma harzianum and Azospirillum brasilense increases nutrition and yield of hydroponic lettuce

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The use of beneficial fungi and bacteria stimulate plant growth and serve to improve yield and food quality in a sustainable manner. The electrical conductivity of nutrients solution is closely linked to better nutrition of vegetable plants in a hydroponic system. Therefore, objectives of current study were to evaluate the effect of isolated and combined inoculation with Azospirillum brasilense and Trichoderma harzianum under two electrical conductivities on growth, nutrition, and yield of lettuce in hydroponic cultivation. 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) and electrical conductivities (1.2 and 1.4 dS m−1). Inoculation with A. brasilense and T. harzianum increased lettuce root growth by 47% and 20%, respectively. The single inoculation of T. harzianum provided higher fresh leaves yield (24%) at electrical conductivity of 1.2 dS m−1, while single inoculation with A. brasilense increased fresh leaves yield by 17% at electrical conductivity 1.4 dS m−1. The lowest shoot NO3− accumulation (40%) was observed with inoculation of A. brasilense and highest (28%) with inoculation T. harzianum in both electrical conductivities. Inoculation with A. brasilense increased leaf accumulation of K, P, Ca, Mg, Fe, Mn, Cu, and Zn, which are essential for human nutrition and being recommended to improve yield of lettuce plants in hydroponics. It is recommended to use EC 1.4 dS m−1 of the nutrients solution to improve accumulation of K, Mn, Cu, and Zn, regardless of inoculations for biofortification of lettuce with application of fertilizers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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

    Article  Google Scholar 

  • Artés F, Allende A (2014) Minimal fresh processing of vegetables, fruits and juices. Emerging technologies for food processing. Elsevier, London, UK, pp 583–597

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Boleta EH, Shintate Galindo F, Jalal A, Santini JM, Rodrigues WL, Lima BH, Arf O, Silva MR, Buzetti S, Teixeira Filho MCM (2020) Inoculation with growth-promoting bacteria Azospirillum brasilense and its effects on productivity and nutritional accumulation of wheat cultivars. Front Sustain Food Syst 4:265

    Article  Google Scholar 

  • Bulegon LG, Guimarães VF, Laureth JCU (2016) Azospirillum brasilense affects the antioxidant activity and leaf pigment content of Urochloa ruziziensis under water stress. Pesqui Agropecu Trop 46:343–349

    Article  Google Scholar 

  • Carvalho RSC, Bastos RG, Souza CF (2018) Influence of the use of wastewater on nutrient absorption and production of lettuce grown in a hydroponic system. Agric Water Manag 203:311–321

    Article  Google Scholar 

  • 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 6:71–80

    Article  CAS  Google Scholar 

  • Chirino-Valle I, Kandula D, Littlejohn C (2016) Potential of the beneficial fungus Trichoderma to enhance eco-system-service provision in the biofuel grass Miscanthus x giganteus in agriculture. Sci Rep 6:25109

    Article  CAS  Google Scholar 

  • Dalastra C, Teixeira Filho MCM, Silva MR, Nogueira TAR, Fernandes GC (2020a) Head lettuce production and nutrition in relation to nutrient solution flow. Hortic Bras 38:21–26

    Article  CAS  Google Scholar 

  • Dalastra C, Teixeira Filho MCM, Vargas PF (2020b) Periodicity of exposure of hydroponic lettuce plants to nutrient solution. Rev Caatinga 33:81–89

    Article  Google Scholar 

  • Das P, Pramanick B, Goswami SB, Maitra S, Ibrahim SM, Laing AM, Hossain A (2021) Innovative land arrangement in combination with irrigation methods improves the crop and water productivity of rice (Oryza sativa L.) grown with okra (Abelmoschus esculentus L.) under raised and sunken bed systems. Agronomy 11:2087. https://doi.org/10.3390/agronomy11102087

    Article  CAS  Google Scholar 

  • 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 Microbiol 8:2414

    Article  Google Scholar 

  • FAOSTAT—food and agriculture organization of the United Nations, statistics division (2021) Forestry production and trade. Available online: http://www.fao.org/faostat/en/#data/FO. Accessed 4 Sept 2021

  • Fukami J, Nogueira MA, Araujo RS, Hungria M (2016) Accessing inoculation methods of maize and wheat with Azospirillum brasilense. AMB Express 6:1–13

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Galindo FS, Buzetti S, Rodrigues WL, Boleta EHM, Silva VM, Tavanti RFR, Fernandes GC, Biagini ALC, Rosa PAL, Teixeira Filho MCM (2020) Inoculation of Azospirillum brasilense associated with silicon as a liming source to improve nitrogen fertilization in wheat crops. Sci Reports 10:6160

    CAS  Google Scholar 

  • Galindo FS, Bellotte JL, Santini JM, Buzetti S, Rosa PA, Jalal A, Teixeira Filho MCM (2021) Zinc use efficiency of maize-wheat cropping after inoculation with Azospirillum brasilense. Nutr Cycl Agroecosyst 120(2):205–221

    Article  CAS  Google Scholar 

  • Garnica-Vergara A, Barrera-Ortiz S, Muñoz-Parra E, Raya-González J, Méndez-Bravo A, Macías-Rodriguez 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

    Article  Google Scholar 

  • Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agri 2:1127500

    Google Scholar 

  • Hathazi D, Scurtu F, Bischin C, Mot A, Attia AAA, Kongsted J, Silaghi-Dumitrescu R (2018) The reaction of oxy hemoglobin with nitrite: mechanism, antioxidant-modulated effect, and implications for blood substitute evaluation. Molecules 23(2):350

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jalal A, da Silva Oliveira CE, Freitas LA, Galindo FS, Lima BH, Boleta EH, da Silva EC, do Nascimento V, Nogueira TA, Buzetti S, Teixeira Filho MCM (2022) Agronomic biofortification and productivity of wheat with soil zinc and diazotrophic bacteria in tropical savannah. Crop Pasture Sci. https://doi.org/10.1071/CP21457

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Kappel N, Boros IF, Ravelombola FS, Sipos L (2021) EC sensitivity of hydroponically grown lettuce (Lactuca sativa L.) types in terms of nitrate accumulation. Agriculture 11:315

    Article  CAS  Google Scholar 

  • Kumar A, Pramanick B, Mahapatra BS, Singh SP, Shuka DK (2019) Growth, yield and quality improvement of flax (Linum usitattisimum L.) grown under Tarai region of Uttarakhand, India through integrated nutrient management practices. Ind Crops Prod 140:111710. https://doi.org/10.1016/j.indcrop.2019.111710

    Article  CAS  Google Scholar 

  • Laik R, Kumara BH, Pramanick B, Singh SK, Nidhi Alhomrani M, Gaber A, Hossain A (2021) Labile soil organic matter pools are influenced by 45 years of applied farmyard manure and mineral nitrogen in the wheat—pearl millet cropping system in the sub-tropical condition. Agronomy 11:2190. https://doi.org/10.3390/agronomy11112190

    Article  CAS  Google Scholar 

  • Malavolta E, Vitti GC, Oliveira SA (1997) Assessment of the nutritional status of plants: principles and applica-tions, 2nd edn. Brazilian Association for the Research of Potash and Phosphate, Piracicaba

    Google Scholar 

  • Malmierca MG, Barua J, McCormick SP, Izquierdo-Bueno I, Cardoza RE, Alexander NJ, Hermosa R, Collado IG, Monte E, Gutíerrez S (2015) Novel aspinolide production by Trichoderma arundinaceum with a potential role in Botrytis cinerea antagonis-tic activity and plant defence priming. Environ Microbiol 17:1103–1118

    Article  CAS  Google Scholar 

  • Mangmang JS, Deaker R, Rogers G (2015) Azospirillum brasilense enhances recycling of fish effluent to support growth of tomato seedlings. Horticulturae 1:14–26

    Article  Google Scholar 

  • Marques DM, Magalhães PC, Marriel IE, Gomes Junior CC, Silva AB, Melo IG, Souza TC (2020) Azospirillum brasilense favors morphophysiological characteristics and nutrient accumulation in maize cultivated under two water regimes. Revista Brasileira De Milho e Sorgo 19:e1152

    Article  Google Scholar 

  • Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, Vanhaecke M, Cammue BPA, 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 8:27

    Article  Google Scholar 

  • Paulus D, Dourado Neto D, Paulus E (2012) Sensory analysis, nitrate and nutrient concentration of lettuce grown in hydroponics under saline water. Hortic Bras 30:18–25

    Article  Google Scholar 

  • Pereira-Defilippi L, Pereira EM, Silva FM, Moro GV (2017) Expressed sequence tags related to nitrogen metabolism in maize inoculated with Azospirillum brasilense. Genet Mol Res 16:16029682. https://doi.org/10.4238/gmr16029682

    Article  CAS  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Robles H (2014) Nitrosamines. In: Wexler P (ed) Encyclopedia of toxicology, 3rd edn. Elsevier, pp 584–585

    Chapter  Google Scholar 

  • Santos FT, Piebiep Goufo P, Cátia Santos C, Botelho D, Fonseca J, Queirós A, Trindade H (2016) Comparison of five agro-industrial waste-based composts as growing media for lettuce: effect on yield, phenolic compounds and vitamin C. Food Chem 209:293–301

    Article  CAS  Google Scholar 

  • Singh SK, Reddy VR (2017) Potassium starvation limits soybean growth more than the photosynthetic processes across CO2 levels. Front Plant Science 8:991

    Article  Google Scholar 

  • Singh SP, Mahapatra BS, Pramanick B, Yadav VR (2021) Effect of irrigation levels, planting methods and mulching on nutrient uptake, yield, quality, water and fertilizer productivity of field mustard (Brassica rapa L.) under sandy loam soil. Agric Water Manag 244:106539. https://doi.org/10.1016/j.agwat.2020.106539

    Article  Google Scholar 

  • Stael S, Rocha AG, Robinson AJ, Kmiecik P, Vothknecht UC, Teige M (2011) Arabidopsis calcium-binding mitochondrial carrier proteins as potential facilitators of mitochondrial ATP-import and plastid SAM-import. FEBS Lett 585:3935

    Article  CAS  Google Scholar 

  • Tabaglio V, Boselli R, Fiorini A, Ganimede C, Beccari P, Santelli S, Nervo G (2020) Reducing nitrate accumulation and fertilizer use in lettuce with modified intermittent nutrient film technique (NFT) system. Agronomy 10:1208

    Article  CAS  Google Scholar 

  • Tränkner M, Travakol E, Jákli B (2018) Functioning of potassium and magnesium in photosynthesis, photosynthate translocation and photoprotection. Physiol Plant 163:414–431

    Article  Google Scholar 

  • 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, Heidelberg, pp 333–365

    Google Scholar 

  • Wang Q, Yang S, Wan S, Li X (2019) The significance of calcium in photosynthesis. Int J Mol Sci 20:1353

    Article  CAS  Google Scholar 

  • Yoneyama T, Suzuki A (2020) Light-independent nitrogen assimilation in plant leaves: nitrate incorporation into glutamine, glutamate, aspartate, and asparagine traced by 15N. Plants 9(10):1303

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The research was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the doctoral studies of second author with a grant number 2020/11621-0, and CNPq productivity research grant (award number 311308/2020-1) of the corresponding author.

Funding

Fundação de Amparo à Pesquisa do Estado de São Paulo, 2020/11621-0.

Author information

Authors and Affiliations

  1. Department of Plant Protection, Rural Engineering and Soils, São Paulo State University-UNESP-FEIS, School of Engineering, Ilha Solteira, São Paulo, 15385-000, Brazil

    Vitoria de Almeida Moreira, Carlos Eduardo da Silva Oliveira, Arshad Jalal, Isabela Martins Bueno Gato, Thaissa Julyanne Soares Sena Oliveira, Guilherme Henrique Marcandalli Boleta, Victoria Moraes Giolo, Letícia Schenaide Vitória, Karen Vicentini Tamburi & Marcelo Carvalho Minhoto Teixeira Filho

Authors
  1. Vitoria de Almeida Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlos Eduardo da Silva Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arshad Jalal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabela Martins Bueno Gato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thaissa Julyanne Soares Sena Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guilherme Henrique Marcandalli Boleta
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Victoria Moraes Giolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Letícia Schenaide Vitória
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Karen Vicentini Tamburi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marcelo Carvalho Minhoto Teixeira Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, VAM, CESO, and MCMTF; methodology, CESO, TJSSO, and AJ; software, GHMB and IMBG; validation, VAM, IMBG, VMG, and LSV; formal analysis, GHMB, VMG, and LSV; investigation, CESO and VAM; resources, CESO and MCMTF; data curation, CESO; writing—original draft preparation, VAM and AJ; writing—review and editing, CESO and MCMTF; supervision, MCMTF and CESO; project administration, CESO and MCMTF; funding acquisition, CESO 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 contributed substantially to the work reported.

Corresponding authors

Correspondence to Carlos Eduardo da Silva Oliveira or Marcelo Carvalho Minhoto Teixeira Filho.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moreira, V.d.A., Oliveira, C.E.d.S., Jalal, A. et al. Inoculation with Trichoderma harzianum and Azospirillum brasilense increases nutrition and yield of hydroponic lettuce. Arch Microbiol 204, 440 (2022). https://doi.org/10.1007/s00203-022-03047-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-022-03047-w

Keywords

Search

Navigation