Skip to main content
SpringerLink
Log in

Positive impact of vermicompost leachate on salt stress resistance in tomato (Solanum lycopersicum L.) at the seedling stage: a phytohormonal approach

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aim

Vermicompost leachate (VCL) produced by earthworms is a valuable biostimulant but its hormonal impact on salt-treated plants remains elusive.

Methods

Plants of Solanum lycopersicum L. were cultivated in nutrient solution and exposed during 7 days to 125 mM NaCl in the presence or absence of VCL (18 mL.L−1). Mineral nutrition, water and hormonal status were quantified in roots, young and old leaves and analyzed in relation to phytohormone content of VCL.

Results

VCL improved plant growth and reduced Na+ accumulation in salt-stressed plants. It delayed senescence in young leaves through a decrease in ethylene synthesis and an increase in proline and anthocyanin contents. VCL contains high amounts of salicylic acid, benzoic acid and aminocyclopropane carboxylic acid (ACC) but low concentrations of jasmonates, cytokinins and proline. VCL did not increase abscisic acid content in salt-stressed plants and did not lead to ACC accumulation while it increased jasmonate accumulation and modified the pattern of cytokinin profile with an increase in dihydrozeatin-types in old leaves and N6-(∆2-isopentenyl)adenine-types in young ones.

Conclusion

VCL reduces the impact of salinity on leaf senescence, which is related to its impact on endogenous phytohormones rather than to a passive absorption of exogenous hormonal compounds.

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

  • Alam MZ, Braun G, Norrie J, Hodges DM (2013) Effect of Ascophyllum extract application on plant growth, fruit yield and soil microbial communities of strawberry. Can J Plant Sci 93:23–36

    Google Scholar 

  • Albacete A, Martinez-Andujar C, Ghanem M, Acosta M, Sanchez-Bravo J, Asins MJ, Cuartero J, Lutts S, Dodd IC, Pérez-Alfocea F (2009) Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence and increased leaf area and crop productivity in salinized tomato. Plant Cell Environ 32:928–9238

    CAS  PubMed  Google Scholar 

  • Aremu AO, Masondo NA, Van Staden J (2014) Physiological and phytochemical responses of three nutrient-stressed bulbous plants subjected to vermicompost leachate treatment. Acta Physiol Plant 36:721–731

    Google Scholar 

  • Aremu AO, Stirk WA, Kulkarni MG, Tarkowská D, Turečková V, Gruz J, Bílba O, Novák O, Stirk WA, Doležal K (2015) Evidence of phytohormones and phenolic acids variability in garden-waste-derived vermicompost leachate, a well-known plant growth stimulant. Plant Growth Regul 75:483–492

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Benazzouk S, Djazouli ZE, Lutts S (2018) Assessment of the preventive effect of vermicompost on salinity resistance in tomato (Solanum lycopersicum cv. Ailsa Craig). Acta Physiol Plant 40:121

    Google Scholar 

  • Bui EN (2013) Soil salinity: a neglected factor in plant ecology and biogeography. J Arid Environ 92:14–25

    Google Scholar 

  • Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41

    CAS  Google Scholar 

  • Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaichi W (2018) Effets des Biofertilisants sur la Bio-fourniture et la Correction du Stress. PhD Thesis. Université de Blida 1, Algeria, 324 p

  • Chinsamy M, Kulkarni MG, Van Staden J (2013) Garden-waste-vermicompost leachate alleviates salinity stress in tomato seedlings by mobilizing salt tolerance mechanisms. Plant Growth Regul 71:41–47

    CAS  Google Scholar 

  • Chinsamy M, Kulkarni MG, Van Staden J (2014) Vermicompost leachate reduces temperature and water stress effects in tomato seedlings. HortScience 49:1183–1187

    Google Scholar 

  • Chmielowska-Bak J, Lefèvre I, Lutts S, Deckert J (2013) Short term signaling responses in roots of young soybean seedlings exposed to cadmium stress. J Plant Physiol 170:1585–1594

    CAS  PubMed  Google Scholar 

  • Ciura J, Kruk F (2018) Phytohormones as targets for improving plant productivity and stress tolerance. J Plant Physiol 229:32–40

    CAS  PubMed  Google Scholar 

  • Cristescu SM, De Martinis D, Te Lintel HS, Parker DH, Harren FJM (2002) Ethylene production by Botrytis cinerea in vitro and in tomatoes. Appl Environ Microbiol 68:5342–5350

    CAS  PubMed  PubMed Central  Google Scholar 

  • Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M (2007) The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ 30:497–507

    CAS  PubMed  Google Scholar 

  • Dewanto V, Wu X, Adom KK, Liu RH (2002) Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 50:3010–3014

    CAS  PubMed  Google Scholar 

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defense against lipid peroxidation. J Exp Bot 32:79–91

    CAS  Google Scholar 

  • Djilianov DL, Dobrev PI, Moyankova DP, Vankova R, Georgieva DT, Gadjošová S, Motyka V (2013) Dynamics of endogenous phytohormones during desiccation and recovery of the resurrection, plant species Haberlea rhodopensis. J Plant Growth Regul 32:564–574

    CAS  Google Scholar 

  • Dobrev P, Kaminek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid phase extraction. J Chrom A 950:21–29

    Google Scholar 

  • Dobrev PI, Vankova R (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. In plant salt tolerance: methods and protocols, methods in molecular biology. Vol. 913, springer science + business media, eds. Shabala S., and Ann Cuin T; 17; 251-261

    Google Scholar 

  • Du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hort 196:3–14

    Google Scholar 

  • Fita A, Rodriguez-Burruezo A, Boscaiu M, Prohens J, Vicente O (2015) Breeding and domesticated crops adapted to drought and salinity : a new paradigm for increasing food production. Front Plant Sci 6:978

    PubMed  PubMed Central  Google Scholar 

  • Fukuda A, Tanaka Y (2006) Effects of ABA, auxin, and gibberellin on the expression of genes for vacuolar H+-inorganic pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter in barley. Plant Physiol Biochem 44:351–358

    CAS  PubMed  Google Scholar 

  • Gajdošová S, Spíchal L, Kamínek M, Hoyerová K, Novák O, Dobrev PI, Galuszka P, Klíma P, Gaudinová A, Žižková E, Hanuš J, Dančák M, Trávníček B, Pešek B, Krupička M, Vaňková R, Strnad M, Motyka V (2011) Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J Exp Bot 62:2827–2840

    PubMed  Google Scholar 

  • Ghanem ME, Albacete A, Martinez-Andujar C, Acosta M, Romero-Aranda R, Dodd IC, Lutts S, Pérez-Alfocea F (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59:3039–3050

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghanem ME, Albacete A, Smigocki AC, Frebort I, Pospisilova H, Martinez-Andujar C, Acosta M, Sanchez-Bravo J, Lutts S, Dodd IC, Pérez-Alfocea F (2011) Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 62:124–140

    Google Scholar 

  • Gharbi E, Martínez JP, Benahmed H, Fauconnier ML, Lutts S, Quinet M (2016) Salicylic acid differently impacts ethylene and polyamine synthesis in the glycophyte Solanum lycopersicum and the wild-related halophyte Solanum chilense exposed to mild salt stress. Physiol Plant 158:152–167

    CAS  PubMed  Google Scholar 

  • Gharbi E, Martínez JP, Benahmed H, Hichri I, Dobrev PI, Motyka V, Quinet M, Lutts S (2017) Phytohormone profiling in relation to osmotic adjustment in NaCl-treated plants of the halophyte tomato wild relative species Solanum chilense comparatively to the cultivated glycophyte Solanum lycopersicum. Plant Sci 258:77–89

    CAS  PubMed  Google Scholar 

  • Gharbi E, Lutts S, Dailly H, Quinet M (2018) Before or during the stress? Comparison between the impacts of two different modes of salicylic acid application on tomato (Solanum lycopersicum) responses to salinity. Plant Signal Behav 13(5):e1469361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gurmani AR, Bano A, Ullah N, Khan H, Jahangir M, Flowers TJ (2013) Exogenous abscisic acid (ABA) and silicon (Si) promote salinity tolerance by reducing sodium (Na+) transport and bypass flow in rice (Oryza sativa indica). Aust J Crop Sci 7:1219–1226

    Google Scholar 

  • Gutiérrez-Miceli FA, Santiago-Borraz J, Montes Molina JA, Nafate CC, Abud-Archila M, Oliva Llaven MA, Rincón-Rosales R, Dendooven L (2007) Vermicompost as a soil supplement to improve growth, yield and fruit quality of tomato (Lycoperscum esculentum). Bioresour Technol 98:2781–2786

    PubMed  Google Scholar 

  • Hernandez OL, Calderín A, Huelva R, Martínez-Balmori D, Guridi F, Aguiar NO, Olivares LP, Canellas LP (2015) Humic substances from vermicompost enhance urban lettuce production. Agron Sust Dev 35:225–232

    CAS  Google Scholar 

  • Kaminek M, Brezinova A, Gaudinova A, Motyka V, Vankova R, Zazimalova E (2000) Purine cytokinins: a proposal of abbreviations. Plant Growth Regul 32:253–256

    CAS  Google Scholar 

  • Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59:609–619

    CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M, Khan MMA (2010) Calcium chloride and gibberellic acid protect linseed (Linum usitatissimum L.) from NaCl stress by inducing antioxidative defence system and osmoprotectant accumulation. Acta Physiol Plant 32:121

    Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    CAS  Google Scholar 

  • Lutts S, Bouharmont J, Kinet JM (1999) Physiological characterization of salt-resistant rice somaclones. Aust J Bot 47:835–849

    Google Scholar 

  • Manaa A, Gharbi E, Mimouni H, Wasti S, Aschi-Smiti S, Lutts S, Ahmed HB (2014) Simultaneous application of salicylic acid and calcium improves salt tolerance in two contrasting tomato (Solanum lycopersicum) cultivars. South Afr J Bot 95:32–39

    CAS  Google Scholar 

  • Mancinelli AL (1984) Red-far red reversibility of anthocyanin synthesis in dark-grown and light-pretreated seedlings. Plant Physiol 76:281–283

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mimouni H, Wasti S, Manaa A, Gharbi E, Chalh A, Vandoorne B, Lutts S, Ahmed HB (2016) Does salicylic acid (SA) improve tolerance to salt stress in plants? A study of SA effects on tomato plant growth, water dynamics, photosynthesis, and biochemical parameters. Omics 20:180–190

    CAS  PubMed  Google Scholar 

  • Nardi S, Pizzeghello D, Muscolo A, Vianello A (2002) Physiological effects of humic substances on higher plants. Soil Biol Biochem 34:1527–1536

    CAS  Google Scholar 

  • Pizzeghello D, Francioso O, Ertani A, Muscolo A, Nardi S (2013) Isopentenyladenosine and cytokinin-like activity of different humic substances. J Geochem Expl 129:70–75

    CAS  Google Scholar 

  • Plett DC, Møller IS (2010) Na+ transport in glycophytic plants: what we know and would like to know. Plant Cell Environ 33:612–626

    CAS  Google Scholar 

  • Quinet M, Bataille G, Dobrev PI, Capel C, Gómez P, Capel J, Lutts S, Motyka V, Angosto T, Lozano R (2014) Transcriptional and hormonal regulation of petal and stamen development by STAMENLESS, the tomato (Solanum lycopersicum L.) orthologue to the B-class APETALA3 gene. J Exp Bot 65:2243–2256

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rady MM, Mohamed GF (2015) Modulation of salt stress effects on the growth, physio-chemical attributes and yields of Phaseolus vulgaris L. plants by the combined application of salicylic acid and Moringa oleifera leaf extract. Scientia Hort 193:105–113

    CAS  Google Scholar 

  • Rupani PDF, Embrandiri A, Ibrahim MH, Ghole W, Lee CT, Abbaspour M (2018) Effects of different vermicompost extracts of palm oil effluent and palm-pressed fiber mixture on seed germination of mung bean and its relative toxicity. Environ Sci Poll Res 25:35805–35810

    CAS  Google Scholar 

  • Schäfer M, Brütting C, Meza-Canales ID, Großkisky DK, Vankova R, Baldwin IT, Meldau S (2015) The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to envoironmental interactions. J Exp Bot 66:4873–4884

    PubMed  PubMed Central  Google Scholar 

  • Shkolnik-Inbar D, Adler G, Bar-Zvi D (2013) ABI4 downregulates expression of the sodium transporter HKT1;1 in Arabidopsis roots and affects salt tolerance. Plant J 73:993–1005

    CAS  PubMed  Google Scholar 

  • Singh SNB (2015) Alleviation of allelopathic stress of benzoic acid by indole acetic acid in Solanum lycopersicum. Scientia Hort 192:211–217

    Google Scholar 

  • Singh R, Sharma R, Kumar S, Gupta R, Patil R (2008) Vermicompost substitution influences growth, physiological disorders, fruit yield and quality of strawberry (Fragaria x ananassa Duch.). Bioress Technol 99:8507–8511

    CAS  Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics and phosphomolybdic-phosphotungstic reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Trevisan S, Pizzeghello S, Ruperti B, Fransisco O, Sassi A, Palme K, Quaggiotti S, Nardi S (2010) Humic substances induce lateral root formation and expression of the early auxin-responsive IAA19 gene and DR5 synthetic element of Arabidopsis. Plant Biol 12:604–614

    CAS  PubMed  Google Scholar 

  • Truong HA, Lee WJ, Jeong CY, Trinh CS, Lee S, Kang CS, Cheong YK, Hong SW, Lee H (2018) Enhanced anthocyanin accumulation confers increased growth performance in plants under low nitrate and high salt stress conditions owing to active modulation of nitrate metabolism. J Plant Physiol 231:41–48

    CAS  PubMed  Google Scholar 

  • Wassman R, Hien NX, Hoang CT, Tuong TP (2004) Sea level rise affecting the vietnamienese Mekong Delta: water elevation in the flood season and implication for rice production. Climate Change 66:89–107

    Google Scholar 

  • Wu X, He J, Chen J, Yang S, Zha D (2014) Alleviation of exogenous 6-benzyladenine on two genotypes of eggplant (Solanum melongena Mill.) growth under salt stress. Protoplasma 251:169–176

    CAS  Google Scholar 

  • Xiao Z, Liu M, Jiang L, Chen X, Griffiths BS, Li H, Hu F (2016) Vermicompost increases defense against root-knot nematode (Meloidogyne incognita) in tomato plants. Appl Soil Ecol 105:177–186

    Google Scholar 

  • Yang L, Zhao F, Chang Q, Li T, Li F (2015) Effects of vermicomposts on tomato yield and quality and soil fertility in greenhouse under different soil water regimes. Agric Water Manag 160:98–105

    Google Scholar 

  • Yuan F, Liang X, Li Y, Yin S, Wang B (2019) Methyl jasmonate improves tolerance to high salt stress in the recretohalophyte Limonium bicolor. Funct Plant Biol 46:82–92

    CAS  Google Scholar 

  • Zaller JG (2007) Vermicompost as a substitute for peat in potting media: effects on germination, biomass allocation, yields and fruit quality of three tomato varieties. Sci Hort 112:191–199

    Google Scholar 

  • Zarei M, Abadi VAJM, Moridi A (2018) Ciomparison of vermiwash and vermicompost tea properties produced from different organic beds under greenhouse conditions. Int J Recylc Org Waste Agric 7:25–32

    Google Scholar 

  • Zhang H, Tan SN, Wong WS, Ng CYL, Teo CH, Ge L, Chen X, Yong JWH (2014) Mass spectrometric evidence for the occurrence of plant growth promoting cytokinins in vermicompost tea. Biol Fert Soils 50:401–403

    CAS  Google Scholar 

  • Zhang H, Tan SN, Teo CH, Yew YR, Ge L, Chen X, Yong JWH (2015) Analysis of phytohormones in vermicompost using a novel combinative sample preparation strategy of ultrasound-assisted extraction and solid-phase extraction coupled with liquid chromatography–tandem mass spectrometry. Talanta 139:189–197

    CAS  PubMed  Google Scholar 

  • Zhang Y, Tian Y, Hu D, Fan J, Shen M, Zeng G (2019) Is vermicompost the possible in situ sorbent? Immobilization of Pb, Cd and Cr in sediment with sludge derived vermicompost, a column study. J Hazard Mat 367:83–90

    CAS  Google Scholar 

  • Zheng M, Yang T, Peng T, Zhu T, Zhu G, Fu Y, Hsu YF (2019) Arabidopsis GSM1 is involved in ABI4-regulated ABA signaling under high-glucose condition in early seedling growth. Plant Sci 287:110183

    CAS  PubMed  Google Scholar 

  • Zhu M, Zhou M, Shabala L, Shabala S (2017) Physiological and molecular mechanisms mediating xylem Na+ loading in barley in the context of salinity tolerance. Plant Cell Physiol 40:1009–1020

    CAS  Google Scholar 

  • Žižková E, Dobrev PI, Muhovski Y, Hošek P, Hoyerová K, Haisel D, Procházková D, Lutts S, Motyka V, Hichri I (2015) Tomato (Solanum lycopersicum L.) SlIPT3 and SlIPT4 isopentenyltransferases mediate salt stress response in tomato. BMC Plant Biol 15:85

    PubMed  PubMed Central  Google Scholar 

  • Zucco MA, Walters SA, Chong SK, Klubek BP, Masabni JG (2015) Effect of soil type and vermicompost applications on tomato growth. Int J Recycl Org Was Agric 4:135–141

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to Marie-Eve Renard, Brigitte Vanpee and Marie Korecka for invaluable technical support. This research was supported by the Czech Science Foundation (grant No. 19-12262S) and by the Ministry of Education, Youth and Sports of CR from European Regional Development Fund-Project “Centre for Experimental Plant Biology” (No. CZ.02.1.01/0.0/0.0/16_019/0000738).

Author information

Authors and Affiliations

  1. Groupe de Recherche en Physiologie Végétale, Earth and Life Institute - Agronomy (ELI-A), Université Catholique de Louvain, 5 (Bte 7.07.13) Place Croix du Sud, 138, Louvain-la-Neuve, Belgium

    Salima Benazzouk & Stanley Lutts

  2. Faculté des Sciences de la Nature et de la Vie, Université de Blida 1, Ouled yaich, Blida, Algeria

    Salima Benazzouk & Zahr-Eddine Djazouli

  3. Institute of Experimental Botany of the Czech Academy of Sciences, Prague, Czechia

    Petre I. Dobrev & Vaclav Motyka

Authors
  1. Salima Benazzouk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Petre I. Dobrev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zahr-Eddine Djazouli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vaclav Motyka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stanley Lutts
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stanley Lutts.

Additional information

Responsible Editor: Wieland Fricke.

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 46 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Benazzouk, S., Dobrev, P.I., Djazouli, ZE. et al. Positive impact of vermicompost leachate on salt stress resistance in tomato (Solanum lycopersicum L.) at the seedling stage: a phytohormonal approach. Plant Soil 446, 145–162 (2020). https://doi.org/10.1007/s11104-019-04361-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04361-x

Keywords

Search

Navigation