Skip to main content
SpringerLink
Log in

Biochemical changes by Azospirillum brasilense enhance jojoba rooting under salt stress

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Simmondsia chinensis “Jojoba” is an ever-green shrub, cultivated for its valuable liquid wax. This species is a dioecious plant and its sex cannot be phenotypically discriminated before flowering (3–4 years old plants). Therefore, in vitro culture allows mass propagation of jojoba and it may be used as a model system to study saline stress and biofertilization. The aim of this work was to evaluate biochemical changes induced by Azospirillum brasilense on jojoba in vitro rooting subjected to salt stress. Shoots were induced with 24.6 or 49.2 μM indole-3-butyric acid for 6 days in half-strength Murashige–Skoog medium with Gamborg vitamins and grown in an auxin-free medium supplemented with 0, 40 or 80 mM NaCl for 45 days. Inoculation was performed with 107 cfu of A. brasilense Az39 or Cd strains when shoots were transferred to auxin free medium. Non-inoculated shoots were used as controls. Azospirillum brasilense inoculation significantly enhanced growth and biochemical parameters, pigments, proteins, total sugars, lignin, phenolics and proline of salt-affected jojoba plants. Biochemical changes observed on salt-stressed jojoba plants were mitigated by both A. brasilense strains and could explain the higher tolerance to salinity of inoculated plants.

Key message

Azospirillum brasilense mitigated salt stress in jojoba in vitro rooting by changes in biochemical parameters.

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

  • Abdel Latef AAH, Abu Alhmad MF, Kordrostami M, Abo-Baker A-BA-E, Zakir A (2020) Inoculation with Azospirillum lipoferum or Azotobacter chroococum reinforces maize growth by improving physiological activities under saline conditions. J Plant Growth Regul 39(3):1293–1306

    CAS  Google Scholar 

  • Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7(1):18

    Google Scholar 

  • Agami RA, Medani RA, Abd El-Mola IA, Taha RS (2016) Exogenous application with plant growth promoting rhizobacteria (PGPR) or proline induces stress tolerance in basil plants (Ocimum basilicum L.) exposed to water stress. Int J Environ Agric Res 2(5):78

    Google Scholar 

  • Akbari M, Mahna N, Ramesh K, Bandehagh A, Mazzuca S (2018) Ion homeostasis, osmoregulation, and physiological changes in the roots and leaves of pistachio rootstocks in response to salinity. Protoplasma 255(5):1349–1362

    CAS  PubMed  Google Scholar 

  • Alghamdi BA, Bafeel SO, Edris S, Atef A, Al-Matary M, Bahieldin A (2021) Physiological and molecular mechanisms underlying salt stress tolerance in jojoba (Simmondsia chinensis). Appl Ecol Environ Res 19(3):1953–1982

    Google Scholar 

  • Al-Obaidi JR, Halabi MF, AlKhalifah NS, Asanar S, Al-Soqeer AA, Attia MF (2017) A review on plant importance, biotechnological aspects, and cultivation challenges of jojoba plant. Biol Res 50(1):1–9

    Google Scholar 

  • Bafeel SO, Galal HK, Basha AZ (2016) Effect of seawater irrigation on growth and some metabolites of jojoba plants. Am Eurasian J Agric Environ Sci 16:49–59

    CAS  Google Scholar 

  • Bashan Y, de-Bashan, L. E. (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. Adv Agron 108:77–136

    CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    CAS  Google Scholar 

  • Behrooz A, Vahdati K, Rejali F, Lotfi M, Sarikhani S, Leslie C (2019) Arbuscular mycorrhiza and plant growth-promoting bacteria alleviate drought stress in walnut. HortScience 54(6):1087–1092

    CAS  Google Scholar 

  • Behzadi Rad P, Roozban MR, Karimi S, Ghahremani R, Vahdati K (2021) Osmolyte accumulation and sodium compartmentation has a key role in salinity tolerance of pistachios rootstocks. Agriculture 11(8):708

    CAS  Google Scholar 

  • Benzioni A, Nerd A, Rosenärtner Y, Mills D (1992) Effect of NaCl salinity on growth and development of jojoba clones: I. Young plants. J Plant Physiol 139(6):731–736

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    CAS  PubMed  Google Scholar 

  • Cao Y-Y, Yang M-T, Chen S-Y, Zhou Z-Q, Li X, Wang X-J, Bai J-G (2015) Exogenous sucrose influences antioxidant enzyme activities and reduces lipid peroxidation in water-stressed cucumber leaves. Biol Plant 59(1):147–153

    CAS  Google Scholar 

  • Cassán F, Coniglio A, López G, Molina R, Nievas S, de Carlan CLN, Donadio F, Torres D, Rosas S, Pedrosa FO (2020) Everything you must know about Azospirillum and its impact on agriculture and beyond. Biol Fertil Soils 56(4):461–479

    Google Scholar 

  • Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58(15–16):4245–4255

    CAS  PubMed  Google Scholar 

  • Chen L, Liu Y, Wu G, Veronican Njeri K, Shen Q, Zhang N, Zhang R (2016) Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiol Plant 158(1):34–44

    CAS  PubMed  Google Scholar 

  • Drummond L, Maher W (1995) Determination of phosphorus in aqueous solution via formation of the phosphoantimonylmolybdenum blue complex. Re-examination of optimum conditions for the analysis of phosphate. Anal Chim Acta 302(1):69–74

    CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers P, t, & Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356

    CAS  Google Scholar 

  • Elmongy MS, Wang X, Zhou H, Xia Y (2020) Humic acid and auxins induced metabolic changes and differential gene expression during adventitious root development in Azalea microshoots. HortScience 55(6):926–935

    CAS  Google Scholar 

  • Fukami J, Ollero FJ, Megías M, Hungria M (2017) Phytohormones and induction of plant-stress tolerance and defense genes by seed and foliar inoculation with Azospirillum brasilense cells and metabolites promote maize growth. AMB Express 7(1):1–13

    CAS  Google Scholar 

  • Gamborg OL, Miller R, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50(1):151–158

    CAS  PubMed  Google Scholar 

  • García JE, Maroniche G, Creus C, Suárez-Rodríguez R, Ramirez-Trujillo JA, Groppa MD (2017) In vitro PGPR properties and osmotic tolerance of different Azospirillum native strains and their effects on growth of maize under drought stress. Microbiol Res 202:21–29

    PubMed  Google Scholar 

  • Gonzalez AJ, Larraburu EE, Llorente BE (2015) Azospirillum brasilense increased salt tolerance of jojoba during in vitro rooting. Ind Crops Prod 76:41–48. https://doi.org/10.1016/j.indcrop.2015.06.017

    Article  CAS  Google Scholar 

  • Gonzalez AJ, Larraburu EE, Llorente BE (2021) Azospirillum brasilense mitigates anatomical alterations produced by salt stress in jojoba in vitro plants. Vegetos 34(4):725–737. https://doi.org/10.1007/s42535-021-00275-1

    Article  Google Scholar 

  • Gurr SI, McPherson J, Bowles DJ (1992) Lignin and associated phenolic acids in cell walls. Mol Plant Pathol Pract Approach 3:62

    Google Scholar 

  • Hatfield R, Fukushima RS (2005) Can lignin be accurately measured? Crop Sci 45(3):832–839

    CAS  Google Scholar 

  • Hussain M, Park H-W, Farooq M, Jabran K, Lee D-J (2013) Morphological and physiological basis of salt resistance in different rice genotypes. Int J Agric Biol 15(1):113–118

    Google Scholar 

  • Iiyama K, Wallis AF (1990) Determination of lignin in herbaceous plants by an improved acetyl bromide procedure. J Sci Food Agric 51(2):145–161

    CAS  Google Scholar 

  • Jha Y (2017) Cell water content and lignification in maize regulated by rhizobacteria under salinity. Braz J Biol Sci 4(7):9–18

    Google Scholar 

  • Khadr A, Wang G-L, Wang Y-H, Zhang R-R, Wang X-R, Xu Z-S, Tian Y-S, Xiong A-S (2020) Effects of auxin (indole-3-butyric acid) on growth characteristics, lignification, and expression profiles of genes involved in lignin biosynthesis in carrot taproot. PeerJ 8:e10492

    PubMed  PubMed Central  Google Scholar 

  • Kumar A, Singh S, Gaurav AK, Srivastava S, Verma JP (2020) Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front Microbiol 11:1216

    PubMed  PubMed Central  Google Scholar 

  • Lastochkina O, Aliniaeifard S, Garshina D, Garipova S, Pusenkova L, Allagulova C, Fedorova K, Baymiev A, Koryakov I, Sobhani M (2021) Seed priming with endophytic Bacillus subtilis strain-specifically improves growth of Phaseolus vulgaris plants under normal and salinity conditions and exerts anti-stress effect through induced lignin deposition in roots and decreased oxidative and osmotic damages. J Plant Physiol 263:153462

    CAS  PubMed  Google Scholar 

  • Lima TR, Carvalho EC, Martins FR, Oliveira RS, Miranda RS, Müller CS, Pereira L, Bittencourt PR, Sobczak JC, Gomes-Filho E (2018) Lignin composition is related to xylem embolism resistance and leaf life span in trees in a tropical semiarid climate. N Phytol 219(4):1252–1262

    CAS  Google Scholar 

  • Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19(2):335

    PubMed  PubMed Central  Google Scholar 

  • Llorente BE, Apóstolo NM (2013) In vitro propagation of jojoba. In: Protocols for micropropagation of selected economically-important horticultural plants. Humana Press, Totowa, pp 19–31

  • Mahadik S, Kumudini BS (2020) Enhancement of salinity stress tolerance and plant growth in finger millet using fluorescent Pseudomonads. Rhizosphere 15:100226

    Google Scholar 

  • Mahmood S, Daur I, Hussain MB, Nazir Q, Al-Solaimani SG, Ahmad S, Bakhashwain AA, Elsafor AK (2017) Silicon application and rhizobacterial inoculation regulate mung bean response to saline water irrigation. Clean: Soil, Air, Water 45(8):1600436

    Google Scholar 

  • Mills D, Wenkart S, Benzioni A (1997) Micropropagation of Simmondsia chinensis (jojoba). In: High-tech and micropropagation VI. Springer, Berlin, pp 370–393

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651

    CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497

    CAS  Google Scholar 

  • Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22(6):4056–4075

    CAS  Google Scholar 

  • Patil SV, Kumudini BS (2019) Seed priming induced blast disease resistance in finger millet plants through phenylpropanoid metabolic pathway. Physiol Mol Plant Pathol 108:101428

    CAS  Google Scholar 

  • Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34(4):737–752

    Google Scholar 

  • Pérez-López AV, Lim SD, Cushman JC (2023) Tissue succulence in plants: carrying water for climate change. J Plant Physiol 189(11):154081

    Google Scholar 

  • Perez-Rosales E, Alcaraz-Meléndez L, Puente ME, Vázquez-Juárez R, Zenteno-Savín T, Morales-Bojórquez E (2018) Endophytic bacteria isolated from wild jojoba [Simmondsia chinensis L. (Schneider)] roots improve in vitro propagation. Plant Cell Tissue Organ Cult 135(3):515–522

    CAS  Google Scholar 

  • Qasim M, Younis A, Zahir ZA, Riaz A, Raza H, Tariq U (2014) Microbial inoculation increases the nutrient uptake efficiency for quality production of Gladiolus grandiflorus. Pak J Agric Sci 51(4):875–880

    Google Scholar 

  • Reddy MP, Chikara J (2010). Biotechnology advances in jojoba (Simmondsia chinensis). In: Desert plants. Springer, Berlin, pp 407–421

  • Rivarola V, Castro S, Mori G, Jofre E, Fabra A, Garnica R, Balegno H (1998) Response of Azospirillum brasilense Cd to sodium chloride stress. Antonie Van Leeuwenhoek 73:255–261

    CAS  PubMed  Google Scholar 

  • Rodríguez Cáceres EAR (1982) Improved medium for isolation of Azospirillum spp. Appl Environ Microbiol 44(4):990–991

    Google Scholar 

  • Roussos PA, Pontikis CA (2003) Long term effects of sodium chloride salinity on growing in vitro, proline and phenolic compound content of jojoba explants. Eur J Hortic Sci 68(1):38–44

    CAS  Google Scholar 

  • Taha RA (2014) Effect of growth regulators and salinity levels on in vitro cultures of jojoba plants. World Appl Sci J 31(5):751–758

    Google Scholar 

  • Telesiñski A, Nowak J, Smolik B, Dubowska A, Skrzypiec N (2008) Effect of soil salinity on activity of antioxidant enzymes and content of ascorbic acid and phenols in bean [Phaseolus vulgaris L.] plants. J Elementol 13(3):401–409

    Google Scholar 

  • Ueno K, Cheplick S, Shetty K (1998) Reduced hyperhydricity and enhanced growth of tissue culture-generated raspberry (Rubus sp.) clonal lines by Pseudomonas sp. Isolated from oregano. Process Biochem 33(4):441–445. https://doi.org/10.1016/S0032-9592(98)00011-9

    Article  CAS  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144(3):307–313

    CAS  Google Scholar 

  • Zafari F, Amiri ME, Noroozisharaf A, Almasi P (2018) Physiological and morphological responses of the ‘Dargazi’ pear (Pyrus communis) to in vitro salinity. Agric Conspectus Sci 83(2):169–174

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Yaacov Okon (Faculty of Agriculture, the Hebrew University of Jerusalem, Israel), Ing. Enrique Rodríguez Cáceres [National Agricultural Technology Institute (INTA), Castelar, Argentina] for kindly providing A. brasilense Cd and A. brasilense Az39 and Ing. NorbertoVinelli (La Semillera Riojana, La Rioja, Argentina) for kindly providing plant material. This research was supported by a grant from Departamento de Ciencias Básicas, Universidad Nacional de Luján, Luján (Bs As) Argentina.

Funding

This work was supported by Departamento de Ciencias Básicas, Universidad Nacional de Luján [Disp CD-CB 284/21].

Author information

Authors and Affiliations

  1. Laboratorio de Cultivo de Tejidos Vegetales (CULTEV), Departamento de Ciencias Básicas, Universidad Nacional de Luján, Luján, Buenos Aires, Argentina

    Ana J. Gonzalez, Mauro E. Yarte, Berta E. Llorente & Ezequiel E. Larraburu

  2. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Ezequiel E. Larraburu

Authors
  1. Ana J. Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mauro E. Yarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Berta E. Llorente
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ezequiel E. Larraburu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BEL, EEL, MEY and AJG were involved in research design, data analysis, and paper preparation. MEY and AJG were involved in plant cell tissue culture management and biochemicals techniques.

Corresponding author

Correspondence to Ezequiel E. Larraburu.

Ethics declarations

Conflict of interest

The authors have not disclosed any competing interests. The data that support the findings of this study are available from the corresponding author upon reasonable request.

Additional information

Communicated by Heidi Halbwirth.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gonzalez, A.J., Yarte, M.E., Llorente, B.E. et al. Biochemical changes by Azospirillum brasilense enhance jojoba rooting under salt stress. Plant Cell Tiss Organ Cult 156, 56 (2024). https://doi.org/10.1007/s11240-023-02665-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11240-023-02665-6

Keywords

Search

Navigation