Log in

Immobilized microalgae and bacteria improve salt tolerance of tomato seedlings grown hydroponically

  • 5th Congress of the International Society for Applied Phycology
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Wild-type Azospirillum brasilense Cd, mutant Azospirillum brasilense Cd transformed bacteria with a plasmid harboring a trehalose biosynthesis gene fusion from Saccharomyces cerevisiae, and Chlorella vulgaris were used as immobilized inoculants for tomato seedlings growing in hydroponic media prepared with different proportions of NaCl. Stem and main root length, number and length of leaves, and secondary roots of seedlings were measured and compared between treatments as indicator of biomass production. A positive effect in tomato seedlings was observed when co-cultured with Azospirillum (transformed and wild type) and C. vulgaris. Those seedlings growing with wild-type Azospirillum and Chlorella showed longer stems for lower salinities. Conversely, longer stems were observed when transformed Azospirillum and C. vulgaris were used as inoculant in the highest salinity tested (250 mM NaCl).

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Albacete A, Martínez-Andújar C, Ghanem ME, Acosta M, Sánchez-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 32:928–938

    Article  CAS  PubMed  Google Scholar 

  • Almeida P, Feron R, de Boer G-J, de Boer AH (2014) Role of Na+, K+, Cl, proline and sucrose concentrations in determining salinity tolerance and their correlation with the expression of multiple genes in tomato. AoB Plants 6:1–13

    Article  Google Scholar 

  • Bacilio M, Rodriguez H, Moreno M et al (2004) Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum. Biol Fertil Soils 40:188–193

    Article  CAS  Google Scholar 

  • Bashan Y (1991) Changes in membrane potential of intact soybean root elongation zone cells induced by Azospirillum brasilense. Can J Microbiol 37:958–963

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bashan Y, Alcaraz-Melendez L, Toledo G (1992) Responses of soybean and cowpea root membranes to inoculation with Azospirillum brasilense. Symbiosis 13:217–228

    Google Scholar 

  • Bashan Y, Hernandez J-P, Leyva L, Bacilio M (2002) Alginate microbeads as inoculant carriers for plant growth-promoting bacteria. Biol Fertil Soils 35:359–368

    Article  Google Scholar 

  • Bashan Y, Salazar B, Puente ME, Bacilio M, Linderman R (2009) Enhanced establishment and growth of giant cardon cactus in an eroded field in the Sonoran Desert using native legume trees as nurse plants aided by plant growth-promoting microorganisms and compost. Biol Fertil Soils 45:585–594

    Article  Google Scholar 

  • Bashan Y, Salazar BG, Moreno M, Lopez BR, Linderman RG (2012) Restoration of eroded soil in the Sonoran Desert with native leguminous trees using plant growth-promoting microorganisms and limited amounts of compost and water. J Env Manage 102:26–36

  • Bischoff H, Bold H (1963) Some soil algae from Enchanted Rock and related algal species. Phycol Stud Univ Tex Publ 4:1–95

    Google Scholar 

  • Cong PT, Dung TD, Hien TM, Hien NT, Choudhury ATMA, Kecskés ML, Kennedy IR (2009) Inoculant plant growth-promoting microorganisms enhance utilisation of urea-N and grain yield of paddy rice in southern Vietnam. Eur J Soil Biol 45:52–61

    Article  CAS  Google Scholar 

  • Cuartero J, Fernández-Muñoz R (1999) Tomato and salinity. Sci Hortic 78:83–125

    Article  CAS  Google Scholar 

  • de-Bashan L, Bashan Y (2003) Bacterias promotoras de crecimiento de microalgas: una nueva aproximación en el tratamiento de aguas residuales. Rev Colomb Biotecnol 5:85–90

    CAS  Google Scholar 

  • de-Bashan L, Bashan Y (2010) Immobilized microalgae for removing pollutants: review of practical aspects. Bioresour Technol 101:1611–1627

    Article  CAS  PubMed  Google Scholar 

  • de-Bashan L, Hernandez J-P, Morey T, Bashan Y (2004) Microalgae growth-promoting bacteria as “helpers” for microalgae: a novel approach for removing ammonium and phosphorus from municipal wastewater. Water Res 38:466–474

    Article  CAS  PubMed  Google Scholar 

  • de-Bashan L, Antoun H, Bashan Y (2008a) Involvement of indole-3-acetic acid produced by the growth-promoting bacterium Azospirillum spp. in promoting growth of Chlorella vulgaris. J Phycol 44:938–947

    Article  CAS  PubMed  Google Scholar 

  • de-Bashan L, Magallon P, Antoun H, Bashan Y (2008b) Role of glutamate dehydrogenase and glutamine synthetase in Chlorella vulgaris during assimilation of ammonium when jointly immobilized with the microalgae-growth-promoting bacterium Azospirillum brasilense. J Phycol 44:1188–1196

    Article  CAS  PubMed  Google Scholar 

  • de-Bashan L, Hernandez J-P, Bashan Y (2012) The potential contribution of plant growth-promoting bacteria to reduce environmental degradation—a comprehensive evaluation. Appl Soil Ecol 61:171–189

    Article  Google Scholar 

  • Debouba M, Gouia H, Suzuki A, Ghorbel MH (2006a) NaCl stress effects on enzymes involved in nitrogen assimilation pathway in tomato “Lycopersicon esculentum” seedlings. J Plant Physiol 163:1247–1258

    Article  CAS  PubMed  Google Scholar 

  • Debouba M, Gouia H, Valadier M-H, Ghorbel MH, Suzuki A (2006b) Salinity-induced tissue-specific diurnal changes in nitrogen assimilatory enzymes in tomato seedlings grown under high or low nitrate medium. Plant Physiol Biochem 44:409–419

    Article  CAS  PubMed  Google Scholar 

  • Eskew D, Focht D, Ting I (1977) Nitrogen fixation, denitrification, and pleomorphic growth in a highly pigmented Spirillum lipoferum. Appl Environ Microbiol 34:582–585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez LE, Bashan Y (2000) Increased growth of the microalga Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant-growth-promoting bacterium Azospirillum brasilense. Appl Environ Microbiol 66:1527–1531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallmann A (2007) Algal transgenics and biotechnology. Transgenic Plant J 1:81–98

    Google Scholar 

  • Hernandez J-P, de-Bashan L, Bashan Y (2006) Starvation enhances phosphorus removal from wastewater by the microalga Chlorella spp. co-immobilized with Azospirillum brasilense. Enzym Microb Technol 38:190–198

    Article  CAS  Google Scholar 

  • Jensen MH, Malter AJ (1995) Protected agriculture: a global review World Bank Technical Paper #253. 157

  • Long X-H, Chi J-H, Liu L, Li Q, Liu Z-P (2009) Effect of seawater stress on physiological and biochemical responses of five Jerusalem Artichoke ecotypes. Pedosphere 19:208–216

  • López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 62:176–184

    Article  Google Scholar 

  • Miransari M (2011) Soil microbes and plant fertilization. Appl Microbiol Biotechnol 92:875–885

    Article  CAS  PubMed  Google Scholar 

  • Mohammad M, Shibli R, Ajlouni M, Nimri L (1998) Tomato root and shoot responses to salt stress under different levels of phosphorus nutrition. J Plant Nutr 21:1667–1680

    Article  CAS  Google Scholar 

  • Najafpour G, Younesi H, Syahidah Ku Ismail K (2004) Ethanol fermentation in an immobilized cell reactor using Saccharomyces cerevisiae. Bioresour Technol 92:251–260

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechnol 75:1143–1150

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Rodríguez A, Stella A, Storni M, Zulpa G, Zaccaro MC (2006) Effects of cyanobacterial extracellular products and gibberellic acid on salinity tolerance in Oryza sativa L. Saline Syst 2:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Salazar J, Suárez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59

    Article  PubMed  Google Scholar 

  • Snapp SS, Shennan C (1992) Effects of salinity on root growth and death dynamics of tomato, Lycopersicon esculentum Mill. New Phytol 121:71–79

    Article  Google Scholar 

  • Suárez R, Wong A, Ramírez M, Barraza A, Orozco Mdel C, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in Rhizobia. Mol Plant Microbe Interact 21:958–966

    Article  PubMed  Google Scholar 

  • Trivedi P, Pandey A (2008) Recovery of plant growth-promoting rhizobacteria from sodium alginate beads after 3 years following storage at 4 degrees C. J Ind Microbiol Biotechnol 35:205–209

    Article  CAS  PubMed  Google Scholar 

  • Yabur R, Bashan Y, Hernández-Carmona G (2007) Alginate from the macroalgae Sargassum sinicola as a novel source for microbial immobilization material in wastewater treatment and plant growth promotion. J Appl Phycol 19:43–53

    Article  CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  CAS  PubMed  Google Scholar 

  • Zawoznik MS, Ameneiros M, Benavides MP, Vázquez S, Groppa MD (2011) Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings. Appl Microbiol Biotechnol 90:1389–1397

    Article  CAS  PubMed  Google Scholar 

  • Zribi L, Fatma G, Fatma R, Salwa R, Hassan R, Néjib RM (2009) Application of chlorophyll fluorescence for the diagnosis of salt stress in tomato “Solanum lycopersicum (variety Rio Grande)”. Sci Hort 120:367–372

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Froylán M. E. Escalante.

Additional information

Froylán M. E. Escalante and Ramón Suárez contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure 13

Comparison of the averaged salinity (NaCl) effects in stem length for different inoculants. Columns denoted by a different lower case letter for each salinity level differ significantly at p≤0.05 using a multifactorial ANOVA. Bars represent LSD intervals. (GIF 63 kb)

High resolution image (TIFF 24680 kb)

Figure 14

Comparison of the averaged salinity (NaCl) effects in main root length for different inoculants. Columns denoted by a different lower case letter for each salinity level differ significantly at p≤0.05 using a multifactorial ANOVA. Bars represent LSD intervals. (GIF 68 kb)

High resolution image (TIFF 24677 kb)

Figure 15

Comparison of the averaged salinity (NaCl) effects in secondary roots length for different inoculants. Columns denoted by a different lower case letter for each salinity level differ significantly at p≤0.05 using a multifactorial ANOVA. Bars represent LSD intervals. (GIF 67 kb)

High resolution image (TIFF 24677 kb)

Figure 16

Comparison of the averaged inoculant effects in the number of secondary roots at different salinities, expressed as sodium chloride. Columns denoted by a different lower case letter for each inoculating treatment differ significantly at p≤0.05 using a multifactorial ANOVA. Bars represent LSD intervals. (GIF 60 kb)

High resolution image (TIFF 24677 kb)

Figure 17

Comparison of the averaged salinity (NaCl) effects in the number of secondary roots for different inoculants. Columns denoted by a different lower case letter for each salinity level differ significantly at p≤0.05 using a multifactorial ANOVA. Bars represent LSD intervals. (GIF 60 kb)

High resolution image (TIFF 24677 kb)

Figure 18

Comparison of the averaged salinity (NaCl) effects in leaves length for different inoculants. Columns denoted by a different lower case letter for each salinity level differ significantly at p≤0.05 using a multifactorial ANOVA. Bars represent LSD intervals. (GIF 62 kb)

High resolution image (TIFF 24677 kb)

Figure 19

Averaged number of leaves in seedlings grouped by inoculant used. Columns denoted by a different lower case letter differ significantly at p≤0.05 using a one-way ANOVA. Bars represent LSD intervals. (GIF 14 kb)

High resolution image (TIFF 24675 kb)

Table 1

(DOC 36 kb)

Table 2

(DOC 36 kb)

Table 3

(DOC 36 kb)

Table 4

(DOC 36 kb)

Table 5

(DOC 36 kb)

Table 6

(DOC 36 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Escalante, F.M.E., Cortés-Jiménez, D., Tapia-Reyes, G. et al. Immobilized microalgae and bacteria improve salt tolerance of tomato seedlings grown hydroponically. J Appl Phycol 27, 1923–1933 (2015). https://doi.org/10.1007/s10811-015-0651-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-015-0651-0

Keywords

Navigation