Skip to main content
SpringerLink
Log in

Case study of a biological control: Geobacillus caldoxylosilyticus (IRD) contributes to alleviate salt stress in maize (Zea mays L.) plants

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The inevitable exposure of crop plants to salt stress is a major environmental problem emerged from the presence of excess NaCl radicals in the soil. Handling the problem in maize plants using a biological agent was the main interest of the present study. The non-pathogenic, halophytic, facultative aerobic bacterium Geobacillus caldoxylosilyticus IRD that was isolated from Marakopara pond in the Atoll Tikehau (French Polynesian, 2005) and found tolerant to salt stress until 3.5% NaCl (w/v). An artificial symbiosis was achieved by inoculating Geobacillus sp. into 5-day-old maize cultivars of triple hybrids (321 and 310) and singlet hybrids (10 and 162). Thereafter, maize seedlings were exposed to 350 mmol NaCl for 10 days. The data revealed that Geobacillus sp. had interacted with salinized maize and improved maize overall growth, dry weight and relative water content. Na+ accumulation was six times less and Cl− accumulation was 13 times less in the tips of salinized maize seedlings upon Geobacillus sp. inoculation. Salinized maize without Geobacillus viewed decayed cortical cells of seedlings. In addition, proline content was two times higher in salinized seedlings lacking Geobacillus. Photosynthetic pigments and antioxidant enzymes were significantly regulated upon inoculation. Beyond this study, we presented a novel insight into a possible role of Geobacillus caldoxylosilyticus bacteria in controlling/protecting maize plants against high salt stress.

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

Similar content being viewed by others

References

  • Abdelkader AF, Henrik A, Katalin S, Bela B, Christer S (2007) High salt stress induces swollen prothylakoids in dark grown wheat and alters both prolamellar body transformation and alters both prolamellar body transformation and reformation after irradiation. J Exp Bot 58:2553–2564

    Article  PubMed  CAS  Google Scholar 

  • Aebi HE (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. 3:273–286

  • Ahmed S, Scopes RK, Rees GN, Patel KC (2000) Saccharococcus caldoxylosilyicus sp.nov., an obligatory thermophilic, xylose-utilizing, endospore-forming bacterium. Int J Syst Evol Microbiol 50:517–523

    Article  Google Scholar 

  • Alberico GL, Cramer GR (1993) Is the salt tolerance of maize related to sodium exclusion? I. Preliminary screening of seven cultivars. J Plant Nutr 16:2289–2303

    Article  Google Scholar 

  • Aspinall D, Paleg LG (1981) Proline accumulation: physiological aspects. In: Paleg LG, Aspinall D (eds) The physiology and biochemistry of drought resistance in plants. Academic Press, Sydney, pp 205–241

    Google Scholar 

  • Azevedo Neto AD, Tabosa JN (2000) Salt stress in maize seedlings: I. Growth analysis. Rev Bras Eng Agric Amb 4:159–164

    Google Scholar 

  • Azevedo Neto AD, Prisco JT, Enéas-Filho J, De Lacerda CF, Silva JV, Da Costa PHA, Gomes-Filho E (2004) Effects of salt stress on plant growth, stomatal response and solute accumulation of different maize genotypes. Braz J Plant Physiol 16:31–38

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Binzel ML, Hasegawa PM, Rhodes D, Handa S, Handa AK, Bressan RA (1987) Solute accumulation in tobacco cells adapted to NaCl. Plant Physiol 84:1408–1415

    Article  PubMed  CAS  Google Scholar 

  • Bohnert HJ, Shen B (1999) Transformation and compatible solutes. Sci Hortic 78:237–260

    Article  CAS  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 1158–1203

    Google Scholar 

  • Brown JD, Lilleland O (1946) determination of potassium and sodium in plant material and soil extracts by flame photometry. Proc Am Soc Hort Sci 12:341–364

    Google Scholar 

  • Chanway CP (1997) Inoculation of tree roots with plant growth promoting soil bacteria (an emerging technique for reforestation. For Sci 43:99–112

    Google Scholar 

  • Chapman SB (1976) Methods in plant ecology. Blackwell, Oxford, pp 96–97

  • Chen CT, Chen LM, Lin CC, Kao CH (2001) Regulation of proline accumulation in detected rice leaves exposed to excess copper. Plant Sci 160:283–290

    Article  PubMed  CAS  Google Scholar 

  • Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168:241–248

    Article  CAS  Google Scholar 

  • Curtis PS, Lauchli A (1987) The effect of moderate salt stress on leaf anatomy in Hibiscus cannabinus (kenaf) and its relation to leaf area. Am J Bot 74:538–542

    Article  CAS  Google Scholar 

  • Esawy MA, Wafaa A, Samia H, Ahmed A, Combet Y (2007) Natural material role in production, activation and stabilization of alkaline protease produced from a new isolated Geobacillus caldoxylosilyticus IRD. J Appl Sci Res 10:1062–1068

    Google Scholar 

  • Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142

    Article  Google Scholar 

  • Fortmeier R, Schubert S (2006) Salt tolerance of maize (Zea mays L.): the role of sodium exclusion. Plant Cell Environ 11:1041–1047

    Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  CAS  Google Scholar 

  • Fricke W, Peters WS (2002) The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Plant Physiol 129:374–388

    Article  PubMed  CAS  Google Scholar 

  • Gadallah MAA (1993) Effect of water stress, abscisic acid and proline in cotton plants. J Arid Environ 30:315–325

    Article  Google Scholar 

  • Gilbert GA, Gadush MV, Wilson C, Madore MA (1998) Amino acid accumulation in sink and source tissues of Coleus blumei Benth during salinity stress. J Exp Bot 49:107–114

    Article  CAS  Google Scholar 

  • Gzik A (1996) Accumulation of proline and α-amino acids in sugar beet plants in response to osmotic, water and salt stress. Environ Exp Bot 36:29–38

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1993) Free radicals in biology and medicine, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • Havir EA, Mellate NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455

    Article  PubMed  CAS  Google Scholar 

  • Hungate RE, Macy J (1973) The roll-tube method for cultivation of strict anaerobes. In: Norris JR, Ribbons DW (eds) Method in microbiology, 3B. Academic Press Inc., New York, p 132

    Google Scholar 

  • Israr M, Sahi SV (2006) Antioxidative responses to mercury in the cell cultures of Sebania drummondii. Plant Physiol Biochem 44:590–595

    Article  PubMed  CAS  Google Scholar 

  • Jain S, Nainawatee HS, Jain RK, Chowdhury JB (1991) Proline status of genetically stable salt-tolerant Brassica juncea L. somaclones and their parent cv. Prakash. Plant Cell Rep 9:684–687

    Article  CAS  Google Scholar 

  • Jordan BR, James PE, Strid A, Anthony RG (1994) The effect of ultraviolet-B radiation on gene expression and pigment composition in etiolated and green pea leaf tissue UV-B induced changes are gene-specific and dependent upon the developmental stage. Plant Cell Environ 17:45–54

    Article  CAS  Google Scholar 

  • Katerji N, Van Hoorn JW, Hamdy A, Karam F, Mastrorilli A (1996) Effect of salinity on water stress, growth, and yield of maize and sunflower. Agric Water Manage 30:237–249

    Article  Google Scholar 

  • Kijne JW (2006) Abiotic stress and water scarcity: identifying and resolving conflicts from plant level to global level. Field Crop Res 97:3–18

    Article  Google Scholar 

  • Kong FX, Hu W, Chso SY, Sang WL, Wang LS (1999) Physiology responses of the lichen Xanthoparmelia mexicana to oxidative stress of SO2. Environ Exp Bot 42:201–209

    Article  CAS  Google Scholar 

  • Lafitte R (2002) Relationship between leaf relative water content during reproductive stage water deficit and grain formation in rice. Field Crop Res 76:165–174

    Article  Google Scholar 

  • Liu J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 2:591–596

    Article  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  PubMed  CAS  Google Scholar 

  • Mansour MMF (2000) Nitrogen containing compounds and adaptation of plants to salinity stress. Biol Plant 43:491–500

    Article  CAS  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    Article  PubMed  CAS  Google Scholar 

  • Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76

    Article  CAS  Google Scholar 

  • Metzner H, Ranum H, Senger H (1965) Unterschungen zur sychno-nisier-Barkiet einze-Iner Pigmenmangel- Mutanten-von Chloprella. Planta 65:186

    Article  CAS  Google Scholar 

  • Monreal JA, Jiménez ET, Remesal E, Morillo-Velarde R, García-Mauriño S, Echevarría C (2007) Proline content of sugar beet storage roots: response to water deficit and nitrogen fertilization at field conditions. Environ Exp Bot 60:257–267

    Article  CAS  Google Scholar 

  • Moradi F, Ismail AM, Gregoria GB, Egdane JA (2003) Salinity tolerance of rice during reproductive development and association with tolerance at the seedling level. Ind J Plant Physiol 8:276–278

    Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  PubMed  CAS  Google Scholar 

  • Ozturk A, Unlukara A, Ipek A, Gurbuz B (2004) Effects of salt stress and water deficit on plant growth and essential oil content of lemon balm (Melisa officinalis L.). Pak J Bot 36:787–792

    Google Scholar 

  • Parmar NG, Vithalani SD, Chanda SV (2002) Alteration in growth and peroxidase activity by heavy metals in Phaseolus vulgaris. Acta Physiol Plant 24:89–95

    Article  CAS  Google Scholar 

  • Rai AK, Takabe T (2006) A biotic stress tolerance in plants toward the improvement of global environment and food. Springer, Berlin, pp 1–267

  • Rai V, Vajpayee P, Singh SN, Mehrotra S (2004) Effect of Chromium accumulation in photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167:1159–1169

    Article  CAS  Google Scholar 

  • Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1046

    Article  CAS  Google Scholar 

  • Sari AO, Ceylan A (2002) Yield characteristics and essential oil composition of lemon balm (Melissa officinalis L.) grown in the Aegean region in Turkey. Turk J Agric For 26:217–224

    CAS  Google Scholar 

  • Sudhakar C, Lakshmi A, Giridarakumar S (2002) Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161:613–619

    Article  Google Scholar 

  • Sun Y (1990) Free radicals, antioxidant enzymes, and carcinogenesis. Free Radic Biol Med 8:583–599

    Article  PubMed  CAS  Google Scholar 

  • Turcsányi E, Vass I (2000) Inhibition of photosynthetic electron transport by UV-A radiation targets the photosystem II complex. Photochem Photobiol 72:513–520

    Article  PubMed  Google Scholar 

  • Weatherley PE (1950) Studies in the water relations of the cotton plant 10 the field measurements of water deficits in leaves. New Phytol 49:81–87

    Article  Google Scholar 

  • Weatherley PE, Barrs C (1962) A re-examination of the relative turgidity technique for estimating water deficit in leaves. Aust J Biol Sci 15:413–428

    Google Scholar 

  • Weller DM (1988) Biological control of soil borne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407

    Article  Google Scholar 

  • Yilmaz K, Akinci IE, Akinci S (2004) Response of tomato (Lycopersicon esculentum Mill.) to salinity in the early growth stages for agricultural cultivation in saline environments. J Environ Biol 25:351–357

    PubMed  Google Scholar 

  • Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 112:152–166

    Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Yannick Combet for offering facilities in ‘Laboratoire de microbiologie, IRD, IFR-BAIM, Universités de Provence et de la Méditerranée, ESIL case 925, 13288 Marseille Cedex 9, France’ during isolation and characterization of Geobacillus caldoxylosilyticus. The authors would like to thank the technician Medhat Zareef for his assistance during the microscopic examinations.

Author information

Authors and Affiliations

  1. Department of Botany, Faculty of Science, Ain Shams University, Abbassia, Cairo, 11566, Egypt

    Amal Fadl Abdelkader

  2. Department of Chemistry of Natural and Microbial Products, National Research Center, Dokki, Giza, 12622, Egypt

    Mona Abdeltawab Esawy

  3. Department of Plant Science, Faculty of Science, Ain Shams University, Abbassia, Cairo, 11566, Egypt

    Amal Fadl Abdelkader

Authors
  1. Amal Fadl Abdelkader
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mona Abdeltawab Esawy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amal Fadl Abdelkader.

Additional information

Communicated by B. Barna.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abdelkader, A.F., Esawy, M.A. Case study of a biological control: Geobacillus caldoxylosilyticus (IRD) contributes to alleviate salt stress in maize (Zea mays L.) plants. Acta Physiol Plant 33, 2289–2299 (2011). https://doi.org/10.1007/s11738-011-0769-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-011-0769-x

Keywords

Search

Navigation