Skip to main content
Log in

Biochemical mechanisms of induced resistance by rhizobial lipopolysaccharide in pea against crenate broomrape

  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Lipopolysaccharides (LPS) isolated from rhizobia have been demonstrated as inducer of systemic resistance against plant diseases. The role of bacterial LPS in induced resistance in plant has not been extensively reported. The capacity of Rhizobium leguminosarum Mabrouk et al. 2007 strain P.SOM to reduce parasitism of pea by Orobanche crenata Mabrouk et al. 2007 was previously demonstrated under greenhouse and field trials. The objective of this study was to examine the capacity of LPS isolated from strain P.SOM to induce resistance in pea against crenate broomrape, with more emphasis on the biochemical mechanisms of host plant defense reaction induced by LPS. Root chamber experiments using Petri dishes revealed that LPS reduce broomrape seed germination and restricted the broomrape attachment to the host root as well as retarded tubercle formation and development. In pot experiments, pea roots treatment with LPS reduced the total number of broomrape by up to 95 %. No biomass reduction of pea was observed after application of LPS. Broomrape necrosis was observed both before and after parasite attachment to treated pea roots in Petri dishes and pots experiments. Concomitantly, reduction in infection was accompanied by enhanced phenylalanine ammonia lyase, peroxidase, and polyphenoloxidase activities. As a consequence, the derived products, phenolics, and pisatin accumulated in response to LPS and conferred mechanical and chemical barriers to the invading parasite. Our findings indicate an important role for LPS as a direct inducer of defenses in pea against broomrape.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Bailey BA, Bae H, Strem MD, Crozier J, Thomas SE, Samuels GJ, Vinyard BT, Holmes KA (2008) Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biol Control 46:24–35

    Article  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe associated molecular patterns and danger signals by pattern recognition receptors. Annu Rev Plant Biol 60:379–406

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein dye binding. Anal Biochem 72:248–254

  • Crews LJ, McCully ME, Canny MJ (2003) Mucilage production by wounded xylem tissue of maize roots time course and stimulus. Funct Plant Biol 30:755–766

    Article  CAS  Google Scholar 

  • Daayf F, Bel-Rhlad R, Belanger RR (1997) Methyl ester of p-coumaric acid- a phytoalexin like compound from long English cucumber leaves. J Chem Ecol 23:1517–1526

    Article  CAS  Google Scholar 

  • De Meyer G, Höfte M (1998) Induction of systemic resistance by the rhizobacterium Pseudomonas aeruginosa 7NSK2 is a salicylic acid dependent phenomenon in tobacco. IOBC Bull 21:117–122

    Google Scholar 

  • Downie JA (2010) The roles of extracellular proteins polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 342:150–170

    Article  Google Scholar 

  • Gerber IB, Zeidler D, Durner J, Dubery IA (2004) Early perception responses of Nicotianasacum cells in response to lipopolysaccharides from Burkholderia cepacia. Planta 218:647–657

    Article  CAS  PubMed  Google Scholar 

  • Hasky-Günther K, Hoffmann-Hergarten S, Sikora RA (1998) Resistanceagainst the potato cyst nematode Globodera pallida systemically induced by the rhizobacteria Agrobacterium radiobacter G12. and Bacillus sphaericus B43. Fundam Appl Nematol 21:511–517

    Google Scholar 

  • Hassanein AM, El-Garhy AM, Mekhemar GAA (2006) Symbiotic nitrogen fixation process in faba bean and chickpea as affected by biological and chemical control of root–rot. J Agric Sci Mansoura Univ 31:963–980

    Google Scholar 

  • Hemissi I, Mabrouk Y, Abdi N, Bouraoui M, Saidi M, Sifi B (2013) Growth promotion and protection against Orobanche foetida of chickpea Cicer aerietinum. by two Rhizobium strains under greenhouse conditions. Afr J Biotechnol 12:1371–1377

    Google Scholar 

  • Jetiyanon K, Plianbangchang P (2013) Lipopolysaccharide of Enterobacter asburiae strain RS83: a bacterial determinant for induction of early defensive enzymes in Lactuca sativa against soft rot disease. Biol Control 67:301–307

    Article  CAS  Google Scholar 

  • Kutkowska J, Turska-Szewczuk A, Janczarek M, Paduch R, Kamińska T, Urbanik-Sypniewska T (2011) Biological activity of lipo.polysaccharides of the exopolysaccharide-deficient mutant Rt120 derived from Rhizobium leguminosarum bv. trifolii strain TA1. Biochem Mosc 767:840–850

    Article  Google Scholar 

  • Labrousse P, Arnaud MC, Serieys H, Berville A, Thalouarn P (2001) Several mechanisms are involved in resistance of Helianthus to Orobanche cumana Wallr. Ann Bot 88:859–868

    Article  Google Scholar 

  • Leeman M, Van Pelt JA, Den Ouden FM, Heinsbroek M, Bakker PAHM, Schippers B (1995) Induction of systemic resistance against Fusarium wilt of radish by lipopolysaccharides of Pseudomonas yuorescens. Phytopathology 85:1021–1027

    Article  CAS  Google Scholar 

  • Liu L, Kloepper J, Tuzun S (1995) Induction of systemic resistance in cucumber against Fusarium wilt by plant growth-promoting rhizobacteria. Phytopathology 85:695–698

    Article  Google Scholar 

  • Mabrouk Y, Belhadj O (2014) Effect of the inoculation of chickpea by rhizobia on growth promotion and protection against Orobanche crenata. Glob J Biol Agric Health Sci 3:55–59

    Google Scholar 

  • Mabrouk Y, Zourgui L, Sifi B, Delavault P, Simier P, Belhadj O (2007) Some compatible Rhizobium leguminosarum strains in peas decrease infections when parasitised by Orobanche crenata. Weed Res 47:44–53

    Article  Google Scholar 

  • Madala NE, Molinaro A, Dubery IA (2012) Distinct carbohydrate and lipid-based molecular patterns within lipopolysaccharides from Burkholderia cepacia contribute to defense-associated differential gene expression in Arabidopsis thaliana. Innate Immun 18:140–154

    Article  CAS  PubMed  Google Scholar 

  • Müller P, Zähringer U, Rudolph K (1998) Induced resistance bybacterial lipopolysaccharides LPS. Plant pathogenic bacteria. In: Proceedings of the 9th international conference, Centre for Advanced Study in Botany, University of Madras, Madras, 569–575

  • Newman M, Dow JM, Molinaro A, Parrilli M (2007) Priming induction and modulation of plant defense responses by bacterial lipopolysaccharides. J Endotoxin Res 13:69–84

    Article  CAS  PubMed  Google Scholar 

  • Novák K, Lisá L, Skrdleta V (2004) Rhizobial nod gene-inducing activity in pea nodulation mutants: dissociation of nodulation and flavonoid response. Physiol Plant 120:546–555

    Article  PubMed  Google Scholar 

  • Reitz M, Rudolph K, Schröder I, Hoffmann-Hergarten S, Hallman J, Sikora RA (2000) Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl Environ Microbiol 66:3515–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reitz M, Oger P, Meyer A, Niehaus K, Farrand SK, Hallmann J, Sikora RA (2002) Importance of the O-antigen core-region and lipid A of rhizobial lipopolysaccharides for the induction of systemic resistance in potato to Globodera pallida. Nematology 4:73–79

    Article  CAS  Google Scholar 

  • Sahm A, Pfanz H, Grunsfelder M, Czygan FC, Proksch P (1995) Anatomy and phenyl propanoid metabolism in the incompatible interaction of Lycopersicom esculentum and Cuscuta reflexa. Bot Acta 108:358–364

    Article  CAS  Google Scholar 

  • Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14:54–61

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui ZA, Akhtar MS (2007) Biocontrol of a chickpea root rot disease complex with phosphate- solubilizing microorganisms. J Plant Pathol 9:67–77

    Google Scholar 

  • Sidhu VK, Vorhölter FJ, Niehaus K, Watt SA (2008) Analysis of outer membrane vesicle associated proteins isolated from the plant pathogenic bacterium Xanthomonas campestris pv. campestris. BMC Microbiol 8:87

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Peer R, Schippers B (1992) Lipopolysaccharides of plant growth promoting Pseudomonas spp. Strain WCS417r induce resistance in carnation to Fusarium wilt. Neth J Plant Pathol 98:129–139

    Article  CAS  Google Scholar 

  • van Peer R, Niewmann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728–734

    Article  Google Scholar 

  • Van Wees SCM, Pieterse CMJ, Trijssenaar A, Van ‘t westende Y, Hartog F, Van Loon LC (1997) Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant-Microbe Interact 10:716–724

    Article  CAS  PubMed  Google Scholar 

  • Waterman PG, Mole S (1994) Analysis of phenolics plant metabolites. Blackwell Scientific Publications, Oxford

  • Westphal O, Jann K (1965) Bacterial lipopolysaccharides. Methods Carbohydr Chem 5:83–91

    CAS  Google Scholar 

  • Zeidler D, Zähringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana, lipopolysaccharides activate nitric oxide synthase NOS. and induce defense genes. Proc Natl Acad Sci USA 101(44):15811–15816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Zhou JM (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work is funded by the project “PHC Utique 13G0925” managed by the Joint University Committee of Cooperation (Tunisia-France).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yassine Mabrouk.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mabrouk, Y., Mejri, S. & Belhadj, O. Biochemical mechanisms of induced resistance by rhizobial lipopolysaccharide in pea against crenate broomrape. Braz. J. Bot 39, 107–114 (2016). https://doi.org/10.1007/s40415-015-0219-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-015-0219-x

Keywords

Navigation