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Cyanobacteria-mediated phenylpropanoids and phytohormones in rice (Oryza sativa) enhance plant growth and stress tolerance

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Abstract

Phenylpropanoids, flavonoids and plant growth regulators in rice (Oryza sativa) variety (UPR 1823) inoculated with different cyanobacterial strains namely Anabaena oryzae, Anabaena doliolum, Phormidium fragile, Calothrix geitonos, Hapalosiphon intricatus, Aulosira fertilissima, Tolypothrix tenuis, Oscillatoria acuta and Plectonema boryanum were quantified using HPLC in pot conditions after 15 and 30 days. Qualitative analysis of the induced compounds using reverse phase HPLC and further confirmation with LC-MS/MS showed consistent accumulation of phenolic acids (gallic, gentisic, caffeic, chlorogenic and ferulic acids), flavonoids (rutin and quercetin) and phytohormones (indole acetic acid and indole butyric acid) in rice leaves. Plant growth promotion (shoot, root length and biomass) was positively correlated with total protein and chlorophyll content of leaves. Enzyme activity of peroxidase and phenylalanine ammonia lyase and total phenolic content was fairly high in rice leaves inoculated with O. acuta and P. boryanum after 30 days. Differential systemic accumulation of phenylpropanoids in plant leaves led us to conclude that cyanobacterial inoculation correlates positively with plant growth promotion and stress tolerance in rice. Furthermore, the study helped in deciphering possible mechanisms underlying plant growth promotion and stress tolerance in rice following cyanobacterial inoculation and indicated the less explored avenue of cyanobacterial colonization in stress tolerance against abiotic stress.

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References

  • Ahmad F, Ahmad I, Aqil F, Khan MS, Hayat S (2008) Diversity and potential of nonsymbiotic diazotrophic bacteria in promoting plant growth. In: Ahmad I, Pitchel J, Hayat S (eds) Plant–bacteria interactions: strategies and techniques to promote plant growth. KGaA, Wiley-VCH, Verlag Gmbh and Co, Germany, pp 81–109

    Google Scholar 

  • Barriuso J, Ramos Solano B, Gutierrez Manero FJ (2008) Protection against pathogen and salt stress by four plant growth-promoting rhizobcteria isolated from Pinus sp. on Arabidopsis thaliana. Phytopathology 98:666–672

    Article  PubMed  CAS  Google Scholar 

  • Basha SA, Sarma BK, Singh DP, Annapurna K, Singh UP (2006) Differential methods of inoculation of plant growth-promoting rhizobacteria induce synthesis of phenylalanine-ammonia-lyase and phenolic compounds differentially in chickpea. Folia Microbiol 51:463–468

    Article  CAS  Google Scholar 

  • Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350

    Article  PubMed  CAS  Google Scholar 

  • Carreno-Lopez R, Campos-Reales N, Elmerich C, Baca BE (2000) Physiological evidence for differently regulated tryptophan-dependent pathways for indole-3-acetic acid synthesis in Azospirillum brasilance. Mol Gen Genet 264:521

    Article  PubMed  CAS  Google Scholar 

  • Cryl P, Karl G (2008) Secondary metabolites from cyanobacteria: complex structures and powerful bioactivities. Curr Org Chem. 12:326–341

    Article  Google Scholar 

  • Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    Article  PubMed  CAS  Google Scholar 

  • Egley GH, Paul RN, Vaughn KC, Duke SO (1983) Role of peroxidase in the development of water impermeable seeds coats in Sida spinosa L. Planta 157:224–232

    Article  CAS  Google Scholar 

  • Fadzilla NM, Finch RP, Burdon RH (1997) Salinity, oxidative stress and antioxidant responses in shoot cultures of rice. J Exp Biol 48:325–331

    CAS  Google Scholar 

  • Ferjani A, Mustardy L, Sulpice R, Marin K, Suzuki I, Hageman M, Murata N (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131:1628–1637

    Article  PubMed  CAS  Google Scholar 

  • Fernández VE, Ucha A, Quesada A, Leganés F, Carreres R (2000) Contribution of N2 fixing cyanobacteria to rice production: availability of nitrogen from 15N-labelled cyanobacteria and ammonium sulphate to rice. Plant Soil 221:107–112

    Article  Google Scholar 

  • Fletcher JS, Hedge RS (1995) Release of phenols by perennial plant roots and their potential importance in bioremediation. Environ Toxicol Chem 31:3009–3016

    CAS  Google Scholar 

  • Gao D, Du L, Yang J, Wu W-M, Hong Liang H (2010) A critical review of the application of white rot fungus to environmental pollution control. Crit Rev Biotechnol 30:70–77

    Article  PubMed  CAS  Google Scholar 

  • Glick B (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  • Graham HG (1992) Stabilization of the Prussian blue color in the determination of polyphenols. J Agri Food Chem 40:801–805

    Article  CAS  Google Scholar 

  • Gutierrez MFJ, Ramos Solano B, Probanja A, Mebouachi J, Tadeo FR, Talon M (2001) The plant growth-promoting rhizobcteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol. Plantarum 111:1–7

    Article  Google Scholar 

  • Inderjit, Keating KI (1999) Allelopathy: principles, procedures, processes and promises for biological control. In: Sparks DL (ed) Advances in agronomy. Academic Press, London, pp 142–207

    Google Scholar 

  • Karthikeyan N, Prasanna R, Lata N, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30

    Article  CAS  Google Scholar 

  • Kent AD, Triplet EW (2002) Microbial communities and their interactions in soil and rhizosphere ecosystems. Annu Rev Microbiol 56:211–236

    Article  PubMed  CAS  Google Scholar 

  • Khalid A, Arshad M, Zahir A (2006) Phytohormones: microbial production and applications. In: Uphoff N (ed) Biological approaches to sustainable soil systems. CRC Press, London, pp 207–220

    Chapter  Google Scholar 

  • Khan ZUM, Tahmida Begum ZN, Mandal R, Hossain MZ (1994) Cyanobacteria in rice soils. World J Microbiol Biotechnol 10:296–298

    Article  Google Scholar 

  • Kloepper JW, Scrhoth MN, Miller TD (1980) Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield. Phytopathology 70:1078–1082

    Article  Google Scholar 

  • Kothandaraman N, Chanbasha B, Vladimir BB, Swarup S (2003) Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153

    Article  Google Scholar 

  • Kumar A, Singh DP, Tyagi MB, Kumar A, Prasuna EG, Thakur JK (2000) Production of hepatotoxin by the cyanobacterium Scytonema sp. Strain BT 23. J Microbiol Biotechnol 10:375–380

    CAS  Google Scholar 

  • Lavania M, Chauhan PS, Chauhan SVS, Singh HB, Nautiyal CS (2006) Induction of plant defense enzymes and phenolics by treatment with plant growth—promoting rhizobacteria Serratia marcescens NBRI1213. Curr Microbiol 52:363–368

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  PubMed  CAS  Google Scholar 

  • Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signalling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368

    Article  PubMed  CAS  Google Scholar 

  • Moon CD, Giddens SR, Zhang X-X, Jackson RW (2008) Molecular mechanisms underpinning plant colonization by a plant growth promoting rhizobacterium. In: Ahmad I, Pitchel J, Hayat S (eds) Plant–bacteria interactions: strategies and techniques to promote plant growth. KGaA, Wiley-VCH, Verlag Gmbh and Co., Germany, pp 111–128

    Google Scholar 

  • M’Piga P, Belanger RR, Paulitz TC, Benhamou N (1997) Increased resistance to Fusarium oxysporum f. sp. radicis-lycopersici in tomato plants treated with endophytic bacterium Pseudomonas fluorescens strain 63–28. Physiol Mol Plant Pathol 50:301–320

    Article  Google Scholar 

  • Naher UA, Othman R, Shamsuddin ZHJ, Saud HM, Ismail MR (2009) Growth enhancement and root colonization of rice seedlings by Rhizobium and Corynebacterium spp. Int J Agric Biol 11:586–590

    Google Scholar 

  • Nelson LM (2004) Plant growth promoting rhizobacteria (PGPR): prospects for new inoculants. Crop Management doi: 10.1094/CM-2004-0301-05-RV

  • Niranjan A, Barthwal J, Lehri A, Singh DP, Govindrajan R, Rawat AKS, Amla DV (2009) Development and validation of an HPLC-UV-MS–MS method for identification and quantification of polyphenols in Artemisia pallens L. Acta Chromatogr 21:105–116

    Article  CAS  Google Scholar 

  • Peters NK, Verma DPS (1990) Phenolic compounds as regulators of gene expression in plant-microbe interactions. Mol Plant Microbe Interact 3:4–8

    Article  PubMed  CAS  Google Scholar 

  • Pieterse CMJ, van Wees SCM, van Pelt JA, Trijssenaar A, Van’t Westende YAM, Bolink EM, van Loon LC (1996a) Systemic resistance in Arabidopsis thaliana induced by biocontrol bacteria. Meded Fac Land bouwkd Toegep Biol Wet Univ Gent 61:209–220

    Google Scholar 

  • Pieterse CMJ, van Wees SCM, Hoffland E, van Pelt JA, van Loon LC (1996b) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237

    Article  PubMed  CAS  Google Scholar 

  • Rai AN, S¨oderb¨ack E, Bergman B (2000) Cyanobacterial-plant symbioses: a review. New Phytol 147:449–481

    Article  CAS  Google Scholar 

  • Ramos Solano B, Barriuso Maicas J, Pereyra de la Iglesia MT, Domenech J, Gutiérrez Mañero FJ (2008) Systemic disease protection elicited by plant growth promoting rhizobacteria strains: relationship between metabolic responses, systemic disease protection, and biotic elicitors. Biol Control 98:451–457

    CAS  Google Scholar 

  • Rastogi RP, Sinha RP (2009) Biotechnological and industrial significance of cyanobacterial secondary metabolites. Biotechnol Adv 27:521–539

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Diaz M, Rodelas-Gonzales B, Pozo-Clemente C, Martinez-Toledo MC, Gonzalez-Lopez J (2008) A review of the taxonomy and possible screening traits of plant growth promoting rhizobacteria. In: Ahmad I, Pitchel J, Hayat S (eds) Plant–bacteria interactions: strategies and techniques to promote plant growth. KGaA, Germany-Wiley-VCH, Verlag Gmbh and Co, Germany, pp 55–80

    Google Scholar 

  • Sarma BK, Singh DP, Mehta S, Singh HB, Singh UP (2002) Plant growth-promoting rhizobacteria-elicited alterations in phenolic profile of chickpea (Cicer arietinum) infected by Sclerotium rolfsii. J Phytopathol 150:277–282

    Article  CAS  Google Scholar 

  • Sedmak B, Carmeli S, Pompe-Novak M, Tusek-Znidaric M, Grach-Pogrebinski O, Elersek T, Zuzek MC, Bubik A, Frangez R (2009) Cyanobacterial cytoskeleton immunostaining: the detection of cyanobacterial cell lysis induced by planktopeptin BL1125. J Plankton Res 31:1321–1330

    Article  CAS  Google Scholar 

  • Segura A, Rodriguez-Conde S, Ramos C, Ramos JL (2009) Bacterial responses and interactions with plants during rhizoremediation. Microbial Biotechnol 2:452–464

    Article  CAS  Google Scholar 

  • Senaratna T, McKersie BD, Borochov A (1987) Desiccation and free radical mediated changes in plant membranes. J Exp Bot 38:2005–2014

    Article  CAS  Google Scholar 

  • Senaratna T, Touchell D, Bunn E, Dixon K (2000) Acetyl salicylic acid (aspirin) and salicylic acid induced multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161

    Article  CAS  Google Scholar 

  • Singer AC, Crowley DE, Thompson IP (2003) Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol 21:123–130

    Article  PubMed  CAS  Google Scholar 

  • Singh UP, Sarma BK, Singh DP, Bahadur A (2002) Plant growth-promoting rhizobacteria-mediated induction of phenolics in pea (Pisum sativum) after infection with Erysiphe pisi. Curr Microbiol 44:396–400

    Article  PubMed  CAS  Google Scholar 

  • Singh UP, Sarma BK, Singh DP (2003) Effect of plant growth-promoting rhizobacteria and culture filtrate of Sclerotium rolfsii on phenolic and salicylic acid contents in chickpea (Cicer arietinum). Curr Microbiol 46:131–140

    Article  PubMed  CAS  Google Scholar 

  • Singh BN, Singh BR, Singh RL, Prakash D, Singh DP, Sarma BK, Upadhyay G, Singh HB (2009) Polyphenolics from various extracts/fractions of red onion (Allium cepa) peel with potential antioxidants and antimutagenic activities. Food Chem Toxicol 47:1161–1167

    Article  PubMed  CAS  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205

    PubMed  CAS  Google Scholar 

  • Vaishampayan A, Sinha RP, Haider D-P, Dey T, Gupta AK, Bhan U, Rao AL (2001) Cyanobacterial biofertilizers in rice agriculture. Bot Rev 67:453–516

    Article  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003a) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    Article  PubMed  CAS  Google Scholar 

  • Walker TS, Bais HP, Halligan KM, Stermitz FR, Vivanco JM (2003b) Metabolic profiling of root exudates of Arabidopsis thaliana. J Agri Food Chem 41:2548–2554

    Article  Google Scholar 

  • Wink M, Schimmer O (1999) Modes of action of defence secondary metabolites. In: Wink M (ed) Functions of plant secondary metabolites and their exploitation in biotechnology. CRC Press, Boca Raton, Florida, pp 17–112

    Google Scholar 

  • Yandigeri MS, Yadav AK, Meena KK, Pabbi S (2010) Effect of mineral phosphates on growth and nitrogen fixation of diazotrophic cyanobacteria Anabaena variabilis and Westiellopsis prolifica. Antonie van Leeuwenhoek. 97:297–306

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu C-M (2008) Rhizosphere bacteria help plants tolerate abiotic stress. Cell Press. doi:10.1016/j.tplants.2008.10.0

  • Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070

    PubMed  CAS  Google Scholar 

  • Yedidia I, Shoresh M, Kerem Z, Benhamou N, Kapulnik Y, Chet I (2003) Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl Environ Microbiol 69:7343–7353

    Article  PubMed  CAS  Google Scholar 

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Authors gratefully acknowledge Indian Council of Agricultural Research (ICAR), India for financial support.

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Correspondence to Dhananjaya P. Singh.

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Singh, D.P., Prabha, R., Yandigeri, M.S. et al. Cyanobacteria-mediated phenylpropanoids and phytohormones in rice (Oryza sativa) enhance plant growth and stress tolerance. Antonie van Leeuwenhoek 100, 557–568 (2011). https://doi.org/10.1007/s10482-011-9611-0

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