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Growth promotion and protection of lentil (Lens esculenta) against herbicide stress by Rhizobium species

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Abstract

This study was designed to recover lentil-specific rhizobial strains tolerant to herbicides (quizalafop-p-ethyl and clodinafop) and synthesizing plant growth regulators even in the presence of herbicide stress. Furthermore, the impact of rhizobial strain was assessed on lentil plants grown in herbicide-treated soils. Quizalafop-p-ethyl- and clodinafop-tolerant Rhizobium sp. isolate MRL3 recovered from the nodules of lentil produced plant growth-promoting substances in substantial amount both in the absence and presence of herbicides. In addition, each herbicide at recommended, two and three times the recommended dose adversely affected lentil growth in pot trials. Both herbicides at recommended and higher rate generally decreased biomass, symbiotic properties, nutrients uptake and seed yield of lentil. Interestingly, the herbicide-tolerant Rhizobium isolate MRL3, when used with any concentration of the two herbicides, significantly increased the measured parameters compared to the plants grown in soils treated solely (without inoculant) with the same individual treatment of each herbicide. The present findings suggest that the rhizobial isolate MRL3 endowed with multiple properties could be used to facilitate the productivity of lentil under herbicide-stressed soils.

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References

  • Ahemad M, Khan MS (2009) Toxicity assessment of herbicides quizalafop-p-ethyl and clodinafop towards Rhizobium pea symbiosis. Bull Environ Contam Toxicol 82:761–766

    Article  CAS  PubMed  Google Scholar 

  • Ahemad M, Khan MS, Zaidi A, Wani PA (2009) Remediation of herbicides contaminated soil using microbes. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes in sustainable agriculture. Nova, USA, pp 261–284

    Google Scholar 

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12:39–45

    Article  CAS  Google Scholar 

  • Alikhani HA, Saleh-Rastin N, Antoun H (2006) Phosphate solubilization activity of rhizobia native to Iranian soils. Plant Soil 287:35–41

    Article  CAS  Google Scholar 

  • Athar (1998) Drought tolerance by lentil rhizobia (Rhizobium leguminosarum) from arid and semiarid areas of Pakistan. Lett Appl Microbiol 26:38–42

    Article  Google Scholar 

  • Bakker AW, Schipper B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp mediated plant growth stimulation. Soil Biol Biochem 19:451–457

    Article  CAS  Google Scholar 

  • Barker SJ, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Reg 19:144–154

    CAS  Google Scholar 

  • Brick JM, Bostock RM, Silversone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Appl Environ Microbiol 57:535–538

    Google Scholar 

  • Costerton JW (1985) The role of bacterial exopolysaccharides in nature and disease. Dev Ind Microbiol 26:249–261

    CAS  Google Scholar 

  • Courtois J, Jean-Paul S, Corinne R, Alain H, Claude G, Luciana D, Jean-Noël B, Bernard C (1994) Exopolysaccharide production by the Rhizobium meliloti M5N1 CS strain. Location and quantitation of the sites of O-acetylation. Carbohydr Polym 25:7–12

    Article  CAS  Google Scholar 

  • Devi KK, Seth N, Kothamasi S, Kothamasi D (2007) Hydrogen cyanide-producing rhizobacteria kill subterranean termite Odontotermes obesus (rambur) by cyanide poisoning under in vitro conditions. Curr Microbiol 54:74–78

    Article  CAS  PubMed  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Critical Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Duan J, Müller KM, Charles TC, Vesely S, Glick BR (2009) 1-aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from southern Saskatchewan. Microb Ecol 57:423–436

    Article  CAS  PubMed  Google Scholar 

  • Dye DW (1962) The inadequacy of the usual determinative tests for the identification of xanthomonas spp. Nat Sci 5:393–416

    Google Scholar 

  • Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proc Natl Acad Sci USA 104:10282–10287

    Article  CAS  PubMed  Google Scholar 

  • Frankenberger WT Jr, Arshad M (1995) Phytohormones in soils: microbial production and function. Dekker, New York

    Google Scholar 

  • Ghosh AC, Ghosh S, Basu PS (2005) Production of extracellular polysaccharide by a Rhizobium species from root nodules of the leguminous tree Dalbergia lanceolaria. Eng Life Sci 5:378–382

    Article  CAS  Google Scholar 

  • Gigliotti C, Allievi L (2001) Differential effects of the herbicides bensulfuron and cinosulfuron on soil microorganisms. J Environ Sci Health B 36:775–782

    Article  CAS  PubMed  Google Scholar 

  • Gordon S, Weber RP (1951) The calorimetric estimation of IAA. Plant Physiol 26:192–195

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Zheng H, Yang Y, Wang H (2007) Characterization of Pseudomonas corrugata strain P94 isolated from soil in Beijing as a potential biocontrol agent. Curr Microbiol 55:247–253

    Article  CAS  PubMed  Google Scholar 

  • Herman PL, Behrens M, Chakraborty S, Crastil BM, Barycki J, Weeks DP (2005) A three component dicamba O-demethylase from Pseudomonas maltiphilia strain DI-6: gene isolation, characterization and heterologous expression. J Biol Chem 280:24759–24767

    Article  CAS  PubMed  Google Scholar 

  • Holt JG, Krieg NR, Sneath PHA, Staley JT, Willams ST (1994) Bergeys manual of determinative bacteriology (9th Edition). Williams and Wilkins, USA

    Google Scholar 

  • Indiragandhi P, Anandham R, Madhaiyan M, Sa TM (2008) Characterization of plant growth–promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Curr Microbiol 56:327–333

    Article  CAS  PubMed  Google Scholar 

  • Iswaran V, Marwah TS (1980) A modified rapid Kjeldahl method for determination of total nitrogen in agricultural and biological materials. Geobios 7:281–282

    Google Scholar 

  • Jackson ML (1967) Soil chemical analysis. Prentice-Hall, New Delhi, pp 134–144

    Google Scholar 

  • Joseph B, Patra RR, Lawrence R (2007) Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). Int J Plant Prod 2:141–152

    Google Scholar 

  • Karadeniz A, Topcuoğlu SF, İnan S (2006) Auxin, gibberellin, cytokinin and abscisic acid production in some bacteria. World J Microbiol Biotechnol 22:1061–1064

    Article  CAS  Google Scholar 

  • Khan MS, Zaidi A, Rizvi PQ (2006a) Biotoxic effects of herbicides on growth, nodulation, nitrogenase activity, and seed production in chickpeas. Comm Soil Sci Pl Anal 37:1783–1793

    Article  CAS  Google Scholar 

  • Khan MS, Chaudhry P, Wani PA, Zaidi A (2006b) Biotoxic effects of the herbicides on growth, seed yield, and grain protein of greengram. J Appl Sci Environ Mgt 10:141–146

    Google Scholar 

  • Kucey RMN, Chaiwanakupt P, Arayangkool T, Snitwongse P, Siripaibool C, Wadisirisuk P, Boonkerd N (1988) Effect of herbicides and water application schedule. Plant Soil 108:87–92

    Article  CAS  Google Scholar 

  • Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14:23–34

    Article  CAS  PubMed  Google Scholar 

  • Mody BR, Bindra MO, Modi VV (1989) Extracellular polysaccharides of cowpea rhizobia: compositional and functional studies. Arch Microbiol 1:2–5

    Google Scholar 

  • Neiland JB (1981) Microbial iron compounds. Annu Rev Biochem 50:715–731

    Article  Google Scholar 

  • Pattan C, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    Article  Google Scholar 

  • Powles SB (2008) Evolved glyphosate-resistant weeds around the world: lessons to be learnt. Pest Manage Sci 64:360–365

    Article  CAS  Google Scholar 

  • Reeves MW, Pine L, Neilands JB, Balows A (1983) Absence of siderophore activity in Legionella species grown in iron-deficient media. J Bacteriol 154:324–329

    CAS  PubMed  Google Scholar 

  • Remans R, Beebe S, Blair M, Manrique G, Tovar E, Rao I, Croonenborghs A, Torres-Gutierrez R, El-Howeity M, Michiels J, Vanderleyden J (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161

    Article  CAS  Google Scholar 

  • Sadasivam S, Manikam A (1992) Biochemical methods for agricultural sciences. Wiley, New Delhi

    Google Scholar 

  • Singh G, Wright D (2002) Effects of herbicides on nodulation and growth of two varieties of peas (Pisum sativum). Acta Agron Hung 50:337–348

    Article  CAS  Google Scholar 

  • Sinha S, Mukherjee SK (2008) Cadmium-induced siderophore production by a high cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Curr Microbiol 56:55–60

    Article  CAS  PubMed  Google Scholar 

  • Somasegaran P, Hoben HJ (1994) Handbook for rhizobia: methods in legume Rhizobium technology. Springer, New York

    Google Scholar 

  • Song NH, Yin XL, Chen GF, Yang H (2007) Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere 68:1779–1787

    Article  CAS  PubMed  Google Scholar 

  • Spaepen S, Das F, Luyten E, Michiels J, Vanderleyden J (2009) Indole-3-acetic acid-regulated genes in Rhizobium etli CNPAF512. FEMS Microbiol Lett 291:195–200

    Article  CAS  PubMed  Google Scholar 

  • Sridevi M, Yadav NCS, Mallaiah KV (2008) Production of indole-acetic-acid by Rhizobium isolates from Crotalaria species. Res J Microbiol 3:276–281

    Article  CAS  Google Scholar 

  • Tank N, Saraf M (2003) Phosphate solubilization, exopolysaccharide production and indole acetic acid secretion by rhizobacteria isolated from Trigonella foenum-graecum. Ind J Microbiol 43:37–40

    Google Scholar 

  • van Noorden GE, Ross JJ, Reid JB, Rolfe BG, Mathesius U (2006) Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant 1[W]. Plant Physiol 140:1494–1506

    Article  PubMed  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root nodule bacteria, IBP Handbook No. 15. Blackwell, Oxford

    Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007) Effect of metal tolerant plant growth promoting Bradyrhizobium sp (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 70:36–45

    Article  CAS  PubMed  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Lee C (2008) Enrichment, isolation, and characterization of 4-chlorophenol-degrading bacterium Rhizobium sp. 4-CP-20. Biodegradation 19:329–336

    Article  CAS  PubMed  Google Scholar 

  • Yi Y, Huang W, Ge Y (2007) Exopolysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World J Microbiol Biotechnol 24:1059–1065

    Article  Google Scholar 

  • Zablotowicz RM, Reddy KN (2004) Impact of glyphosate on the Bradyrhizobium japonicum symbiosis with glyphosate-resistant transgenic soybean: A mini review. J Environ Qual 33:825–831

    Article  CAS  PubMed  Google Scholar 

  • Zawoznik MS, Tomaro ML (2005) Effect of chlorimuron-ethyl on Bradyrhizobium japonicum and its symbiosis with soybean. Pest Manage Sci 61:1003–1008

    Article  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge Dr. Nakhat Ara Naqvi, Parijat Agrochemicals, New Delhi, India, for providing technical grade insecticides and University Grants Commission, New Delhi, India, for providing fellowships.

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Correspondence to Mohammad Saghir Khan.

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Ahemad, M., Khan, M.S. Growth promotion and protection of lentil (Lens esculenta) against herbicide stress by Rhizobium species. Ann Microbiol 60, 735–745 (2010). https://doi.org/10.1007/s13213-010-0124-2

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