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Changes in Root Exudates and Root Proteins in Groundnut–Pseudomonas sp. Interaction Contribute to Root Colonization by Bacteria and Defense Response of the Host

  • Sravani Ankati
  • T. Swaroopa Rani
  • Appa Rao Podile
Article
  • 52 Downloads

Abstract

Selection and application of rhizobacteria, for improved plant health will benefit from a complete understanding of the plant–bacteria interaction. Root exudates (REs) are known to contain signal molecules that facilitate beneficial association of plants with microbes. We have selected a tentatively identified Pseudomonas sp. (RP2), from 126 groundnut (Arachis hypogaea L.)-associated bacterial isolates that significantly promoted growth of groundnut and also induced resistance against the stem rot pathogen Sclerotium rolfsii. REs were collected from 12 to 24 days grown RP2-bacterized and non-bacterized plants and analyzed through gas chromatography coupled with mass spectrometer. Several organic acids, fatty acids, sugars, hydrocarbons, and alcohols were detected. In the untargeted multivariate analysis of the REs, relative content of eight compounds varied significantly on RP2 bacterization. Among these eight compounds, myristic acid, stearic acid, and palmitic acid, positively influenced the root colonization by RP2. Benzoic acid and salicylic acid, increased in RP2-bacterized REs, showed the highest growth inhibition of S. rolfsii. In root proteomics, 11 differentially expressed proteins were identified by 2D-gel electrophoresis followed by matrix-assisted laser desorption ionization-time of flight. Chitinase, thaumatin-like protein, ascorbate peroxidase, and glutathione S-transferase, known to have a role in plant defense against phytopathogens, were upregulated in RP2 interaction. Similarly, upregulation of enolase in roots is likely to improve plant growth in RP2-bacterized groundnut. We conclude that colonization of groundnut roots by RP2 resulted in exudation of metabolites that facilitated root colonization, suppressed fungal growth, promoted plant growth, and also increased the expression of defense-related proteins in the roots.

Keywords

Groundnut Pseudomonas sp. PGPR Root exudates Root proteins Antifungal 

Notes

Acknowledgements

We thank Department of Biotechnology (DBT), Government of India (GoI) for financial support under project No: BT/PR4175/AGR/21/350/2011 dated 01.03.2012. SA thanks Council of Scientific and Industrial Research, GoI for Senior research fellowship. TSR acknowledges financial support from Dr. D. S. Kothari postdoctoral fellowship scheme (BSR/BL/16-17/0344). We also thank the Department of Science and Technology (DST), GoI, Funds for Infrastructure in Science and Technology, Level II support (DST-FIST level II), and Special Assistance Programme-UGC (SAP-UGC) to the Department of Plant Sciences, School of Life Sciences. The authors are grateful to Groundnut division, International Crops Research Institute for the Semi-Arid Tropics, Hyderabad, for providing Arachis hypogaea L. seeds and Dr. Vincent Vadez, Principal Scientist, Division of Crop Physiology, ICRISAT, Hyderabad, for allowing the use of WinRHIZO Pro 5.0 root analyzer facility.

Author Contributions

ARP designed the experiment. SA isolated and screened groundnut PGPR, and analyzed REs by GC-MS. TSR carried out root proteomics using 2DE. ARP, SA, and TSR analyzed the data and wrote the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

344_2018_9868_MOESM1_ESM.docx (5.1 mb)
Supplementary material 1 (DOCX 5188 KB)

References

  1. Amborabe B, Fleurat-lessard P, Chollet J (2002) Antifungal effects of salicylic acid and other benzoic acid derivatives towards Eutypa lata: structure-activity relationship. Plant Physiol Biochem 40:1051–1060CrossRefGoogle Scholar
  2. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512CrossRefGoogle Scholar
  3. Bae H, Herman E, Bailey B, Bae H, Sicher R (2005) Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol Plant 125:114–126CrossRefGoogle Scholar
  4. Banaeiasl F, Bandehagh A, Dorani E, Farajzadeh D, Sakata K, Mustafa G, Komatsu S (2015) Proteomic analysis of canola root inoculated with bacteria under salt stress. J Proteomics 124:88–111CrossRefGoogle Scholar
  5. Brown E, Swinburne TR (1971) Benzoic acid:an antifungal compound formed in Bramley’s seedling apple fruits following infection by Necfria galligena. Bres Physiol Plant Pathol 1:469–475CrossRefGoogle Scholar
  6. Cezar A, Maraschin M, Marcelo R, Piero D (2015) Antifungal activity of salicylic acid against Penicillium expansum and its possible mechanisms of action. Int J Food Microbiol 215:64–70CrossRefGoogle Scholar
  7. Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. Plant Physiol Biochem 72:169–177CrossRefGoogle Scholar
  8. Chen WP, Chen PD, Liu DJ, Kynast R, Friebe B, Velazhahan R, Muthukrishnan S, Gill BS (1999) Development of wheat scab symptoms is delayed in transgenic wheat plants that constitutively express a rice thaumatin-like protein gene. Theor Appl Genet 99:755–760CrossRefGoogle Scholar
  9. Chen Z, Chen B, Guo Q, Shi L, He M, Qin Z (2015) A time-course proteomic analysis of rice triggered by plant activator BTH. J Plant Growth Regul 34:392–409CrossRefGoogle Scholar
  10. Dam VNM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265CrossRefGoogle Scholar
  11. Das SN, Dutta S, Kondreddy A, Chilukoti N, Pullabhotla SVSRN, Vadlamudi S, Podile AR (2010) Plant growth-promoting chitinolytic Paenibacillus elgii responds positively to tobacco root exudates. J Plant Growth Regul 29:409–418CrossRefGoogle Scholar
  12. De Campos MKF, Schaaf G (2017) The regulation of cell polarity by lipid transfer proteins of the SEC14 family. Curr Opin Plant Biol 40:158–168CrossRefGoogle Scholar
  13. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394CrossRefGoogle Scholar
  14. Dutta S, Podile AR (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36:232–244CrossRefGoogle Scholar
  15. Dutta S, Rani TS, Podile AR (2013) Root exudate-induced alterations in Bacillus cereus cell wall contribute to root colonization and plant growth promotion. PLoS ONE 8:1–12Google Scholar
  16. Garcia-Cristobal J, Garcia-Villaraco A, Ramos B, Gutierrez-Manero J, Lucas JA (2015) Priming of pathogenesis related-proteins and enzymes related to oxidative stress by plant growth promoting rhizobacteria on rice plants upon abiotic and biotic stress challenge. J Plant Physiol 188:72–79CrossRefGoogle Scholar
  17. George E, Kumar SN, Jacob J, Bommasani B, Lankalapalli RS, Morang P, Kumar BSD (2015) Characterization of the bioactive metabolites from a plant growth-promoting rhizobacteria and their exploitation as antimicrobial and plant growth-promoting agents. Appl Biochem Biotechnol 176:529–546CrossRefGoogle Scholar
  18. Gómez-Lama Cabanás C, Legarda G, Ruano-Rosa D, Pizarro-Tobías P, Valverde-Corredor A, Niqui JL, Triviño JC, Roca A, Mercado-Blanco J (2018) Indigenous Pseudomonas spp. strains from the olive (Olea europaea L.) rhizosphere as effective biocontrol agents against Verticillium dahliae: from the host roots to the bacterial genomes. Front Microbiol 277:1–19Google Scholar
  19. Goswami D, Dhandhukia P, Patel P, Thakker JN (2014) Screening of PGPR from saline desert of Kutch: growth promotion in Arachis hypogaea by Bacillus licheniformis A2. Microbiol Res 169:66–75CrossRefGoogle Scholar
  20. Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant Growth Promoting Rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:96–102Google Scholar
  21. Han HS, Lee KD (2005a) Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agri Biol Sci 1:210–215Google Scholar
  22. Han HS, Lee KD (2005b) Physiological responses of soybean-inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Res J Agri Biol Sci 1:216–221Google Scholar
  23. Herman PPL, Ramberg H, Baack RRD, Markwell J, Osterman JC (2002) Formate dehydrogenase in Arabidopsis thaliana: overexpression and subcellular localization in leaves. Plant Sci 163:1137–1145CrossRefGoogle Scholar
  24. Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, Davy de Virville J, Remy R, Colas de Francs-Small C (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol 116:627–635CrossRefGoogle Scholar
  25. Jones DL (1998) Organic acids in the rhizosphere-a critical review. Plant Soil 205:25–44CrossRefGoogle Scholar
  26. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91CrossRefGoogle Scholar
  27. Kandasamy S, Loganathan K, Muthuraj R, Duraisamy S, Seetharaman S, Thiruvengadam R, Ponnusamy B, Ramasamy S (2009) Understanding the molecular basis of plant growth promotional effect of Pseudomonas fluorescens on rice through protein profiling. Proteome Sci 8:1–8Google Scholar
  28. Kavino M, Harish S, Kumar N, Saravanakumar D, Samiyappan R (2010) Effect of chitinolytic PGPR on growth, yield and physiological attributes of banana (Musa spp.) under field conditions. Appl Soil Ecol 45:71–77CrossRefGoogle Scholar
  29. Kim J, Lee J, Lee C, Woo SY, Kang H, Seo S, Kim S (2015) Activation of pathogenesis-related genes by the Rhizobacterium, Bacillus sp. JS, which induces systemic resistance in tobacco plants. Plant Pathol J 31:195–201CrossRefGoogle Scholar
  30. Kishore GK, Pande S, Podile AR (2005a) Chitin-supplemented foliar application of Serratia marcescens GPS 5 improves control of late leaf spot disease of groundnut by activating defence-related enzymes. J Phytopathol 153:169–173CrossRefGoogle Scholar
  31. Kishore GK, Pande S, Podile AR (2005b) Phylloplane bacteria increase seedling emergence, growth and yield of field-grown groundnut (Arachis hypogaea L.). Lett Appl Microbiol 40:260–268CrossRefGoogle Scholar
  32. Kishore GK, Pande S, Rao JN, Podile AR (2005c) Pseudomonas aeruginosa inhibits the plant cell wall degrading enzymes of Sclerotium rolfsii and reduces the severity of groundnut stem rot. Eur J Plant Pathol 113:315–320CrossRefGoogle Scholar
  33. Kishore GK, Pande S, Podile AR (2005d) Management of late leaf spot of groundnut (Arachis hypogaea) with chlorothalonil-tolerant isolates of Pseudomonas aeruginosa. Plant Pathol 54:401–408CrossRefGoogle Scholar
  34. Kishore GK, Pande S, Podile AR (2006) Pseudomonas aeruginosa GSE 18 inhibits the cell wall degrading enzymes of Aspergillus niger and activates defence-related enzymes of groundnut in control of collar rot disease. Australas Plant Pathol 35:259–263CrossRefGoogle Scholar
  35. Kloss M, Iwannekl KH, Fendrik I, Niemann EG (1984) Organic acids in the root exudates of Diplachne fusca (linn.) beauv. Environ Exp Bot 24:179–188CrossRefGoogle Scholar
  36. Kwon YS, Lee DY, Rakwal R, Baek S, Lee JH et al (2016) Proteomic analyses of the interaction between the plant-growth promoting rhizobacterium Paenibacillus polymyxa E681 and Arabidopsis thaliana. Proteomics 16:122–135CrossRefGoogle Scholar
  37. Lee J, Lim YP, Han CT, Nou IS, Hur Y (2013) Genome-wide expression profiles of contrasting inbred lines of Chinese cabbage, Chiifu and Kenshin, under temperature stress. Genes Genome 35:273–288CrossRefGoogle Scholar
  38. Li J, McConkey BJ, Cheng Z, Guo S, Glick BR (2013a) Identification of plant growth-promoting bacteria responsive proteins in cucumber roots under hypoxic stress using a proteomic approach. J Proteomics 84:119–131CrossRefGoogle Scholar
  39. Li X, Zhang T, Wang X, Hua K, Zhao L, Han Z (2013b) The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. Int J Biol Sci 9:164–173CrossRefGoogle Scholar
  40. Ling N, Raza W, Ma J, Huang Q, Shen Q (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Eur J Soil Biol 47:374–379CrossRefGoogle Scholar
  41. Liu W, Hou J, Wang Q (2015) Collection and analysis of root exudates of Festuca arundinacea L. and their role in facilitating the phytoremediation of petroleum-contaminated soil. Plant Soil 389:109–119CrossRefGoogle Scholar
  42. Liu Y, Chen L, Wu G, Feng H, Zhang G, Shen Q, Zhang R (2017) Identification of root-secreted compounds involved in the communication between cucumber, the beneficial Bacillus amyloliquefaciens, and the soil-borne pathogen Fusarium oxysporum. Mol Plant Microbe Interact 30:53–62CrossRefGoogle Scholar
  43. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real- time quantitative PCR and the 2–∆∆Ct method. Methods 408:402–408CrossRefGoogle Scholar
  44. Maina S, Emongor Q, Sharma K (2010) Surface sterilant effect on the regeneration efficiency from cotyledon explants of groundnut (Arachis hypogea L.) varieties adapted to eastern and Southern Africa. Afr J Biotechnol 9:2866–2871Google Scholar
  45. Manjula K, Podile AR (2001) Chitin-supplemented formulations improve biocontrol and plant growth promoting efficiency of Bacillus subtilis AF 1. Can J Microbiol 47:618–625CrossRefGoogle Scholar
  46. Manjula K, Podile AR (2005) Production of fungal cell wall degrading enzymes by a biocontrol strain of Bacillus subtilis AF 1. Indian J Exp Biol 43:892–896PubMedGoogle Scholar
  47. Mostafa H, Amir G (2012) Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J Saudi Society of Agri Sci 98:57–61Google Scholar
  48. Mwita L, Chan WY, Pretorius T, Lyantagaye SL, Lapa SV, Avdeeva LV, Reva ON (2016) Gene Expression regulation in the plant growth promoting Bacillus atrophaeus Ucmb-5137 stimulated by maize root exudates. Gene 590:18–28CrossRefGoogle Scholar
  49. Nagahashi G, Douds DD (2000) Partial separation of root exudate components and their effects upon the growth of germinated spores of AM fungi. Mycological Res 104:1453–1464CrossRefGoogle Scholar
  50. Neumann G, Bott S, Ohler MA, Mock HP, Lippmann R, Grosch R, Smalla K (2014) Root exudation and root development of lettuce (Lactuca sativa L. cv. Tizian) as affected by different soils. Trends Plant Sci 5:1–6Google Scholar
  51. Oburger E, Schmidt H (2016) New methods to unravel rhizosphere processes. Trends Plant Sci 21:243–255CrossRefGoogle Scholar
  52. Parray JA, Jan S, Kamili AN, Qadri RA (2016) Current perspectives on plant growth-promoting rhizobacteria. J Plant Growth Regul 35:877–902CrossRefGoogle Scholar
  53. Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J, Pelagio-Flores R, López-Bucio J, García-Juárez P, Macías-Rodríguez L (2017) Bacillus methylotrophicus M4-96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 254:2201–2213CrossRefGoogle Scholar
  54. Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Environ 26:189–199CrossRefGoogle Scholar
  55. Podile AR, Kishore GK (2002) Biological control of peanut diseases. In: Gnanamanickam SS (ed) Biological control of crop diseases, CRC Press, New York, pp 131–160Google Scholar
  56. Podile AR, Vukanti R, Sravani A, Kalam S, Dutta S, Durgeshwar P, Papa Rao V (2014) Root colonization and quorum sensing are the driving forces of plant growth promoting rhizobacteria (PGPR) for growth promotion. Proc Indian Natl Sci Acad 80:407–413CrossRefGoogle Scholar
  57. Rani TS, Podile AR (2014) Extracellular matrix-associated proteome changes during non-host resistance in citrus—Xanthomonas interactions. Physiol Plant 150:565–579CrossRefGoogle Scholar
  58. Rani TS, Durgeshwar P, Podile AR (2015) Accumulation of transcription factors and cell signaling-related proteins in the nucleus during citrus-Xanthomonas interaction. J Plant Physiol 184:20–27CrossRefGoogle Scholar
  59. Sanchez L, Weidmann S, Brechenmacher L, Batoux M, Tuinen DV, Lemanceau P, Gianinazzi S, Gianinazzi-Pearson V (2004) Common gene expression in Medicago truncatula roots in response to Pseudomonas fluorescens colonization, mycorrhiza development and nodulation. New Phytol 161:855–863CrossRefGoogle Scholar
  60. Saravanan RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4:2522–2532CrossRefGoogle Scholar
  61. Sayyed RZ, Gangurde NS, Patel PR, Joshi SA, Chincholkar SB (2010) Siderophore production by Alcaligenes faecalis and its application for growth promotion in Arachis hypogaea. Indian J Biotechnol 9:302–307Google Scholar
  62. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660CrossRefGoogle Scholar
  63. Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 16:1–16CrossRefGoogle Scholar
  64. Sherathia D, Dey R, Thomas M, Dalsania T, Savsani K, Pal KK (2016) Biochemical and molecular characterization of DAPG-producing plant growth promoting rhizobacteria (PGPR) of groundnut (Arachis hypogaea L.). Legume Res 39:614–622Google Scholar
  65. Singh NK, Raja K, Kumar R, Kumar D, Shukla P, Kirti PB (2013) Characterization of a pathogen induced thaumatin-like protein gene AdTLP from Arachis diogoi, a wild peanut. PLoS ONE 8:1–18CrossRefGoogle Scholar
  66. Slavov S, Onckelen H, Van Batchvarova R, Atanassov A, Prinsen E (2004) IAA production during germination of Orobanche spp. seeds. J Plant Physiol 161:847–853CrossRefGoogle Scholar
  67. Sood SG (2003) Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiol Ecol 45:219–227CrossRefGoogle Scholar
  68. Sturrock JLR, Ekramoddoullah AKM (2010) The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Rep 29:419–436CrossRefGoogle Scholar
  69. Sujitha A, Bhaskara Reddy BV, Sivaprasad Y, Prathyusha M, Murali Krishna T, Vijay Krishna Kumar K, Raja Reddy K (2013) Characterisation, genetic diversity and antagonistic potential of 2,4-diacetylphloroglucinol producing Pseudomonas fluorescens isolates in groundnut-based cropping systems of Andhra Pradesh, India. Arch Phytopathology Plant Protect 46:1966–1977CrossRefGoogle Scholar
  70. Sun L, Lu Y, Kronzucker HJ, Shi W (2016) Quantification and enzyme targets of fatty acid amides from duckweed root exudates involved in the stimulation of denitrification. J Plant Physiol 198:81–88CrossRefGoogle Scholar
  71. Tan S, Yang C, Mei X, Shen S, Raza W, Shen Q, Xu Y (2013) The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl Soil Ecol 64:15–22CrossRefGoogle Scholar
  72. Taurian T, Anzuay MS, Angelini JG, Tonelli ML, Luduena L, Pena D, Ibanez F, Fabra A (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431CrossRefGoogle Scholar
  73. Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18:555–561CrossRefGoogle Scholar
  74. Tripura C, Sashidhar B, Podile AR (2007) Ethyl methanesulfonate mutagenesis—enhanced mineral phosphate solubilization by groundnut-associated Serratia marcescens GPS-5. Curr Microbiol 54:79–84CrossRefGoogle Scholar
  75. Vaikuntapu PR, Dutta S, Samudrala RB, Rao VRVN, Kalam S, Podile AR (2014) Preferential promotion of Lycopersicon esculentum (Tomato) growth by plant growth promoting bacteria associated with tomato. Indian J Microbiol 54:403–412CrossRefGoogle Scholar
  76. Venturi V, Keel C (2016) Signaling in the Rhizosphere. Trends Plant Sci 21:187–198CrossRefGoogle Scholar
  77. Vigers AJ, Wiedemann S, Roberts WK, Legrand M (1992) Thaumatin-like pathogenesis-related proteins are antifungal. Plant Sci 83:155–161CrossRefGoogle Scholar
  78. Wu H, Raza W, Fan J, Sun Y, Bao W, Liu D (2008) Chemosphere antibiotic effect of exogenously applied salicylic acid on in vitro soil borne pathogen, Fusarium oxysporum f. sp. niveum Chemosphere 74:45–50CrossRefGoogle Scholar
  79. Xia J, Wishart DS (2016) Using metaboanalyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinform 55:14CrossRefGoogle Scholar
  80. Yeole RD, Dube HC (2000) Siderophore-mediated antibiosis of rhizobacterial fluorescent Pseudomonads against certain soil-borne fungal plant pathogens. J Mycol Plant Pathol 30:335–338Google Scholar
  81. Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Sci Rep 5:1–8Google Scholar
  82. Zhang N, Wang D, Liu Y (2014) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374:689–700CrossRefGoogle Scholar

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Authors and Affiliations

  • Sravani Ankati
    • 1
  • T. Swaroopa Rani
    • 1
  • Appa Rao Podile
    • 1
  1. 1.Department of Plant SciencesUniversity of HyderabadHyderabadIndia

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