Bacterial rhizosphere community profile at different growth stages of Umorok (Capsicum chinense) and its response to the root exudates

Abstract

The role of microflora is an indispensable part of the living organisms. Plants actively recruit specific microbial community to establish favorable habitat with the distinct microbiome, essentially unique for each species, offering new opportunities for plant growth and productivity. Umorok, an indigenous chili variety of northeastern India, production is highly affected by various factors; therefore, rhizosphere bacteria and their relationship with the root exudates released were analyzed to demonstrate rhizosphere bacterial impact on plant growth and health. Culturable and metagenomic bacterial DNA was characterized and the chemical nature of the root exudate was analyzed using chemotaxis assay after its basic analysis in HPLC. Juvenile stage exhibited diverse bacterial species of gammaproteobacteria, alphaproteobacteria, and actinobacteria but lacked the betaproteobacteria while the microbial diversity was reduced in flowering and fruiting stages. However, every growth stage maintained a similar amount of bacterial population regardless of diversity. The population of Pseudomonas, Bacillus, and Burkholderia species was increased several folds in flowering and fruiting stage. Further, the chemotaxis assay unveiled the advantage of root exudate chemical composition for specific microbial recruitment. The chemical composition analysis of root exudates showed substantial variation in the concentration of organic acids, phenolics, and flavonoids that are favoring unique bacterial species. Thus, root exudates confer and limit the related microbial population besides typical plant-bacterial synergetic association. This study emphasized information about the type of microbial load present in each growth stage, which is essential to develop a microbial consortia package for Umorok overall crop improvement.

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References

  1. Altieri MA, Nicholls CI (2003) Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems. Soil Tillage Res 72:203–211. https://doi.org/10.1016/S0167-1987(03)00089-8

    Article  Google Scholar 

  2. Asaff-Torres A, Armendáriz-Ruiz M, Kirchmayr M, Rodríguez-Heredia R, Orozco M, Mateos-Díaz JC, Figueroa-Yáñez L, Baqueiro-Peña I, Verdín J (2017) Rhizospheric microbiome profiling of Capsicum annuum L. cultivated in amended soils by 16S and internal transcribed spacer 2 rRNA amplicon metagenome sequencing. Genome Announc 5:e00626–e00617. https://doi.org/10.1128/genomeA.00626-17

    Article  PubMed  PubMed Central  Google Scholar 

  3. Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148. https://doi.org/10.1055/s-2001-12905

    CAS  Article  Google Scholar 

  4. Bacilio-Jiménez M, Aguilar-Flores S, Ventura-Zapata E, Pérez-Campos E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249:271–277. https://doi.org/10.1023/A:1022888900465

    Article  Google Scholar 

  5. Bai Y, Liang J, Liu R, Hu C, Qu J (2014) Metagenomic analysis reveals microbial diversity and function in the rhizosphere soil of a constructed wetland. Environ Technol 35:2521–2527. https://doi.org/10.1080/09593330.2014.911361

    CAS  Article  PubMed  Google Scholar 

  6. Bakker PA, Berendsen RL, Doornbos RF et al (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4:1–7. https://doi.org/10.3389/fpls.2013.00165

    Article  Google Scholar 

  7. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001

    CAS  Article  PubMed  Google Scholar 

  8. Cavaglieri L, Orlando J, Etcheverry M (2009) Rhizosphere microbial community structure at different maize plant growth stages and root locations. Microbiol Res 164:391–399. https://doi.org/10.1016/j.micres.2007.03.006

    Article  PubMed  Google Scholar 

  9. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803. https://doi.org/10.1038/ismej.2013.196

    CAS  Article  PubMed  Google Scholar 

  10. Cui H, Yang X, Lu D, Jin H, Yan Z, Chen J, Li X, Qin B (2015) Isolation and characterization of bacteria from the rhizosphere and bulk soil of Stellera chamaejasme L. Can J Microbiol 61:171–181. https://doi.org/10.1139/cjm-2014-0543

    CAS  Article  PubMed  Google Scholar 

  11. Currier WW, Strobel GA (1976) Chemotaxis of Rhizobium spp. to plant root exudates. Plant Physiol 57:820–823

    CAS  Article  Google Scholar 

  12. Datta M, Sengupta C, Pandit MK (2010) Isolation and characterization of bacterial isolates from chilli (Capsicum annuum L.) rhizosphere as potent plant growth promoter. J Crop Weed 6:50–58

    Google Scholar 

  13. De-la-Pena C, Badri DV, Lei Z et al (2010) Root secretion of defense-related proteins is development-dependent and correlated with flowering time. J Biol Chem 285:30654–30665. https://doi.org/10.1074/jbc.M110.119040

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci 106:16428–16433. https://doi.org/10.1073/pnas.0905240106

    Article  PubMed  Google Scholar 

  15. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327. https://doi.org/10.1111/j.1574-6941.2010.00860.x

    CAS  Article  PubMed  Google Scholar 

  16. Derrien D, Marol C, Balesdent J (2004) The dynamics of neutral sugars in the rhizosphere of wheat. An approach by13C pulse-labelling and GC/C/IRMS. Plant Soil 267:243–253. https://doi.org/10.1007/s11104-005-5348-8

    CAS  Article  Google Scholar 

  17. Devi SI, Somkuwar B, Potshangbam M, Talukdar NC (2012) Genetic characterization of Burkholderia cepacia strain from Northeast India : a potential bio-control agent. Adv Biosci Biotechnol 3:1179–1188

    Article  Google Scholar 

  18. Di Cello F, Bevivino A, Chiarini L et al (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl Environ Microbiol 63:4485–4493

    Article  Google Scholar 

  19. Fang C, Zhuang Y, Xu T, Li Y, Li Y, Lin W (2013) Changes in rice allelopathy and rhizosphere microflora by inhibiting rice phenylalanine ammonia-lyase gene expression. J Chem Ecol 39:204–212. https://doi.org/10.1007/s10886-013-0249-4

    CAS  Article  PubMed  Google Scholar 

  20. Johnston-Monje D, Lundberg DS, Lazarovits G, Reis VM, Raizada MN (2016) Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil 405:337–355. https://doi.org/10.1007/s11104-016-2826-0

    CAS  Article  Google Scholar 

  21. Lucas García JA, Barbas C, Probanza A, Barrientos ML, Gutierrez Mañero FJ (2001) Low molecular weight organic acids and fatty acids in root exudates of two Lupinus cultivars at flowering and fruiting stages. Phytochem Anal 12:305–311. https://doi.org/10.1002/pca.596

    Article  PubMed  Google Scholar 

  22. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. https://doi.org/10.1038/nature11237

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2013) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. https://doi.org/10.1038/nature11237

    CAS  Article  Google Scholar 

  24. Malangmeih L, Dey G, Sagolsem S (2015) Rural livelihood system in Manipur with special reference to cultivation of king chilli L. J Crop Weed 11:144–151

    Google Scholar 

  25. Marchesi JR, Sato T, Weightman AJ et al (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    CAS  Article  Google Scholar 

  26. Mathur R, Dangi RS, Das SC, Malhotra RC (2000) The hottest chilli variety in India. Curr Sci 79:287–288

    Google Scholar 

  27. Meghvansi MK, Siddiqui S, Khan MH, Gupta VK, Vairale MG, Gogoi HK, Singh L (2010) Naga chilli: a potential source of capsaicinoids with broad-spectrum ethnopharmacological applications. J Ethnopharmacol 132:1–14. https://doi.org/10.1016/j.jep.2010.08.034

    CAS  Article  PubMed  Google Scholar 

  28. Meharg AA (1994) A critical review of labelling techniques used to quantify rhizosphere carbon-flow. Plant Soil 166:55–62. https://doi.org/10.1007/BF02185481

    CAS  Article  Google Scholar 

  29. Mubarik NR, Mahagiani I, Anindyaputri A et al (2010) Chitinolytic bacteria isolated from chili rhizosphere: Chitinase characterization and its application as biocontrol for whitefly (Bemisia tabaci genn.). Am J Agric Biol Sci 5:430–435. https://doi.org/10.3844/ajabssp.2010.430.435

    CAS  Article  Google Scholar 

  30. Muthukumar A, Eswaran A, Sanjeevkumas K (2011) Exploitation of Trichoderma species on the growth of Pythium Aphanidermatum in Chilli. Braz J Microbiol 42:1598–1607. https://doi.org/10.1590/S1517-838220110004000047

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  Article  Google Scholar 

  32. Nokku PK, Audipudi VA (2015) Exploration of a novel plant growth promoting bacteria Stenotrophomonas maltophilia AVP27 isolated from the chilli rhizosphere soil. Int J Eng Res Gen Sci 3:265–276

    Google Scholar 

  33. Oyeyiola G, Ajokpaniovo H, Aliyu M (2012) Bacterial flora of the rhizosphere of Capsicum frutescens. World J Biol Res 5:61–66

    Google Scholar 

  34. Pii Y, Borruso L, Brusetti L, Crecchio C, Cesco S, Mimmo T (2016) The interaction between iron nutrition, plant species and soil type shapes the rhizosphere microbiome. Plant Physiol Biochem 99:39–48. https://doi.org/10.1016/j.plaphy.2015.12.002

    CAS  Article  PubMed  Google Scholar 

  35. Rovira AD (1956) A study of the development of the root surface microflora during the initial stages. J Appl Bacteriol 19:72–79

    Article  Google Scholar 

  36. Sanatombi K, Sharma GJ (2008) Capsaicin content and pungency of different Capsicum spp. cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 36:89–90. https://doi.org/10.1021/jf970695w

    Article  Google Scholar 

  37. Schulz-Bohm K, Zweers H, de Boer W, Garbeva P (2015) A fragrant neighborhood: volatile mediated bacterial interactions in soil. Front Microbiol 6:1–11. https://doi.org/10.3389/fmicb.2015.01212

    Article  Google Scholar 

  38. Sonawane V, Saler R (2015) Tolerance of Balyton by rhizosphere Mycoflora of Capsicum Annuum Linn. (Chilli). Bionano Frontier 8:195–197

    Google Scholar 

  39. Strzelczyk E, Rózycki H (1985) Production of B-group vitamins by bacteria isolated from soil, rhizosphere, and mycorrhizosphere of pine (Pinus sylvestris L.). Zentralbl Mikrobiol 140:293–301

    CAS  Article  Google Scholar 

  40. Sun H, Wang Y (2013) Hollow fiber liquid-phase microextraction with in situ derivatization combined with gas chromatography–mass spectrometry for the determination of root exudate phenylamine compounds in hot pepper (Capsicum annuum L.). J Agric Food Chem 61:5494–5499. https://doi.org/10.1021/jf4003973

    CAS  Article  PubMed  Google Scholar 

  41. Surapat W, Pukahuta C, Rattanachaikunsopon P et al (2013) Characteristics of phosphate solubilization by phosphate-solubilizing bacteria isolated from agricultural chili soil and their efficiency on the growth of chili (Capsicum frutescens L. cv. Hua Rua). Chiang Mai J Sci 40:11–25

    CAS  Google Scholar 

  42. Talukdar J, Saikia A, Borah P (2015) Survey and detection of the diseases of Bhut Jolokia (Capsicum chinense Jacq.) in Assam. J Crop Weed 11:186–192

    Google Scholar 

  43. Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209. https://doi.org/10.1186/gb-2013-14-6-209

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Wang L-Y, Wang T-S, Chen S-F (2015) Cohnella capsici sp. nov., a novel nitrogen-fixing species isolated from Capsicum annuum rhizosphere soil, and emended description of Cohnella plantaginis. Antonie Van Leeuwenhoek 107:133–139. https://doi.org/10.1007/s10482-014-0310-5

    CAS  Article  PubMed  Google Scholar 

  45. Waterhouse AL, Waterhouse LA (2002) Determination of total phenolics. In: Current protocols in food analytical chemistry. Wiley, Hoboken, pp I1.1.1–I1.1.8

    Google Scholar 

  46. Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM, Shen Q (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Sci Rep 5:13438. https://doi.org/10.1038/srep13438

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Zhang X, Yan X, Gao P et al (2005) Optimized sequence retrieval from single bands of temperature gradient gel electrophoresis profiles of the amplified 16S rDNA fragments from an activated sludge system. J Microbiol Methods 60:1–11. https://doi.org/10.1016/j.mimet.2004.08.015

    CAS  Article  PubMed  Google Scholar 

  48. Zhishen J, Tang M, Wu J (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    CAS  Article  Google Scholar 

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Funding

This study received financial support from the funding agency Department of Biotechnology (DBT), Ministry of Science & Technology, Government of India.

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Correspondence to Indira Devi S..

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T. A., P.D., Sahoo, D., Setti, A. et al. Bacterial rhizosphere community profile at different growth stages of Umorok (Capsicum chinense) and its response to the root exudates. Int Microbiol 23, 241–251 (2020). https://doi.org/10.1007/s10123-019-00097-x

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Keywords

  • Rhizosphere
  • Microflora
  • Umorok
  • Root exudate
  • Chemotaxis