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Exploration of microbiome of medicinally important plants as biocontrol agents against Phytophthora parasitica

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Abstract

In a preliminary plant-based microbiome study, diverse bacterial taxa were identified from different medicinal plants using 16S rRNA gene sequencing. Based on initial antimicrobial screening, eight (8) bacterial endophytes in six (6) different genera, Streptomyces, Pseudomonas, Enterobacter, Bacillus, Arthrobacter, and Delftia, from four important medicinal plants Dodonaea viscosa, Fagonia indica, Caralluma tuberculata, and Calendula arvensis were selected for further analyses. Antimicrobial assays revealed that Pseudomonas taiwanensis MOSEL-RD23 has strong anti-Phytophthora activity. Volatiles produced by P. taiwanensis MOSEL-RD23and Bacillus flexus MOSEL-MIC5 inhibited the growth of Phytophthora parasitica by more than 80%. Ethyl acetate extracts of Streptomyces alboniger MOSEL-RD3, P. taiwanensis MOSEL-RD23, Enterobacter hormaechei MOSEL-FLS1, and Bacillus tequilensis MOSEL-FLS3, and Delftia lacustris MB322 displayed high potency against P. parasitica. All these bacterial extracts showed strong inhibition of more than 80% inhibition in vitro against P. parasitica at different concentrations (4–400 µg/mL). Bacterial extracts showing strong antimicrobial activity were selected for bioactivity-driven fractionation and showed anti-Phytophthoral activity in multiple fractions and different peaks observed in UV–Vis spectroscopy. In the detached-leaf assay against P. parasitica on tobacco, 1% ethyl acetate bacterial extract of S. alboniger MOSEL-RD3, P. taiwanensis MOSEL-RD23, E. hormaechei MOSEL-FLS1, B. tequilensis MOSEL-FLS3, and D. lacustris MB322 reduced lesion sizes and lesion frequencies caused by P. parasitica by 68 to 81%. Overall, P. taiwanensis MOSEL-RD23 showed positive activities for all the assays. Analyzing the potential of bacterial endophytes as biological control agents can potentially lead to the formulation of broad-spectrum biopesticides for the sustainable production of crops.

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References

  • Afzal IMRAN, Shinwari ZK, Iqrar I (2015) Selective isolation and characterization of agriculturally beneficial endophytic bacteria from wild hemp using canola. Pak J Bot 47(5):1999–2008

    CAS  Google Scholar 

  • Afzal I, Iqrar I, Shinwari ZK, Yasmin A (2017) Plant growth-promoting potential of endophytic bacteria isolated from roots of wild Dodonaea viscosa L. Plant Growth Regul 81(3):399–408

    CAS  Google Scholar 

  • Ahmad F, Ahmad I, Khan M (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163(2):173–181

    CAS  PubMed  Google Scholar 

  • Ahmad B, Abbas SJ, Hussain F, Bashir S, Ahmad D (2014) Study on Caralluma tuberculata nutritional composition and its importance as medicinal plant. Pak J Bot 46(5):1677–1684

    Google Scholar 

  • Ali GS, Norman D, El-Sayed AS (2015a) Soluble and volatile metabolites of plant growth-promoting rhizobacteria (PGPRs): role and practical applications in inhibiting pathogens and activating induced systemic resistance (ISR). Advances in botanical research. Academic Press, London, pp 241–284

    Google Scholar 

  • Ali M, Kim B, Belfield KD, Norman D, Brennan M, Ali GS (2015b) Inhibition of Phytophthora parasitica and P. capsici by silver nanoparticles synthesized using aqueous extract of Artemisia absinthium. Phytopathology 105(9):1183–1190

    CAS  PubMed  Google Scholar 

  • Ali GS, El-Sayed AS, Patel JS, Green KB, Ali M, Brennan M et al (2016) Ex vivo application of secreted metabolites produced by soil-inhabiting Bacillus spp. efficiently controls foliar diseases caused by Alternaria spp. Appl Environ Microbiol 82(2):478–490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anil P, Nikhil B, Manoj G, Prakash N (2012) Phytochemicals and biological activities of Fagonia indica. Int Res J Pharm 3:56–59

    Google Scholar 

  • Berg G, Köberl M, Rybakova D, Müller H, Grosch R, Smalla K (2017) Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fix050

    Article  PubMed  Google Scholar 

  • Bibi Y, Tabassum S, Zahara K, Bashir T, Haider S (2015) Ethnomedicinal and pharmacological properties of Caralluma tuberculata NE Brown: a review. Pure Appl Biol 4(4):503

    Google Scholar 

  • Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kroon LP, Brouwer H, de Cock AW, Govers F (2012) The genus Phytophthora anno. Phytopathology 102(4):348–364

    Article  PubMed  Google Scholar 

  • Chen L, Luo S, Xiao X, Guo H, Chen J, Wan Y, Li B, Xu T, Xi Q, Rao C, Liu C (2010) Application of plant growth-promoting endophytes (PGPE) isolated from Solanum nigrum L. for phytoextraction of Cd-polluted soils. Appl Soil Ecol 46(3):383–389

    Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71(9):4951–4959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cook RJ (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Annu Rev Phytopathol 31(1):53–80

    CAS  PubMed  Google Scholar 

  • Dagdas YF, Belhaj K, Maqbool A, Chaparro-Garcia A, Pandey P, Petre B et al (2016) An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. Elife. https://doi.org/10.7554/eLife.10856

    Article  PubMed  PubMed Central  Google Scholar 

  • El-Sayed ASA, Akbar A, Iqrar I, Ali R, Norman D, Brennan M et al (2018) A glucanolytic Pseudomonas sp. associated with Smilax bona-nox L. displays strong activity against Phytophthora parasitica. Microbiol Res 207:140–152. https://doi.org/10.1016/j.micres.2017.11.018

    Article  CAS  PubMed  Google Scholar 

  • Fai PB, Grant A (2009) A rapid resazurin bioassay for assessing the toxicity of fungicides. Chemosphere 74(9):1165–1170

    CAS  PubMed  Google Scholar 

  • Fravel D (2005) Commercialization and implementation of biocontrol 1. Annu Rev Phytopathol 43:337–359

    CAS  PubMed  Google Scholar 

  • Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16(10):463–471

    CAS  PubMed  Google Scholar 

  • Heyn C, Joel A (1983) Reproductive relationships between annual species of Calendula (Compositae). Plant Syst Evol 143(4):311–329

    Google Scholar 

  • Hu HQ, Li XS, He H (2010) Characterization of an antimicrobial material from a newly isolated Bacillus amyloliquefaciens from mangrove for biocontrol of Capsicum bacterial wilt. Biol Control 54(3):359–365

    Google Scholar 

  • Hudzicki J (2009) Kirby-Bauer disk diffusion susceptibility test protocol. American Society for Microbiology

  • Hunziker L, Bönisch D, Groenhagen U, Bailly A, Schulz S, Weisskopf L (2015) Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl Environ Microbiol 81(3):821–830

    PubMed  PubMed Central  Google Scholar 

  • Kang SH, Cho H, Cheong H, Ryu C-M, Kim JF, Park S-H (2007) Two bacterial entophytes eliciting both plant growth promotion and plant defense on pepper (Capsicum annuum L.). J Microbiol Biotechnol 17(1):96

    CAS  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62(3):716–721

    CAS  PubMed  Google Scholar 

  • Kim WJ, Kim YO, Kim JH, Nam B-H, Kim D-G, An CM et al (2016) Liquid chromatography-mass spectrometry-based rapid secondary-metabolite profiling of marine Pseudoalteromonas sp. M2. Mar Drugs 14(1):24

    PubMed  PubMed Central  Google Scholar 

  • Kjer J, Debbab A, Aly AH, Proksch P (2010) Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat Protoc 5(3):479–490

    CAS  PubMed  Google Scholar 

  • Köberl M, Schmidt R, Ramadan EM, Bauer R, Berg G (2013) The microbiome of medicinal plants: diversity and importance for plant growth, quality and health. Front Microbiol 4:400

    PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lodewyckx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M et al (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21(6):583–606

    Google Scholar 

  • Meng Y, Zhang Q, Ding W, Shan W (2014) Phytophthora parasitica: a model oomycete plant pathogen. Mycology 5(2):43–51

    PubMed  Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16(3):115–125

    CAS  PubMed  Google Scholar 

  • Panabieres F, Ali GS, Alagui MB, Dalio RJD, Gudmestad NC, Kuhn ML et al (2016) Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathol Mediterr 55(1):20–40. https://doi.org/10.14601/Phytopathol_Mediterr-16423

    Article  CAS  Google Scholar 

  • Paolini J, Barboni T, Desjobert J-M, Djabou N, Muselli A, Costa J (2010) Chemical composition, intraspecies variation and seasonal variation in essential oils of Calendula arvensis L. Biochem Syst Ecol 38(5):865–874

    CAS  Google Scholar 

  • Patel JS, Vitoreli A, Palmateer AJ, El-Saycd A, Norman DJ, Goss EM et al (2016) Characterization of Phytophthora spp. isolated from ornamental plants in Florida. Plant Dis 100(2):500–509. https://doi.org/10.1094/Pdis-05-15-0598-Re

    Article  CAS  PubMed  Google Scholar 

  • Rahman L, Shinwari ZK, Iqrar I, Rahman L, Tanveer F (2017) An assessment on the role of endophytic microbes in the therapeutic potential of Fagonia indica. Ann Clin Microbiol Antimicrob 16(1):53

    PubMed  PubMed Central  Google Scholar 

  • Rajamanickam V, Rajasekaran A, Anandarajagopal K, Sridharan D, Selvakumar K, Rathinaraj BS (2010) Anti-diarrheal activity of Dodonaea viscosa root extracts. Int J Pharm Bio Sci 1(4):182–185

    Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278(1):1–9

    CAS  PubMed  Google Scholar 

  • Senthilkumar M, Govindasamy V, Annapurna K (2007) Role of antibiosis in suppression of charcoal rot disease by soybean endophyte Paenibacillus sp. HKA-15. Curr Microbiol 55(1):25–29

    CAS  PubMed  Google Scholar 

  • Shinwari ZK, Tanveer F, Iqrar I (2019) Role of microbes in plant health, disease management, and abiotic stress management. Microbiome in plant health and disease. Springer, Singapore, pp 231–250

    Google Scholar 

  • Strobel G (2007) Plant-associated microorganisms (Endophytes) as a new source of bioactive natural products. Medicinal plant biotechnology: from basic research to industrial applications. Springer, Berlin, pp 49–72

    Google Scholar 

  • Sturz A, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl Soil Ecol 15(2):183–190

    Google Scholar 

  • Ulloa-Ogaz A, Muñoz-Castellanos L, Nevárez-Moorillón G (2015) Biocontrol of phytopathogens: antibiotic production as mechanism of control. The battle against microbial pathogens: basic science, technological advances and educational programes. Formatex Research Center, Badajoz, pp 305–309

    Google Scholar 

  • Waheed A, Barker J, Barton SJ, Owen CP, Ahmed S, Carew MA (2012) A novel steroidal saponin glycoside from Fagonia indica induces cell-selective apoptosis or necrosis in cancer cells. Eur J Pharm Sci 47(2):464–473

    CAS  PubMed  Google Scholar 

  • Wang H, Wen K, Zhao X, Wang X, Li A, Hong H (2009) The inhibitory activity of endophytic Bacillus sp. strain CHM1 against plant pathogenic fungi and its plant growth-promoting effect. Crop Prot 28(8):634–639

    Google Scholar 

  • Wang Y, Meng Y, Zhang M, Tong X, Wang Q, Sun Y et al (2011) Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity. Mol Plant Pathol 12(2):187–201. https://doi.org/10.1111/j.1364-3703.2010.00659.x

    Article  CAS  PubMed  Google Scholar 

  • Wiegand I, Hilpert K, Hancock RE (2008) Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 3(2):163

    CAS  PubMed  Google Scholar 

  • Yau JA, Diánez F, Marín F, Carretero F, Santos M (2013) Screening and evaluation of potential biocontrol fungi and bacteria foliar endophytes against Phytophthora capsici and Phytophthora parasitica on pepper. J Food Agric Environ 11:490–495

    Google Scholar 

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Acknowledgements

This work was supported by funding from the Higher Education Commission of Pakistan to I.I. and by the National Institute of Food and Agriculture–United States Department of Agriculture (Accession number 1017239 and FL-APO-005155) to G.A.

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Correspondence to Irum Iqrar.

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Iqrar, I., Shinwari, Z.K., El-Sayed, A.S.A.F. et al. Exploration of microbiome of medicinally important plants as biocontrol agents against Phytophthora parasitica. Arch Microbiol 203, 2475–2489 (2021). https://doi.org/10.1007/s00203-021-02237-2

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