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Bacterial and fungal endophyte communities in healthy and diseased oilseed rape and their potential for biocontrol of Sclerotinia and Phoma disease

  • 1.

    Carré, P. & Pouzet, A. Rapeseed market, worldwide and in Europe. OCL 21(1), D102. https://doi.org/10.1051/ocl/201h3054 (2014).

    Article  Google Scholar 

  • 2.

    Hammond, K. E. & Lewis, B. E. The timing and sequence of events leading to stem canker disease in populations of Brassica napus var. oleifera in the field. Plant Pathol. 35, 551–556. https://doi.org/10.1111/j.1365-3059.1986.tb02054.x (1986).

    Article  Google Scholar 

  • 3.

    Deb, D., Khan, A. & Dey, N. Phoma diseases: Epidemiology and control. Plant. Pathol. 00, 1–15. https://doi.org/10.1111/ppa.13221 (2020).

    CAS  Article  Google Scholar 

  • 4.

    Fitt, B. D. L., Brun, H., Barbetti, M. J. & Rimmer, S. R. World-wide importance of Phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114, 3–15. https://doi.org/10.1007/s10658-005-2233-5 (2006).

    Article  Google Scholar 

  • 5.

    Winter, M. & Koopmann, B. Race spectra of Leptosphaeria maculans, the causal agent of blackleg disease of oilseed rape, in different geographic regions in northern Germany. Eur. J. Plant Pathol. 145, 629–641. https://doi.org/10.1007/s10658-016-0932-8 (2016).

    Article  Google Scholar 

  • 6.

    Derbyshire, M. C. & Denton-Giles, M. The control of Sclerotinia stem rot on oilseed rape (Brassica napus): current practices and future opportunities. Plant. Pathol. 65, 859–877. https://doi.org/10.1111/ppa.12517 (2016).

    CAS  Article  Google Scholar 

  • 7.

    Gladders, P., Symonds, B. V., Hardwick, N. V. & Sansford, C. E. Opportunities to control canker (Leptosphaeria maculans) in winter oilseed rape by improved spray timing. IOBC/WPRS Bull. 21, 111–120 (1998).

    Google Scholar 

  • 8.

    Kuai, J. et al. The effect of nitrogen application and planting density on the radiation use efficiency and the stem lignin metabolism in rapeseed (Brassica napus L.). Field Crops Res. 199, 89–98. https://doi.org/10.1016/j.fcr.2016.09.025 (2016).

    Article  Google Scholar 

  • 9.

    Card, S. D. et al. Beneficial endophytic microorganisms of Brassica —A review. Biol. Control 90, 102–112. https://doi.org/10.1016/j.biocontrol.2015.06.001 (2015).

    Article  Google Scholar 

  • 10.

    Weyens, N., van der Lelie, D., Taghavi, S., Newman, L. & Vangronsveld, J. Exploiting plant–microbe partnerships to improve biomass production and remediation. Trends Biotechnol. 27, 591–598. https://doi.org/10.1016/j.tibtech.2009.07.006 (2009).

    CAS  Article  PubMed  Google Scholar 

  • 11.

    Müller, H. & Berg, G. Impact of formulation procedures on the effect of the biocontrol agent Serratia plymuthica HRO-C48 on Verticillium wilt in oilseed rape. Biocontrol 53, 905–916. https://doi.org/10.1007/s10526-007-9111-3 (2008).

    Article  Google Scholar 

  • 12.

    Granér, G., Persson, P., Meijer, J. & Alström, S. A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol. Lett. 224, 269–276. https://doi.org/10.1016/S0378-1097(03)00449-X (2003).

    CAS  Article  PubMed  Google Scholar 

  • 13.

    Croes, S. et al. Bacterial communities associated with Brassica napus L. grown on trace-element-contaminated and non-contaminated fields: a genotypic and phenotypic comparison. Microb. Biotechnol. 6, 371–384. https://doi.org/10.1111/1751-7915.12057 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 14.

    Zhang, Q. et al. Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biol. Control 72, 98–102. https://doi.org/10.1016/j.biocontrol.2014.02.018 (2014).

    Article  Google Scholar 

  • 15.

    Berg, G. et al. The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol. Ecol. 56, 250–261. https://doi.org/10.1111/j.1574-6941.2005.00025.x (2006).

    CAS  Article  PubMed  Google Scholar 

  • 16.

    Berg, G. et al. Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Appl. Environ. Microbiol. 71, 4203–4213. https://doi.org/10.1128/AEM.71.8.4203-4213.2005 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 17.

    Robin, A. H. K. et al. Leptosphaeria maculans alters glucosinolate profiles in blackleg disease-resistant and -susceptible cabbage lines. Front. Plant Sci. 8, 1789. https://doi.org/10.3389/fpls.2017.01769 (2017).

    Article  Google Scholar 

  • 18.

    Garrido-Sanz, D. et al. Genomic and genetic diversity within the Pseudomonas fluorescens complex. PLoS ONE 11(2), e0150183. https://doi.org/10.1371/journal.pone.0153733 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 19.

    Taylor, A. Fungal diversity in ectotomycorrhizal communities: sampling effort and species distribution. Plant Soil 244, 19–28. https://doi.org/10.1023/A:1020279815472 (2002).

    ADS  CAS  Article  Google Scholar 

  • 20.

    Schmidt, C. S. et al. Distinct communities of poplar endophytes on an unpolluted and a risk elements-polluted site and their plant growth promoting potential in vitro. Microb. Ecol. 75, 955–969. https://doi.org/10.1007/s00248-017-1103-y (2018).

    CAS  Article  PubMed  Google Scholar 

  • 21.

    Jedryczka, M. Epidemiology and damage caused by stem canker of oilseed rape in Poland. Phytopathol. Pol. 45, 73–75 (2007).

    Article  Google Scholar 

  • 22.

    Mazáková, J., Urban, J., Zouhar, M. & Ryšánek, P. Analysis of Leptosphaeria species complex causing Phoma leaf spot and stem canker of winter oilseed rape (Brassica napus) in the Czech Republic. Crop Pasture Sci. 68, 254–264. https://doi.org/10.1071/CP16308 (2017).

    CAS  Article  Google Scholar 

  • 23.

    El Hadrami, A., Fernando, W. G. D. & Daayf, F. Variations in relative humidity modulate Leptosphaeria spp. pathogenicity and interfere with canola mechanisms of defence. Eur. J. Plant Pathol. 126, 187–202. https://doi.org/10.1007/s10658-009-9532-1 (2010).

    Article  Google Scholar 

  • 24.

    Hilton, S., Bennett, A. J., Chandler, D., Mills, P. & Bending, G. D. Preceding crop and seasonal effects influence fungal, bacterial and nematode diversity in wheat and oilseed rape rhizosphere and soil. Appl. Soil Ecol. 126, 34–46. https://doi.org/10.1016/j.apsoil.2018.02.007 (2018).

    Article  Google Scholar 

  • 25.

    Glynou, K. et al. The local environment determines the assembly of root endophytic fungi at a continental scale. Environ. Microbiol. 18, 2418–2434. https://doi.org/10.1111/1462-2920.13112 (2016).

    CAS  Article  PubMed  Google Scholar 

  • 26.

    Croes, S., Weyens, N., Colpaet, J. & Vangronveld, J. Characterization of the cultivable bacterial populations associated with field grown Brassica napus L.: An evaluation of sampling and isolation protocols. Environ. Microbiol. 17, 2379–2392., https://doi.org/10.1111/1462-2920.12701 (2015).

  • 27.

    Alström, S. Characteristics of bacteria from oilseed rape in relation to their biocontrol activity against Verticillium dahliae. J. Phytopathol. 149, 57–64. https://doi.org/10.1046/j.1439-0434.2001.00585.x (2001).

    Article  Google Scholar 

  • 28.

    Cope-Selby, N. et al. Endophytic bacteria in Miscanthus seed: Implications for germination, vertical inheritance of endophytes, plant evolution and breeding. GCB Bioenergy 9, 57–77. https://doi.org/10.1111/gcbb.12364 (2017).

    CAS  Article  Google Scholar 

  • 29.

    Rathore, R. et al. Crop establishment practices are a driver of the plant microbiota in winter oilseed rape (Brassica napus). Front. Microbiol. 8, 1489. https://doi.org/10.3389/fmicb.2017.01489 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 30.

    Lay, C. Y. et al. Canola-Root-Associated microbiomes in the Canadian prairies. Front. Microbiol. 9, 1189. https://doi.org/10.3389/fmicb.2018.01188 (2018).

    Article  Google Scholar 

  • 31.

    Sundara-Rao, W. V. B. & Sinha, M. K. Phosphate dissolving microorganisms in the soil and rhizosphere. Indian J. Agric. Sci. 33, 272–278. https://doi.org/10.1007/BF01372637 (1963).

    Article  Google Scholar 

  • 32.

    Bashan, Y., Kamnev, A. A. & de-Bashan, L. E. Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: A proposal for an alternative procedure. Biol. Fertil. Soils 49, 465–479. https://doi.org/10.1007/s00374-012-0737-7 (2013).

    CAS  Article  Google Scholar 

  • 33.

    Pii, Y. et al. Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol. Fertil. Soils 51, 403–415. https://doi.org/10.1007/s00374-015-0996-1 (2015).

    CAS  Article  Google Scholar 

  • 34.

    Reddy, C. A. & Saravanan, R. S. Polymicrobial multi-functional approach for enhancement of crop productivity. in Advances in Applied Microbiology (eds. Gadd, G. M. & Sariaslani, S.) 53–113 (Oxford Academic, Oxford, 2013).

  • 35.

    Lally, R. D. et al. Application of endophytic Pseudomonas fluorescens and a bacterial consortium to Brassica napus can increase plant height and biomass under greenhouse and field conditions. Front. Plant Sci. 8, 2193. https://doi.org/10.3389/fpls.2017.02193 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 36.

    Parikh, L., Eskelson, M. J. & Adesemoye, A. O. Relationship of in vitro and in planta screening: improving the selection process for biological control agents against Fusarium root rot in row crops. Arch. Phytopathol. Plant Protect. 51, 156–169. https://doi.org/10.1080/03235408.2018.1441098 (2018).

    Article  Google Scholar 

  • 37.

    Bakker, P. A. H. M., Pieterse, C. M. J. & van Loon, L. C. Induced systemic resistance by fluorescent Pseudomonas sp. Phytopathology 97, 239–243. https://doi.org/10.1094/PHYTO-97-2-0239 (2007).

    Article  PubMed  Google Scholar 

  • 38.

    Youssef, S. A., Tartoura, K. A. & Greash, A. G. Serratia proteamaculans mediated alteration of tomato defense system and growth parameters in response to early blight pathogen Alternaria solani infection. Physiol. Mol. Plant Pathol. 103, 16–22. https://doi.org/10.1016/j.pmpp.2018.04.004 (2018).

    CAS  Article  Google Scholar 

  • 39.

    Li, H. et al. The use of Pseudomonas fluorescens P13 to control Sclerotinia stem rot (Sclerotinia sclerotiorum) of oilseed rape. J. Microbiol. 49, 884–889. https://doi.org/10.1007/s12275-011-1261-4 (2011).

    Article  PubMed  Google Scholar 

  • 40.

    Smolińska, U. & Kowalska, B. Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum—A review. J. Plant Pathol. 100, 1–12. https://doi.org/10.1007/s42161-018-0023-0 (2018).

    Article  Google Scholar 

  • 41.

    Shaukat, M. F. Seed bio-priming with Serratia plymuthica HRO-C48 for the control of Verticillium longisporum and Phoma lingam in Brassica napus L. spp. oleifera. (PhD Dissertation, University of Uppsala, Sweden, 2013).

  • 42.

    Castellano-Hinojosa, A., Pérez-Tapia, V., Bedmar, E. J. & Santillana, N. Purple corn-associated rhizobacteria with potential for plant growth promotion. J. Appl. Microbiol. 124, 1254–1264. https://doi.org/10.1111/jam.13708 (2018).

    CAS  Article  PubMed  Google Scholar 

  • 43.

    Li, L. et al. Synergistic plant–microbe interactions between endophytic bacterial communities and the medicinal plant Glycyrrhiza uralensis F. Antonie Van Leeuwenhoek 111, 1735–1748. https://doi.org/10.1007/s10482-018-1062-4 (2018).

    Article  PubMed  Google Scholar 

  • 44.

    Barnawal, D., Bharti, N., Maji, D., Chanotiya, C. S. & Kalra, A. 1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation. Plant Physiol. Biochem. 58, 227–235. https://doi.org/10.1016/j.plaphy.2012.07.008 (2012).

    CAS  Article  PubMed  Google Scholar 

  • 45.

    Egamberdieva, D., Wirth, S., Behrendt, U., Ahmad, P. & Berg, G. Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front. Microbiol. 8, 199. https://doi.org/10.3389/fmicb.2017.00199 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  • 46.

    Joe, M. M. et al. Resistance responses of rice to rice blast fungus after seed treatment with the endophytic Achromobacter xylosoxidans AUM54 strains. Crop Protect. 42, 141–148. https://doi.org/10.1016/j.cropro.2012.07.006 (2012).

    Article  Google Scholar 

  • 47.

    Bertrand, H. et al. Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can. J. Microbiol. 46, 229–236 (2000).

    CAS  Article  Google Scholar 

  • 48.

    Abuamsha, R., Salman, M. & Ehlers, R. U. Role of different additives on survival of Serratia plymuthica HRO-C48 on oilseed rape seeds and control of Phoma lingam. Br. Microbiol. Res. J. 4, 737–748 (2014).

    Article  Google Scholar 

  • 49.

    Garrity, G. M., Winters, M. & Searles, D. B. Taxonomic outline of the prokaryotes. in Bergey’s Manual of Systematic Bacteriology, 2nd Edn, Release 1.0 (Springer, New York, 2001).

  • 50.

    Unterseher, M. & Schnittler, M. Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)—Different cultivation techniques influence fungal biodiversity assessment. Mycol. Res. 113, 645–654. https://doi.org/10.1016/j.mycres.2009.02.002 (2009).

    Article  PubMed  Google Scholar 

  • 51.

    Zadok, J. C., Chang, T. T. & Konzak, A. A decimal code for the growth stages of cereals. Weed Res. 14, 415–421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x (1974).

    Article  Google Scholar 

  • 52.

    Schmidt, C. S., Mrnka, L., Frantík, T., Lovecká, P. & Vosátka, M. Plant growth promotion of Miscanthus × giganteus by endophytic bacteria and fungi on non-polluted and polluted soils. World J. Microbiol. Biotechnol. 34, 48. https://doi.org/10.1007/s11274-018-2426-7 (2018).

    CAS  Article  PubMed  Google Scholar 

  • 53.

    Koubek, J. et al. Whole-cell MALDI-TOF: Rapid screening method in environmental microbiology. Int. Biodeter. Biodegr. 69, 82–86. https://doi.org/10.1016/j.ibiod.2011.12.007 (2012).

    CAS  Article  Google Scholar 

  • 54.

    Uhlik, O. et al. Matrix-assisted laser desorption ionization (MALDI)–time of flight mass spectrometry- and MALDI biotyper-based identification of cultured biphenyl-metabolizing bacteria from contaminated horseradish rhizosphere soil. Appl. Environ. Microb. 77, 6858–6866. https://doi.org/10.1128/AEM.05465-11 (2011).

    CAS  Article  Google Scholar 

  • 55.

    Štorchová, H. et al. An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon 49, 79–84. https://doi.org/10.2307/1223934 (2000).

    Article  Google Scholar 

  • 56.

    White, T. J., Bruns, T. D., Lee, S. & Taylor, J. Analysis of phylogenetic relationship by amplification and direct sequencing of ribosomal RNA genes. in PCR Protocols: A Guide to Methods and Applications (eds. Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J.) 315–322 (Academic Press Inc., New York, 1990).

  • 57.

    Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Mol. Ecol. 2, 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x (1993).

    CAS  Article  PubMed  Google Scholar 

  • 58.

    McLaughlin, D. J., Hibbett, D. S., Lutzoni, F., Spatafora, J. W. & Vilgalys, R. The search for the fungal tree of life. Trends Microbiol. 11, 488–497. https://doi.org/10.1016/j.tim.2009.08.001 (2009).

    CAS  Article  Google Scholar 

  • 59.

    Alexander, D. B. & Zuberer, D. A. Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fertil. Soils 12, 39–45. https://doi.org/10.1007/BF00369386 (1991).

    CAS  Article  Google Scholar 

  • 60.

    Penrose, D. M. & Glick, B. R. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plant. 118, 10–15. https://doi.org/10.1034/j.1399-3054.2003.00086.x (2003).

    CAS  Article  PubMed  Google Scholar 

  • 61.

    Li, Z., Chang, S., Lin, L., Li, Y. & An, Q. A colorimetric assay of 1-aminocyclopropane-1-carboxylate (ACC) based on ninhydrin reaction for rapid screening of bacteria containing ACC deaminase. Lett. Appl. Microbiol. 53, 178–185. https://doi.org/10.1111/j.1472-765X.2011.03088.x (2011).

    CAS  Article  PubMed  Google Scholar 

  • 62.

    Villano, D., Fernandez-Pachon, M. S., Moya, M. L., Troncoso, A. M. & Garcıa-Parrilla, M. C. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta 71, 230–235. https://doi.org/10.1016/j.talanta.2006.03.050 (2007).

    CAS  Article  PubMed  Google Scholar 

  • 63.

    Hajšlová, J., Fenclová, M. & Zachariašová, M. Methodology for the Rapid Screening of Isolates of Endophytic Microorganisms and Identification of Strains with Phytohormonal Activity (in Czech, ISBN 978-80-7080-869-6 ) (2013).

  • 64.

    Veprikova, Z. et al. Mycotoxins in plant-based dietary supplements: Hidden health risk for consumers. J. Agric. Food Chem. 63, 6633–6643. https://doi.org/10.1021/acs.jafc.5b02105 (2015).

    CAS  Article  PubMed  Google Scholar 

  • 65.

    Zhou, Q. Untersuchungen zum Infektionsmodus, immunologischen Nachweis und zur biologischen Bekämpfung von Leptosphaeria maculans (Desm) Ces. & de Not., dem Erreger der Wurzelhals- und Stängelfäule an Winterraps (Brassica napus L.). (Ph.D Dissertation, University of Göttingen, Göttingen, 2001).

  • 66.

    Chèvre, A. M. et al. Stabilization of resistance to Leptosphaeria maculans in Brassica napus–B. juncea recombinant lines and its introgression into spring-type Brassica napus. Plant Dis. 92, 1208–1214. https://doi.org/10.1094/PDIS-92-8-1208 (2008).

    Article  PubMed  Google Scholar 

  • 67.

    El-Tarabily, K. A. et al. Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes. Plant Pathol. 49, 573–583. https://doi.org/10.1046/j.1365-3059.2000.00494.x (2000).

    Article  Google Scholar 

  • 68.

    Clarke, K. R. & Warwick, R. M. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation 2nd edn. (Primer-E, Plymouth, 2001).

    Google Scholar 

  • 69.

    Frisvad, J. C., Smedsgaard, J., Larsen, T. O. & Samson, R. A. Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud. Mycol. 49, 201–241 (2004).

    Google Scholar 

  • 70.

    Romero, F. M., Rossi, F. R., Gárriz, A., Carrasco, P. & Ruíz, O. A. A bacterial endophyte from apoplast fluids protects canola plants from different pathogens via antibiosis and induction of host resistance. Phytopathology 109, 375–383 (2019).

    CAS  Article  Google Scholar 

  • 71.

    Kamal, M. M., Lindbeck, K. D., Savocchia, S. & Ash, G. J. Biological control of Sclerotinia stem rot of canola using antagonistic bacteria. Plant Pathol. 64, 1375–1384 (2015).

    CAS  Article  Google Scholar 

  • 72.

    Fernando, W. G. D., Nakkeeran, S., Zhang, Y., Savchuk, S. Biological control of Sclerotinia sclerotiorum (Lib.) de Bary by Pseudomonas and Bacillus species on canola petals. Crop Protect. 26, 100–107. https://doi.org/10.1016/j.cropro.2006.04.007 (2007)

  • 73.

    Peng, G., McGregor, L., Lahlali, R., Gossen, B. D., Hwang, S. F., Adhikari, K. K., Strelkov, S. E., McDonald, M. R. Potential biological control of clubroot on canola and crucifer vegetable crops. Plant Pathol. 60, 566–574. https://doi.org/10.1111/j.1365-3059.2010.02400.x (2011)

  • 74.

    Wu, Y., Yuan, J., Raza, W., Shen, Q., Huang, Q. Biocontrol traits and antagonistic potential of Bacillus amyloliquefaciens strain NJZJSB3 against Sclerotinia sclerotiorum, a causal agent of canola stem rot. J. Microbiol. Biotechnol. 24, 1327–1336. https://doi.org/10.4014/jmb.1402.02061 (2014)

  • 75.

    Auer, S. & Ludwig-Müller, J. Biological control of clubroot (Plasmodiophora brassicae) by an endophytic fungus. Integrated control in oilseed crops. IOBC-WPRS Bull. 136, 155–156 (2018).

    Google Scholar 

  • 76.

    Huang, H.-C. & Erickson, R. S. Biological control of Sclerotinia stem rot of canola using Ulocladium atrum. Plant Pathol. Bull. 16, 55–59 (2007).

    CAS  Google Scholar 

  • 77.

    Marques, A. P. G. C., Pires, C., Moreira, H., Rangel, A. O. S. S., Castro, P.M.L. Assessment of the plant growth promoting abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol. Biochem. 42, 1229–1235. https://doi.org/10.1016/j.soilbio.2010.04.014 (2010)


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