Bacterial and fungal endophyte communities in healthy and diseased oilseed rape and their potential for biocontrol of Sclerotinia and Phoma disease
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33589671
PubMed Central
PMC7884388
DOI
10.1038/s41598-021-81937-7
PII: 10.1038/s41598-021-81937-7
Knihovny.cz E-zdroje
- MeSH
- Achromobacter genetika růst a vývoj MeSH
- Ascomycota genetika růst a vývoj MeSH
- Brassica napus genetika růst a vývoj mikrobiologie MeSH
- endofyty genetika růst a vývoj MeSH
- kořeny rostlin genetika mikrobiologie MeSH
- mykobiom genetika MeSH
- nemoci rostlin genetika mikrobiologie MeSH
- odolnost vůči nemocem genetika MeSH
- Phoma genetika růst a vývoj MeSH
- Stenotrophomonas genetika růst a vývoj MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Phoma stem canker (caused by the ascomycetes Leptosphaeria maculans and Leptosphaeria biglobosa) is an important disease of oilseed rape. Its effect on endophyte communities in roots and shoots and the potential of endophytes to promote growth and control diseases of oilseed rape (OSR) was investigated. Phoma stem canker had a large effect especially on fungal but also on bacterial endophyte communities. Dominant bacterial genera were Pseudomonas, followed by Enterobacter, Serratia, Stenotrophomonas, Bacillus and Staphylococcus. Achromobacter, Pectobacter and Sphingobacterium were isolated only from diseased plants, though in very small numbers. The fungal genera Cladosporium, Botrytis and Torula were dominant in healthy plants whereas Alternaria, Fusarium and Basidiomycetes (Vishniacozyma, Holtermaniella, Bjerkandera/Thanatephorus) occurred exclusively in diseased plants. Remarkably, Leptosphaeria biglobosa could be isolated in large numbers from shoots of both healthy and diseased plants. Plant growth promoting properties (antioxidative activity, P-solubilisation, production of phytohormones and siderophores) were widespread in OSR endophytes. Although none of the tested bacterial endophytes (Achromobacter, Enterobacter, Pseudomonas, Serratia and Stenotrophomonas) promoted growth of oilseed rape under P-limiting conditions or controlled Phoma disease on oilseed rape cotyledons, they significantly reduced incidence of Sclerotinia disease. In the field, a combined inoculum consisting of Achromobacter piechaudii, two pseudomonads and Stenotrophomonas rhizophila tendencially increased OSR yield and reduced Phoma stem canker.
Zobrazit více v PubMed
Carré P, Pouzet A. Rapeseed market, worldwide and in Europe. OCL. 2014;21(1):D102. doi: 10.1051/ocl/201h3054. DOI
Hammond KE, Lewis BE. The timing and sequence of events leading to stem canker disease in populations of Brassica napus var. oleifera in the field. Plant Pathol. 1986;35:551–556. doi: 10.1111/j.1365-3059.1986.tb02054.x. DOI
Deb D, Khan A, Dey N. Phoma diseases: Epidemiology and control. Plant. Pathol. 2020;00:1–15. doi: 10.1111/ppa.13221. DOI
Fitt BDL, Brun H, Barbetti MJ, Rimmer SR. World-wide importance of Phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus) Eur. J. Plant Pathol. 2006;114:3–15. doi: 10.1007/s10658-005-2233-5. DOI
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. 2016;145:629–641. doi: 10.1007/s10658-016-0932-8. DOI
Derbyshire MC, Denton-Giles M. The control of Sclerotinia stem rot on oilseed rape (Brassica napus): current practices and future opportunities. Plant. Pathol. 2016;65:859–877. doi: 10.1111/ppa.12517. DOI
Gladders P, Symonds BV, Hardwick NV, Sansford CE. Opportunities to control canker (Leptosphaeria maculans) in winter oilseed rape by improved spray timing. IOBC/WPRS Bull. 1998;21:111–120.
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. 2016;199:89–98. doi: 10.1016/j.fcr.2016.09.025. DOI
Card SD, Hume DE, Roodi D, McGill CR, Millner JP, Johnson RD. Beneficial endophytic microorganisms of Brassica —A review. Biol. Control. 2015;90:102–112. doi: 10.1016/j.biocontrol.2015.06.001. DOI
Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J. Exploiting plant–microbe partnerships to improve biomass production and remediation. Trends Biotechnol. 2009;27:591–598. doi: 10.1016/j.tibtech.2009.07.006. PubMed DOI
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. 2008;53:905–916. doi: 10.1007/s10526-007-9111-3. DOI
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. 2003;224:269–276. doi: 10.1016/S0378-1097(03)00449-X. PubMed DOI
Croes S, Weyens N, Janssen J, Vercampt H, Colpaert JV, Carleer R, Vangronsveld J. Bacterial communities associated with Brassica napus L. grown on trace-element-contaminated and non-contaminated fields: a genotypic and phenotypic comparison. Microb. Biotechnol. 2013;6:371–384. doi: 10.1111/1751-7915.12057. PubMed DOI PMC
Zhang Q, Zhang J, Yang L, Zhang L, Jiang D, Chen W, Li G. Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biol. Control. 2014;72:98–102. doi: 10.1016/j.biocontrol.2014.02.018. DOI
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. 2006;56:250–261. doi: 10.1111/j.1574-6941.2005.00025.x. PubMed DOI
Berg G, Zachow C, Lottmann J, Götz M, Costa R, Smalla K. Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Appl. Environ. Microbiol. 2005;71:4203–4213. doi: 10.1128/AEM.71.8.4203-4213.2005. PubMed DOI PMC
Robin AHK, Yi G-E, Laila R, Hossain MR, Park J-I, Kim HR, Nou I-S. Leptosphaeria maculans alters glucosinolate profiles in blackleg disease-resistant and -susceptible cabbage lines. Front. Plant Sci. 2017;8:1789. doi: 10.3389/fpls.2017.01769. PubMed DOI PMC
Garrido-Sanz D, Meier-Kolthoff JP, Göker M, Martín M, Rivilla R, Redondo-Nieto M. Genomic and genetic diversity within the Pseudomonas fluorescens complex. PLoS ONE. 2016;11(2):e0150183. doi: 10.1371/journal.pone.0153733. PubMed DOI PMC
Taylor A. Fungal diversity in ectotomycorrhizal communities: sampling effort and species distribution. Plant Soil. 2002;244:19–28. doi: 10.1023/A:1020279815472. DOI
Schmidt CS, 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. 2018;75:955–969. doi: 10.1007/s00248-017-1103-y. PubMed DOI
Jedryczka M. Epidemiology and damage caused by stem canker of oilseed rape in Poland. Phytopathol. Pol. 2007;45:73–75. doi: 10.1146/annurev.phyto.45.062806.094401. DOI
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. 2017;68:254–264. doi: 10.1071/CP16308. DOI
El Hadrami A, Fernando WGD, Daayf F. Variations in relative humidity modulate Leptosphaeria spp. pathogenicity and interfere with canola mechanisms of defence. Eur. J. Plant Pathol. 2010;126:187–202. doi: 10.1007/s10658-009-9532-1. DOI
Hilton S, Bennett AJ, Chandler D, Mills P, Bending GD. Preceding crop and seasonal effects influence fungal, bacterial and nematode diversity in wheat and oilseed rape rhizosphere and soil. Appl. Soil Ecol. 2018;126:34–46. doi: 10.1016/j.apsoil.2018.02.007. DOI
Glynou K, et al. The local environment determines the assembly of root endophytic fungi at a continental scale. Environ. Microbiol. 2016;18:2418–2434. doi: 10.1111/1462-2920.13112. PubMed DOI
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., 10.1111/1462-2920.12701 (2015). PubMed
Alström S. Characteristics of bacteria from oilseed rape in relation to their biocontrol activity against Verticillium dahliae. J. Phytopathol. 2001;149:57–64. doi: 10.1046/j.1439-0434.2001.00585.x. DOI
Cope-Selby N, Cookson A, Squance M, Donnison I, Flavell R, Farrar K. Endophytic bacteria in Miscanthus seed: Implications for germination, vertical inheritance of endophytes, plant evolution and breeding. GCB Bioenergy. 2017;9:57–77. doi: 10.1111/gcbb.12364. DOI
Rathore R, Dowling DN, Forristal PD, Spink J, Cotter PD, Bulgarelli D, et al. Crop establishment practices are a driver of the plant microbiota in winter oilseed rape (Brassica napus) Front. Microbiol. 2017;8:1489. doi: 10.3389/fmicb.2017.01489. PubMed DOI PMC
Lay CY, et al. Canola-Root-Associated microbiomes in the Canadian prairies. Front. Microbiol. 2018;9:1189. doi: 10.3389/fmicb.2018.01188. PubMed DOI PMC
Sundara-Rao WVB, Sinha MK. Phosphate dissolving microorganisms in the soil and rhizosphere. Indian J. Agric. Sci. 1963;33:272–278. doi: 10.1007/BF01372637. DOI
Bashan Y, Kamnev AA, de-Bashan LE. 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. 2013;49:465–479. doi: 10.1007/s00374-012-0737-7. DOI
Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C. Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol. Fertil. Soils. 2015;51:403–415. doi: 10.1007/s00374-015-0996-1. DOI
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). PubMed
Lally RD, Galbally P, Moreira AS, Spink J, Ryan D, Germaine KJ, Dowling DN. 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. 2017;8:2193. doi: 10.3389/fpls.2017.02193. PubMed DOI PMC
Parikh L, Eskelson MJ, Adesemoye AO. 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. 2018;51:156–169. doi: 10.1080/03235408.2018.1441098. DOI
Bakker PAHM, Pieterse CMJ, van Loon LC. Induced systemic resistance by fluorescent Pseudomonas sp. Phytopathology. 2007;97:239–243. doi: 10.1094/PHYTO-97-2-0239. PubMed DOI
Youssef SA, Tartoura KA, Greash AG. Serratia proteamaculans mediated alteration of tomato defense system and growth parameters in response to early blight pathogen Alternaria solani infection. Physiol. Mol. Plant Pathol. 2018;103:16–22. doi: 10.1016/j.pmpp.2018.04.004. DOI
Li H, Li H, Bai Y, Wang J, Nie M, Li B, Xiao M. The use of Pseudomonas fluorescens P13 to control Sclerotinia stem rot (Sclerotinia sclerotiorum) of oilseed rape. J. Microbiol. 2011;49:884–889. doi: 10.1007/s12275-011-1261-4. PubMed DOI
Smolińska U, Kowalska B. Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum—A review. J. Plant Pathol. 2018;100:1–12. doi: 10.1007/s42161-018-0023-0. DOI
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).
Castellano-Hinojosa A, Pérez-Tapia V, Bedmar EJ, Santillana N. Purple corn-associated rhizobacteria with potential for plant growth promotion. J. Appl. Microbiol. 2018;124:1254–1264. doi: 10.1111/jam.13708. PubMed DOI
Li L, et al. Synergistic plant–microbe interactions between endophytic bacterial communities and the medicinal plant Glycyrrhiza uralensis F. Antonie Van Leeuwenhoek. 2018;111:1735–1748. doi: 10.1007/s10482-018-1062-4. PubMed DOI
Barnawal D, Bharti N, Maji D, Chanotiya CS, 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. 2012;58:227–235. doi: 10.1016/j.plaphy.2012.07.008. PubMed DOI
Egamberdieva D, Wirth S, Behrendt U, Ahmad P, Berg G. Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front. Microbiol. 2017;8:199. doi: 10.3389/fmicb.2017.00199. PubMed DOI PMC
Joe MM, Islam MR, Karthikeyan B, Bradeepa K, Sivakumaar PK, Sa T. Resistance responses of rice to rice blast fungus after seed treatment with the endophytic Achromobacter xylosoxidans AUM54 strains. Crop Protect. 2012;42:141–148. doi: 10.1016/j.cropro.2012.07.006. DOI
Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel JC. Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.) Can. J. Microbiol. 2000;46:229–236. doi: 10.1139/w99-137. PubMed DOI
Abuamsha R, Salman M, Ehlers RU. Role of different additives on survival of Serratia plymuthica HRO-C48 on oilseed rape seeds and control of Phoma lingam. Br. Microbiol. Res. J. 2014;4:737–748. doi: 10.9734/BMRJ/2014/8390. DOI
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).
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. 2009;113:645–654. doi: 10.1016/j.mycres.2009.02.002. PubMed DOI
Zadok JC, Chang TT, Konzak A. A decimal code for the growth stages of cereals. Weed Res. 1974;14:415–421. doi: 10.1111/j.1365-3180.1974.tb01084.x. DOI
Schmidt CS, 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. 2018;34:48. doi: 10.1007/s11274-018-2426-7. PubMed DOI
Koubek J, et al. Whole-cell MALDI-TOF: Rapid screening method in environmental microbiology. Int. Biodeter. Biodegr. 2012;69:82–86. doi: 10.1016/j.ibiod.2011.12.007. DOI
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. 2011;77:6858–6866. doi: 10.1128/AEM.05465-11. PubMed DOI PMC
Štorchová H, Hrdličková R, Chrtek J, Jr, Tetera M, Fitze D, Fehrer J. An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon. 2000;49:79–84. doi: 10.2307/1223934. DOI
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).
Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993;2:113–118. doi: 10.1111/j.1365-294X.1993.tb00005.x. PubMed DOI
McLaughlin DJ, Hibbett DS, Lutzoni F, Spatafora JW, Vilgalys R. The search for the fungal tree of life. Trends Microbiol. 2009;11:488–497. doi: 10.1016/j.tim.2009.08.001. PubMed DOI
Alexander DB, Zuberer DA. Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fertil. Soils. 1991;12:39–45. doi: 10.1007/BF00369386. DOI
Penrose DM, Glick BR. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plant. 2003;118:10–15. doi: 10.1034/j.1399-3054.2003.00086.x. PubMed DOI
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. 2011;53:178–185. doi: 10.1111/j.1472-765X.2011.03088.x. PubMed DOI
Villano D, Fernandez-Pachon MS, Moya ML, Troncoso AM, Garcıa-Parrilla MC. Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta. 2007;71:230–235. doi: 10.1016/j.talanta.2006.03.050. PubMed DOI
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).
Veprikova Z, et al. Mycotoxins in plant-based dietary supplements: Hidden health risk for consumers. J. Agric. Food Chem. 2015;63:6633–6643. doi: 10.1021/acs.jafc.5b02105. PubMed DOI
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).
Chèvre AM, 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. 2008;92:1208–1214. doi: 10.1094/PDIS-92-8-1208. PubMed DOI
El-Tarabily KA, et al. Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes. Plant Pathol. 2000;49:573–583. doi: 10.1046/j.1365-3059.2000.00494.x. DOI
Clarke KR, Warwick RM. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2. Plymouth: Primer-E; 2001.
Frisvad JC, Smedsgaard J, Larsen TO, Samson RA. Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud. Mycol. 2004;49:201–241.
Romero FM, Rossi FR, Gárriz A, Carrasco P, Ruíz OA. A bacterial endophyte from apoplast fluids protects canola plants from different pathogens via antibiosis and induction of host resistance. Phytopathology. 2019;109:375–383. doi: 10.1094/PHYTO-07-18-0262-R. PubMed DOI
Kamal MM, Lindbeck KD, Savocchia S, Ash GJ. Biological control of Sclerotinia stem rot of canola using antagonistic bacteria. Plant Pathol. 2015;64:1375–1384. doi: 10.1111/ppa.12369. DOI
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. 10.1016/j.cropro.2006.04.007 (2007)
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. 10.1111/j.1365-3059.2010.02400.x (2011)
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. 10.4014/jmb.1402.02061 (2014) PubMed
Auer S, Ludwig-Müller J. Biological control of clubroot (Plasmodiophora brassicae) by an endophytic fungus. Integrated control in oilseed crops. IOBC-WPRS Bull. 2018;136:155–156.
Huang H-C, Erickson RS. Biological control of Sclerotinia stem rot of canola using Ulocladium atrum. Plant Pathol. Bull. 2007;16:55–59.
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. 10.1016/j.soilbio.2010.04.014 (2010)