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Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards

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Abstract

Background and aims

High-throughput 454 pyrosequencing was applied to investigate differences in bacterial and fungal communities between replant and closely situated control non-replant (fallow) soils.

Methods

The V1-V3 region of the bacterial 16S rRNA gene and the ITS1 region of fungi from the different soils were sequenced using 454 pyrosequencing (Titanium chemistry), and data were analysed using the MOTHUR pipeline.

Results

The bacterial phyla Proteobacteria, Actinobacteria and Acidobacteria dominated in both fallow and replant apple orchard soils, and community composition at both phylum and genus level did not significantly differ according to NP-MANOVA. The fungal phyla Ascomycota, Zygomycota and Basidiomycota were dominant, and communities also did not differ in composition at either phylum or genus level. High positive Pearson correlations with plant growth in a plant growth assay performed with apple rootstocks plantlets were detected for the bacterial genera Gp16 and Solirubrobacter (r: >0.82) and fungal genera Scutellinia, Penicillium, Lecythophora and Paecilomyces (r: >0.65). Strong negative correlations with plant growth were detected for the bacterial genera Chitinophaga and Hyphomicrobium (r: <−0.78) and the fungal genera Acremonium, Fusarium and Cylindrocarpon (r: <−0.81).

Conclusions

Study findings are in part consistent with those of previous research, but also highlight associations between apple plants and certain microbial genera. The functional role of these genera in affecting soil health and fertility should be further investigated.

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References

  • Abdo Z, Schuette UM, Bent SJ, Williams CJ, Forney LJ, Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938

    Article  PubMed  Google Scholar 

  • Blok WJ, Bollen GJ (1995) Fungi on roots and stem bases of asparagus in the Netherlands: species and pathogenicity. Eur J Plant Pathol 101:15–24

    Article  Google Scholar 

  • Browne GT, Connell JH, Schneider SM (2006) Almond replant disease and its management with alternative pre-plant soil fumigation treatments and rootstocks. Plant Dis 90:869–876

    Article  Google Scholar 

  • Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456

    Article  CAS  PubMed  Google Scholar 

  • Catska V, Vancura V, Prikryl Z, Hudska G (1988) Artificial induction of the apple replant problem by Penicillium claviforme inoculation. Plant Soil 107:127–136

    Article  Google Scholar 

  • Chakravarty PH, Hiratsuka Y (1994) Evaluation of Lecythophora hoffmannii as a potential biological control agent against a blue stain fungus on Populus tremuloides. J Plant Dis Protect 101:74–79

    CAS  Google Scholar 

  • Chaverri P, Salgado C, Hirooka Y, Rossman AY, Samuels GJ (2011) Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with Cylindrocarpon-like anamorphs. Stud Mycol 68:57–78

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chemidlin Prévost-Bouré N, Dequiedt S, Thioulouse J, Lelièvre M, Saby NPA, Jolivet C, Arrouays D, Plassart P, Lemanceau P, Ranjard L (2014) Similar processes but different environmental filters for soil bacterial and fungal community composition turnover on a broad spatial scale. PLoS ONE 9:e111667

    Article  PubMed Central  PubMed  Google Scholar 

  • Di Menna ME (1954) Cryptococcus terreus n.sp., from soil in New Zealand. J Gen Microbiol 11:195–197

    Article  Google Scholar 

  • Domsch KH, Gams W, Anderson T-H (2007) Compendium of soil fungi. APS, New York

    Google Scholar 

  • Dullahide S, Stirling G, Nikulin A, Stirling A (1994) The role of nematodes, fungi, bacteria, and abiotic factors in the etiology of apple replant problems in the Granite Belt of Queensland. Aust J Exp Agric 34:1177–1182

    Article  Google Scholar 

  • Garcia-Jimenez J, Velazquez M, Jorda C, Alfaro-Garcia A (1994) Acremonium species as the causal agent of muskmelon collapse in Spain. Plant Dis 78:416–419

    Article  Google Scholar 

  • Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M, Karpinets T, Uberbacher E, Tuskan GA, Vilgalys R, Doktycz MJ, Schadt CW (2011) Distinct microbial communities within the endosphere and rhizosphere of populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77:5934–5944

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hammer O, Harper D, Ryan P (2001) PAST: paleontological statistics software package for evolution and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hartmann M, Frey B, Kolliker R, Widmer F (2005) Semi-automated genetic analyses of soil microbial communities: comparison of T-RFLP and RISA based on descriptive and discriminative statistical approaches. J Microbiol Methods 61:349–360

    Article  CAS  PubMed  Google Scholar 

  • Innerebner G, Knief C, Vorholt JA (2011) Protection of Arabidopsis thaliana against leaf-pathogenic Pseudomonas syringae by Sphingomonas strains in a controlled model system. Appl Environ Microbiol 77:3202–3210

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jaffee BA (1982) Fungi associated with roots of apple seedlings grown in soil from an apple replant site. Plant Dis 66:942–944

    Article  Google Scholar 

  • Kelderer MM, Manici L, Caputo F, Thalheimer M (2012) Planting in the ‘inter-row’ to overcome replant disease in apple orchards: a study on the effectiveness of the practice based on microbial indicators. Plant Soil 357:381–393

    Article  CAS  Google Scholar 

  • Khan SA, Hamayun M, Yoon H, Kim HY, Suh SJ, Hwang SK, Kim JM, Lee IJ, Choo YS, Yoon UH, Kong WS, Lee BM, Kim JG (2008) Plant growth promotion and Penicillium citrinum. BMC Microbiol 8:231

    Article  PubMed Central  PubMed  Google Scholar 

  • Khan A, Hamayun M, Kang S-M, Kim Y-H, Jung H-Y, Lee J-H, Lee I-J (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  Google Scholar 

  • Kovacs A, Yacoby K, Gophna U (2010) A systematic assessment of automated ribosomal intergenic spacer analysis (ARISA) as a tool for estimating bacterial richness. Res Microbiol 161:192–197

    Article  CAS  PubMed  Google Scholar 

  • La Duc MT, Vaishampayan P, Nilsson H, Torok T, Venkateswaran K (2012) Pyrosequencing-derived bacterial, archaeal, and fungal diversity of spacecraft hardware destined for mars. Appl Environ Microbiol 78:5912–5922

    Article  PubMed Central  PubMed  Google Scholar 

  • Maheshwari DK (2011) Bacteria in Agrobiology: Plant Growth Responses. Springer

  • Mai WF, Abawi GS (1981) Controlling replant diseases of pome and stone fruits in Northeastern United States by preplant fumigation. Plant Dis 65:859–864

  • Manici L, Ciavatta C, Kelderer M, Erschbaumer G (2003) Replant problems in South Tyrol: role of fungal pathogens and microbial population in conventional and organic apple orchards. Plant Soil 256:315–324

    Article  CAS  Google Scholar 

  • Manici LM, Kelderer M, Franke-Whittle IH, Rühmer T, Baab G, Nicoletti F, Caputo F, Topp A, Insam H, Naef A (2013) Relationship between root-endophytic microbial communities and replant disease in specialized apple growing areas in Europe. Appl Soil Ecol 72:207–214

    Article  Google Scholar 

  • Maxin P, Weber RWS, Pedersen HL, Williams M (2012) Control of a wide range of storage rots in naturally infected apples by hot-water dipping and rinsing. Postharvest Biol Technol 70:25–31

    Article  Google Scholar 

  • Mazzola M (1998) Elucidation of the microbial complex having a causal role in the development of apple replant disease in washington. Phytopathology 88:930–938

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M (1999) Transformation of soil microbial community structure and Rhizoctonia-suppressive potential in response to apple roots. Phytopathology 89:920–927

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M, Manici LM (2012) Apple replant disease: Role of microbial ecology in cause and control. Annu Rev Phytopathol 50:45–65

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M, Granatstein DM, Elfving DC, Mullinix K, Gu YH (2002) Cultural management of microbial community structure to enhance growth of apple in replant soils. Phytopathology 92:1363–1366

    Article  PubMed  Google Scholar 

  • Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100

    Article  CAS  PubMed  Google Scholar 

  • Methe B, Nelson K, Pop M (2012) A framework for human microbiome research. Nature 486:215–221

    Article  PubMed Central  CAS  Google Scholar 

  • Nicoletti R, de Stefano M (2012) Penicillium restrictum as an antagonistc of plant pathogenic fungi. In Dynamic Biochemistry, Process Biotechnology and Molecular Biology. Global Science books

  • Nielsen MN, Winding, A (2002) Microorganisms as indicators of soil health. National Environmental Research Institute

  • Op De Beeck M, Lievens B, Busschaert P, Declerck S, Vangronsveld J, Colpaert JV (2014) Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PLoS One 9:e97629

    Article  PubMed Central  PubMed  Google Scholar 

  • Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9:980–989

    Article  CAS  PubMed  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ranjard L, Poly F, Nazaret S (2000) Monitoring complex bacterial communities using culture-independent molecular techniques: application to soil environment. Res Microbiol 151:167–177

    Article  CAS  PubMed  Google Scholar 

  • Sanzani SM, Cariddi C, Roccotelli A, Garganese F, Fallanaj F, Ippolito A (2013) First report of Gibberella avenacea causing wet apple core rot in Italy. J Plant Pathol 95:217

    Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schutte UM, Abdo Z, Bent SJ, Shyu C, Williams CJ, Pierson JD, Forney LJ (2008) Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl Microbiol Biotechnol 80:365–380

    Article  CAS  PubMed  Google Scholar 

  • Scotto La Massese C, Minot JC, Voisin R, Palmieri M (1988) Value of a biological test for estimating the influence of soil type, previous crop, and soil sterilization on the growth of peach and apple. Acta Horticult 233:53–59

    Google Scholar 

  • Spath M, Insam H, Peintner U, Kelderer M, Kuhnert-Finkernagel R, Franke-Whittle IH (2015) Linking soil biotic and abiotic factors to apple replant disease: a greenhouse approach. J Phytopathol 163:287–299

    Article  CAS  Google Scholar 

  • St. Laurent A, Merwin I, Thies J (2008) Long-term orchard groundcover management systems affect soil microbial communities and apple replant disease severity. Plant Soil 304:209–225

    Article  CAS  Google Scholar 

  • Sun J, Zhang Q, Zhou J, Wei Q (2014a) Illumina amplicon sequencing of 16S rRNA tag reveals bacterial community development in the rhizosphere of apple nurseries at a replant disease site and a new planting site. PLoS One 9, e111744

  • Sun J, Zhang Q, Zhou J, Wei Q (2014b) Pyrosequencing technology reveals the impact of different manure doses on the bacterial community in apple rhizosphere soil. Appl Soil Ecol 78:28–36

    Article  Google Scholar 

  • Tewoldemedhin YT, Mazzola M, Labuschagne I, McLeod A (2011) A multi-phasic approach reveals that apple replant disease is caused by multiple biological agents, with some agents acting synergistically. Soil Biol Biochem 43:1917–1927

    Article  CAS  Google Scholar 

  • Turner T, James E, Poole P (2013) The plant microbiome. Genome Biol 14:209

    Article  PubMed Central  PubMed  Google Scholar 

  • Uhlik O, Musilova L, Ridl J, Hroudova M, Vlcek C, Koubek J, Holeckova M, Mackova M, Macek T (2013) Plant secondary metabolite-induced shifts in bacterial community structure and degradative ability in contaminated soil. Appl Microbiol Biotechnol 97:9245–9256

    Article  CAS  PubMed  Google Scholar 

  • Utkhede RS, Vrain TC, Yorston JM (1992) Effects of nematodes, fungi and bacteria on the growth of young apple trees grown in apple replant disease soil. Plant Soil 139:1–6

    Article  Google Scholar 

  • Vega FE, Simpkins A, Aime MC, Posada F, Peterson SW, Rehner SA, Infante F, Castillo A, Arnold AE (2010) Fungal endophyte diversity in coffee plants from Colombia, Hawaii, Mexico and Puerto Rico. Fungal Ecol 3:122–138

    Article  Google Scholar 

  • Xiong W, Zhao Q, Zhao J, Xun W, Li R, Zhang R et al (2014) Different continuous cropping spans significantly affect microbial community membership and structure in a vanilla-grown soil as revealed by deep pyrosequencing. Microb Ecol. doi:10.1007/s00248-014-0516-0

    Google Scholar 

  • Yang J-I, Ruegger PM, McKenry MV, Becker JO, Borneman J (2012) Correlations between root-associated microorganisms and peach replant disease symptoms in a California soil. PLoS One 7:e46420

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yim B, Smalla K, Winkelmann T (2013) Evaluation of apple replant problems based on different soil disinfection treatments—links to soil microbial community structure? Plant Soil 366:617–631

    Article  CAS  Google Scholar 

  • Yin C, Hulbert SH, Schroeder KL, Mavrodi O, Mavrodi D, Dhingra A, Schillinger WF, Paulitz TC (2013) Role of bacterial communities in the natural suppression of Rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.). Appl Environ Microbiol 79:7428–7438

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang Q, Sun J, Liu S, Wei Q (2013) Manure refinement affects apple rhizosphere bacterial community structure: a study in sandy soil. PLoS One 8:e76937

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao X, Tewoldemedhin Y, Mcleod A, Mazzola M (2009) Multiple personalities of Streptomyces spp. isolated from the rhizosphere of apple cultivated in brassica seed meal amended soils. Phytopathology 99:S150–S160

    Google Scholar 

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Acknowledgments

Financial support for the BIO-INCROP project was provided by the CORE Organic II Funding Body, partners of the FP7 ERA-Net project, CORE Organic II (Coordination of European Transnational Research in Organic Food and Farming systems, project no. 249667). Ljubica Begovic is gratefully acknowledged for her assistance.

Compliance with Ethical Standards

In the work conducted, there were no potential conflicts of interest. In addition, no humans or animals were used in the study. The content and authorship of the submitted manuscript has been approved by all authors, and all of the reported work is original.

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Authors and Affiliations

  1. Institut für Mikrobiologie, Universität Innsbruck, Technikerstraße 25d, 6020, Innsbruck, Austria

    Ingrid H. Franke-Whittle & Heribert Insam

  2. Research Institute for Industrial Crops, Council for Agricultural Research and Economics (CRA), Via di Corticella 133, 40128, Bologna, Italy

    Luisa M. Manici

  3. Biotechnical Faculty, Department of Animal Science, Group for Microbiology and Microbial Biotechnology, University of Ljubljana, Groblje 3, SI-1230, Domzale, Slovenia

    Blaz Stres

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  1. Ingrid H. Franke-Whittle
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Correspondence to Ingrid H. Franke-Whittle.

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Fig. ESM1

Principal component analysis of physical-chemical characteristics, microbial biomass and basal respiration in fallow and replant soil samples. Abbreviations: EF (Egma fallow), ER (Egma replant), HF (Haidegg fallow), HR (Haidegg replant), NF (Nachtweih fallow) and NR (Nachtweih replant). (DOCX 2330 kb)

Fig. ESM2

Comparison of bacterial communities in fallow and replant soils at the order level. A) Proteobacteria. B) Acidobacteria. and C) Actinobacteria. Only orders present at an abundance >1 % are shown. Abbreviations: EF (Egma fallow), ER (Egma replant), HF (Haidegg fallow), HR (Haidegg replant), NF (Nachtweih fallow) and NR (Nachtweih replant). (DOCX 93 kb)

Fig. ESM3

Comparison of fungal communities in fallow and replant soils at the family level. Only families present at an abundance >5 % are shown. Abbreviations: EF (Egma fallow), ER (Egma replant), HF (Haidegg fallow), HR (Haidegg replant), NF (Nachtweih fallow) and NR (Nachtweih replant). (DOCX 43 kb)

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Franke-Whittle, I.H., Manici, L.M., Insam, H. et al. Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards. Plant Soil 395, 317–333 (2015). https://doi.org/10.1007/s11104-015-2562-x

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