Advertisement

Structure and variation of root-associated microbiomes of potato grown in alfisol

  • Ayslu MardanovaEmail author
  • Marat Lutfullin
  • Guzel Hadieva
  • Yaw Akosah
  • Daria Pudova
  • Daniil Kabanov
  • Elena Shagimardanova
  • Petr Vankov
  • Semyon Vologin
  • Natalia Gogoleva
  • Zenon Stasevski
  • Margarita Sharipova
Original Paper

Abstract

Root-associated fungi and bacteria play a pivotal role in the plant–soil ecosystem by influencing both plant growth and immunity. The aim of this study was to unravel the biodiversity of the bacterial and fungal rhizosphere (RS) and rhizoplane (RP) microbiota of Zhukovskij rannij potato (Solanum tuberosum L.) cultivar growing in the Alfisol of Tatarstan, Russia. To assess the structure and diversity of microbial communities, we employed the 16S rRNA and internal transcribed spacer gene library technique. Overall, sequence analysis showed the presence of 3982 bacterial and 188 fungal operational taxonomic units (OTUs) in the RP, and 6018 bacterial and 320 fungal OTUs for in the RS. Comparison between microbial community structures in the RS and RP showed significant differences between these compartments. Biodiversity was higher in the RS than in the RP. Although members of Proteobacteria (RS—59.1 ± 4.9%; RP—54.5 ± 9.2%), Bacteroidetes (RS—23.19 ± 10.2%; RP—34.52 ± 10.4%) and Actinobacteria (RS—11.55 ± 4.9%; RP—7.7 ± 5.1%) were the three most dominant phyla, accounting for 94–98% of all bacterial taxa in both compartments, notable variations were observed in the primary dominance of classes and genera in RS and RP samples. In addition, our results demonstrated that the potato rhizoplane was significantly enriched with the genera Flavobacterium, Pseudomonas, Acinetobacter and other potentially beneficial bacteria. The fungal community was predominantly inhabited by members of the Ascomycota phylum (RS—81.4 ± 8.1%; RP—81.7 ± 5.7%), among which the genera Fusarium (RS—10.34 ± 3.41%; RP—9.96 ± 4.79%), Monographella (RS—7.66 ± 4.43%; RP—9.91 ± 5.87%), Verticillium (RS—4.6 ± 1.43%; RP—8.27 ± 3.63%) and Chaetomium (RS—4.95 ± 2.07%; RP—8.33 ± 4.93%) were particularly abundant. Interestingly, potato rhizoplane was significantly enriched with potentially useful fungal genera, such as Mortierella and Metacordiceps. A comparative analysis revealed that the abundance of Fusarium (a cosmopolitan plant pathogen) varied significantly depending on rotation variants, indicating a possible control of phytopathogenic fungi via management-induced shifts through crop rotational methods. Analysis of the core microbiome of bacterial and fungal community structure showed that the formation of bacterial microbiota in the rhizosphere and rhizoplane is dependent on the host plant.

Keywords

Rhizosphere Rhizoplane Potato Illumina amplicon sequencing Microbiota Microbial diversity 

Notes

Acknowledgements

The work was performed in accordance with the Russian Government Program of Competitive Growth of Kazan Federal University and supported by Grant from Russian Scientific Foundation (Project No. 16-16-04062), and basic scientific research Project No. AAAA-A18-118031390148-1 of the Ministry of Science and Higher Education of the Russian Federation (field investigations and cultivation potato plants).

Supplementary material

11274_2019_2761_MOESM1_ESM.xlsx (230 kb)
Supplementary file1 (XLSX 229 kb)
11274_2019_2761_MOESM2_ESM.xlsx (128 kb)
Supplementary file2 (XLSX 127 kb)

References

  1. Akosah Y, Malova A, Hadieva G, Lutfullin M, Vologin S, Mardanova A (2018) Resistance of different potato cultivars against latent infection of Fusarium spp. in plants and microbes: the future of biotechnology (Ufa) 8. https://plamic.ru/sbornik/
  2. Aleti G, Nikolić B, Brader G, Pandey RV, Antonielli L, Pfeiffer S et al (2017) Secondary metabolite genes encoded by potato rhizosphere microbiomes in the Andean highlands are diverse and vary with sampling site and vegetation stage. Sci Rep 7:1–10.  https://doi.org/10.1038/s41598-017-02314-x CrossRefGoogle Scholar
  3. Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E (1995) Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 170:47–62.  https://doi.org/10.1007/BF02183054 CrossRefGoogle Scholar
  4. Alzubaidy H, Essack M, Malas TB, Bokhari A, Motwalli O, Kamanu FK et al (2016) Rhizosphere microbiome metagenomics of gray mangroves (Avicennia marina) in the Red Sea. Gene 576:626–636.  https://doi.org/10.1016/j.gene.2015.10.032 CrossRefPubMedGoogle Scholar
  5. Anderson CR, Peterson ME, Frampton RA, Bulman SR, Keenan S, Curtin D (2018) Rapid increase in soil pH solubilises organic matter, dramatically increases denitrification potential and strongly stimulates microorganisms from the Firmicutes phylum. PeerJ 6:1–31.  https://doi.org/10.7717/peerj.6090 CrossRefGoogle Scholar
  6. Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C (2014) Jvenn: an interactive Venn diagram viewer. BMC Bioinform 15:293.  https://doi.org/10.1186/1471-2105-15-293 CrossRefGoogle Scholar
  7. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13.  https://doi.org/10.1111/j.1574-6941.2009.00654.x CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272.  https://doi.org/10.1128/JB.185.24.7266-7272.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Choi J, Yang F, Stepanauskas R, Cardenas E, Garoutte A, Williams R et al (2017) Strategies to improve reference databases for soil microbiomes. ISME J 11:829–834.  https://doi.org/10.1038/ismej.2016.168 CrossRefPubMedGoogle Scholar
  10. Clairmont LK, Stevens KJ, Slawson RM (2019) Site-specific differences in microbial community structure and function within the rhizosphere and rhizoplane of wetland plants is plant species dependent. Rhizosphere 9:56–68.  https://doi.org/10.1016/j.rhisph.2018.11.006 CrossRefGoogle Scholar
  11. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal phathogens in molecular plant pathology. Mol Plant Pathol 13:414–430.  https://doi.org/10.1111/j.1364-3703.2011.00783.x CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. CRC Crit Rev Plant Sci 22:107–149.  https://doi.org/10.1080/713610853 CrossRefGoogle Scholar
  13. Dombrowski N, Schlaeppi K, Agler MT, Hacquard S, Kemen E, Garrido-Oter R et al (2017) Root microbiota dynamics of perennial Arabis alpina are dependent on soil residence time but independent of flowering time. ISME J 11:43–55.  https://doi.org/10.1038/ismej.2016.109 CrossRefPubMedGoogle Scholar
  14. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S et al (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112:E911–E920.  https://doi.org/10.1073/pnas.1414592112 CrossRefPubMedGoogle Scholar
  15. FAOSTAT (2017) Production: potatoes. https://www.fao.org/faostat/en/#data/QC/visualize. Food and Agriculture Organization of the United Nations, Rome, Italy. Accessed 23 Aug 2019
  16. Franks PJ, Adams MA, Amthor JS, Barbour MM, Berry JA, Ellsworth DS et al (2013) Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytol 197:1077–1094.  https://doi.org/10.1111/nph.12104 CrossRefPubMedGoogle Scholar
  17. Gachango E, Hanson LE, Rojas A, Hao JJ, Kirk WW (2012) Fusarium spp. causing dry rot of seed potato tubers in Michigan and their sensitivity to fungicides. Plant Dis 96:1767–1774.  https://doi.org/10.1094/PDIS-11-11-0932-RE CrossRefPubMedGoogle Scholar
  18. Granada SD, Bedoya-Pérez JC, Scherlach K, Hertweck C (2016) Serratia marcescens metabolites are promising candidates for biocontrol of avocado pathogens. Planta Med 82:P598.  https://doi.org/10.1055/s-0036-1596657 CrossRefGoogle Scholar
  19. Gschwendtner S, Esperschütz J, Buegger F, Reichmann M, Müller M, Munch JC et al (2011) Effects of genetically modified starch metabolism in potato plants on photosynthate fluxes into the rhizosphere and on microbial degraders of root exudates. FEMS Microbiol Ecol 76:564–575.  https://doi.org/10.1111/j.1574-6941.2011.01073.x CrossRefPubMedGoogle Scholar
  20. Hadieva G, Lutfullin M, Akosah Y, Malova A, Mochalova N, Vologin S et al (2018) Analysis of Fusarium micromycetes, isolated from infected potato tubers grown in the Republic of Tatarstan. Dostizheniya Nauk i tekhniki APK 32:34–39.  https://doi.org/10.24411/0235-2451-2018-10307In Russian CrossRefGoogle Scholar
  21. Hadieva GF, Karamova NS, Stasevski Z, Djabbarova EM, Mardanova AM, Sharipova MR (2016) Dry rot causing species of fusarium prevalent in Republic of Tatarstan. Res J Pharm Biol Chem Sci 7:2824–2827Google Scholar
  22. Hamel C, Gan Y, Sokolski S, Bainard LD (2018) High frequency cropping of pulses modifies soil nitrogen level and the rhizosphere bacterial microbiome in 4-year rotation systems of the semiarid prairie. Appl Soil Ecol 126:47–56.  https://doi.org/10.1016/j.apsoil.2018.01.003 CrossRefGoogle Scholar
  23. Heltoft P, Brurberg MB, Skogen M, Le VH, Razzaghian J, Hermansen A (2016) Fusarium spp. causing dry rot on potatoes in Norway and development of a real-time PCR method for detection of Fusarium coeruleum. Potato Res 59:67–80.  https://doi.org/10.1007/s11540-015-9313-5 CrossRefGoogle Scholar
  24. Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME j 5(10):1571.  https://doi.org/10.1038/ismej.2011.41 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hilber-Bodmer M, Schmid M, Ahrens CH, Freimoser FM (2017) Competition assays and physiological experiments of soil and phyllosphere yeasts identify Candida subhashii as a novel antagonist of filamentous fungi. BMC Microbiol 17:1–15.  https://doi.org/10.1186/s12866-016-0908-z CrossRefGoogle Scholar
  26. Humphreys J, Brye KR, Rector C, Gbur EE (2018) Methane emissions from rice across a soil organic matter gradient in Alfisols of Arkansas, USA. Geoderma Reg 15:e00200.  https://doi.org/10.1016/j.geodrs.2018.e00200 CrossRefGoogle Scholar
  27. Inceoǧlu Ö, Al-Soud WA, Salles JF, Semenov AV, van Elsas JD (2011) Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS ONE 6:1–11.  https://doi.org/10.1371/journal.pone.0023321 CrossRefGoogle Scholar
  28. Inceoǧlu Ö, Salles JF, van Elsas JD (2012) Soil and cultivar type shape the bacterial community in the potato rhizosphere. Microb Ecol 63:460–470.  https://doi.org/10.1007/s00248-011-9930-8 CrossRefPubMedGoogle Scholar
  29. Inceoǧlu Ö, Salles JF, Van Overbeek L, Van Elsas JD (2010) Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl Environ Microbiol 76:3675–3684.  https://doi.org/10.1128/AEM.00040-10 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991.  https://doi.org/10.1016/j.soilbio.2008.08.017 CrossRefGoogle Scholar
  31. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453.  https://doi.org/10.1038/ismej.2008.127 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Karim NF, Mohd M, Nor NM, Zakaria L (2016) Saprophytic and potentially pathogenic Fusarium species from peat soil in Perak and Pahang. Trop Life Sci Res. 27:1–20CrossRefGoogle Scholar
  33. Kielak A, Pijl AS, Van Veen JA, Kowalchuk GA (2008) Differences in vegetation composition and plant species identity lead to only minor changes in soil-borne microbial communities in a former arable field. FEMS Microbiol Ecol 63:372–382.  https://doi.org/10.1111/j.1574-6941.2007.00428.x CrossRefPubMedGoogle Scholar
  34. Klingler JM, Stowe RP, Obenhuber DC, Groves TO, Mishra SK, Pierson DL (1992) Evaluation of the biolog automated microbial identification system. Appl Environ Microbiol 58:2089–2092PubMedPubMedCentralGoogle Scholar
  35. Konstantinidis KT, Tiedje JM (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci 102:2567–2572.  https://doi.org/10.1073/pnas.0409727102 CrossRefPubMedGoogle Scholar
  36. Koo SY, Cho KS (2009) Isolation and characterization of a plant growth-promoting rhizobacterium, Serratia sp. SY5. J Microbiol Biotechnol 19:1431–1438.  https://doi.org/10.4014/jmb.0904.04014 CrossRefPubMedGoogle Scholar
  37. Lareen A, Burton F, Schäfer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90:575–587.  https://doi.org/10.1007/s11103-015-0417-8 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120.  https://doi.org/10.1128/AEM.00335-09 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Leslie JF, Summerell BA (2007) The Fusarium laboratory manual. Wiley, New York.  https://doi.org/10.1002/9780470278376 CrossRefGoogle Scholar
  40. Li T, Liu T, Zheng C, Kang C, Yang Z, Yao X et al (2017) Changes in soil bacterial community structure as a result of incorporation of Brassica plants compared with continuous planting eggplant and chemical disinfection in greenhouses. PLoS ONE 12:1–17.  https://doi.org/10.1371/journal.pone.0173923 CrossRefGoogle Scholar
  41. Li W, Zhang H, Li P, Apaliya MT, Yang Q, Peng Y et al (2016) Biocontrol of postharvest green mold of oranges by Hanseniaspora uvarum Y3 in combination with phosphatidylcholine. Biol Control 103:30–38.  https://doi.org/10.1016/j.biocontrol.2016.07.014 CrossRefGoogle Scholar
  42. Lu H, Wu W, Chen Y, Wang H, Devare M, Thies JE (2010) Soil microbial community responses to Bt transgenic rice residue decomposition in a paddy field. J Soils Sedim 10:1598–1605.  https://doi.org/10.1007/s11368-010-0264-9 CrossRefGoogle Scholar
  43. Ma LJ, Geiser DM, Proctor RH, Rooney AP, O'Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K (2013) Fusarium pathogenomics. Annu Rev Microbiol 67:399–416.  https://doi.org/10.1146/annurev-micro-092412-155650 CrossRefPubMedGoogle Scholar
  44. Medina-Martínez MS, Allende A, Barberá GG, Gil MI (2015) Climatic variations influence the dynamic of epiphyte bacteria of baby lettuce. Food Res Int 68:54–61.  https://doi.org/10.1016/j.foodres.2014.06.009 CrossRefGoogle Scholar
  45. Meng QX, Yin JF, Rosenzweig N, Douches D, Hao JJJ (2012) Culture-based assessment of microbial communities in soil suppressive to potato common scab. Plant Dis 96:712–717.  https://doi.org/10.1094/PDIS-05-11-0441 CrossRefPubMedGoogle Scholar
  46. Mezzasalma V, Sandionigi A, Guzzetti L, Galimberti A, Grando MS, Tardaguila J et al (2018) Geographical and cultivar features differentiate grape microbiota in Northern Italy and Spain vineyards. Front Microbiol 9:946.  https://doi.org/10.3389/fmicb.2018.00946 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2017) Microbial diversity and soil functions. Eur J Soil Sci 68:12–26.  https://doi.org/10.1111/ejss.4_12398 CrossRefGoogle Scholar
  48. Nunes da Rocha U, Plugge CM, George I, van Elsas JD, van Overbeek LS (2013) The rhizosphere selects for particular groups of acidobacteria and verrucomicrobia. PLoS ONE 8:e82443.  https://doi.org/10.1371/journal.pone.0082443 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Olayemi OP, Odedara OO (2017) Screening of endophytic plant growth-promoting bacteria isolated from two Nigerian rice varieties. Niger J Biotechnol 33:1–10.  https://doi.org/10.4314/njb.v33i1.1 CrossRefGoogle Scholar
  50. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125.  https://doi.org/10.1016/j.tim.2007.12.009 CrossRefPubMedGoogle Scholar
  51. Ozimek E, Jaroszuk-Ściseł BJ, Korniłłowicz-Kowalska T, Tyśkiewicz Słomka A et al (2018) Synthesis of indoleacetic acid, gibberellic acid and ACC-deaminase by Mortierella strains promote winter wheat seedlings growth under different conditions. Int J Mol Sci 19:1–17.  https://doi.org/10.3390/ijms19103218 CrossRefGoogle Scholar
  52. Pageni BB, Lupwayi NZ, Akter Z, Larney FJ, Kawchuk LM, Gan Y (2014) Plant growth-promoting and phytopathogen-antagonistic properties of bacterial endophytes from potato (Solanum tuberosum L.) cropping systems. Can J Plant Sci 94:835–844.  https://doi.org/10.4141/cjps2013-356 CrossRefGoogle Scholar
  53. Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97:9621–9636.  https://doi.org/10.1007/s00253-013-5206-1 CrossRefPubMedGoogle Scholar
  54. Peters RD, Sturz AV, Carter MR, Sanderson JB (2003) Developing disease-suppressive soils through crop rotation and tillage management practices. Soil Tillage Res 72:181–192.  https://doi.org/10.1016/S0167-1987(03)00087-4 CrossRefGoogle Scholar
  55. Pfeiffer S, Mitter B, Oswald A, Schloter-Hai B, Schloter M, Declerck S et al (2017) Rhizosphere microbiomes of potato cultivated in the High Andes show stable and dynamic core microbiomes with different responses to plant development. FEMS Microbiol Ecol.  https://doi.org/10.1093/femsec/fiw242 CrossRefPubMedGoogle Scholar
  56. Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375.  https://doi.org/10.1146/annurev-phyto-082712-102340 CrossRefPubMedGoogle Scholar
  57. Qin S, Yeboah S, Xu X, Liu Y, Yu B (2017) Analysis on fungal diversity in rhizosphere soil of continuous cropping potato subjected to different furrow-ridge mulching managements. Front Microbiol 8:845.  https://doi.org/10.3389/fmicb.2017.00845 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361.  https://doi.org/10.1007/s11104-008-9568-6 CrossRefGoogle Scholar
  59. Rathore R, Dowling DN, Forristal PD, Spink J, Cotter PD, Bulgarelli D et al (2017) 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 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Reinhold-Hurek B, Bünger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annu Rev Phytopathol 53:403–424.  https://doi.org/10.1146/annurev-phyto-082712-102342 CrossRefPubMedGoogle Scholar
  61. Richter-Heitmann T, Eickhorst T, Knauth S, Friedrich MW, Schmidt H (2016) Evaluation of strategies to separate root-associated microbial communities: a crucial choice in rhizobiome research. Front Microbiol 7:773.  https://doi.org/10.3389/fmicb.2016.00773 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Rodriguez-R LM, Konstantinidis KT (2014) Estimating coverage in metagenomic data sets and why it matters. ISME J 8:2349–2351.  https://doi.org/10.1038/ismej.2014.76 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Santhanam R, Weinhold A, Goldberg J, Oh Y, Baldwin IT (2015) Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci 112:E5013–E5020.  https://doi.org/10.1073/pnas.1505765112 CrossRefPubMedGoogle Scholar
  64. Schirmer M, Ijaz UZ, D’Amore R, Hall N, Sloan WT, Quince C (2015) Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform. Nucleic Acids Res 43:e37.  https://doi.org/10.1093/nar/gku1341 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Schmidt R, Mitchell J, Scow K (2018) Cover cropping and no-till increase diversity and symbiotroph:saprotroph ratios of soil fungal communities. Soil Biol Biochem.  https://doi.org/10.1016/j.soilbio.2018.11.010 CrossRefGoogle Scholar
  66. Sharma SK, Gautam N (2017) Chemical composition and antioxidant and antibacterial activities of cultured mycelia of four clavicipitaceous mushrooms (Ascomycetes) from the Indian Himalayas. Int J Med Mushrooms 19:45–54.  https://doi.org/10.1615/IntJMedMushrooms.v19.i1.50 CrossRefPubMedGoogle Scholar
  67. Simonson RW (2018) Soil classification. In: Hanson AA, Kilmer VJ (eds) Handbook of soils and climate in agriculture. CRC Press, Boca Raton, pp 103–130CrossRefGoogle Scholar
  68. Smith O (1940) Potato research at Cornell University. Am J Potato Res 17:27–37.  https://doi.org/10.1007/BF02879239 CrossRefGoogle Scholar
  69. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120.  https://doi.org/10.1073/pnas.0605127103 CrossRefPubMedGoogle Scholar
  70. Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240.  https://doi.org/10.1080/10408410490468786 CrossRefPubMedGoogle Scholar
  71. The European Cultivated Potato Database (2005) Zhukovskij rannij. https://www.europotato.org/varieties/view/Zhukovskij%20Rannij-E. Accessed 24 June 2019
  72. Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PloS one 7(7):e40863.  https://doi.org/10.1371/journal.pone.0040863 CrossRefPubMedPubMedCentralGoogle Scholar
  73. USDA (2014) Keys to soil taxonomy. USDA, Washington, D.C.  https://doi.org/10.1063/1.1698257 CrossRefGoogle Scholar
  74. Van Overbeek L, Van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296.  https://doi.org/10.1111/j.1574-6941.2008.00469.x CrossRefPubMedGoogle Scholar
  75. Vladimirov VP, Ravilevich GI, Mostyakova AA, Sitnikova NV (2015) Ways to increase the use of photosynthetic active radiation by early ripening varieties of potato in Middle Volga Region, Russia. Biol Med 7 Article ID: BM-066-15.Google Scholar
  76. Wagner MR, Lundberg DS, Del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T (2016) Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun 7:12151.  https://doi.org/10.1038/ncomms12151 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Weinert N, Meincke R, Gottwald C, Heuer H, Gomes NCM, Schloter M et al (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75:3859–3865.  https://doi.org/10.1128/AEM.00414-09 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Wen X, Dubinsky E, Yao WU, Rong Y, Fu C (2016) Wheat, maize and sunflower cropping systems selectively influence bacteria community structure and diversity in their and succeeding crop’s rhizosphere. J Integr Agric 15:1892–1902.  https://doi.org/10.1016/S2095-3119(15)61147-9 CrossRefGoogle Scholar
  79. Williams ST, Foster PG, Littlewood DTJ (2014) The complete mitochondrial genome of a turbinid vetigastropod from MiSeq Illumina sequencing of genomic DNA and steps towards a resolved gastropod phylogeny. Gene 533:38–47.  https://doi.org/10.1016/j.gene.2013.10.005 CrossRefPubMedGoogle Scholar
  80. Yapparov AK, Bikkinina L-K, Yapparov IA, Aliev SA, Ezhkova AM, Ezhkov VO et al (2015) Changes in the properties and productivity of leached chernozem and gray forest soil under the impact of ameliorants. Eurasian Soil Sci 48:114901158.  https://doi.org/10.1134/s1064229315100130 CrossRefGoogle Scholar
  81. Yi Y, de Jong A, Frenzel E, Kuipers OP (2017) Comparative transcriptomics of Bacillus mycoides root exudates reveals different genetic adaptation of endophytic and soil isolates. Front Microbiol 8:1487.  https://doi.org/10.3389/fmicb.2017.01487 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Yi Y, Li Z, Kuipers OP (2018) Plant-microbe interaction: transcriptional response of Bacillus Mycoides to potato root exudates. J Vis Exp.  https://doi.org/10.3791/57606 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Zamalieva FF, Zaizeva TW, Rygih LY, Salikhova ZZ (2015) Fusarium wilt of potato and recommendations for a protection. Zashchita kartofelia 2:3–9 (In Russian) Google Scholar
  84. Zhang N, Wang D, Liu Y, Li S, Shen Q, Zhang R (2014) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374:689–700.  https://doi.org/10.1007/s11104-013-1915-6 CrossRefGoogle Scholar
  85. Zhang H, Fen X, Yu W, Hu H, Dai X (2017a) Progress of potato staple food research and industry development in China. J Integr Agric 16:2924–2932.  https://doi.org/10.1016/S2095-3119(17)61736-2 CrossRefGoogle Scholar
  86. Zhang Y, Xu J, Riera N, Jin T, Li J, Wang N (2017b) Huanglongbing impairs the rhizosphere-to-rhizoplane enrichment process of the citrus root-associated microbiome. Microbiome 5:97.  https://doi.org/10.1186/s40168-017-0304-4 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Ayslu Mardanova
    • 1
    Email author
  • Marat Lutfullin
    • 1
  • Guzel Hadieva
    • 1
  • Yaw Akosah
    • 1
  • Daria Pudova
    • 1
  • Daniil Kabanov
    • 1
  • Elena Shagimardanova
    • 2
  • Petr Vankov
    • 1
  • Semyon Vologin
    • 3
  • Natalia Gogoleva
    • 2
    • 4
  • Zenon Stasevski
    • 3
  • Margarita Sharipova
    • 1
  1. 1.Laboratory of Microbial Biotechnology, Institute of Fundamental Medicine and BiologyKazan (Volga Region) Federal UniversityKazanRussia
  2. 2.Laboratory of Extreme Biology, Institute of Fundamental Medicine and BiologyKazan (Volga region) Federal UniversityKazanRussia
  3. 3.Tatar Research Institute of AgricultureKazan Scientific Center of Russian Academy of SciencesKazanRussia
  4. 4.Kazan Institute of Biochemistry and BiophysicsKazan Scientific Centre of Russian Academy of SciencesKazanRussia

Personalised recommendations