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Distinct Communities of Poplar Endophytes on an Unpolluted and a Risk Element-Polluted Site and Their Plant Growth-Promoting Potential In Vitro

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Numerous studies demonstrated that endophytic microbes can promote plant growth and increase plant stress resistance. We aimed at isolating poplar endophytes able to increase their hosts’ fitness both in nutrient-limited and polluted environments. To achieve this goal, endophytic bacteria and fungi were isolated from roots and leaves of hybrid poplars (Populus nigra × P. maximowiczii clone Max-4) on an unpolluted and a risk element-polluted site in the Czech Republic and subsequently screened by a number of in vitro tests. Bacterial communities at the unpolluted site were dominated by Gammaproteobacteria with Pseudomonas sp. as the prominent member of the class, followed by Bacilli with prevailing Bacillus sp., whereas Alphaproteobacteria, mostly Rhizobium sp., prevailed at the polluted site. The fungal endophytic community was dominated by Ascomycetes and highly distinct on both sites. Dothideomycetes, mostly Cladosporium, prevailed at the non-polluted site while unclassified Sordariomycetous fungi dominated at the polluted site. Species diversity of endophytes was higher at the unpolluted site. Many tested endophytic strains solubilized phosphate and produced siderophores, phytohormones, and antioxidants. Some strains also exhibited ACC-deaminase activity. Selected bacteria showed high tolerance and the ability to accumulate risk elements, making them promising candidates for use in inocula promoting biomass production and phytoremediation.

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Abbreviations

AA:

Ascorbic acid

ACC:

1-Aminocyclopropane-1-carboxylate

CAS:

Chrome azurol S

DSE:

Dark septate endophytes

DW:

Dry weight

DPPH:

2,2-Diphenyl-1-picrylhydrazyl

HDTMA:

Hexadecyltrimethylammonium bromide

IAA:

Indole-3-acetic acid

iP:

N6-(Δ2-isopentenyl)adenine

iPR:

N6-(Δ2-isopentenyl)adenosine

LB:

Luria-Bertani broth

MALDI-TOF MS:

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

MEA:

Malt extract agar

MIC:

Minimum inhibitory concentration

PGP:

Plant growth promoting

SNA:

Synthetic nutrient poor agar

SD:

Standard deviation

TSA:

Tryptic soy agar

References

  1. Schulz BJE, Boyle CJC (2006) What are endophytes? In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 15–31

    Chapter  Google Scholar 

  2. 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  CAS  PubMed  PubMed Central  Google Scholar 

  3. Martín-García J, Müller MM, Diez JJ (2012) ITS-based comparison of endophytic mycota in twigs of native Populus nigra and cultivated P. x euramericana (cv. I-214) stands in Northern Spain. Ann. For. Sci. 69:49–57

    Article  Google Scholar 

  4. Bálint M, Bartha L, O’Hara RB, Olson MS, Otte J, Pfennninger M, Robertson AL, Tiffin P, Schmitt I (2015) Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars. Mol. Ecol. 24:235–248

    Article  PubMed  Google Scholar 

  5. Ulrich K, Ulrich A, Ewald D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol. Eco. 63:169–180

    Article  CAS  Google Scholar 

  6. Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, Labbé J, Muchero W, Bonito G, Vilgalys R, Tuskan G, Podar M, Schadt CW (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLOS ONE e76382.https://doi.org/10.1371/journal.pone.0076382

  7. Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenped S, Woyke T, North G, Visel A, Partida-Martínez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol. 209:798–811

    Article  CAS  PubMed  Google Scholar 

  8. Fonsecca-Garcia C, Coleman-Derr D, Garrido E, Visel A, Tringe SG, Partida-Martínez LP (2016) The cacti microbiome: interplay between habitat filtering and host-specificity. Front. Microbiol. 7:150. https://doi.org/10.3389/fmicb.2016.00150

    Article  Google Scholar 

  9. Beckers De Beeck MO, Weyens N, Boerjan W, Vangronsveld J (2017) Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome 5:25. https://doi.org/10.1186/s40168-017-0241-2

    Article  Google Scholar 

  10. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Advances 17:319–339

    Article  CAS  Google Scholar 

  11. Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol. Biochem. 41:154–162

    Article  CAS  Google Scholar 

  12. Hoffman MT, Gunatilaka MK, Wijeratne K, Gunatilaka L, Arnold AE (2013) Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS One 8:e73132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Li Z, Chang S, Lin L, Li Y, An Q (2011) A colorimetric assay of 1-aminocyclopropane-1-carboxylate (ACC) based on ninhydrin reaction for rapid screening of bacteria containing ACC deaminase. Let. Appl. Microbiol. 53:178–185

    Article  CAS  Google Scholar 

  14. Khan AL, Hamayun M, Waqas M, Kang SM, Kim YH, Kim DH, Lee IJ (2012) Exophiala sp. LHL08 association gives heat stress tolerance by avoiding oxidative damage to cucumber plants. Biol. Fert. Soils 48:519–529

    Article  CAS  Google Scholar 

  15. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol. Advances 29:248–258

    Article  CAS  Google Scholar 

  16. Gamalero E, Cesaro P, Cicatelli A, Todeschini V, Musso C, Castiglione S, Fabiani A, Lingua G (2012) Poplar clones of different sizes, grown on a heavy metal polluted site, are associated with microbial populations of varying composition. Sci. Tot. Environ. 425:262–270

    Article  CAS  Google Scholar 

  17. Sun LN, Zhang YF, He LY, Chen ZJ, Wang QY, Quian M, Sheng XF (2010) Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Bioresour. Technol. 101:501–509

    Article  CAS  PubMed  Google Scholar 

  18. Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A (2012) Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonisation of barley roots. New Phytol. 196:520–534

    Article  CAS  PubMed  Google Scholar 

  19. Lodewycks C, Mergeay M, Vangronsveld J, van der Lelie D (2002) Isolation, characterisation and identification of bacteria associated with the Zink hyperaccumuator Thlaspi caerulescens subsp. calaminaria. Int. J. Phytoremed. 4:110–115

    Google Scholar 

  20. Gamalero E, Lingua G, Berta G, Glick BR (2009) Beneficial role of plant growth promoting bacteria and arbuscular mycorrhizal fungi on plant responses to heavy metal stress. Can. J. Microbiol. 55:501–514

    Article  CAS  PubMed  Google Scholar 

  21. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 75:748–757

    Article  CAS  PubMed  Google Scholar 

  22. Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J. Appl. Microbiol. 108:1471–1484

    Article  CAS  PubMed  Google Scholar 

  23. Dickmann D (2006) Silviculture and biology of short-rotation woody crops in temperate regions: then and now. Biomass Bioenergy 30:696–705

    Article  Google Scholar 

  24. Pulford I, Dickinson N (2005) Phytoremediation technologies using trees. Trace elements in the environment. Lewis, Boca Raton, pp 375–395

    Google Scholar 

  25. Marmiroli M, Imperiale D, Maestri E, Marmiroli N (2013) The response of Populus spp. to cadmium stress: chemical, morphological and proteomics study. Chemosphere 93:1333–1344

    Article  CAS  PubMed  Google Scholar 

  26. Samuilov S, Lang F, Djukic M, Djunisijevic-Bojovic D, Rennenberg H (2016) Lead uptake increases drought tolerance of wild type and transgenic poplar (Populus tremula x P alba) overexpressing gsh 1. Environ. Pollut. 216:773–785

    Article  CAS  PubMed  Google Scholar 

  27. Novaes E, Osorio L, Drost DR, Miles BL, Boaventura-Novaes CRD, Benedict C, Dervinis C, Yu Q, Sykes R, Davis M, Martin TA, Peter GF, Kirst M (2009) Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol. 182:878–890

    Article  CAS  PubMed  Google Scholar 

  28. Newcombe G (1996) The specificity of fungal pathogens of Populus. In: Stettler RF, Bradshaw Jr HD, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, National Research Council of Canada, Ottawa, pp 223–246

    Google Scholar 

  29. Bonito G, Hameed K, Ventura R, Krishnan J, Schadt CV, Vigaly R (2016) Identifying a functional guild of fungi from the root microbiome of Populus. Fungal Ecol. 22:35–42

    Article  Google Scholar 

  30. Foulon J, Zappelini C, Durand A, Valot B, Girardclos O, Blaudez D, Chalot M (2016) Environmental metabarcoding reveals contrasting microbial communities at two poplar phytomanagement sites. Sci. Total Environ. 571:1230–1240

    Article  CAS  PubMed  Google Scholar 

  31. Lacercat-Didier L, Berthelot C, Foulon J, Errard A, Martino E, Chalot M, Blaudez D (2016) New mutualistic fungal fungal endophytes isolated from poplar roots display high metal tolerance. Mycorrhiza 26:657–671

    Article  CAS  PubMed  Google Scholar 

  32. Durand A, Maillard A, Foulon J, Gweon HS, Valot B (2017) Environmental metabarcoding reveals contrasting belowground and aboveground fungal communities from poplar at a Hg phytomanagement site. Microbial Ecol. https://doi.org/10.1007/s00248-017-0984-0

  33. Karliński L, Rudawska M, Kieliszewska-Rokicka B, Leski T (2010) Relationship between genotype and soil environment during colonization of poplar roots by mycorrhizal and endophytic fungi. Mycorrhiza 20:315–324

    Article  PubMed  Google Scholar 

  34. Quoreshi AM, Khasa DP (2008) Effectiveness of mycorrhizal inoculation in the nursery on root colonisation growth and nutrient uptake of aspen and balsam poplar. Biomass Bioenergy 32:381–391

    Article  CAS  Google Scholar 

  35. Ciadamidaro L, Girardclos O, Bert V, Zappelini C, Yung L, Foulon J, Papin A, Roy S, Blaudez D, Chalot M (2017) Poplar biomass production at phytomanagement sites is significantly enhanced by mycorrhizal inoculation. Env. Exp. Botany 139:48–56

    Article  Google Scholar 

  36. Martín-García J, Espiga E, Pando V, Diez JJ (2011) Factors influencing endophytic communities in poplar plantations. Silva Fennica 45:169–180

    Article  Google Scholar 

  37. Unterseher M, Petzold A, Schnittler M (2012) Xerotolerant foliar fungi from the Tarin River basin, Central China are conspecific to endophytic ITS phylotypes of Populus tremula from temperate Europa. Fungal Divers. 54:133–142

    Article  Google Scholar 

  38. Berthelot C, Leyval C, Foulon J, Chalot M, Blaudez D (2016) Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiol. Ecol. 92, doi: https://doi.org/10.1093/femsec/fiw144

  39. Trnka M, , Trnka M, Fialová J, Kouteck V, Fajman M, Žalud Z, Hejduk S (2008) Biomass production and survival rates of selected poplar clones grown under a short rotation system on arable land. Plant Soil Environ. 244:78–88

    Google Scholar 

  40. Weger J, Havlíčková K, Bubeník J (2011) Results of testing of native willows and poplars for short rotation coppice after three harvests. Asp. Appl. Biol. 112:335–340

    Google Scholar 

  41. Zárubová P, Hejcman M, Vondráčková S, Mrnka L, Száková J, Tlustoš P (2015) Distribution of P, K, Ca, Mg, Cd, Cu, Fe, Mn, Pb and Zn in wood and bark age classes of willows and poplars used for phytoextraction on soils contaminated by risk elements. Environ. Sci. Pollut. Res. Int. 22:18801–18813

    Article  PubMed  Google Scholar 

  42. FAO (2006) World reference base for soil resources. A framework for international classification, correlation and communication. Food and Agriculture Organisation of the United Nations, Rome, pp 1–127

    Google Scholar 

  43. Ettler V, Mihaljevič M, Šebek O, Molek M, Grygar T, Zeman J (2006) Geochemical and Pb isotopic evidence for sources and dispersal of metal contamination in stream sediments from the mining and smelting district of Příbram, Czech Republic. Environ. Pollut. 142:409–417

    Article  CAS  PubMed  Google Scholar 

  44. Rieuwerts J, Farago M (1996) Heavy metal pollution in the vicinity of a secondary lead smelter in the Czech Republic. Appl. Geochem. 11:17–23

    Article  CAS  Google Scholar 

  45. Unterseher M, Schnittler M (2009) Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.)—different cultivation techniques influence fungal biodiversity assessment. Mycological Res. 113:645–654

    Article  Google Scholar 

  46. Koubek J, Uhlik O, Jecna K, Junkova P, Vrkoslavova J, Lipov J, Kurzawova V, Macek T, Mackova M (2012) Whole-cell MALDI-TOF: rapid screening method in environmental microbiology. Int. Biodeter. Biodegr. 69:82–86

    Article  CAS  Google Scholar 

  47. Uhlik O, Strejcek M, Junkova P, Sanda M, Hroudova M, Vlcek C, Mackova M, Macek T (2011) 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

    Article  CAS  Google Scholar 

  48. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic acid techniques. In: Stackebrand E, Goodfellow M (eds) Bacterial systematics. John Wiley and Sons, New York, pp 115–175

    Google Scholar 

  49. Cole J, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell MD, Garrity GM, Tiedje JM (2005) The ribosomal database project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucelic Acids Res 33:294–296

    Article  Google Scholar 

  50. Štorchová H, Hrdličková R, Chrtek Jr J, Tetera M, Fitze D, Fehrer J (2000) An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon 49:79–84

    Article  Google Scholar 

  51. White TJ, Bruns TD, Lee S, Taylor J (1990) Analysis of phylogenetic relationship by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc., New York, pp 315–322

    Google Scholar 

  52. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol. Ecol. 2:113–118

    Article  CAS  PubMed  Google Scholar 

  53. Villaño D, Fernández-Pachón MS, Moyá ML, Troncoso AM, García-Parrilla MC (2007) Radical scavenging ability of polyphenolic compounds towards DPPH free radical. Talanta 71:230–235

    Article  PubMed  Google Scholar 

  54. Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS (2007) O-CAS a fast and universal method for siderophore detection. J. Microbiol. Met. 70:127–131

    Article  Google Scholar 

  55. Jasim B, Joseph AA, John CJ, Mathew J, Radhakrishnan EK (2014) Isolation and characterization of plant growth promoting endophytic bacteria from the rhizome of Zingiber officinale. 3. Biotech 4:197–204

    CAS  Google Scholar 

  56. Hajšlová J, Fenclová M, Zachariášová M (2013) 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

  57. Grison CM, Jackson S, Merlot S, Dobson A, Grison C (2015) Rhizobium metallidurans sp. nov., a symbiotic heavy metal resistant bacterium isolated from the Anthyllis vulneraria Zn-hyperaccumulator. Int. J. Syst. Evol. Micr. 65:1525–1530

    Article  CAS  Google Scholar 

  58. Weyens N, Beckers B, Schellingen K, Ceulemans R, Croes S, Janssen J, Haenen S, Witters N, Vangronsveld J (2013) Plant-associated bacteria and their role in the success or failure of metal phytoextraction projects: first observations of a field-related experiment. Microbial. Biotechnol. 6:288–299

    Article  Google Scholar 

  59. Ruiz-Díez B, Quiñones MA, Fajardo S, López MA, Higueras P, Fernández-Pascual M (2012) Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl Microb. Biot. 96:543–554

    Article  Google Scholar 

  60. Humphry DR, Andrews M, Santos SR, James EK, Vinogradova LV, Perin L, Reis VM, Cummings SP (2007) Phylogenetic assignment and mechanism of action of a crop growth promoting Rhizobium radiobacter strain used as a biofertiliser on graminaceous crops in Russia. Anton Leeuw. Int. J. G. 91:105–113

    Article  Google Scholar 

  61. Doty SL, Dosher MR, Singleton GL, Moore AL, Van Aken B, Stettler RF, Strand SE, Gordon MP (2005) Identification of an endophytic Rhizobium in stems of Populus. Symbiosis 39:27–35

    CAS  Google Scholar 

  62. Santamaría O, Diez JJ (2005) Fungi in leaves, twigs and stem bark of Populus tremula from Northern Spain. Forest Pathol. 35:94–105

    Article  Google Scholar 

  63. Albrectsen BR, Björkén L, Varad A, Hagner Å, Wedin M, Karlsson J, Jansson S (2010) Endophytic fungi in European aspen (Populus tremula) leaves—diversity, detection, and a suggested correlation with herbivory resistance. Fungal Divers. 41:17–28

    Article  Google Scholar 

  64. Sharma JK, Heather WA (1978) Parasitism of uredospores of Melampsora larici-populina Kleb. by Cladosporium sp. Eur. J. Forest Pathol. 8:48–54

    Article  Google Scholar 

  65. Hur M, Lim YW, Yu JJ, Cheon SU, Choi YI, Yoon S-H, Park S-C, Kim D-I, Yi H (2012) Fungal community associated with genetically modified poplar during metal phytoremediation. J. Microbiol. 50:910–915

    Article  CAS  PubMed  Google Scholar 

  66. Ban Y, Tang M, Chen H, Xu Z, Zhang H, Yang Y (2012) The response of dark septate endophytes (DSE) to risk elements in pure culture. PLoS One 7:e47968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zhang N, Castlebury LA, Miller AN, Huhndorf SM, Schoch CL, Seifert KA, Rossman AY, Rogers JD, Kohlmeyer J, Volkmann-Kohlmeyer B, Sung GH (2006) An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny. Mycologia 98:1076–1087

    Article  CAS  PubMed  Google Scholar 

  68. Van Bael SA, Fernandez-Marin H, Valencia MC, Rojas EI, Wcislo WT, Herre EA (2009) Two fungal symbioses collide: endophytic fungi are not welcome in leaf-cutting ant gardens. Proc. Biol. Sci. 276:2419–2426

    Article  PubMed  PubMed Central  Google Scholar 

  69. Panno L, Bruno M, Voyron S, Anastasi A, Gnavi G, Miserere L, Varese GC (2013) Diversity, ecological role and potential biotechnological applications of marine fungi associated to the seagrass Posidonia oceanica. New Biotechnol. 30:685–694

    Article  CAS  Google Scholar 

  70. Vázquez-Nion D, Rodríguez-Castro J, López-Rodríguez MC, Fernández-Silva I, Prieto B (2016) Subaerial biofilms on granitic historic buildings: microbial diversity and development of phototrophic multi-species cultures. Biofouling 32:657–669

    Article  PubMed  Google Scholar 

  71. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucl. Acids. Symp. Ser. 41:95–98

    CAS  Google Scholar 

  72. Walker DM, Castlebury LA, Rossman AY, White Jr JF (2012) New molecular markers for fungal phylogenetics: two genes for species-level systematics in the Sordariomycetes (Ascomycota). Mol. Phylogenet. Evol. 64:500–512

    Article  CAS  PubMed  Google Scholar 

  73. Regvar M, Likar M, Piltaver A, Kugonič N, Smith JE (2009) Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil 330:345–356

    Article  Google Scholar 

  74. Rodrigues MG, Fonseca A (2003) Molecular systematics of the dimorphic ascomycete genus Taphrina. Int. J. Syst. Evol. Microbiol. 53:607–616

    Article  CAS  PubMed  Google Scholar 

  75. Likar M, Regvar M (2013) Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil 370:593–604

    Article  CAS  Google Scholar 

  76. Croes S, Weyens N, Colpaet J, Vangronveld J (2015) Characterization of the cultivable bacterial populations associated with field grown Brassica napus L.: an evaluation of sampling and isolation protocols. Env. Microbiol. 17:2379–2392

    Article  CAS  Google Scholar 

  77. Cordier T, Robin C, Capdeville X, Desprex Loustau M-L, Vacher C (2012) Spatial variability of phyllosphere fungal assemblages: genetic distance dominates over geographic distance in an European beech stand (Fagus sylvatica). Fungal Ecol. 5:509–520

    Article  Google Scholar 

  78. Taylor A (2002) Fungal diversity in ectotomycorrhizal communities: sampling effort and species distribution. Plant Soil 244:19–28

    Article  CAS  Google Scholar 

  79. Hacquard S, Schadt CW (2015) Towards a holistic understanding of the beneficial interactions across the Populus microbiome. New Phytol. 205:1424–1430

    Article  PubMed  Google Scholar 

  80. Nautiyal (1999) An efficient microbiological growth medium for screening phosphate solibilising microorganisms. FEMS Microbiol. Lett. 170:265–270

    Article  CAS  PubMed  Google Scholar 

  81. Du RJ, He EK, Tang JT, Hu PJ, Ying RR, Morel JL, Qiu RL (2011) How phytohormone IAA and chelator EDTA affect lead uptake by Zn/Cd hyperaccumulator Picris divaricata. Int. J. Phytorem. 13:1024–1036

    Article  CAS  Google Scholar 

  82. UmaMaheswari T, Anbukkarasi K, Hemalatha T, Chendrayan K (2013) Studies on phytohormone producing ability of indigenous endophytic bacteria isolated from tropical legume crops. Int. J. Curr. Microbiol. App. Sci. 2:127–136

    Google Scholar 

  83. Ma Y, Rajkumar M, Luo JM, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J. Hazard. Mater. 195:230–237

    Article  CAS  PubMed  Google Scholar 

  84. Visioli G, D’Egidio S, Vamerali T, Mattarozzi M, Sanangelantoni AM (2014) Culturable endophytic bacteria enhance Ni translocation in the hyperaccumulator Noccaea caerulescens. Chemosphere 117:538–544

    Article  CAS  PubMed  Google Scholar 

  85. Xu R, Li T, Cui H, Wang J, Yu X, Ding Y, Wang C, Yang Z, Zhao Z (2015) Diversity and characterization of Cd-tolerant dark septate endophytes (DSEs) associated with the roots of Nepal alder (Alnus nepalensis) in a metal mine tailing of southwest China. Appl. Soil Ecol. 93:11–18

    Article  Google Scholar 

  86. Bonfim JA, Vasconcellos RLF, Baldesin LF, Sieber TN, Cardoso EJBN (2016) Dark septate endophytic fungi of native plants along an altitudinal gradient in the Brazilian Atlantic forest. Fungal Ecol. 20:202–210

    Article  Google Scholar 

  87. Wang JL, Li T, Liu GY, Smith JM, Zhao ZW (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Sci. Reports 6:22028. https://doi.org/10.1038/srep22028

    Article  CAS  Google Scholar 

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Acknowledgements

We are indebted to MSc. Dušan Kunc and RNDr. Helena Koblihová for the skillful technical assistance and to Judith Fehrer, Ph.D., for valuable comments on the manuscript. We thank the Silva Tarouca Research Institute for Landscape and Ornamental Gardening in Průhonice (RILOG) for their permission to sample on their site. This work was supported by the Technological Agency of the Czech Republic, project “Improvement of phytoremediation capacity and production potential of energy crops grown in contaminated and poor soils by means of endophytic and mycorrhizal symbionts” [grant no. TA03011184], and The Czech Academy of Sciences within the long-term research development project RVO [no. 67985939].

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Authors and Affiliations

  1. Institute of Botany ASCR, Zámek 1, 252 43, Průhonice, Czech Republic

    C. S. Schmidt & L. Mrnka

  2. University of Chemistry and Technology Prague, Technická 5, 166 28, Praha 6, Czech Republic

    P. Lovecká, A. Vychodilová, M. Strejček, M. Fenclová & K. Demnerová

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  1. C. S. Schmidt
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Conception and design: PL, LM, CS; Data acquisition: PL, AV, MF, LM, CS, MS; Analysis and interpretation of the data: PL, CS, LM, AV, MF, MS, KD; Drafting of the article: CS, PL, LM; Critical revision of the manuscript: CS, LM, KD, PL.

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Correspondence to C. S. Schmidt.

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No animals or data from human participants were used in the study.

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Highlights Communities of poplar endophytic bacteria and fungi were largely distinct on a risk elements-polluted and an unpolluted site. Rhizobia and a novel yet undescribed group of Sordariomycetous fungi dominated the risk elements-polluted site. Many poplar endophytes showed promising plant growth promoting and/or stress attenuating traits when studied in vitro.

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Schmidt, C.S., Lovecká, P., Mrnka, L. et al. Distinct Communities of Poplar Endophytes on an Unpolluted and a Risk Element-Polluted Site and Their Plant Growth-Promoting Potential In Vitro. Microb Ecol 75, 955–969 (2018). https://doi.org/10.1007/s00248-017-1103-y

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  • DOI: https://doi.org/10.1007/s00248-017-1103-y

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