Plant and Soil

, Volume 437, Issue 1–2, pp 397–411 | Cite as

Endophytic community of Pb-Zn hyperaccumulator Arabis alpina and its role in host plants metal tolerance

  • Vijay K. Sharma
  • Xin-ya Li
  • Guang-li Wu
  • Wei-xiao Bai
  • Shobhika Parmar
  • James F. White Jr
  • Hai-yan LiEmail author
Regular Article



Endophytes benefit host plants by increasing biotic and abiotic stress tolerance. The aims of this study were to evaluate endophytic community (EC) of Arabis alpina, a Pb-Zn hyperaccumulator and investigate role of EC in host plants metal tolerance.


EC of A. alpina growing at Pb–Zn mining area was evaluated by Illumina MiSeq sequencing. Pot experiments were conducted for the role of EC in metal accumulation and tolerance of host.


Fungal EC of shoots showed greater similarity to roots than to seeds; and Chao1 and Shannon indices for shoots and roots were significantly higher than for seeds. Inoculation of EC significantly improved host plants growth under multi-metal stress (p < 0.05, T test). The shoot length, root length and dry biomass of the treatment were improved when compared with the control. EC inoculation significantly altered accumulation of Pb, Cd and Zn in plant tissues. Particularly decreased the accumulation of Pb (p < 0.05) and Cd (p > 0.05) in the shoots of the treatment.


Hyperaccumulator A. alpina growing in metals contaminated soils was colonized by a diverse assemblage of endophytic fungi, and the EC played a key role in increasing host plants metal tolerance.


Hyperaccumulator Endophytic community High-throughput sequencing Potentially toxic metals Phytoremediation 



The authors are thankful to Prof. Zhiwei Zhao for his assistance in plant identification. The authors are also grateful for support from USDA-NIFA Multistate Project W3147, and the New Jersey Agricultural Experiment Station. This study was financially supported by Natural Science Foundation of China (31560566, 41867026, 31360128).

Supplementary material

11104_2019_3988_MOESM1_ESM.doc (36 kb)
ESM 1 (DOC 36 kb)
11104_2019_3988_MOESM2_ESM.doc (34 kb)
ESM 2 (DOC 34 kb)
11104_2019_3988_MOESM3_ESM.doc (28 kb)
ESM 3 (DOC 28 kb)
11104_2019_3988_MOESM4_ESM.doc (36 kb)
ESM 4 (DOC 36 kb)
11104_2019_3988_MOESM5_ESM.doc (36 kb)
ESM 5 (DOC 36.5 kb)


  1. Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi–recent updates and future perspectives. New Phytol 186:281–285CrossRefGoogle Scholar
  2. Akinsanya MA, Goh JK, Lim SP, Ting ASY (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genom Data 6:159–163. CrossRefGoogle Scholar
  3. Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M (2017) Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proc Natl Acad Sci U S A 114:E9403–E9412. CrossRefGoogle Scholar
  4. Aravind P, Prasad MN (2005) Cadmium-zinc interactions in a hydroponic system using Ceratophyllum demersum L.: adaptive ecophysiology, biochemistry and molecular toxicology. Braz J Plant Physiol 17:3–20. CrossRefGoogle Scholar
  5. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66. CrossRefGoogle Scholar
  6. Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106. CrossRefGoogle Scholar
  7. Deng Z, Cao L, Huang H, Jiang X, Wang W, Shi Y, Zhang R (2011) Characterization of cd-and Pb-resistant fungal endophyte Mucor sp. CBRF59 isolated from rapes (Brassica chinensis) in a metal-contaminated soil. J Hazard Mater 185:717–724. CrossRefGoogle Scholar
  8. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. CrossRefGoogle Scholar
  9. Etesami H (2018) Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol Environ Saf 147:175–191. CrossRefGoogle Scholar
  10. Facchinelli A, Sacchi E, Mallen L (2001) Multivariate statistical and GIS-based approach to identify heavy metal sources in soils. Environ Pollut 114:313–324. CrossRefGoogle Scholar
  11. Fisher PJ, Petrini O (1992) Fungal saprobes and pathogens as endophytes of rice (Oryza sativa L.). New Phytol 120:137–143. CrossRefGoogle Scholar
  12. Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327. CrossRefGoogle Scholar
  13. Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3:240–254. CrossRefGoogle Scholar
  14. Gerhardt KE, Huang XD, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30. CrossRefGoogle Scholar
  15. Hardoim PR, Hardoim CC, Van Overbeek LS, Van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e30438. CrossRefGoogle Scholar
  16. Huang WY, Cai YZ, Hyde KD et al (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33:61–75Google Scholar
  17. Khan AR, Waqas M, Ullah I, Khan AL, Khan MA, Lee IJ, Shin JH (2017) Culturable endophytic fungal diversity in the cadmium hyperaccumulator Solanum nigrum L. and their role in enhancing phytoremediation. Environ Exp Bot 135:126–135. CrossRefGoogle Scholar
  18. Kidd KA, Muir DC, Evans MS et al (2012) Biomagnification of mercury through lake trout (Salvelinus namaycush) food webs of lakes with different physical, chemical and biological characteristics. Sci Total Environ 438:135–143. CrossRefGoogle Scholar
  19. Letourneau A, Seena S, Marvanová L, Bärlocher F (2010) Potential use of barcoding to identify aquatic hyphomycetes. Fungal Divers 40:51–64. CrossRefGoogle Scholar
  20. Li T, Liu MJ, Zhang XT, Zhang HB, Sha T, Zhao ZW (2011) Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Sci Total Environ 409:1069–1074. CrossRefGoogle Scholar
  21. Li HY, Wei DQ, Shen M, Zhou ZP (2012a) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18. CrossRefGoogle Scholar
  22. Li HY, Li DW, He CM, Zhou ZP, Mei T, Xu HM (2012b) Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb–Zn mine wasteland in China. Fungal Ecol 5:309–315. CrossRefGoogle Scholar
  23. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258. CrossRefGoogle Scholar
  24. Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25. CrossRefGoogle Scholar
  25. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. CrossRefGoogle Scholar
  26. Miersch J, Bärlocher F, Bruns I (1997) Effects of cadmium, copper, and zinc on growth and thiol content of aquatic hyphomycetes. Hydrobiologia 346:77–84. CrossRefGoogle Scholar
  27. Novas MV, Collantes M, Cabral D (2007) Environmental effects on grass-endophyte associations in the harsh conditions of South Patagonia. FEMS Microbiol Ecol 61:164–173. CrossRefGoogle Scholar
  28. Orfali RS, Ebrahim W, El-Shafae AM (2017) Secondary metabolites from Alternaria sp., a fungal endophyte isolated from the seeds of Ziziphus jujuba. Chem Nat Compd 53:1031–1034. CrossRefGoogle Scholar
  29. Parmar S, Singh V (2015) Phytoremediation approaches for heavy metal pollution: a review. J Plant Sci Res 2:135Google Scholar
  30. Peršoh D, Melcher M, Flessa F, Rambold G (2010) First fungal community analyses of endophytic ascomycetes associated with Viscum album ssp. austriacum and its host Pinus sylvestris. Fungal Biol 114:585–596. CrossRefGoogle Scholar
  31. Qin Y, Pan X, Yuan Z (2016) Seed endophytic microbiota in a coastal plant and phytobeneficial properties of the fungus Cladosporium cladosporioides. Fungal Ecol 24:53–60. CrossRefGoogle Scholar
  32. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. CrossRefGoogle Scholar
  33. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149. CrossRefGoogle Scholar
  34. Sati SC, Arya P, Belwal M (2009) Tetracladium nainitalense sp. nov., a root endophyte from Kumaun Himalaya, India. Mycologia 101:692–695. CrossRefGoogle Scholar
  35. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: Open-Source, Platform- Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl Environ Microbiol 75:7537–7541. CrossRefGoogle Scholar
  36. Shahzad R, Khan AL, Bilal S, Waqas M, Kang SM, Lee IJ (2017) Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environ Exp Bot 136:68–77. CrossRefGoogle Scholar
  37. Shearin ZR, Filipek M, Desai R et al (2018) Fungal endophytes from seeds of invasive, non-native Phragmites australis and their potential role in germination and seedling growth. Plant Soil 422:183–194. CrossRefGoogle Scholar
  38. Shen M, Liu L, Li DW, Zhou WN, Zhou ZP, Zhang CF, Luo YY, Wang HB, Li HY (2013) The effect of endophytic Peyronellaea from heavy metal-contaminated and uncontaminated sites on maize growth, heavy metal absorption and accumulation. Fungal Ecol 6:539–545. CrossRefGoogle Scholar
  39. Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143. Google Scholar
  40. Solgi E, Esmaili-Sari A, Riyahi-Bakhtiari A, Hadipour M (2012) Soil contamination of metals in the three industrial estates, Arak, Iran. Bull Environ Contam Toxicol 88:634–638. CrossRefGoogle Scholar
  41. Spellerberg IF, Fedor PJ (2003) A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon–wiener’ index. Glob Ecol Biogeogr 12:177–179. CrossRefGoogle Scholar
  42. Street RA, Kulkarni MG, Stirk WA, Southway C, van Staden J (2010) Effect of cadmium on growth and micronutrient distribution in wild garlic (Tulbaghia violacea). S Afr J Bot 76:332–336. CrossRefGoogle Scholar
  43. Sun W, Xiong Z, Chu L et al (2018) Bacterial communities of three plant species from Pb-Zn contaminated sites and plant-growth promotional benefits of endophytic Microbacterium sp.(strain BXGe71). J Hazard Mater.
  44. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2013) Changes in the population of seed bacteria of transgenerationally cd-exposed Arabidopsis thaliana. Plant Biol 15:971–981. CrossRefGoogle Scholar
  45. 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, Hawai'i, Mexico and Puerto Rico. Fungal Ecol 3:122–138. CrossRefGoogle Scholar
  46. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391. CrossRefGoogle Scholar
  47. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. App Environ Microbiol 73:5261–5267. CrossRefGoogle Scholar
  48. 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 Rep 6:22028. CrossRefGoogle Scholar
  49. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009a) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254. CrossRefGoogle Scholar
  50. Weyens N, van der Lelie D, Taghavi S et al (2009b) Exploiting plant–microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598. CrossRefGoogle Scholar
  51. Wu F, Zhang G (2002) Genotypic variation in kernel heavy metal concentrations in barley and as affected by soil factors. J Plant Nutr 25:1163–1173. CrossRefGoogle Scholar
  52. Yamaji K, Watanabe Y, Masuya H, Shigeto A, Yui H, Haruma T (2016) Root fungal endophytes enhance heavy-metal stress tolerance of Clethra barbinervis growing naturally at mining sites via growth enhancement, promotion of nutrient uptake and decrease of heavy-metal concentration. PLoS One 11:e0169089. CrossRefGoogle Scholar
  53. Zu Y, Li Y, Chen J et al (2005) Hyperaccumulation of Pb, Zn and cd in herbaceous grown on lead–zinc mining area in Yunnan, China. Environ Int 31:755–762. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Vijay K. Sharma
    • 1
  • Xin-ya Li
    • 1
  • Guang-li Wu
    • 1
  • Wei-xiao Bai
    • 1
  • Shobhika Parmar
    • 1
  • James F. White Jr
    • 2
  • Hai-yan Li
    • 1
    Email author
  1. 1.Medical School of Kunming University of Science and TechnologyKunmingChina
  2. 2.Department of Plant BiologyRutgers UniversityNew BrunswickUSA

Personalised recommendations