Abstract
Aims
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.
Methods
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.
Results
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.
Conclusions
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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 186:281–285
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. https://doi.org/10.1016/j.gdata.2015.09.004
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. https://doi.org/10.1073/pnas.1710455114
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. https://doi.org/10.1590/S1677-04202005000100002
Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66. https://doi.org/10.1016/j.fbr.2007.05.003
Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106. https://doi.org/10.1016/j.chemosphere.2016.10.097
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. https://doi.org/10.1016/j.jhazmat.2010.09.078
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
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. https://doi.org/10.1016/j.ecoenv.2017.08.032
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. https://doi.org/10.1016/S0269-7491(00)00243-8
Fisher PJ, Petrini O (1992) Fungal saprobes and pathogens as endophytes of rice (Oryza sativa L.). New Phytol 120:137–143. https://doi.org/10.1111/j.1469-8137.1992.tb01066.x
Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110:318–327. https://doi.org/10.1016/j.mycres.2005.10.005
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. https://doi.org/10.1016/j.funeco.2009.12.001
Gerhardt KE, Huang XD, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30. https://doi.org/10.1016/j.plantsci.2008.09.014
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. https://doi.org/10.1371/journal.pone.0030438
Huang WY, Cai YZ, Hyde KD et al (2008) Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers 33:61–75
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. https://doi.org/10.1016/j.envexpbot.2016.03.005
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. https://doi.org/10.1016/j.scitotenv.2012.08.057
Letourneau A, Seena S, Marvanová L, Bärlocher F (2010) Potential use of barcoding to identify aquatic hyphomycetes. Fungal Divers 40:51–64. https://doi.org/10.1007/s13225-009-0006-8
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. https://doi.org/10.1016/j.scitotenv.2010.12.012
Li HY, Wei DQ, Shen M, Zhou ZP (2012a) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18. https://doi.org/10.1007/s13225-012-0165-x
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. https://doi.org/10.1016/j.funeco.2011.06.002
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. https://doi.org/10.1016/j.biotechadv.2010.12.001
Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25. https://doi.org/10.1016/j.jenvman.2016.02.047
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
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. https://doi.org/10.1023/A:1002957830704
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. https://doi.org/10.1111/j.1574-6941.2007.00319.x
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. https://doi.org/10.1007/s10600-017-2195-9
Parmar S, Singh V (2015) Phytoremediation approaches for heavy metal pollution: a review. J Plant Sci Res 2:135
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. https://doi.org/10.1016/j.funbio.2010.04.009
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. https://doi.org/10.1016/j.funeco.2016.08.011
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. https://doi.org/10.1093/nar/gks1219
Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149. https://doi.org/10.1016/j.tibtech.2009.12.002
Sati SC, Arya P, Belwal M (2009) Tetracladium nainitalense sp. nov., a root endophyte from Kumaun Himalaya, India. Mycologia 101:692–695. https://doi.org/10.3852/08-192
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. https://doi.org/10.1128/AEM.01541-09
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. https://doi.org/10.1016/j.envexpbot.2017.01.010
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. https://doi.org/10.1007/s11104-017-3241-x
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. https://doi.org/10.1016/j.funeco.2013.08.001
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. https://doi.org/10.3389/fpls.2015.01143
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. https://doi.org/10.1007/s00128-012-0553-7
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. https://doi.org/10.1046/j.1466-822X.2003.00015.x
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. https://doi.org/10.1016/j.sajb.2009.12.006
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. https://doi.org/10.1016/j.jhazmat.2018.02.003
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. https://doi.org/10.1111/j.1438-8677.2012.00711.x
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. https://doi.org/10.1016/j.funeco.2009.07.002
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. https://doi.org/10.1073/pnas.0504423102
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. https://doi.org/10.1128/AEM.00062-07
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. https://doi.org/10.1038/srep22028
Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009a) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254. https://doi.org/10.1016/j.copbio.2009.02.012
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. https://doi.org/10.1016/j.tibtech.2009.07.006
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. https://doi.org/10.1081/PLN-120004380
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. https://doi.org/10.1371/journal.pone.0169089
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. https://doi.org/10.1016/j.envint.2005.02.004
Acknowledgements
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Antony Van der Ent.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sharma, V.K., Li, Xy., Wu, Gl. et al. Endophytic community of Pb-Zn hyperaccumulator Arabis alpina and its role in host plants metal tolerance. Plant Soil 437, 397–411 (2019). https://doi.org/10.1007/s11104-019-03988-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-03988-0