Abstract
The microbial diversity of Verbascum lychnitis community from industrial areas was investigated. The plants harbor a variety of endophytic fungi most of which belong to the Ascomycetes. The isolated fungal endophytes were identified according to ITS1-5.8S-ITS2 rDNA sequence similarity and were found to belong to 22 genera and 12 orders. The most frequently isolated genera were Diaporthe spp., Alternaria spp. and Pichia spp. An unidentified species from the Xylaria genus was isolated from V. lychnitis, which is a novel finding since most Xylaria species were reported to be solely wood-inhabiting fungi. The composition of fungal endophytes from the tailings site showed higher diversity, particularly in leaf tissues, than in non-tailings sites.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Abkhoo J, Sabbagh SK (2013) Evidence of Alternaria alternata causing leaf spot of Aloe vera in Iran. J Phytopathol 162:516–518
Akdemir ZŞ, Tatli Bedir E, Khan IA (2003) Antioxidant Flavonoids from Verbascum salviifolium Boiss. FABAD J Pharm Sci 28:71–75
Akdemir ZŞ, Tatli Bedir E, Khan IA (2004) Acylatediridoid glycosides from Verbascum lasianthum. Turk J Chem 28:101–110
Akkol EK, Tatli II, Akdemir ZS (2007) Antinociceptive and anti-inflammatory effects of saponin and iridoid glycosides from Verbascum pterocalycinum var. mutense Hub.-Mor. Z Naturforsch C 62:813–820
Alipieva KI, Orhan IE, Cankaya IIT, Kostadinova EP, Georgiev MI (2014) Treasure from garden: chemical profiling, pharmacology and biotechnology of mulleins. Phytochem Rev 13:417–444
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Aly AH, Edrada-Ebel R, Indriani ID, Wray V, Muller WE, Totzke F, Zirrgiebel U, Schachtele C, Kubbutat MHG, Lin WH, Proksch P, Ebel R (2008) Cytotoxic metabolites from the fungal endophyte Alternaria sp. and their subsequent detection in its host plant Polygonum senegalense. J Nat Prod 71:972–980
Anaissie EJ, Bodey GP, Rinaldi MG (1989) Emerging fungal pathogens. Eur J Clin Microbiol 8:323–330
Bacon CW, White JF Jr (1994) Stains, media, and procedures for analyzing endophytes. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press Inc, Boca Raton, pp 47–56
Bayman P (2007) Fungal endophytes. In: Kubicek CP, Druzhinina IS (eds) The Mycota, vol 4, Environmental and Microbial Relationships, 2nd edn. Springer, Berlin, pp 213–27
Bhagat J, Kaur A, Sharma M, Saxena AK, Chadha BS (2012) Molecular and functional characterization of endophytic fungi from traditional medicinal plants. World J Microbiol Biotechnol 28:963–971
Buzzini P, Martini A, Cappelli F, Pagnoni UM, Davoli P (2003) A study on volatile organic compounds (VOCs) produced by tropical ascomycetous yeasts. A Van Leeuw J Microb 84:301–311
Camatti-Sartori V, da Silva-Ribeiro RT, Valdebenito-Sanhueza RM, Pagnocca FC, Echeverrigaray S, Azevedo JL (2005) Endophytic yeasts and filamentous fungi associated with southern Brazilian apple (Malus domestica) orchards subjected to conventional, integrated or organic cultivation. J Basic Microbiol 45:397–402
Cheplick GP, Perera A, Koulouris K (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct Ecol 14:657–667
Clay K (1984) The effect of the fungus Atkinsonella hypoxylon (Clavicipitaceae) on the reproductive system and demography of the grass Danthonia spicata. New Phytol 98:165–175
Compant S, Mitter B, Colli-Mull JG, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microbiol Ecol 62:188–197
Crous PW, Summerell BA, Swart L, Denman S, Taylor JE, Bezuidenhout CM, Groenewald JZ (2011) Fungal pathogens of Proteaceae. Persoonia: Mol Phylogeny Evol Fungi 27:20–45
Dai CC, Yu BY, Li X (2008) Screening of endophytic fungi that promote the growth of Euphorbia pekinensis. Afr J Biotechnol 7:3505–3510
Farina C, Gotti E, Parma A, Naldi L, Goglio A (2007) Pheohyphomycotic soft tissue disease caused by Alternaria alternata in a kidney transplant patient: a case report and literature review. Transplant Proc 39:1655–1659
Fernandes MDRV, Pfenning LH, Costa-Neto CMD, Heinrich TA, Alencar SMD, Lima MAD, Ikegaki M (2009) Biological activities of the fermentation extract of the endophytic fungus Alternaria alternata isolated from Coffea arabica L. Braz J Pharm Sci 45:677–685
Fukasawa Y, Osono T, Takeda H (2009) Effects of attack of saprobic fungi on twig litter decomposition by endophytic fungi. Ecol Res 24:1067–1073
Gai CS, Lacava PT, Maccheroni W, Glienke C, Araújo WL, Miller TA, Azevedo JL (2009) Diversity of endophytic yeasts from sweet orange and their localization by scanning electron microscopy. J Basic Microbiol 49:441–451
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
Ghimire SR, Hyde KD (2004) Fungal endophytes. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, pp 281–292
Góralska K (2014) Zastosowanie mikroorganizmów w rekultywacji hałdy cynkowej Z.G.”Trzebionka”. Dissertation, Jagiellonian University
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hallmann J, Berg G, Schulz B (2006) Isolation procedures for endophytic microorganisms. In: Schulz B, Boyle C, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 299–319
Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 105:1–102
Heller A, Gierth K (2001) Cytological observations of the infection process by Phomopsis helianthi (Munt.‐ Cvet) in leaves of sunflower. J Phytopathol 149:347–357
Hisinger P (2013) Plant induced changes in soil processes and properties. In: Gregory PJ, Nortcliff S (eds) Soil conditions and plant growth. Wiley, New York, pp 323–365
Jurc M, Jurc D, Gogala N, Simoncic P (1996) Air pollution and fungal endophytes in needles of Austrian pine. Phyton Ann Rei Botanicae 36:111–114
Kahraman C, Ekizoglu M, Kart D, Akdemir ZŞ, Tatli II (2011) Antimicrobial activity of some Verbascum species growing in Turkey. FABAD J Pharm Sci 36:11–15
Kowalska J, Stryjewska E, Bystrzejewska-Piotrowska G, Lewandowski K, Tobiasz M, Paldyna J, Golimowski J (2012) Studies of plants useful in the re-cultivation of heavy metals-contaminated wasteland - a new hyper accumulator of barium? Pol J Environ Stud 21:401–405
Lappalainen JH, Koricheva J, Helander ML, Haukioja E (1999) Densities of endophytic fungi and performance of leafminers (Lepidoptera: Eriocraniidae) on birch along a pollution gradient. Environ Pollut 104:99–105
Larran S, Perello A, Simon MR, Moreno V (2002) Isolation and analysis of endophytic microorganisms in wheat (Triticum aestivum L.) leaves. World J Microbiol Biotechnol 18:683–686
Lee JH, Kim J, Kwak YS (2013) First report of black spot disease caused by Alternaria alternata on sweet persimmon fruits. Mycobiology 41:167–169
Leporatti ML, Ivancheva S (2003) Preliminary comparative analysis of medicinal plants used in the traditional medicine of Bulgaria and Italy. J Ethnopharmacol 87:123–142
Lewis GC (2004) Effects of biotic and abiotic stress on the growth of three genotypes of Lolium perenne with and without infection by the fungal endophyte Neotyphodium lolii. Ann Appl Biol 144:53–63
Maiti CK, Sen S, Paul AK, Acharya K (2007) First report of leaf blight disease of Gloriosa superba L. caused by Alternaria alternata (Fr.) Keissler in India. J Gen Plant Pathol 73:377–378
Mastretta C, Taghavi S, van der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267
Monnet F, Vaillant N, Hitmi A, Coudret A, Sallanon H (2001) Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Physiol Plant 113:557–563
Ohkura M, Abawi GS, Smart CD, Hodge KT (2009) Diversity and aggressiveness of Rhizoctonia solani and Rhizoctonia-like fungi on vegetables in New York. Plant Dis 93:615–624
Orłowska E, Jurkiewicz A, Anielska T, Godzik B, Turnau K (2005a) Influence of different arbuscularmycorrhiza fungal (AMF) strains on heavy metal uptake by Plantago lanceolata (Plantaginaceae). Pol Bot Stud 19:65–72
Orłowska E, Ryszka P, Jurkiewicz A, Turnau K (2005b) Effectiveness of arbuscular mycorrhizal fungal (AMF) strains in colonisation of plants involve in phytostabilisation of zinc wastes. Geoderma 129:92–98
Oses R, Valenzuela S, Freer J, Sanfuentes E, Rodriguez J (2008) Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Divers 33:77–86
Parmeter JR (1970) Rhizoctonia solani, biology and pathology. Univ of California Press
Pendleton RL, Smith BN (1983) Vesicular-arbuscular mycorrhizae of weedy and colonizer plant species at disturbed sites in Utah. Oecologia 59:296–301
Petersson S, Schnürer J (1995) Biocontrol of mold growth in high-moisture wheat stored under airtight conditions by Pichia anomala, Pichia guilliermondii, and Saccharomyces cerevisiae. Appl Environ Microbiol 61:1027–1032
Petrini O (1991) Fungal endophytes in tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 179–197
Promputtha I, Hyde KD, McKenzie EH, Peberdy JF, Lumyong S (2010) Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers 41:89–99
Purmale L, Apine I, Nikolajeva V, Grantina L, Verkley G, Tomsone S (2012) Endophytic fungi in evergreen rhododendrons cultivated in vitro and in vivo. Environ Exp Bot 10:1–7
Ravel C, Courty C, Coudret A, Charmet G (1997) Beneficial effects of Neotyphodium lolii on the growth and the water status in perennial ryegrass cultivated under nitrogen deficiency or drought stress. Agronomie 17:173–181
Rebele F (2008) Vegetation development on deposit soils starting at different seasons. Plant Ecol 195:1–12
Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581–1581
Rocha AC, Garcia D, Uetanabaro AP, Carneiro RT, Araújo IS, Mattos CR, Góes-Neto A (2011) Foliar endophytic fungi from Hevea brasiliensis and their antagonism on Microcyclus ulei. Fungal Divers 47:75–84
Ryszka P, Turnau K (2007) Arbuscular mycorrhiza of introduced and native grasses colonizing zinc wastes: implications for restoration practices. Plant Soil 298:219–229
Sagiroglu A, Sasmaz A, Sen O (2006) Hyperaccumulator plants of the Keban mining district and their possible impact on the environment. Pol J Environ Stud 15:317–325
Sánchez Márquez S, Bills GF, Herrero N, Zabalgogeazcoa Í (2012) Non-systemic fungal endophytes of grasses. Fungal Ecol 5:289–297
Santamarı’a J, Bayman P (2005) Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microbiol Ecol 50:1–8
Schardl CL, Phillips TD (1997) Protective grass endophytes: where are they from and where are they going? Plant Dis 81:430–438
Scheper RWA, Crane DC, Whisson DL, Scott ES (2000) The Diaporthe teleomorph of Phomopsis Taxon 1 on grapevine. Mycol Res 104:226–231
Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686
Sezik E, Yeşilada E, Honda G, Takaishi Y, Takeda Y, Tanaka T (2001) Traditional medicine in Turkey X. Folk medicine in central Anatolia. J Ethnopharmacol 75:95–115
Sher H (2011) Ethnoecological evaluation of some medicinal and aromatic plants of Kot Malakand Agency, Pakistan. Sci Res Essays 6:2164–2173
Shimura H, Sadamoto M, Matsuura M, Kawahara T, Naito S, Koda Y (2009) Characterization of mycorrhizal fungi isolated from the threatened Cypripedium macranthos in a northern island of Japan: two phylogenetically distinct fungi associated with the orchid. Mycorrhiza 19:525–534
Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89
Siegel MR, Bush LP (1996) Defensive chemicals in grass-fungal endophyte associations. In: Romeo JT, Saunders JA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions. Springer, US, pp 81–119
Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiol Plant 131:581–589
Spurr HW Jr, Welty RE (1975) Characterization of endophytic fungi in healthy leaves of Nicotiana spp. Phytopathology 65:417–422
Stone JK, Polishook JD, White JF (2004) Endophytic fungi. Biodiversity of Fungi. In: Foster MS, Bills GF (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier Academic Press, Burlington, pp 241–270
Sun X, Guo LD, Hyde KD (2011) Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Divers 47:85–95
Suryanarayanan TS, Murali TS, Venkatesan G (2002) Occurrence and distribution of fungal endophytes in tropical forests across a rainfall gradient. Can J Bot 80:818–826
Suryanarayanan TS, Murali TS, Thirunavukkarasu N, Rajulu MG, Venkatesan G, Sukumar R (2011) Endophytic fungal communities in woody perennials of three tropical forest types of the Western Ghats, southern India. Biodivers Conserv 20:913–928
Turker AU, Gurel E (2005) Common mullein (Verbascum thapsus L.): recent advances in research. Phytother Res 19:733–739
Turker AU, Camper ND, Gürel E (2004) High-Performance Liquid Chromatographic determination of a saponin from Verbascum thapsus L. Biotechnol Biotechnol Equip 18:54–59
Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in southern Poland. Mycorrhiza 10:169–174
Turnau K, Anielska T, Ryszka P, Gawroński S, Ostachowicz B, Jurkiewicz A (2008) Establishment of arbuscular mycorrhizal plants originating from xerothermic grasslands on heavy metal rich industrial wastes–new solution for waste revegetation. Plant Soil 305:267–280
Turnau K, Ostachowicz B, Wojtczak G, Anielska T, Sobczyk Ł (2010) Metal uptake by xerothermic plants introduced into Zn-Pb industrial wastes. Plant Soil 337:299–311
Turnau K, Gawroński S, Ryszka P, Zook D (2012) Mycorrhizal-based phytostabilization of Zn–Pb tailings: lessons from the Trzebionka mining works (Southern Poland). In: Kothe E, Varma A (eds) Bio-geo interactions in metal-contaminated soils. Springer, Berlin, pp 327–348
Udayanga D, Liu X, McKenzie EH, Chukeatirote E, Bahkali HKD (2011) The genus Phomopsis: biology, applications, species concepts and names of common phytopathogens. Fungal Divers 50:189–225
Verma VC, Gond SK, Kumar A, Kharwar RN, Strobel G (2007) The endophytic mycoflora of bark, leaf, and stem tissues of Azadirachtaindica A. Juss (Neem) from Varanasi (India). Microbiol Ecol 54:119–125
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, 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
Wang XN, Huang WY, Du JC, Li CY, Liu JK (2014) Chemical constituents from the fruiting bodies of Xylaria euglossa Fr. and its chemotaxonomic study. Biochem Syst Ecol 54:157–159
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, London, pp 315–322
Wojtczak G (2013) Symbionty mykoryzowej storczyków z terenów skazonych metalami ciężkimi-badania molekularne. Dissertation, Jagiellonian University
Wong MK, Hyde KD (2001) Diversity of fungi on six species of Gramineae and one species of Cyperaceae in Hong Kong. Mycol Res 105:1485–1491
Wood PMR, Sivasithamparam K (1989) Diaporthe woodii (anamorph Phomopsis leptostromiformis)-A toxigenic fungus infecting cultivated lupins. Mycopathologia 105:79–86
Zhao J, Mou Y, Shan T, Li Y, Zhou L, Wang M, Wang J (2010) Antimicrobial metabolites from the endophytic fungus Pichia guilliermondii isolated from Paris polyphylla var. yunnanensis. Molecules 15:7961–7970
Zielińska-Pisklak M, Szeleszczuk Ł, Wilczek K (2013) Dziewanna – starosłowiańska bogini wiosny. Lek w Polsce 3
Acknowledgments
This work was supported by The National Science Center (MAESTRO project) on the basis of DEC-2011/02/A/NZ9/00137 and a Grant from the Jagiellonian University (DS/MND/WBiN0Z/INoŚ/23/2011).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wężowicz, K., Rozpądek, P. & Turnau, K. The diversity of endophytic fungi in Verbascum lychnitis from industrial areas. Symbiosis 64, 139–147 (2014). https://doi.org/10.1007/s13199-015-0312-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-015-0312-8


