Abstract
This paper represents the results of screening a diversity of fungal endophytes associated with Vitis vinifera leaves and canes in the Czech Republic. The characterization of strains is based on morphological and phylogenetic analyses of ITS, EF1α and TUB2 sequence data. Our strain selection covers 16 species and seven orders belonging to Ascomycota and Basidiomycota. Together with ubiquitous fungi, we report on several poorly known plant-associated fungi, Angustimassarina quercicola (= A. coryli, a synonym proposed in this study) and Pleurophoma pleurospora. Other species, such as Didymella negriana, D. variabilis, Neosetophoma sp. (species identical or sister to N. rosae), Phragmocamarosporium qujingensis and Sporocadus rosigena, have so far been little known and rarely found, but are frequent on V. vinifera in different parts of the world and obviously belong to a microbiota with a strong preference for this plant. Detailed taxonomical identification allowed us to identify species with apparent stable associations with V. vinifera, for which further interactions with V. vinifera can be expected. Our study is the first to focus on V. vinifera endophytes in Central Europe and expands the knowledge about their taxonomy, ecology and geography.
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Barcode gene sequences were deposited at the NCBI GenBank (Table 1). Strains were deposited at CCF (Charles University, Prague, Czech R.).
References
Aleynova OA, Nityagovsky NN, Suprun AR, Ananev AA, Dubrovina AS, Kiselev KV (2022) The diversity of fungal endophytes from wild grape Vitis amurensis Rupr. Plants 11:2897. https://doi.org/10.3390/plants11212897
Andreolli M, Lampis S, Poli M, Gullner G, Biró B, Vallini G (2013) Endophytic Burkholderia fungorum DBT1 can improve phytoremediation efficiency of polycyclic aromatic hydrocarbons. Chemosphere 92:688–694. https://doi.org/10.1016/j.chemosphere.2013.04.033
Arora P, Wani ZA, Nalli Y, Ali A, Riyaz-Ul-Hassan S (2016) Antimicrobial potential of thiodiketopiperazine derivatives produced by Phoma sp., an endophyte of Glycyrrhiza glabra Linn. Microb Ecol 72:802–812. https://doi.org/10.1007/s00248-016-0805-x
Aveskamp MM, de Gruyter J, Woudenberg J, Verkley G, Crous PW (2010) Highlights of the Didymellaceae: a polyphasic approach to characterise Phoma and related pleosporalean genera. Stud Mycol 65:1–60. https://doi.org/10.3114/sim.2010.65.01
Baldan E, Nigris S, Romualdi C, D’Alessandro S, Clocchiatti A, Zottini M, Stevanato P, Squartini A, Baldan B (2015) Beneficial bacteria isolated from grapevine inner tissues shape Arabidopsis thaliana roots. PLoS One 10:e0140252. https://doi.org/10.1371/journal.pone.0140252
Bien S, Damm U (2020) Prunus trees in Germany—a hideout of unknown fungi? Mycol Prog 19:667–690. https://doi.org/10.1007/s11557-020-01586-4
Boerema G, Loerakker W, Hamers ME (1996) Contributions towards a monograph of Phoma (Coelomycetes)—III. 2. Misapplications of the type species name and the generic synonyms of section Plenodomus (Excluded species). Persoonia - Molecular Phylogeny and Evolution of Fungi 16:141–189
Boerema GH (2004) Phoma identification manual: differentiation of specific and infra-specific taxa in culture. CABI
Bovo B, Andrighetto C, Carlot M, Corich V, Lombardi A, Giacomini A (2009) Yeast population dynamics during pilot-scale storage of grape marcs for the production of Grappa, a traditional Italian alcoholic beverage. Int J Food Microbiol 129:221–228. https://doi.org/10.1016/j.ijfoodmicro.2008.11.025
Brum MCP, Araújo WL, Maki CS, Azevedo JLD (2012) Endophytic fungi from Vitis labrusca L. (‘Niagara Rosada’) and its potential for the biological control of Fusarium oxysporum. Genet Mol Res 11:4187–4197. https://doi.org/10.4238/2012.December.6.2
Bulgari D, Casati P, Crepaldi P, Daffonchio D, Quaglino F, Brusetti L, Bianco PA (2011) Restructuring of endophytic bacterial communities in grapevine yellows-diseased and recovered Vitis vinifera L. plants. Appl Environ Microbiol 77:5018–5022. https://doi.org/10.1128/AEM.00051-11
Bulgari D, Casati P, Quaglino F, Bianco PA (2014) Endophytic bacterial community of grapevine leaves influenced by sampling date and phytoplasma infection process. BMC Microbiol 14:1–11. https://doi.org/10.1186/1471-2180-14-198
Bundhun D, Jeewon R, Senanayake IC, Camporesi E, Aluthmuhandiram JV, Tang AM, Kang J-C, Bhoyroo V, Hyde KD (2021) Morpho-molecular characterization of Discosia ravennica sp. nov. and a new host record for Sporocadus rosigena. MycoKeys 79:173. https://doi.org/10.3897/mycokeys.79.60662
Campisano A, Antonielli L, Pancher M, Yousaf S, Pindo M, Pertot I (2014) Bacterial endophytic communities in the grapevine depend on pest management. PloS one 9:e112763. https://doi.org/10.1371/journal.pone.0112763
Casieri L, Hofstetter V, Viret O, Gindro K (2009) Fungal communities living in the wood of different cultivars of young Vitis vinifera plants. Phytopathol Mediterr 48:73–83
Chethana K, Zhou Y, Zhang W, Liu M, Xing Q, Li X, Yan J, Chethana K, Hyde K (2017) Coniella vitis sp. nov. is the common pathogen of white rot in Chinese vineyards. Plant Dis 101:2123–2136. https://doi.org/10.1094/PDIS-12-16-1741-RE
Christian N, Sullivan C, Visser ND, Clay K (2016) Plant host and geographic location drive endophyte community composition in the face of perturbation. Microb Ecol 72:621–632. https://doi.org/10.1007/s00248-016-0804-y
Cioch-Skoneczny M, Satora P, Skoneczny S, Skotniczny M (2021) Biodiversity of yeasts isolated during spontaneous fermentation of cool climate grape musts. Arch Microbiol 203:153–162. https://doi.org/10.1007/s00203-020-02014-7
Cueva C, García-Ruiz A, González-Rompinelli E, Bartolome B, Martín-Álvarez P, Salazar O, Vicente M, Bills G, Moreno-Arribas M (2012) Degradation of biogenic amines by vineyard ecosystem fungi. Potential use in winemaking. J Appl Microbiol 112:672–682. https://doi.org/10.1111/j.1365-2672.2012.05243.x
Davari M, Hajieghrari B (2008) Phoma negriana, a new invasive pathogen for Moghan’s vineyards in Iran. Afr J Biotechnol 7:788–791. https://doi.org/10.4314/ajb.v7i6.58531
de Gruyter H, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous PW (2013) Redisposition of phoma-like anamorphs in Pleosporales. Stud Myc 75:1–36. https://doi.org/10.3114/sim0004
DeKrey DH, Klodd AE, Clark MD, Blanchette RA (2022) Grapevine trunk diseases of cold-hardy varieties grown in Northern Midwest vineyards coincide with canker fungi and winter injury. Plos one 17:e0269555. https://doi.org/10.1371/journal.pone.0269555
Del Frari G, Gobbi A, Aggerbeck MR, Oliveira H, Hansen LH, Ferreira RB (2019) Characterization of the wood mycobiome of Vitis vinifera in a vineyard affected by esca. Spatial distribution of fungal communities and their putative relation with leaf symptoms. Front Plant Sci 10:910. https://doi.org/10.3389/fpls.2019.00910
Dutra-Silva L, Pereira GE, Batista LR, Matteoli FP (2021) Fungal diversity and occurrence of mycotoxin producing fungi in tropical vineyards. World J Microbiol Biotechnol 37:112. https://doi.org/10.1007/s11274-021-03081-8
Fan Y, Gao L, Chang P, Li Z (2020) Endophytic fungal community in grape is correlated to foliar age and domestication. Ann Microbiol 70:30. https://doi.org/10.1186/s13213-020-01574-9
Gharwalova L, Hutar D, Masak J, Kolouchova I (2018) Antioxidant activity and phenolic content of organic and conventional vine cane extracts. Czech J Food Sci 36:289–295. https://doi.org/10.17221/19/2018-CJFS
Ghasemi Esfahlan S, Hemmati R, Mohebbi S, Batley J, Arzanlou M (2022) Identification of endophytic fungi of grapevine with emphasis on the causal agents of grapevine trunk disease in the vineyards of Zanjan Province in Iran For Pathol e12784. https://doi.org/10.1111/efp.12784
Gobbi A, Kyrkou I, Filippi E, Ellegaard-Jensen L, Hansen LH (2020) Seasonal epiphytic microbial dynamics on grapevine leaves under biocontrol and copper fungicide treatments. Sci Rep 10:681. https://doi.org/10.1038/s41598-019-56741-z
González V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42. https://doi.org/10.1007/s13225-010-0073-x
Grabka R, d’Entremont TW, Adams SJ, Walker AK, Tanney JB, Abbasi PA, Ali S (2022) Fungal endophytes and their role in agricultural plant protection against pests and pathogens. Plants 11:384. https://doi.org/10.3390/plants11030384
Hall ME, O’Bryon I, Wilcox WF, Osier MV, Cadle-Davidson L (2019) Epiphytic microbiome of grapes berries varies between phenological timepoints, growing seasons and regions. BioRxiv 2019.2012. 2020.884502. https://doi.org/10.1101/2019.12.20.884502
Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S, Campisano A, Doring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/mmbr.00050-14
Hofstetter V, Buyck B, Croll D, Viret O, Couloux A, Gindro K (2012) What if esca disease of grapevine were not a fungal disease? Fungal Divers 54:51–67. https://doi.org/10.1007/s13225-012-0171-z
Hou LW, Groenewald JZ, Pfenning LH, Yarden O, Crous PW, Cai L (2020) The phoma-like dilemma. Stud Mycol 96:309–396. https://doi.org/10.1016/j.simyco.2020.05.001
Hyde K, Chaiwan N, Norphanphoun C, Boonmee S, Camporesi E, Chethana K, Dayarathne M, de Silva N, Dissanayake A, Ekanayaka A (2018) Mycosphere notes 169–224. Mycosphere 9:271–430. https://doi.org/10.5943/mycosphere/9/2/8
Hyde KD, Norphanphoun C, Abreu VP et al (2017) Fungal diversity notes 603–708: taxonomic and phylogenetic notes on genera and species. Fungal Diver 87:1–235. https://doi.org/10.1007/s13225-017-0391-3
Jayawardena R, Hyde K, Chethana K, Daranagama D, Dissanayake A, Goonasekara I, Manawasinghe I, Mapook A, Jayasiri S, Karunarathna A (2018a) Mycosphere notes 102–168: Saprotrophic fungi on Vitis in China, Italy, Russia and Thailand. Mycosphere 9:1–114. https://doi.org/10.5943/mycosphere/9/1/1
Jayawardena RS, Liu M, Maharachchikumbura SS, Zhang W, Xing Q, Hyde KD, Nilthong S, Li X, Yan J (2016) Neopestalotiopsis vitis sp. nov. causing grapevine leaf spot in China. Phytotaxa 258:63–74. https://doi.org/10.11646/phytotaxa.258.1.4
Jayawardena RS, Purahong W, Zhang W, Wubet T, Li X, Liu M, Zhao W, Hyde KD, Liu J, Yan J (2018b) Biodiversity of fungi on Vitis vinifera L. revealed by traditional and high-resolution culture-independent approaches. Fungal Divers 90:1–84. https://doi.org/10.1007/s13225-018-0398-4
Kecskeméti E, Berkelmann-Löhnertz B, Reineke A (2016) Are epiphytic microbial communities in the carposphere of ripening grape clusters (Vitis vinifera L.) different between conventional, organic, and biodynamic grapes? PloS one 11:e0160852. https://doi.org/10.1371/journal.pone.0160852
Kernaghan G, Mayerhofer M, Griffin A (2017) Fungal endophytes of wild and hybrid Vitis leaves and their potential for vineyard biocontrol. Can J Microbiol 63:583–595. https://doi.org/10.1139/cjm-2016-0740
Knapp DG, Lázár A, Molnár A, Vajna B, Karácsony Z, Váczy KZ, Kovács GM (2021) Above-ground parts of white grapevine Vitis vinifera cv. Furmint share core members of the fungal microbiome. Environ Microbiol Rep 13:509–520. https://doi.org/10.1111/1758-2229.12950
Kolařík M, Spakowicz DJ, Gazis R, Shaw J, Kubátová A, Nováková A, Chudíčková M, Forcina GC, Kang KW, Kelnarová I (2017) Biatriospora (Ascomycota: Pleosporales) is an ecologically diverse genus including facultative marine fungi and endophytes with biotechnological potential. Plant Syst Evol 303:35–50. https://doi.org/10.1007/s00606-016-1350-2
Kolouchova I, Melzoch K, Šmidrkal J, Filip V (2005) The content of resveratrol in vegetables and fruit. Chemické Listy 99:492–495
Kulišová M, Vrublevskaya M, Lovecká P, Vrchotová B, Stránská M, Kolařík M, Kolouchová I (2021) Fungal endophytes of Vitis vinifera - plant growth promotion factors. Agriculture 11:1250. https://doi.org/10.3390/agriculture11121250
Liu F, Bonthond G, Groenewald JZ, Cai L, Crous PW (2019) Sporocadaceae, a family of coelomycetous fungi with appendage-bearing conidia. Stud Mycol 92:287–415. https://doi.org/10.1016/j.simyco.2018.11.001
Lücking R, Aime MC, Robbertse B, Miller AN, Ariyawansa HA, Aoki T, Cardinali G, Crous PW, Druzhinina IS, Geiser DM, Hawksworth DL, Hyde KD, Irinyi L, Jeewon R, Johnston PR, Kirk PM, Malosso E, May TW, Meyer W, Öpik M, Robert V, Stadler M, Thines M, Vu D, Yurkov AM, Zhang N, Schoch CL (2020) Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus 11:14. https://doi.org/10.1186/s43008-020-00033-z
Machowicz-Stefaniak Z, Król E (2007) Characterization of Phoma negriana Thum., a new species from grapevine canes. Acta Mycol 42:113–117. https://doi.org/10.5586/am.2007.011
Moloinyane S, Nchu F (2019) The effects of endophytic Beauveria bassiana inoculation on infestation level of Planococcus ficus, growth and volatile constituents of potted greenhouse grapevine (Vitis vinifera L.) Toxins (Basel). 11:72. https://doi.org/10.3390/toxins11020072
Mundy DC, Brown A, Jacobo F, Tennakoon K, Woolley RH, Vanga B, Tyson J, Johnston P, Ridgway HJ, Bulman S (2020) Pathogenic fungi isolated in association with grapevine trunk diseases in New Zealand. N Z J Crop Hortic Sci 48:84–96. https://doi.org/10.1080/01140671.2020.1716813
Núñez-Trujillo G, Cabrera R, Burgos-Reyes R, Silva ED, Giménez C, Cosoveanu A, Brito N (2012) Endophytic fungi from Vitis vinifera L. isolated in Canary Islands and Azores as potential biocontrol agents of Botrytis cinerea Pers. Fr J Hortic Forest Biotechnol 16:1–6
Oliveira M, Arenas M, Lage O, Cunha M, Amorim M (2018) Epiphytic fungal community in Vitis vinifera of the Portuguese wine regions. Lett Appl Microbiol 66:93–102. https://doi.org/10.1111/lam.12826
Pan XX, Yuan MQ, Xiang SY, Ma YM, Zhou M, Zhu Y-Y, Yang M-Z (2020) The symbioses of endophytic fungi shaped the metabolic profiles in grape leaves of different varieties. PLoS One 15:e0238734. https://doi.org/10.1371/journal.pone.0238734
Pancher M, Ceol M, Corneo PE, Longa CMO, Yousaf S, Pertot I, Campisano A (2012) Fungal endophytic communities in grapevines (Vitis vinifera L.) respond to crop management. Appl Environ Microbiol 78:4308–4317. https://doi.org/10.1128/AEM.07655-11
Phukhamsakda C, McKenzie EH, Phillips AJ, Gareth Jones E, Jayarama Bhat D, Stadler M, Bhunjun CS, Wanasinghe DN, Thongbai B, Camporesi E (2020) Microfungi associated with Clematis (Ranunculaceae) with an integrated approach to delimiting species boundaries. Fung Diver 102:1–203. https://doi.org/10.1007/s13225-020-00448-4
Píchová K, Pažoutová S, Kostovčík M, Chudíčková M, Stodůlková E, Novák P, Flieger M, van der Linde E, Kolařík M (2018) Evolutionary history of ergot with a new infrageneric classification (Hypocreales: Clavicipitaceae: Claviceps). Mol Phylogen Evol 123:73–87. https://doi.org/10.1016/j.ympev.2018.02.013
Ranade Y, Sawant I, Saha S, Chandrashekar M, Pathak P (2021) Epiphytic microbial diversity of Vitis vinifera fructosphere: present status and potential applications. Curr Microbiol 78:1086–1098. https://doi.org/10.1007/s00284-021-02385-0
Rashmi M, Kushveer J, Sarma V (2019) A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10:798–1079. https://doi.org/10.5943/mycosphere/10/1/19
Sayed SM, AM El-Shehawi SA, Elarnaouty SA, Al-Otaibi SA, El-Shazly SS, Alotaibi R, Ibrahim MM, Ahmed MM, Elseehy MM (2021) Molecular characterization of endophytic fungal communities associated with Vitis vinifera L. at Taif region of Saudi Arabia. J Environ Biol 42:177–185. https://doi.org/10.22438/jeb/42/2/MRN-1577
Schlegel M, Queloz V, Sieber TN (2018) The endophytic mycobiome of European ash and sycamore maple leaves–geographic patterns, host specificity and influence of ash dieback. Front Microbiol 9:2345. https://doi.org/10.3389/fmicb.2018.02345
Schulz B, Boyle C (2006) What are endophytes? Springer
Šigutová H, Šigut M, Pyszko P, Kostovčík M, Kolařík M, Drozd P (2023) Seasonal sifts in bacterial and fungal microbiomes of leaves and associated leaf-mining larvae reveal persistence of core taxa regardless of diet. Microbiol Spect e03160–03122. https://doi.org/10.1128/spectrum.03160-22
Stranska M, Dzuman Z, Prusova N, Behner A, Kolouchova I, Lovecka P, Rezanka T, Kolarik M, Hajslova J (2022) Fungal endophytes of Vitis vinifera - plant growth promoters or potentially toxinogenic agents? Toxins 14:66. https://doi.org/10.3390/toxins14020066
Thambugala KM, Hyde KD, Tanaka K, Tian Q, Wanasinghe DN, Ariyawansa HA, Jayasiri SC, Boonmee S, Camporesi E, Hashimoto A (2015) Towards a natural classification and backbone tree for Lophiostomataceae, Floricolaceae, and Amorosiaceae fam. nov. Fungal Divers 74:199–266. https://doi.org/10.1007/s13225-015-0348-3
Travadon R, Lecomte P, Diarra P, Lawrence D, Vallance J, Ojeda H, Rey P, Baumgartner K (2015) Influence of pruning systems on trunk pathogens and other fungi colonizing grapevine wood. Phytopathology S4:138
Úrbez-Torres J, Peduto F, Vossen P, Krueger W, Gubler W (2013) Olive twig and branch dieback: etiology, incidence, and distribution in California. Plant Dis 97:231–244. https://doi.org/10.1094/PDIS-04-12-0390-RE
Urbez-Torres JR, Peduto F, Striegler R, Urrea-Romero K, Rupe J, Cartwright R, Gubler W (2012) Characterization of fungal pathogens associated with grapevine trunk diseases in Arkansas and Missouri. Fungal Diver 52:169–189. https://doi.org/10.1007/s13225-011-0110-4
Wanasinghe DN, Phukhamsakda C, Hyde KD, Jeewon R, Lee HB, Gareth Jones EB, Tibpromma S, Tennakoon DS, Dissanayake AJ, Jayasiri SC, Gafforov Y, Camporesi E, Bulgakov TS, Ekanayake AH, Perera RH, Samarakoon MC, Goonasekara ID, Mapook A, Li W-J, Senanayake IC, Li J, Norphanphoun C, Doilom M, Bahkali AH, Xu J, Mortimer PE, Tibell L, Tibell S, Karunarathna SC (2018) Fungal diversity notes 709–839: taxonomic and phylogenetic contributions to fungal taxa with an emphasis on fungi on Rosaceae. Fungal Diver 89:1–236. https://doi.org/10.1007/s13225-018-0395-7
Wijayawardene NN, Dai D-Q, Zhu M-L, Wanasinghe DN, Kumla J, Zhang G-Q, Zhang T-T, Han L-S, Tibpromma S, Chen H-H (2022) Fungi associated with dead branches of Magnolia grandiflora: A case study from Qujing, China. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.954680
Wijekoon C, Quill Z (2020) Fungal endophyte diversity in table grapes. Canad J Microbiol 67:29–36. https://doi.org/10.1139/cjm-2020-0293
Yadav AN, Singh S, Mishra S, Gupta A (2019) Recent advancement in white biotechnology through fungi. Springer
Yağcı A, Akgül DS, Rustem C (2021) Endophytic fungi isolated from grapevines and rootstocks in Tokat Ecology and Their in vitro antagonistic effects on some grapevine pathogens. Book of abstracts: 8th National Plant Protection Congress (Online), 24–28 August 2021, Abant Izzet Baysal University, Bolu, Turkey
Yang MZ, Ma MD, Yuan MQ, Huang ZY, Yang WX, Zhang H-B, Huang L-H, Yun Ren A-Y, Shan H (2016) Fungal endophytes as a metabolic fine-tuning regulator for wine grape. PLoS One 11(9):e0163186. https://doi.org/10.1371/journal.pone.0163186
Zhang G-Q, Dai D-Q, Wijayawardene NN (2022) Three noteworthy pleosporalean fungi on Southern Magnolia (Magnolia grandiflora) and grapevine (Vitis sp.) from Qujing, Yunnan, PR China. MycoAsia – J Mod Mycol 1–21
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Conceptualization, supervision, M.Ko. (Miroslav Kolařík), I.J.K.; writing—original draft preparation, M.Ko. and M.V.; methodology, M.Ko, S.K.; formal analysis, M.Ko, M.Ku. (Markéta Kulišová); investigation and resources, M.Ko, S.K, M.V., I.J.K.; all authors have read and agreed to the published version of the manuscript.
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Kolařík, M., Vrublevskaya, M., Kajzrová, S. et al. Taxonomic analysis reveals host preference of rare fungi in endophytes of Vitis vinifera from the Czech Republic. Folia Microbiol 68, 961–975 (2023). https://doi.org/10.1007/s12223-023-01066-8
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DOI: https://doi.org/10.1007/s12223-023-01066-8