Abstract
Ecological methods are becoming increasingly popular. One of these methods is plant biotization. In our paper, we focus on selection of Vaccinium corymbosum hairy root-inhabiting fungi for plant growth promotion in a single microorganism inoculation setup and then composed a multiorganismal inoculum enriched with a representative of another group of fungi, leaf endophytes. The hairy roots of V. corymbosum hosted 13 fungal taxa. In single inoculation of the plant with fungal strains, the most beneficial for plant growth were Oidiodendron maius and Phialocephala fortinii. Additional inoculation of the plants with three root symbiotic fungi (O. maius, Hymenoscyphus sp. and P. fortinii) and with the endophytic fungus Xylaria sp. increased plant height in laboratory experiments. On a semi-industrial scale, inoculation improved plant biomass and vitality. Therefore, the amendment of root-associated fungal communities with a mixture of ericoid mycorrhizal and endophytic fungi may represent an alternative to conventional fertilization and pesticide application in large-scale blueberry production.
Key points
• O. maius and P. fortinii significantly stimulated V. corymbosum growth in a single inoculation.
• Multimicroorganismal inoculum increased plant biomass and vitality.
• Blueberry biotization with ericoid and endophytic fungi is recommended.
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Data availability
Data generated during this study (nucleotide sequences) have been deposited in the GenBank database with the primary accession numbers OM729672–OM729684.
References
Bizabani C, Dames J (2015) Effects of inoculating Lachnum and Cadophora isolates on the growth of Vaccinium corymbosum. Microbiol Res 181:68–74. https://doi.org/10.1016/j.micres.2015.08.005
Cairney JWG, Burke RM (1998) Extracellular enzyme activities of the ericoid mycorrhizal endophyte Hymenoscyphus ericae (Read) Korf and Kernan: their likely roles in decomposition of dead plant tissue in soil. Plant Soil 205:181–192. https://doi.org/10.1023/A:1004376731209
Cao G, Sofic E, Prior RL (1997) Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships. Free Radic Biol Med 22:749–760. https://doi.org/10.1016/S0891-5849(96)00351-6
Colwell JD (1963) The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Aust J Exp Agric 3:190–197
Dalpé Y (1986) Axenic synthesis of ericoid mycorrhiza in Vaccinium angustifolium Ait. by Oidiodendron species. New Phytol 103:391–396
De Silva A, Patterson K, Rothrock C, Moore J (2000) Growth promotion of highbush blueberry by fungal and bacterial inoculants. HortScience 35:1228–1230. https://doi.org/10.21273/hortsci.35.7.1228
Diamanti J, Capocasa F, Balducci F, Battino M, Hancock J, Mezzetti B (2012) Increasing strawberry fruit sensorial and nutritional quality using wild and cultivated germplasm. PLoS ONE 7(10):e46470. https://doi.org/10.1371/journal.pone.0046470
Douglas GC, Heslin MC, Reid C (1989) Isolation of Oidiodendron maius from Rhododendron and ultrastructural characterization of synthesized mycorrhizas. Can J Bot 67:2206–2212. https://doi.org/10.1139/b89-280
Fan M, Chen X, Luo X, Zhang H, Liu Y, Zhang Y, Wu J, Zhao C, Zhao P (2020) Diversity of endophytic fungi from the leaves of Vaccinium dunalianum. Lett Appl Microbiol 71:479–489. https://doi.org/10.1111/lam.13345
Fehrer J, Réblová M, Bambasová V, Vohník M (2019) The root-symbiotic Rhizoscyphus ericae aggregate and Hyaloscypha (Leotiomycetes) are congeneric: phylogenetic and experimental evidence. Stud Mycol 92:195–225. https://doi.org/10.1016/j.simyco.2018.10.004
Fukumoto LR, Mazza G (2000) Assessing antioxidant and prooxidant activities of phenolic compounds. J Agric Food Chem 48:3597–3604. https://doi.org/10.1021/jf000220w
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
Gaskins MH, Albrecht SL, Hubbell DH (1985) Rhizosphere bacteria and their use to increase plant productivity: a review. Agric Ecosyst Environ 12:99–116. https://doi.org/10.1016/0167-8809(85)90071-4
Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (2002) Mycorrhizal technology in agriculture. From genes to bioproducts. Birkhäuser Verlag, Basel, Boston, Berlin, pp 1–296
Gianinazzi S, Oubaha L, Chahbandar M, Blal B, Lemoine M-C (2003) Biotization of microplants for improved performance. Acta Hortic 625:165–172. https://doi.org/10.17660/ActaHortic.2003.625.17
Gollotte A, Secco B, Mercy L, Lemoine MC, Durand P, Prost M, Gianinazzi S (2009) Raspberry breeding and biotisation for increasing plant stress tolerance and antioxidant activity. Acta Hortic 838:145–150. https://doi.org/10.17660/ActaHortic.2009.838.24
Halmschlager E, Kowalski T (2003) Sporothrix inflata, a root-inhabiting fungus of Quercus robur and Q. petraea. Mycol Prog 2:259–266
Hambleton S, Currah RS (1997) Fungal endophytes from the roots of alpine and boreal Ericaceae. Can J Bot 75:1570–1581. https://doi.org/10.1139/b97-869
Hambleton S, Sigler L (2005) Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (=Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53:1–27
Hamim A, Miché L, Douaik A, Mrabet R, Ouhammou A, Duponnois R, Hafidi M (2017) Diversity of fungal assemblages in roots of Ericaceae in two Mediterranean contrasting ecosystems. Comptes Rendus - Biol 340:226–237. https://doi.org/10.1016/j.crvi.2017.02.003
Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition, 2nd edn. Farnham Royal, Bucks, England: The Commonwealth Agricultural Bureaux 22:1–241. https://doi.org/10.2136/sssaj1953.03615995001700030033x
Hu J, Wei Z, Friman VP, Gu SH, Wang XF, Eisenhauer N, Yang TJ, Ma J, Shen QR, Xu YC, Jousset A (2016) Probiotic diversity enhances rhizosphere microbiome function and plant disease suppression. Mbio 7(6):e01790-e1816. https://doi.org/10.1128/mBio.01790-16
Jansa J, Vosátka M (2000) In vitro and post vitro inoculation of micropropagated Rhododendrons with ericoid mycorrhizal fungi. Appl Soil Ecol 15:125–136. https://doi.org/10.1016/S0929-1393(00)00088-3
Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16. https://doi.org/10.1007/s00374-002-0546-5
Larson RA (1988) The antioxidants of higher plants. Phytochemistry 27:969–978. https://doi.org/10.1016/0031-9422(88)80254-1
Liu R, Dai M, Wu X, Li M, Liu X (2012) Suppression of the root-knot nematode [Meloidogyne incognita (Kofoid & White) Chitwood] on tomato by dual inoculation with arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria. Mycorrhiza 22:289–296. https://doi.org/10.1007/s00572-011-0397-8
Manganaris GA, Goulas V, Vicente AR, Terry LA (2014) Berry antioxidants: small fruits providing large benefits. J Sci Food Agric 94:825–833. https://doi.org/10.1002/jsfa.6432
Nguyen MP, Lehosmaa K, Martz F, Koskimäki JJ, Pirttilä AM, Häggman H (2021) Host species shape the community structure of culturable endophytes in fruits of wild berry species (Vaccinium myrtillus L., Empetrum nigrum L. and Vaccinium vitis-idaea L.). FEMS Microbiol Ecol 97:1–13. https://doi.org/10.1093/femsec/fiab097
Ortiz-Galeana MA, Hernández-Salmerón JE, Valenzuela-Aragón B, Delossantos-Villalobos S, del Carmen Rocha-Granados M, Santoyo G (2018) Diversidad de bacterias endófitas cultivables asociadas a plantas de arándano (Vaccinium corymbosum L.) cv. Biloxi con actividades promotoras del crecimiento vegetal. Chil J Agric Anim Sci 34(2):140–151. https://doi.org/10.4067/s0719-38902018005000403
Pearson V, Read DJ (1973) The biology of mycorrhiza in the Ericaceae, I. The isolation of the endophyte and synthesis of mycorrhizas in aseptic culture. New Phytol 72:371–379. https://doi.org/10.1111/j.1469-8137.1973.tb02044.x
Percival D, MacKenzie JL (2007) Use of plant growth regulators to increase polyphenolic compounds in the wild blueberry. Can J Plant Sci 87:333–336. https://doi.org/10.4141/P06-120
Pietta PG (2000) Flavonoids as antioxidants. J Nat Prod 63:1035–1042. https://doi.org/10.1021/np9904509
Prior RL, Cao G, Martin A, Sofic E, McEwen J, O’Brien C, Lischner N, Ehlenfeldt M, Kalt W, Krewer G, Mike C (1998) Antioxidant capacity as influenced by total phenolic and anthocyanin content, maturity, and variety of Vaccinium species. J Agric Food Chem 46:2686–2693
Remans R, Ramaekers L, Schelkens S, Hernandez G, Garcia A, Reyes JL, Mendez N, Toscano V, Mulling M, Galvez L, Vanderleyden J (2008) Effect of Rhizobium-Azospirillum coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in Cuba. Plant Soil 312:25–37. https://doi.org/10.1007/s11104-008-9606-4
Rozpądek P, Wężowicz K, Stojakowska A, Malarz J, Surówka E, Sobczyk T, Anielska T, Ważny R, Miszalski Z, Turnau K (2014) Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L. (Asteraceae) under metal toxicity. Chemosphere 112:217–224. https://doi.org/10.1016/j.chemosphere.2014.04.023
Rozpądek P, Nosek M, Ślesak I, Kunicki E, Dziurka M, Miszalski Z (2015) Ozone fumigation increases the abundance of nutrients in Brassica vegetables: broccoli (Brassica oleracea var. italica) and Chinese cabbage (Brassica pekinensis). Eur Food Res Technol 240:459–462. https://doi.org/10.1007/s00217-014-2372-z
Rozpądek P, Nosek M, Domka A, Ważny R, Jędrzejczyk R, Tokarz K, Pilarska M, Niewiadomska E, Turnau K (2019) Acclimation of the photosynthetic apparatus and alterations in sugar metabolism in response to inoculation with endophytic fungi. Plant Cell Environ 42:1408–1423. https://doi.org/10.1111/pce.13485
Scagel CF (2005) Inoculation with ericoid mycorrhizal fungi alters fertilizer use of highbush blueberry cultivars. HortScience 40:786–794
Scagel CF, Wagner A, Winiarski P (2005) Inoculation with ericoid mycorrhizal fungi alters root colonization and growth in nursery production of blueberry plants from tissue culture and cuttings. Small Fruits Rev 4:113–135. https://doi.org/10.1300/J301v04n04_11
Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296. https://doi.org/10.1007/s00572-008-0180-7
Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol b: Biol 104(1–2):236–257. https://doi.org/10.1016/j.jphotobiol.2010.12.010
Strasser R, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation & adaptation. Taylor and Francis, London, pp 445–483
Strik BC, Yarborough D (2005) Blueberry production trends in North America, 1992 to 2003, and predictions for growth. Horttechnology 15:391–398. https://doi.org/10.21273/horttech.15.2.0391
Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. https://doi.org/10.4324/9781315839707
Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of stress impact on plant’s vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer-Verlag, Berlin Heidelberg, 679–703. https://doi.org/10.1007/978-3-540-78826-3
Turnau K, Henriques FS, Anielska T, Renker C, Buscot F (2007) Metal uptake and detoxification mechanisms in Erica andevalensis growing in a pyrite mine tailing. Environ Exp Bot 61:117–123. https://doi.org/10.1016/j.envexpbot.2007.05.001
Turnau K, Ważny R, Rozpądek P (2021) Inoculum, a method of preparing inoculum and a method of biotization of highbush blueberry (in Polish). Patent Office of the Republic of Poland, Patent no, p 238335
Villarreal-Ruiz L, Anderson IC, Alexander IJ (2004) Interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol 164:183–192
Vohník M, Lukančič S, Bahor E, Regvar M, Vosátka M, Vodnik D (2003) Inoculation of Rhododendron cv. Belle-Heller with two strains of Phialocephala fortinii in two different substrates. Folia Geobot 38:191–200. https://doi.org/10.1007/BF02803151
Vohník M, Sadowsky JJ, Lukešová T, Albrechtová J, Vosátka M (2012) Inoculation with a ligninolytic basidiomycete, but not root symbiotic ascomycetes, positively affects growth of highbush blueberry (Ericaceae) grown in a pine litter substrate. Ligninolytic basidiomycete enhances growth of blueberry. Plant Soil 355:341–352. https://doi.org/10.1007/s11104-011-1106-2
Vrålstad T, Myhre E, Schumacher T (2002) Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytol 155:131–148
Wang SY, Lin HS (2000) Antioxidant activity in fruits and leaves of blackberry, raspberry, and strawberry varies with cultivar and developmental stage. J Agric Food Chem 48:140–146. https://doi.org/10.1021/jf9908345
Wang MY, Bin HuL, Wang WH, Liu ST, Li M, Liu RJ (2009) Influence of long-term fixed fertilization on diversity of arbuscular mycorrhizal fungi. Pedosphere 19:663–672. https://doi.org/10.1016/S1002-0160(09)60161-2
Ważny R, Rozpądek P, Jędrzejczyk RJ, Śliwa M, Stojakowska A, Anielska T, Turnau K (2018) Does co-inoculation of Lactuca serriola with endophytic and arbuscular mycorrhizal fungi improve plant growth in a polluted environment? Mycorrhiza 28:235–246. https://doi.org/10.1007/s00572-018-0819-y
Wężowicz K, Rozpądek P, Turnau K (2017) Interactions of arbuscular mycorrhizal and endophytic fungi improve seedling survival and growth in post-mining waste. Mycorrhiza 27:1–13. https://doi.org/10.1007/s00572-017-0768-x
White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wilke B-M (2005) Determination of chemical and physical soil properties. In: Morgesin R, Schinner F (eds) Manual of soil analysis. Springer-Verlag, Berlin, Heidelberg, Monitoring and assessing soil bioremediation, pp 47–95
Wu F-L, Li Y, Tian W, Sun Y, Chen F, Zhang Y, Zhai Y, Zhang J, Su H, Wang L (2021) A novel dark septate fungal endophyte positively affected blueberry growth and changed the expression of plant genes involved in phytohormone and flavonoid biosynthesis. Tree Physiol 40:1080–1094. https://doi.org/10.1093/TREEPHYS/TPAA047
Yu YY, Da XuJ, Huang TX, Zhong J, Yu H, Qiu JP, Guo JH (2020) Combination of beneficial bacteria improves blueberry production and soil quality. Food Sci Nutr 8:5776–5784
Acknowledgements
The authors would like to acknowledge Teresa Anielska, Martyna Janicka and Weronika Janas (Jagiellonian University, Poland) for technical support and Niwa Hodowla Roślin Jagodowych (PL company) for cooperation in the project.
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This work was supported by The National Science Centre and The National Centre for Research and Development, Poland, project TANGO (contract No. TANGO1/269101/NCBR/2015).
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RW, KT and PR conceived and designed the research. RW, RJJ and AD performed the research. RW analysed the data and wrote the original draft. RJJ, AD, PR and KT edited the manuscript. KT acquired funding. All authors read and approved the manuscript.
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Ważny, R., Jędrzejczyk, R.J., Rozpądek, P. et al. Biotization of highbush blueberry with ericoid mycorrhizal and endophytic fungi improves plant growth and vitality. Appl Microbiol Biotechnol 106, 4775–4786 (2022). https://doi.org/10.1007/s00253-022-12019-5
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DOI: https://doi.org/10.1007/s00253-022-12019-5