Abstract
Although the lifestyle of Geoglossales remains largely unknown, recent advancements have established a hypothesis regarding the ericoid mycorrhizal lifestyle of geoglossoid fungi. In this study, we focused on one isolate of Geoglossales sp. obtained from surface-sterilized roots of potted Rhododendron transiens. We aimed to reveal the phylogenetic position and in vitro colonizing ability of this species in the hair roots of ericoid mycorrhizal plants. Based on our multigene phylogenetic tree, this species is a sister of the genus Sarcoleotia which has not been reported from either other studies or field environment. Its ascocarps could not be obtained, and conspecific sequences were not found in the databases and repositories examined. The Geoglossales sp. colonized the vital rhizodermal cells of blueberries in vitro with hyphal coils. There were relatively large morphological variations of coils consistent with extraradical hyphae; however, overall, the colonization morphologically resembled those by Sarcoleotia globosa and representative ericoid mycorrhizal fungi. The taxonomy and ecological significance of the species remain to be resolved; nevertheless, our results suggest that the ericoid mycorrhizal lifestyle may be widespread within Geoglossales.
Similar content being viewed by others
Data availability
The cultured isolates were deposited in the School of Pharmacy, Nihon University. Newly obtained sequences were deposited in DDBJ. The isolates and data are available from the corresponding author upon reasonable request.
References
Arauzo S, Iglesias P (2014) La familia Geoglossaceae ss. str. en la península Ibérica la Macaronesia. Errotari 11:166–259
Baba T, Hirose D (2021) Slow-growing fungi belonging to the unnamed lineage in Chaetothyriomycetidae form hyphal coils in vital ericaceous rhizodermal cells in vitro. Fungal Biol 125:1026–1035. https://doi.org/10.1016/j.funbio.2021.07.003
Baba T, Janošík L, Koukol O, Hirose D (2021) Genetic variations and in vitro root-colonizing ability for an ericaceous host in Sarcoleotia globosa (Geoglossomycetes). Fungal Biol 125:971–979. https://doi.org/10.1016/j.funbio.2021.08.005
Boeraeve M, Kohout P, Ceulemans T et al (2022) Changes in the root microbiome of four plant species with different mycorrhizal types across a nitrogen deposition gradient in ombrotrophic bogs. Soil Biol Biochem 169:108673. https://doi.org/10.1016/j.soilbio.2022.108673
Daghino S, Martino E, Voyron S, Perotto S (2022) Metabarcoding of fungal assemblages in Vaccinium myrtillus endosphere suggests colonization of above-ground organs by some ericoid mycorrhizal and DSE fungi. Sci Rep 12:11013. https://doi.org/10.1038/s41598-022-15154-1
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291–294. https://doi.org/10.1093/molbev/msz189
Díaz-Escandón D, Tagirdzhanova G, Vanderpool D et al (2022) Genome-level analyses resolve an ancient lineage of symbiotic ascomycetes. Curr Biol 32:5209–5218. https://doi.org/10.1016/j.cub.2022.11.014
Edler D, Klein J, Antonelli A, Silvestro D (2021) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol Evol 12:373–377. https://doi.org/10.1111/2041-210X.13512
Fedosova AG, Popov ES, Lizoň P, Kučera V (2018) Towards an understanding of the genus Glutinoglossum with emphasis on the Glutinoglossum glutinosum species complex (Geoglossaceae, Ascomycota). Persoonia Mol Phylogeny Evol Fungi 41:18–38. https://doi.org/10.3767/persoonia.2018.41.02
Grunewaldt-Stöcker G, von Alten H (2016) Is the root-colonizing endophyte Acremonium strictum an ericoid mycorrhizal fungus? Mycorrhiza 26:429–440. https://doi.org/10.1007/s00572-016-0682-7
Hustad VP, Miller AN, Moingeon JM, Priou JP (2011) Inclusion of Nothomitra in Geoglossomycetes. Mycosphere 2:646–654. https://doi.org/10.5943/mycosphere/2/6/5
Hustad VP, Miller AN, Dentinger BTM, Cannon PF (2013) Generic circumscriptions in Geoglossomycetes. Persoonia Mol Phylogeny Evol Fungi 31:101–111. https://doi.org/10.3767/003158513X671235
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
Kers LE, Carlsson R (1996) Jordtungan Geoglossum littorale återfunnen - i Sverige. Sven Bot Tidskr 90:65–81
Kobae Y, Ohtomo R (2016) An improved method for bright-field imaging of arbuscular mycorrhizal fungi in plant roots. Soil Sci Plant Nutr 62:27–30. https://doi.org/10.1080/00380768.2015.1106923
Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Lemoine F, Entfellner JBD, Wilkinson E et al (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556:452–456. https://doi.org/10.1038/s41586-018-0043-0
Leopold DR, Peay KG, Vitousek PM, Fukami T (2021) Diversity of putative ericoid mycorrhizal fungi increases with soil age and progressive phosphorus limitation across a 4.1-million-year chronosequence. FEMS Microbiol Ecol 97:fiab016. https://doi.org/10.1093/femsec/fiab016
Lorberau KE, Botnen SS, Mundra S et al (2017) Does warming by open-top chambers induce change in the root-associated fungal community of the arctic dwarf shrub Cassiope tetragona (Ericaceae)? Mycorrhiza 27:513–524. https://doi.org/10.1007/s00572-017-0767-y
Martino E, Morin E, Grelet G et al (2018) Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytol 217:1213–1229. https://doi.org/10.1111/nph.14974
Matheny BP, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Amer J Bot 89:688–698. https://doi.org/10.3732/ajb.89.4.688
Melie T, Pirro S, Miller AN et al (2023) Comparative genomics and phylogenomic investigation of the class Geoglossomycetes provide insights into ecological specialization and the systematics of Pezizomycotina. Mycologia 115:499–512. https://doi.org/10.1080/00275514.2023.2186743
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325. https://doi.org/10.1093/nar/8.19.4321
Nitare J (1982) Geoglossum arenarium, sandjordtunga - ekologi och utbredning i Sverige. Sven Bot Tidskr 76:349–357
Perez-Lamarque B, Petrolli R, Strullu-Derrien C et al (2022) Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities. Environ Microbiome 17:38. https://doi.org/10.1186/s40793-022-00434-0
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Pierret A, Gonkhamdee S, Jourdan C, Maeght JL (2013) IJ_Rhizo: an open-source software to measure scanned images of root samples. Plant Soil 373:531–539. https://doi.org/10.1007/s11104-013-1795-9
Thoen E, Aas AB, Vik U et al (2019) A single ectomycorrhizal plant root system includes a diverse and spatially structured fungal community. Mycorrhiza 29:167–180. https://doi.org/10.1007/s00572-019-00889-z
Toju H, Tanabe AS, Ishii HS (2016) Ericaceous plant-fungus network in a harsh alpine-subalpine environment. Mol Ecol 13:3242-3257. https://doi.org/10.1111/mec.13680
Van Geel M, Jacquemyn H, Peeters G et al (2020) Diversity and community structure of ericoid mycorrhizal fungi in European bogs and heathlands across a gradient of nitrogen deposition. New Phytol 228:1640–1651. https://doi.org/10.1111/nph.16789
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Vohník M (2020) Ericoid mycorrhizal symbiosis: theoretical background and methods for its comprehensive investigation. Mycorrhiza 30:671–695. https://doi.org/10.1007/s00572-020-00989-1
Vohník M, Bruzone MC, Knoblochová T et al (2023) Exploring structural and molecular diversity of Ericaceae hair root mycobionts: a comparison between Northern Bohemia and Patagonia. Mycorrhiza 32:105–122. https://doi.org/10.1007/s00572-023-01125-5
Wang Z, Nilsson RH, Lopez-Giraldez F et al (2011) Tasting soil fungal diversity with earth tongues: phylogenetic test of SATé alignments for environmental ITS data. PLoS One 6:e19039. https://doi.org/10.1371/journal.pone.0019039
Weiß M, Waller F, Zuccaro A, Selosse MA (2016) Sebacinales - one thousand and one interactions with land plants. New Phytol 211:20–40. https://doi.org/10.1111/nph.13977
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 Press, San Diego 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1
Yang H, Zhao X, Liu C et al (2018) Diversity and characteristics of colonization of root-associated fungi of Vaccinium uliginosum. Sci Rep 8:15283. https://doi.org/10.1038/s41598-018-33634-1
Acknowledgements
The authors thank Prof. Nobuo Kobayashi, Masayuki Kurihara, Shinji Miyazaki, and Yasuo Kimura for their helps of sampling of roots and exploration of ascocarps in the Tutsujigaoka park.
Funding
This study was partially supported by the Nihon University Research Grant for (2022).
Author information
Authors and Affiliations
Contributions
TB: design of study, collection of material and data (resynthesis experiment), statistical analysis, writing and revising of the manuscript. DH: design of study, collection of material and data (fungal isolation and molecular data), phylogenetic analysis, writing and revising of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Baba, T., Hirose, D. A cryptic root isolate belonging to Geoglossales from potted Rhododendron: its molecular phylogeny and ability to colonize an ericoid mycorrhizal host in vitro. Mycorrhiza 33, 449–456 (2023). https://doi.org/10.1007/s00572-023-01130-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-023-01130-8