Guapirioid ectomycorrhiza: a novel fungus-plant subtype is described associated to Guapira opposita (Nyctaginaceae) in the Brazilian restinga
Abstract
Aim of study: Despite its recognized ecosystemic importance, knowledge about mycorrhizal associations in Brazil is still dearth, and the diversity of the native mycorrhizal fungi remains unknown. In this study, we characterized morpho-anatomically and molecularly the ectomycorrhizae found associated with Guapira opposita in the restinga, vegetation established on sandy soil.
Area of study: Coastal of the Atlantic Forest of southern Brazil, Florianópolis: Parque Natural Municipal das Dunas da Lagoa da Conceição, Monumento Natural Municipal da Lagoa do Peri and Parque Natural Municipal da Lagoa do Jacaré das Dunas do Santinho.
Material and methods: The ectomycorrhizae found were morphotyped and described according to standard criteria. Plant and fungi were molecularly identified using sequences of the ITS region of rDNA.
Main results: Ten morphotypes were identified associated with G. opposita, including the native threatened species Austroboletus festivus. Members of the clade /tomentella-thelephora were the most representative in our study, with six taxa. Based on particular characteristics, such as short, and simple or long and thin branched ectomycorrhizal systems, close connections between the layered ectomycorrhizal mantle and the cortical root cells, absence of a Hartig net and other fungal elements in the cortex, we propose the name ‘Guapirioid ectomycorrhiza’ for this new morphology.
Research highlights: The results presented in this work confirm the presence of ectomycorrhizae in the restinga and suggest the existence of a diversity, above and below-ground, much greater than previously known. Furthermore, our data confirm the morphological and possibly ecological differences of tropical ectomycorrhizae from those known from temperate forests.
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References
Agerer R, 1991. Characterization of ectomycorrhiza. In: Methods in Microbiology, Vol. 23: Techniques for the study of mycorrhiza; Norris JR, Read DJ, Varma AK (eds). pp: 25-73. Academic Press, San Diego. https://doi.org/10.1016/S0580-9517(08)70172-7
Agerer R, 1995. Anatomical characteristics of identified ectomycorrhizae: an attempt towards a natural classification. In: Mycorrhiza: structure, function, molecular biology and biotechnology; Varma A, Hock B (eds). pp: 685-734. Springer-Verlag, Berlin. https://doi.org/10.1007/978-3-662-08897-5_29
Altschul SF, Gish W, Miller W, Myer EW, Lipman DJ, 1990. Basic local alignment search tool. J Mol Biol 215: 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
Alvarez-Majarrez J, Garibay-Orijel R, Smith ME, 2017. Caryophyllales are the main hosts of a unique set of ectomycorrhizal fungi in a Neotropical dry forest. Mycorrhiza 28: 103-115. https://doi.org/10.1007/s00572-017-0807-7
Asmelash F, Bekele T, Birhane E, 2016. The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol 7: 1095. https://doi.org/10.3389/fmicb.2016.01095
Bidartondo MI, Read D, 2008. Fungal specificity bottlenecks during orchid germination and development. Mol Ecol 17: 3707-3716. https://doi.org/10.1111/j.1365-294X.2008.03848.x
Binfaré RW, Falkenberg DB, 2017. Guia ilustrado da Flora da restinga da Santa Catarina. Thesis dissertation, Universidade Federal de Santa Catarina, Brazil.
Brundrett MC, Tedersoo L, 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220: 1108-1115. https://doi.org/10.1111/nph.14976
Castanho CT, Oliveira AA, Prado PI, 2012. The importance of plant life form on spatial associations along a subtropical coastal dune gradient. J Veg Sci 23: 952-961. https://doi.org/10.1111/j.1654-1103.2012.01414.x
Cheng T, Xu C, Lei L, Li C, Zhang L, Zhou S, 2015. Barcoding the kingdom Plantae: new PCR primers for ITS regions of plants with improved universality and specificity. Mol Ecol Resour 16: 138-149. https://doi.org/10.1111/1755-0998.12438
Corrales A, Henkel TW, Smith ME, 2018. Ectomycorrhizal associations in the tropics-biogeography, diversity patterns and ecosystem roles. New Phytol 220: 1076-1091. https://doi.org/10.1111/nph.15151
Dalotto CES, Sühs RB, Dechoum MS, Pugnaire FI, Peroni N, Castellani TT, 2018. Facilitation influences patterns of perennial species abundance and richness in a subtropical dune system. AoB PLANTS 10: ply017. https://doi.org/10.1093/aobpla/ply017
Dighton J, 2016. Fungi in ecosystem processes. CRC Press, New York. 434 pp. https://doi.org/10.1201/b19652
Furtado ANM, Comandini O, Leonardi M, Rinaldi AC, Neves MA, 2022. Facing the Brazilian restinga diversity: Amanita viscidolutea ectomycorrhiza on Guapira opposita. Mycoscience 63: 73-78. https://doi.org/10.47371/mycosci.2022.02.001
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. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Haug I, Weiss M, Homeier J, Oberwinkler F, Kottke I, 2005. Russulaceae and Thelephoraceae form ectomycorrhizas with members of the Nyctaginaceae (Caryophyllales) in the tropical mountain rain forest of southern Ecuador. New Phytol 165: 923-936. https://doi.org/10.1111/j.1469-8137.2004.01284.x
Hayward J, Horton T, 2014. Phylogenetic trait conservation in the partner choice of a group of ectomycorrhizal trees. Mol Ecol 23: 4886-4898. https://doi.org/10.1111/mec.12903
Huang AC, Jiang T, Liu YX, Bai YC, Reed J, Qu B, et al., 2019. A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364, eaau6389. https://doi.org/10.1126/science.aau6389
Iotti M, Zambonelli A, 2006. A quick and precise technique for identifying ectomycorrhizae by PCR. Mycol Res 110: 60-65. https://doi.org/10.1016/j.mycres.2005.09.010
Jakucs E, Kovács GM, Agerer R, Romsics C, Erös-Honti Z, 2005. Morphological-anatomical characterization and molecular identification of Tomentella stuposa ectomycorrhizae and related anatomotypes. Mycorrhiza 15: 247-258. https://doi.org/10.1007/s00572-004-0326-1
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al., 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649. https://doi.org/10.1093/bioinformatics/bts199
Leonardi M, Iotti M, Oddis M, Lalli G, Pacioni G, Leonardi P, et al., 2013. Assessment of ectomycorrhizal fungal communities in the natural habitats of Tuber magnatum (Ascomycota, Pezizales). Mycorrhiza 23: 349-358. https://doi.org/10.1007/s00572-012-0474-7
Lessa GC, Angulo RJ, Giannini PC, Araújo AD, 2000. Stratigraphy and Holocene evolution of a regressive barrier in south Brazil. Mar Geol 165: 87-108. https://doi.org/10.1016/S0025-3227(99)00130-9
Lu X, Yuan HS, 2021. New species of Tomentella (Thelephorales, Basidiomycota) from temperate continental mountain climate of China (Xinjiang Region). Forests 12: 1531. https://doi.org/10.3390/f12111531
Lu X, Steffen K, Yuan HS, 2018. Morphological and molecular identification of three new species of Tomentella from Finland. Mycologia 4: 677-691. https://doi.org/10.1080/00275514.2018.1474683
Magnago AC, Neves MA, 2014. New record of Austroboletus festivus (Boletaceae) from Santa Catarina, Brazil. Braz J Bot 36(4): 1-4.
Magnago LFS, Martins SV, Schaefer CEGR, Neri AV, 2012. Restinga forests of the Brazilian coast: richness and abundance of tree species on different soils. Ann BAS 84: 807-822. https://doi.org/10.1590/S0001-37652012000300023
Martin F, Kohler A, Murat C, Veneault-Fourrey C, Hibbett D, 2016. Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol 14: 760-773. https://doi.org/10.1038/nrmicro.2016.149
Matheny PB, Hobbs AM, Esteve-Raventós F, 2020. Genera of Inocybaceae: new skin for the old ceremony. Mycologia 112: 83-120. https://doi.org/10.1080/00275514.2019.1668906
McCormick MK, Whigham DF, O'Nell JP, Becker JJ, Werner S, Rasmussen HN, et al., 2009. Abundance and distribution of Corallorhiza odontorhiza reflect variations in climate and ectomycorrhizae. Ecol Monogr 79: 619-635. https://doi.org/10.1890/08-0729.1
Menolli Jr. N, Capelari M, Baseia IG, 2009. Amanita viscidolutea, a new species from Brazil with a key to Central and South American species of Amanita section Amanita. Mycologia 101: 395-400. https://doi.org/10.3852/07-079
Moyersoen B, 1993. Ectomicorrizas y micorrizas vesículo-arbusculares en Caatinga Amazónica del Sur de Venezuela. Scientia Guaianae, 3.
Mrak T, Šibanc N, Brailey-Jones P, Štraus I, Gricar J, Kraigher H, 2021. Extramatricial mycelium and ectomycorrhizal community composition of Quercus pubescens in a sub-Mediterranean stress-pone environment. Front For Glob Changes 4: 599946. https://doi.org/10.3389/ffgc.2021.599946
Neves MA, Furtado ANM, 2020 Amanita viscidolutea. The IUCN Red List of Threatened Species 2020.
Neves MA, Furtado ANM, Cardoso JS, 2020. Austroboletus festivus. The IUCN Red List of Threatened Species 2020.
Reitz R, 1970. Nyctaginaceae. Flora Ilustrada Catarinense. Herbário Barbosa Rodrigues, Itajaí, Brazil.
Roy M, Gonneau C, Rocheteau A, Berveiller D, Thomas JC, Damesin C, Selosse MA, 2013. Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ. Ecol Monogr 83: 95-117. https://doi.org/10.1890/11-2120.1
Roy M, Schimann H, Braga-Neto R, da Silva RAE, Duque J, Frame D, et al., 2016. Diversity and distribution of ectomycorrhizal fungi from Amazonian lowland white-sand forests in brazil and French Guiana. Biotropica 48: 90-100. https://doi.org/10.1111/btp.12297
Sambrook J, Fritsch EF, Maniatis T, 1989. Molecular cloning - Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, New York.
Sayers EW, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, et al., 2009. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 37: D5-D15. https://doi.org/10.1093/nar/gkn741
Schüßler A, Schwarzott D, Walker C, 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105: 1413-1421. https://doi.org/10.1017/S0953756201005196
Seress D, Dima B, Kovács GM, 2015. Characterization of seven Inocybe ectomycorrhizal morphotypes from a semiarid woody steppe. Mycorrhiza 26: 215-225. https://doi.org/10.1007/s00572-015-0662-3
Singer R, 1970. Strobilomycetaceae (Basidiomycetes). In: Flora Neotropica, Monograph 5.
Singer R, Morello JH, 1960. Ectotrophic forest tree mycorrhizae and forest communities. Ecology 41: 549-551. https://doi.org/10.2307/1933331
Singer R, Araujo I, Ivory MH, 1983. The ectotrophically mycorrhizal fungi of the neotropical lowlands, especially Central Amazonia. Beih Nova Hedwigia 77: 1-352.
Smith SE, Read DJ, 2008. Mycorrhizal symbiosis, 3rd ed. Academic Press, New York. 815 pp.
SOS Mata Atlântica, 2021. Mata Atlântica. https://www.sosma.org.br/causas/mata-atlantica/ [20 July 2021].
Steiner AQ, Amaral FMD, do Amaral JRDBC, Sassi R, Barradas JI, 2015. Zonação de recifes emersos da Área de Proteção Ambiental Costa dos Corais, Nordeste do Brasil. Iheringia Ser Zool 105: 184-192. https://doi.org/10.1590/1678-476620151052184192
Sulzbacher MA, Orihara T, Grebenc T, Wartchow F, Smith ME, Martín MP, et al., 2020. Longistriata flava (Boletaceae, Basidiomycota) - A new monotypic sequestrate genus and species from Brazilian Atlantic Forest. MycoKeys 62: 53-73. https://doi.org/10.3897/mycokeys.62.39699
Tedersoo L, Sadam A, Zambrano M, Valencia R, Bahram M, 2010. Low diversity and high host preference of ectomycorrhizal fungi in Western Amazonia, a neotropical biodiversity hotspot. ISME J 4: 1-465. https://doi.org/10.1038/ismej.2009.131
Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yourou N, Wijesundera R, et al., 2014. Global diversity and geography of soil fungi. Science 346: 6213.
Wartchow F, 2018. Inocybe lepidosparta (Agaricales: Basidiomycota): a new species from Pernambuco, Brazil. New Zeal J Bot 56: 438-443. https://doi.org/10.1080/0028825X.2018.1499535
Wartchow F, Maia LC, Cavalcanti MAQ, 2012. Studies on Amanita (Agaricomycetidae, Amanitaceae) in Brazil: two yellow gemmatoid taxa. Beih Nova Hedwigia 96: 61-71. https://doi.org/10.1127/0029-5035/2012/0053
Weidlich EWA, Mioto PT, Furtado ANM, Ferst LM, Ernzen JP, Neves MA, 2020. Using ectomycorrhizae to improve the restoration of neotropical coastal zones. Restor Ecol 28: 1324-1326. https://doi.org/10.1111/rec.13284
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