Novel epiphytic root-fungus symbiosis in the Indo-Pacific seagrass Thalassodendron ciliatum from the Red Sea

. 2024 Nov ; 34 (5-6) : 447-461. [epub] 20240729

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39073598
Odkazy

PubMed 39073598
PubMed Central PMC11604718
DOI 10.1007/s00572-024-01161-9
PII: 10.1007/s00572-024-01161-9
Knihovny.cz E-zdroje

Symbioses with fungi are important and ubiquitous on dry land but underexplored in the sea. As yet only one seagrass has been shown to form a specific root-fungus symbiosis that resembles those occurring in terrestrial plants, namely the dominant long-lived Mediterranean species Posidonia oceanica (Alismatales: Posidoniaceae) forming a dark septate (DS) endophytic association with the ascomycete Posidoniomyces atricolor (Pleosporales: Aigialaceae). Using stereomicroscopy, light and scanning electron microscopy, and DNA cloning, here we describe a novel root-fungus symbiosis in the Indo-Pacific seagrass Thalassodendron ciliatum (Alismatales: Cymodoceaceae) from a site in the Gulf of Aqaba in the Red Sea. Similarly to P. oceanica, the mycobiont of T. ciliatum occurs more frequently in thinner roots that engage in nutrient uptake from the seabed and forms extensive hyphal mantles composed of DS hyphae on the root surface. Contrary to P. oceanica, the mycobiont occurs on the roots with root hairs and does not colonize its host intraradically. While the cloning revealed a relatively rich spectrum of fungi, they were mostly parasites or saprobes of uncertain origin and the identity of the mycobiont thus remains unknown. Symbioses of seagrasses with fungi are probably more frequent than previously thought, but their functioning and significance are unknown. Melanin present in DS hyphae slows down their decomposition and so is true for the colonized roots. DS fungi may in this way conserve organic detritus in the seagrasses' rhizosphere, thus contributing to blue carbon sequestration in seagrass meadows.

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Agerer R (1987) Colour atlas of ectomycorrhizae. Einhorn, Schwäbisch Gmünd

Amend A (2014) From dandruff to deep-sea vents: PubMed DOI PMC

Angiosperm Phylogeny Website (2023) http://www.mobot.org/MOBOT/research/APweb/welcome.html, accessed 30/8/2023

Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66. 10.1016/j.fbr.2007.05.003

Badalamenti F, Alagna A, Fici S (2015) Evidences of adaptive traits to rocky substrates undermine paradigm of habitat preference of the Mediterranean seagrass PubMed DOI PMC

Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73:1377–1383. 10.1139/b95-400 DOI

Borovec O, Vohník M (2018) Ontogenetic transition from specialized root hairs to specific root-fungus symbiosis in the dominant Mediterranean seagrass PubMed DOI PMC

Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304. 10.1046/j.1469-8137.2002.00397.x PubMed DOI

Brundrett MC (2017) Global diversity and importance of mycorrhizal and nonmycorrhizal plants, in: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International Publishing. 10.1007/978-3-319-56363-3_21

Cariello L, Zanetti L, De Stefano S (1979) DOI

Domínguez ER (2017)

Ducomet V (1907) Recherches sur le développement de quelques champignons parasites à Thalle subcuticulaire. Thèse Doctorale. Faculté des sciences de Paris, Rennes

Ekanayaka A, Hyde K, Gentekaki E, McKenzie E, Zhao Q et al (2019) Preliminary classification of Leotiomycetes. Mycosphere 10:310–489. 10.5943/mycosphere/10/1/7 DOI

Elliott JK, Simpson H, Teesdale A, Replogle A, Elliott MG et al (2019) A novel phagomyxid parasite produces sporangia in root hair galls of eelgrass ( PubMed

Ettinger CL, Eisen JA (2019) Characterization of the mycobiome of the seagrass, PubMed DOI PMC

Fehrer J, Réblová M, Bambasová V, Vohník M (2019) The root-symbiotic PubMed DOI PMC

Fourqurean JW, Duarte CM, Kennedy H, Marbà N, Holmer M et al (2012) Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5:505–509. 10.1038/ngeo1477 DOI

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. 10.1111/j.1365-294X.1993.tb00005.x PubMed DOI

Green EP, Short FT (2003) World atlas of seagrasses. University of California Press, USA

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

Hawkins H-J, Cargill RIM, van Nuland ME, Hagen SC, Field KJ et al (2023) Mycorrhizal mycelium as a global carbon pool. Curr Biol 33:R560–R573. 10.1016/j.cub.2023.02.027 PubMed DOI

Hongsanan S, Sánchez-Ramírez S, Crous PW, Ariyawansa HA et al (2016) The evolution of fungal epiphytes. Mycosphere 7:1690–1712. 10.5943/mycosphere/7/11/6 DOI

Hyde KD, Jones EBG, Liu J-K, Ariyawansa H, Boehm E et al (2013) Families of Dothideomycetes. Fungal Divers 63:1–313. 10.1007/s13225-013-0263-4 DOI

Jayasiri SC, Hyde KD, Ariyawansa HA, Bhat J, Buyck B et al (2015) The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Divers 74:3–18. 10.1007/s13225-015-0351-8 DOI

Jumpponen A (2001) Dark septate endophytes – are they mycorrhizal? Mycorrhiza 11:207–211. 10.1007/s005720100112 DOI

Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310 PubMed DOI

Kaldorf M, Renker C, Fladung M, Buscot F (2004) Characterization and spatial distribution of ectomycorrhizas colonizing aspen clones released in an experimental field. Mycorrhiza 14:295–306. 10.1007/s00572-003-0266-1 PubMed DOI

Kariman K, Barker SJ, Jost R, Finnegan PM, Tibbett M (2014) A novel plant–fungus symbiosis benefits the host without forming mycorrhizal structures. New Phytol 201:1413–1422. 10.1111/nph.12600 PubMed DOI

Kohout P, Sýkorová Z, Čtvrtlíková M, Rydlová J, Suda J et al (2012) Surprising spectra of root-associated fungi in submerged aquatic plants. FEMS Microbiol Ecol 80:216–235. 10.1111/j.1574-6941.2011.01291.x PubMed DOI

Kolařík M, Vohník M (2018) When the ribosomal DNA does not tell the truth: the case of the taxonomic position of PubMed DOI

Kolátková V, Vohník M (2019) Adaptive traits in the seagrass DOI

Kolátková V, Mooney M, Kelly K, Hineva E, Gawryluk RMR et al. (2023) Eelgrass ( PubMed

Kumar S, Abedin MM, Singh AK, Das S (2020) Role of phenolic compounds in plant-defensive mechanisms. In: Lone R, Shuab R, Kamili A (eds) Plant phenolics in sustainable agriculture. Springer, Singapore. 10.1007/978-981-15-4890-1_22

Langley JA, Chapman SK, Hungate BA (2006) Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecol Lett 9:955–959. 10.1111/j.1461-0248.2006.00948.x PubMed DOI

Larkum AWD, Waycott M, Conran JG (2018) Evolution and biogeography of seagrasses. in: Larkum AWD, Kendrick GA, Ralph PJ (2018) Seagrasses of Australia. Springer, Cham. 10.1007/978-3-319-71354-0_1

Lawrey JD, Diederich P (2018) Lichenicolous fungi: worldwide checklist, including isolated cultures and sequences available. http://www.lichenicolous.net, accessed 1/9/2023

Le Renard L, Stockey RA, Upchurch GR, Berbee ML (2021) Extending the fossil record for foliicolous Dothideomycetes: PubMed DOI

Lefebvre L, Compère P, Gobert S (2023) The formation of aegagropiles from the Mediterranean seagrass DOI

Lipkin Y (1979) Quantitative aspects of seagrass communities, particularly of those dominated by DOI

Lukešová T, Kohout P, Větrovský T, Vohník M (2015) The potential of dark septate endophytes to form root symbioses with ectomycorrhizal and ericoid mycorrhizal middle European forest plants. PLoS ONE 10:e0124752. 10.1371/journal.pone.0124752 PubMed DOI PMC

Mata JL, Cebrián J (2013) Fungal endophytes of the seagrasses DOI

Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23:119–128. 10.1007/s00572-012-0456-9 PubMed DOI

McMillan C (1984) The condensed tannins (proanthocyanidins) in seagrasses. Aquat Bot 20:351–357. 10.1016/0304-3770(84)90099-8 DOI

Naranjo-Ortiz MA, Gabaldón T (2019) Fungal evolution: major ecological adaptations and evolutionary transitions. Biol Rev 94:1443–1476. 10.1111/brv.12510 PubMed DOI PMC

Newsham KK (1999) PubMed DOI

Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793. 10.1111/j.1469-8137.2010.03611.x PubMed DOI

Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. 10.1016/j.funeco.2015.06.006 DOI

Nilsson RH, Larsson K-H, Taylor AFS, Bengtsson-Palme J, Jeppesen TS et al (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264. 10.1093/nar/gky1022 PubMed DOI PMC

Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974. 10.1007/s11284-007-0390-z DOI

Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. 10.1038/nrmicro1987 PubMed DOI

Piñeiro-Juncal N, Leiva-Dueñas C, Serrano O, Mateo MÁ, Martínez-Cortízas A (2020) Pedogenic processes in a DOI

Podgórska-Kryszczuk I, Solarska E, Kordowska-Wiater M (2022) Biological control of PubMed DOI PMC

Poli A, Prigione V, Bovio E, Perugini I, Varese GC (2021) Insights on Lulworthiales inhabiting the Mediterranean Sea and description of three novel species of the genus PubMed DOI PMC

Powley HR, Cappellen PV, Krom MD (2017) Nutrient cycling in the Mediterranean Sea: The key to understanding how the unique marine ecosystem functions and responds to anthropogenic pressures. in: Mediterranean Identities - Environment, Society, Culture. InTech. 10.5772/intechopen.70878

Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263. 10.1139/B04-123 DOI

Reininger V, Sieber TN Mycorrhiza reduces adverse effects of dark septate endophytes (DSE) on growth of conifers. PLoS ONE 7:e0042865. 10.1371/journal.pone.0042865 PubMed PMC

Rice AV, Currah RS (2006)

Saadatzadeh MR, Ashbee HR, Holland KT, Ingham E (2001) Production of the mycelial phase of PubMed DOI

Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343. 10.1146/annurev.ecolsys.29.1.319 DOI

Sakayaroj J, Preedanon S, Supaphon Jones EBG, Phongpaichit S (2010) Phylogenetic diversity of endophyte assemblages associated with the tropical seagrass DOI

Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD, Karsch-Mizrachi I (2019) GenBank. Nucleic Acids Res 47:D94–D99. 10.1093/nar/gky989 PubMed DOI PMC

Selosse M-A, Le Tacon F (1998) The land flora: a phototroph–fungus partnership? Trends Ecol Evol 13:15–20. 10.1016/S0169-5347(97)01230-5 PubMed DOI

Selosse M, Vohník M, Chauvet E (2008) Out of the rivers: are some aquatic hyphomycetes plant endophytes? New Phytol 178:3–7. 10.1111/j.1469-8137.2008.02390.x PubMed DOI

Serrano O, Mateo MA, Renom P, Julià R (2012) Characterization of soils beneath a DOI

Short FT, McRoy CP (1984) Nitrogen uptake by leaves and roots of the seagrass DOI

Shrestha P, Szaro TM, Bruns TD, Taylor JW (2011) Systematic search for cultivatable fungi that best deconstruct cell walls of PubMed DOI PMC

Singh SM, Tsuji M, Gawas-Sakhalker P, Loonen MJJE, Hoshino T (2016) Bird feather fungi from Svalbard Arctic. Polar Biol 39:523–532. 10.1007/s00300-015-1804-y DOI

Solomon PS, Lowe RGT, Tan K-C, Waters ODC, Oliver RP (2006) PubMed DOI

Špetík M, Berraf-Tebbal A, Pokluda R, Eichmeier A (2021) DOI

Stenglein SA (2009) DOI

Suetrong S, Schoch CL, Spatafora JW, Kohlmeyer J, Volkmann-Kohlmeyer B et al (2009) Molecular systematics of the marine Dothideomycetes. Stud Mycol 64:155–173. 10.3114/sim.2009.64.09 PubMed DOI PMC

Terrados J, Williams SL (1997) Leaf versus root nitrogen uptake by the surfgrass DOI

Torta L, Burruano S, Giambra S, Conigliaro G, Piazza G et al. (2022) Cultivable fungal endophytes in roots, rhizomes and leaves of PubMed DOI PMC

Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, PubMed DOI

van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. 10.1111/nph.13288 PubMed DOI

Vohník M (2020) Ericoid mycorrhizal symbiosis: theoretical background and methods for its comprehensive investigation. Mycorrhiza 30:671–695. 10.1007/s00572-020-00989-1 PubMed DOI PMC

Vohník M (2021) Bioerosion and fungal colonization of the invasive foraminiferan DOI

Vohník M (2022) Are lulworthioid fungi dark septate endophytes of the dominant Mediterranean seagrass PubMed DOI

Vohník M, Réblová M (2023) Fungi in hair roots of PubMed DOI PMC

Vohník M, Lukančič S, Bahor E, Regvar M, Vosátka M et al (2003) Inoculation of DOI

Vohník M, Sadowsky JJ, Kohout P, Lhotáková Z, Nestby R, Kolařík M (2012) Novel root-fungus symbiosis in Ericaceae: sheathed ericoid mycorrhiza formed by a hitherto undescribed basidiomycete with affinities to Trechisporales. PLoS ONE 7:e39524. 10.1371/journal.pone.0039524 PubMed DOI PMC

Vohník M, Borovec O, Župan I, Vondrášek D, Petrtýl M et al (2015) Anatomically and morphologically unique dark septate endophytic association in the roots of the Mediterranean endemic seagrass PubMed

Vohník M, Borovec O, Kolařík M (2016) Communities of cultivable root mycobionts of the seagrass PubMed DOI

Vohník M, Borovec O, Župan I, Kolařík M, Sudová R (2017) Fungal root symbionts of the seagrass DOI

Vohník M, Borovec O, Kolaříková Z, Sudová R, Réblová M (2019) Extensive sampling and high-throughput sequencing reveal PubMed DOI PMC

Wang G, Cao X, Ma X, Guo M, Liu C et al (2016) Diversity and effect of PubMed PMC

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. Elsevier. 10.1016/B978-0-12-372180-8.50042-1

Williams J, Clarkson JM, Mills PR, Cooper RM (2003) Saprotrophic and mycoparasitic components of aggressiveness of PubMed PMC

Yu T, Nassuth A, Peterson RL (2001) Characterization of the interaction between the dark septate fungus PubMed

Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214. 10.1089/10665270050081478 PubMed DOI

Zijlstra JD, Van’t Hof P, Baar J, Verkley GJM, Summerbell RC et al (2005) Diversity of symbiotic root endophytes of the Helotiales in ericaceous plants and the grass,

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