Ontogenetic transition from specialized root hairs to specific root-fungus symbiosis in the dominant Mediterranean seagrass Posidonia oceanica
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30018360
PubMed Central
PMC6050321
DOI
10.1038/s41598-018-28989-4
PII: 10.1038/s41598-018-28989-4
Knihovny.cz E-zdroje
- MeSH
- Alismatales anatomie a histologie růst a vývoj mikrobiologie MeSH
- Ascomycota fyziologie MeSH
- fyziologická adaptace * MeSH
- kořeny rostlin mikrobiologie MeSH
- listy rostlin MeSH
- mycelium fyziologie MeSH
- mykorhiza MeSH
- symbióza * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Středozemní moře MeSH
Terrestrial plants typically take up nutrients through roots or mycorrhizae while freshwater plants additionally utilize leaves. Their nutrient uptake may be enhanced by root hairs whose occurrence is often negatively correlated with mycorrhizal colonization. Seagrasses utilize both leaves and roots and often form root hairs, but seem to be devoid of mycorrhizae. The Mediterranean seagrass Posidonia oceanica is an exception: its adults commonly lack root hairs and regularly form a specific association with a single pleosporalean fungus. Here we show that at two sites in the southern Adriatic, all its seedlings possessed abundant root hairs with peculiar morphology (swollen terminal parts) and anatomy (spirally formed cell walls) as apparent adaptations for better attachment to the substrate and increase of breaking strain. Later on, their roots became colonized by dark septate mycelium while root hairs were reduced. In adults, most of terminal fine roots possessed the specific fungal association while root hairs were absent. These observations indicate for the first time that processes regulating transition from root hairs to root fungal colonization exist also in some seagrasses. This ontogenetic shift in root traits may suggests an involvement of the specific root symbiosis in the nutrient uptake by the dominant Mediterranean seagrass.
Zobrazit více v PubMed
Dumortier, M. Below-ground dynamics in a wet grassland ecosystem in Plant root growth – an ecological perspective (Blackwell, 1991).
Gilroy S, Jones DL. Through form to function: root hair development and nutrient uptake. Trends Plant. Sci. 2000;5:56–60. doi: 10.1016/S1360-1385(99)01551-4. PubMed DOI
Inderjit & Weston, L. A. Root exudates: an overview in Root ecology (Springer, 2003).
van Loon, L. C. & Bakker, P. A. H. M. Signaling in rhizobacteria–plant interactions in Root ecology (Springer, 2003).
Waisel, Y., Eshel, A. & Kafkafi, U. Plant roots: the hidden half (Marcel Dekker, 2002).
Smith, S. E. & Read, D. J. Mycorrhizal symbiosis (Academic Press, 2008).
Linderman RG. Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology. 1988;78:366–371.
Brundrett M. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil. 2009;320:37–77. doi: 10.1007/s11104-008-9877-9. DOI
Raven JA. Nutritional strategies of submerged benthic plants: the acquisition of C, N and P by rhizophytes and haptophytes. New Phytol. 1981;88:1–30. doi: 10.1111/j.1469-8137.1981.tb04564.x. DOI
Madsen TV, Cedergreen N. Sources of nutrients to rooted submerged macrophytes growing in a nutrientrich stream. Freshwater Biol. 2002;47:283–291. doi: 10.1046/j.1365-2427.2002.00802.x. DOI
Shannon EL. The production of root hairs by aquatic plants. Am. Midl. Nat. 1953;50:474–479. doi: 10.2307/2422106. DOI
Wilson J, Bennett I. Nutrient requirements of in vitro cultured Halophila ovalis and Posidonia coriacea: nitrogen source. Plant Cell Tiss. Organ Cult. 2007;92:155–163. doi: 10.1007/s11240-007-9318-0. DOI
Šraj-Kržič N, et al. Mycorrhizal colonization in plants from intermittent aquatic habitats. Aquat. Bot. 2006;85:331–336. doi: 10.1016/j.aquabot.2006.07.001. DOI
Sudová R, Rydlová J, Čtvrtlíková M, Havránek P, Adamec L. The incidence of arbuscular mycorrhiza in two submerged Isoëtes species. Aquat. Bot. 2011;94:183–187. doi: 10.1016/j.aquabot.2011.02.003. DOI
Sondergaard M, Laegaard S. Vesicular-arbuscular mycorrhiza in some aquatic plants. Nature. 1977;268:232–233. doi: 10.1038/268232a0. DOI
Farmer AM. The occurrence of vesicular-arbuscular mycorrhiza in isoetid-type submerged aquatic macrophytes under naturally varying conditions. Aquat. Bot. 1985;21:245–249. doi: 10.1016/0304-3770(85)90052-X. DOI
Pedersen MF, Borum J. Nitrogen dynamics of eelgrass Zostera marina during low nutrient availability. Mar. Ecol. Progr. Ser. 1992;80:65–73. doi: 10.3354/meps080065. DOI
Terrados J, Williams SL. Leaf versus root nitrogen uptake by the surfgrass Phyllospadix torreyi. Mar. Ecol. Progr. Ser. 1997;149:267–277. doi: 10.3354/meps149267. DOI
Stapel J, et al. Nutrient uptake by leaves and roots of the seagrass Thalassia hemprichii in the Spermonde Archipelago, Indonesia. Mar. Ecol. Progr. Ser. 1996;134:195–206. doi: 10.3354/meps134195. DOI
Lepoint G, Millet S, Dauby P, Gobert S, Bouquegneau JM. Annual nitrogen budget of the seagrass Posidonia oceanica as determined by in situ uptake experiments. Mar. Ecol. Progr. Ser. 2002;237:87–96. doi: 10.3354/meps237087. DOI
Kiswara W, et al. Root architecture of six tropical seagrass species, growing in three contrasting habitats in Indonesian waters. Aquat. Bot. 2009;90:235–245. doi: 10.1016/j.aquabot.2008.10.005. DOI
Soong K, Chiu ST, Chen CNN. Novel seed adaptations of a monocotyledon seagrass in the wavy sea. Plos One. 2013;8:e74143. doi: 10.1371/journal.pone.0074143. PubMed DOI PMC
Badalamenti F, Alagna A, Fici S. Evidences of adaptive traits to rocky substrates undermine paradigm of habitat preference of the Mediterranean seagrass Posidonia oceanica. Sci. Rep. 2015;5:8804. doi: 10.1038/srep08804. PubMed DOI PMC
Nielsen SL, Thingstrup I, Wigand C. Apparent lack of vesicular–arbuscular mycorrhiza (VAM) in the seagrasses Zostera marina L. and Thalassia testudinum Banks ex König. Aquat. Bot. 1999;63:261–266. doi: 10.1016/S0304-3770(98)00123-5. DOI
Lukešová T, Kohout P, Větrovský T, Vohník M. The potential of Dark Septate Endophytes to form root symbioses with ectomycorrhizal and ericoid mycorrhizal middle European forest plants. Plos One. 2015;10:e0124752. doi: 10.1371/journal.pone.0124752. PubMed DOI PMC
Wilson D. Endophyte: The evolution of a term, and clarification of its use and definition. Oikos. 1995;73:274–276. doi: 10.2307/3545919. DOI
Cuomo V, Vanzanella F, Fresi E, Cinelli F, Mazzella L. Fungal flora of Posidonia oceanica and its ecological significance. Trans. Br. Mycol. Soc. 1985;84:35–40. doi: 10.1016/S0007-1536(85)80217-5. DOI
Vohník M, et al. Anatomically and morphologically unique dark septate endophytic association in the roots of the Mediterranean endemic seagrass Posidonia oceanica. Mycorrhiza. 2015;25:663–672. doi: 10.1007/s00572-015-0642-7. PubMed DOI
Vohník M, Borovec O, Kolařík M. Communities of cultivable root mycobionts of the seagrass Posidonia oceanica in the northwest Mediterranean Sea are dominated by a hitherto undescribed pleosporalean Dark Septate Endophyte. Microb. Ecol. 2016;71:442–445. doi: 10.1007/s00248-015-0640-5. PubMed DOI
Vohník M, Borovec O, Župan I, Kolařík M, Sudová R. Fungal root symbionts of the seagrass Posidonia oceanica in the central Adriatic Sea revealed by microscopy, culturing and 454-pyrosequencing. Mar. Ecol. Progr. Ser. 2017;583:107–120. doi: 10.3354/meps12337. DOI
Grünig CR, Queloz V, Sieber TN, Holdenrieder O. Dark septate endophytes (DSE) of the Phialocephala fortinii s. l. – Acephala applanata species complex in tree roots: classification, population biology, and ecology. Botany. 2008;86:1355–1369. doi: 10.1139/B08-108. DOI
Knapp DG, Pintye A, Kovács GM. The dark side is not fastidious – Dark Septate Endophytic fungi of native and invasive plants of semiarid sandy areas. Plos One. 2012;7:e32570. doi: 10.1371/journal.pone.0032570. PubMed DOI PMC
Vohník M, Albrechtová J. The co-occurrence and morphological continuum between ericoid mycorrhiza and dark septate endophytes in roots of six European Rhododendron species. Folia Geobot. 2011;46:373–386. doi: 10.1007/s12224-011-9098-5. DOI
Mayerhofer MS, Kernaghan G, Harper KA. The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza. 2013;23:119–128. doi: 10.1007/s00572-012-0456-9. PubMed DOI
Arnaud-Haond S, et al. Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica. Plos One. 2012;7:e30454. doi: 10.1371/journal.pone.0030454. PubMed DOI PMC
Estrada M. Primary production in the northwestern Mediterranean. Sci. Mar. 1996;60:55–64.
Fourqurean JW, et al. Seagrass ecosystems as a globally significant carbon stock. Nat. Geosci. 2012;5:505–509. doi: 10.1038/ngeo1477. DOI
Vohník M, Sadowsky JJ, Lukešová T, Albrechtová J, Vosátka M. Inoculation with wood decomposing basidiomycete, but not with root symbiotic ascomycetes, positively affects growth of highbush blueberry (Ericaceae) grown in a pine litter substrate. Plant Soil. 2012;355:341–352. doi: 10.1007/s11104-011-1106-2. DOI
Kuo, J. & McComb, A. J. Posidoniaceae in Flowering plants–Monocotyledons (Springer, 1998).
Belzunce M, Navarro RM, Rapoport HF. Posidonia oceanica seedling root structure and development. Aquat. Bot. 2008;88:203–210. doi: 10.1016/j.aquabot.2007.10.008. DOI
Marbà N, Cebrián J, Enríquez S, Duarte CM. Growth patterns of Western Mediterranean seagrasses: species-specific responses to seasonal forcing. Mar. Ecol. Progr. Ser. 1996;133:203–215. doi: 10.3354/meps133203. DOI
Pergent G, Boudouresque C-F, Crouzet A, Meinesz A. Cyclic changes along Posidonia oceanica rhizomes (lepidochronology): present state and perspectives. PSZNI Mar. Ecol. 1989;10:221–230. doi: 10.1111/j.1439-0485.1989.tb00474.x. DOI
Diaz-Almela E, et al. Patterns in seagrass (Posidonia oceanica) flowering in the Western Mediterranean. Mar. Biol. 2006;148:723–742. doi: 10.1007/s00227-005-0127-x. DOI
Pergent G, Pergent-Martini C. Some applications of lepidochronological analysis in the seagrass Posidonia oceanica. Bot. Mar. 1990;33:299–310. doi: 10.1515/botm.1990.33.4.299. DOI
Balestri E, Vallerini F. Interannual variability in flowering of Posidonia oceanica in the North-Western Mediterranean Sea, and relationships among shoot age and flowering. Bot. Mar. 2003;46:525–530. doi: 10.1515/BOT.2003.054. DOI
Balestri E, Lardicci C. First evidence of a massive recruitment event in Posidonia oceanica: spatial variation in first-year seedling abundance on a heterogeneous substrate. Estuar. Coast. Shelf. Sci. 2008;76:634–641. doi: 10.1016/j.ecss.2007.07.048. DOI
Balestri E, Cinelli F. Sexual reproductive success in Posidonia oceanica. Aquat. Bot. 2003;75:21–32. doi: 10.1016/S0304-3770(02)00151-1. DOI
Balestri E, Piazzi L, Cinelli F. In vitro germination and seedling development of Posidonia oceanica. Aquat. Bot. 1998;60:83–93. doi: 10.1016/S0304-3770(97)00017-X. DOI
Piazzi L, Acunto S, Cinelli F. In situ survival and development of Posidonia oceanica L. Delile seedlings. Aquat. Bot. 1999;63:103–112. doi: 10.1016/S0304-3770(98)00115-6. DOI
Balestri E, Gobert S, Lepoint G, Lardicci C. Seed nutrient content and nutritional status of Posidonia oceanica seedlings in the northwestern Mediterranean Sea. Mar. Ecol. Progr. Ser. 2009;388:99–109. doi: 10.3354/meps08104. DOI
Schutten J, Dainty J, Davy AJ. Root anchorage and its significance for submerged plants in shallow lakes. J. Ecol. 2005;93:556–571. doi: 10.1111/j.1365-2745.2005.00980.x. DOI
Szmeja J, Gałka A. Phenotypic responses to water flow and wave exposure in aquatic plants. Acta Soc. Bot. Pol. 2008;77:59–65.
Gibbs RE. Phyllospadix as a beach-builder. Am. Nat. 1902;36:101–109. doi: 10.1086/278075. DOI
Infantes E, Orfila A, Bouma TJ, Simarro G, Terrados J. Posidonia oceanica and Cymodocea nodosa seedling tolerance to wave exposure. Limnol. Oceanogr. 2011;56:2223–2232. doi: 10.4319/lo.2011.56.6.2223. DOI
Alagna A, Fernández TV, Terlizzi A, Badalamenti F. Influence of microhabitat on seedling survival and growth of the Mediterranean seagrass Posidonia oceanica (L.) Delile. Estuar. Coast. Shelf. Sci. 2013;119:119–125. doi: 10.1016/j.ecss.2013.01.009. DOI
Duckett JG, Read DJ. Ericoid mycorrhizas and rhizoid‐ascomycete associations in liverworts share the same mycobiont: isolation of the partners and resynthesis of the associations in vitro. New Phytol. 1995;129:439–447. doi: 10.1111/j.1469-8137.1995.tb04315.x. DOI
Bruzone MC, Fehrer J, Fontenla SB, Vohník M. First record of Rhizoscyphus ericae in Southern Hemisphere´s Ericaceae. Mycorrhiza. 2017;27:147–163. doi: 10.1007/s00572-016-0738-8. PubMed DOI
Jäger-Zürn I, Grubert M. Podostemaceae depend on sticky biofilms with respect to attachment to rocks in waterfalls. Int. J. Plant Sci. 2000;161:599–607. doi: 10.1086/314292. DOI
Yang X, Deng W. Morphological and structural characterization of the attachment system in aerial roots of Syngonium podophyllum. Planta. 2017;245:507–521. doi: 10.1007/s00425-016-2621-4. PubMed DOI
Tomasello A, Perrone R, Colombo P, Pirrotta M, Calvo S. Root hair anatomy and morphology in Posidonia oceanica (L.) Delile and substratum typology: First observations of a spiral form. Aquat. Bot. 2018;145:45–48. doi: 10.1016/j.aquabot.2017.12.001. DOI
Bernal AA, De Camargo Smidt E, Bona C. Spiral root hairs in Spiranthinae (Cranichideae: Orchidaceae) Braz. J. Bot. 2015;38:411–415. doi: 10.1007/s40415-015-0141-2. DOI
Almeida ABR, Smidt EC, Amano E. Development and function of root hairs in Acianthera Scheidw. (Orchidaceae: Pleurothallidinae) Aust. J. Basic. Appl. Sci. 2016;10:122–126.
Melzer B, et al. The attachment strategy of English ivy: a complex mechanism acting on several hierarchical levels. J. R. Soc. Interface. 2010;7:1383–1389. doi: 10.1098/rsif.2010.0140. PubMed DOI PMC
Belzunce M, Navarro RM, Rapoport HF. Posidonia oceanica seeds from drift origin: viability, germination and early plantlet development. Bot. Mar. 2008;51:1–9. doi: 10.1515/BOT.2008.005. DOI
Das P, Kayang H. Association of dark septate endophytes and arbuscular mycorrhizal fungi in potato under field conditions in the northeast region of India. Mycology. 2010;1:171–178. doi: 10.1080/21501203.2010.517787. DOI
Selosse, M. A. & Le Tacon, F. The land flora: a phototroph-fungus partnership? Trends Ecol. Evol.13, 15–20. PubMed
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 2015;205:1406–1423. doi: 10.1111/nph.13288. PubMed DOI
Vohník M, Borovec O, Özgür Özbek E, Okudan Alsan E. Rare phytomyxid infection on the alien seagrass Halophila stipulacea in the southeast Aegean Sea. Mediterr. Mar. Sci. 2017;18:433–442. doi: 10.12681/mms.14053. DOI
Pohlert, T. The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR) in R package, http://CRAN.R-project.org/package=PMCMR (2014).