Arbuscular mycorrhizae and septate endophytes in three species of Thelypteridaceae of riparian environments of the Yungas (Tucumán, Argentina)
DOI:
https://doi.org/10.31055/1851.2372.v59.n3.44734Keywords:
Amauropelta, arbuscular mycorrhizae, ferns, fungal endophytes, PelazoneuronAbstract
Background and aims: The status of the presence of arbuscular mycorrhizal fungi (AMF) in lycophytes and ferns has been analysed in 11% of them. This work aims to characterise and quantify the AMF colonisation and to characterise septate endophytes present on the roots of the Thelypteridaceae: Amauropelta jujuyensis, A. nubicola, and Pelazoneuron patens.
M&M: Ten individuals per species were collected in August 2022. Conventional staining and techniques were used to estimate colonisation.
Results: The root of Amauropelta jujuyensis, A. nubicola, and Pelazoneuron patens showed AMF with Arum and Paris morphological types simultaneously. The hyphal colonization showed no significant difference among species, arbuscular colonization was significantly higher in A. jujuyensis, while vesicular colonization was considerably higher in A. nubicola. In addition, septate endophytes were evident in the species of the genus Amauropelta.
Conclusion: The association of AMF and other fungal endophytes with the native Argentine Thelypteridaceae Amauropelta jujuyensis, A. nubicola, and Pelazoneuron patens is evidenced for the first time in riparian environments of the Yungas. The coexistence of Arum and Paris morphological types in the three studied fern species is demonstrated.
References
ALBORNOZ, P. & M. HERNÁNDEZ. 2006. Anatomía y endomicorrizas en Pellaea ternifolia (Cav.) Link subsp. ternifolia (Pteridaceae) en Tucumán (Argentina). Lilloa 43:13-21.
ARANA, M. D., E. S. NATALE, N. E. FERRETTI, G. M. ROMANO & J. J. MORRONE. 2021. Esquema biogeográfico de la República Argentina. Fundación Miguel Lillo. Opera Lilloana 56: 1-240.
ARANA, M. D. & M. M. PONCE. 2021. Contribución de licofitas y helechos endémicos al esquema biogeográfico evolutivo de la Argentina. Bol. Soc. Argent. Bot. 56 (Supl.): 16.
BARROW, J. R. 2003. Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13: 239-247. https://doi.org/10.1007/s00572-003-0222-0
BECERRA, A., M. CABELLO & F. CHIARINI. 2007. Arbuscular mycorrhizal colonization of vascular plants from the Yungas forests, Argentina. Ann. For. Sci. 64: 765-772. https://doi.org/10.1051/forest:2007056
BERCH, S. M. & B. KENDRICK. 1982. Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74: 769-776. https://doi.org/10.1080/00275514.1982.12021584
BERRUETA, P. C., M. PONCE, M. L. LUNA, G. GIUDICE & M. D. ARANA. 2023. Amauropelta platensis (Thelypteridaceae), New combination for the endemic Southern Cone Fern Flora. Rodriguesia 74: e00492023. http://dx.doi.org/10.1590/2175-7860202374064
BOLAN, N. S. 1991. A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant soil. 134: 189-207. https://doi.org/10.1007/BF00012037
BRUNDRETT, M. 2004. Diversity and classification of mycorrhizal associations. Biol. Rev. 79: 473-495. https://doi.org/10.1017/S1464793103006316
BRUNDRETT, M. C. 2009. 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 and Soil 320: 37-77.
BRUNDRETT, M. C. & L. TEDERSOO. 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 220: 1108-1115. https://doi.org/10.1111/nph.14976
CHADHA, N., M. MISHRA, R. PRASAD & A. VARMA. 2014. Root endophytic fungi: research update. J. Biol. Life Sci. 5: 135-158. https://doi.org/10.5296/jbls.v5i2.5960
DICKSON, S. 2004. The Arum-Paris continuum of mycorrhizal symbioses. New Phytol. 163: 187-200. https://doi.org/10.1111/j.1469-8137.2004.01095.x
FAWCETT, S. & A. R. SMITH. 2021. A Generic Classification of the Thelypteridaceae. BRIT Press. Texas.
FAWCETT, S., A. R. SMITH, M. SUNDUE, J. G. BURLEIGH…& D. S. BARRINGTON. 2021. A global phylogenomic study of the Thelypteridaceae. Syst. Bot. 46: 891-915. https://doi.org/10.1600/036364421X16370109698650
FERNÁNDEZ, D. S. & M. A. LUTZ. 2003. Procesos de remoción en masa y erosión fluvial en la quebrada del río Los Sosa, provincia de Tucumán. Rev. Asoc. Geol. Arg. 58: 255-266.
FERNÁNDEZ, N., M. I. MESSUTI & S. FONTENLA. 2008. Arbuscular mycorrhizas and dark septate fungi in Lycopodium paniculatum (Lycopodiaceae) and Equisetum bogotense (Equisetaceae) in a Valdivian temperate forest of Patagonia, Argentina. Am. Fern J. 98: 117-127. https://doi.org/10.1640/0002-8444(2008)98[117:AMADSF]2.0.CO;2
FERNÁNDEZ, N., S. FONTENLA & M. I. MESSUTI. 2010. Mycorrhizal status of obligate and facultative epiphytic ferns in a Valdivian temperate forest of Patagonia, Argentina. Am. Fern J. 100: 16-26. https://doi.org/10.1640/0002-8444-100.1.16
FERNÁNDEZ, N. V., M. I. MESSUTI & S. B. FONTENLA. 2012. Occurrence of arbuscular mycorrhizas and dark septate endophytes in pteridophytes from a patagonian rainforest, Argentina. J. Basic Microbiol. 53: 498-508.
FONTENLA, S., R. GODOY, P. ROSSO, & M. HAVRYLENKO. 1998. Root associations in Austrocedrus forests and seasonal dynamics of arbuscular mycorrhizas. Mycorrhiza 8: 29-33.
FONTENLA, S., J. PUNTIERI & J. A. OCAMPO. 2001. Mycorrhizal associations in the Patagonian steppe, Argentina. Plant Soil 233: 13-29.
FONTENLA, S. B., N. V. FERNÁNDEZ, M. C. MESTRE & J. P. PUNTIERI. 2022. Current Knowledge on Mycorrhizal Symbiosis and Endophytes in Northwest Patagonia, Argentina. En: LUGO, M.A. & M.C. PAGANO (eds.), Mycorrhizal Fungi in South America, pp. 255-279. Fungal Biology, Springer, Cham. https://doi.org/10.1007/978-3-031-12994-0_13
FRACCHIA, S., A. ARANDA, A. GOPAR, V. SILVANI & A. GODEAS. 2009. Mycorrhizal status of plant species in the Chaco Serrano Woodland from central Argentina. Mycorrhiza 19: 205-214.
FREIRE BOADO, M. A. & L. GUITIÁN RIVERA. 2005. Caracterización de la vegetación en los ambientes ribereños del curso medio del río Ulla. Xerográfica 5: 61-83.
GRACE, C. & D. P. STRIBLEY. 1991. A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol. Res. 95: 1160-1162. https://doi.org/10.1016/S0953-7562(09)80005-1
HERNÁNDEZ, M., P. ALBORNOZ, F. RODRÍGUEZ & S. SERRANO. 2008. Anatomía de rizoma, raíz y micorrizas arbusculares en Cheilanthes pruinata Kaulf y C. myriophylla Desv. (Pteridaceae) en el Noroeste Argentino. Lilloa 45: 73-82.
HERNÁNDEZ, M. A., G. TERÁN & P. L. ALBORNOZ. 2010. Morfología, anatomía y endomicorrizas en el esporofito de Doryopteris concolor (Pteridaceae). Lilloa 47: 73-83.
HOYSTED, G. A., J. KOWAL, A. JACOB, W. R. RIMINGTON & M. I. BIDARTONDO. 2018. A mycorrhizal revolution. Curr. Opin. Plant Biol. 44: 1-6. https://doi.org/10.1016/j.pbi.2017.12.004
JUMPPONEN, A. 2001. Dark septate endophytes–are they mycorrhizal? Mycorrhiza 11: 207-211. https://doi.org/10.1007/s005720100112
KHADE, S. W. & B. F. RODRIGUES. 2002. Arbuscular mycorrhizal fungi associated with some pteridophytes from Western Ghats region of Goa. Trop. Ecol. 43: 251-256,
KESSLER, M., R. JONAS, D. CICUZZA, J. KLUGE & M. LEHNERT. 2010. A survey of the mycorrhization of Southeast Asian ferns and lycophytes. Plant Biol. 12: 788-793.
KESSLER, M., R. GÜDEL, L. SALAZAR, J. HOMEIER & J. KLUGE. 2014. Impact of mycorrhization on the abundance, growth and leaf nutrient status of ferns along a tropical elevational gradient. Oecologia 175: 887-900. https://doi.org/10.1007/s00442-014-2941-7
LARA-PÉREZ, L. A., J. C. NOA-CARRAZANA, Á. D. J. LANDA LÓPEZ, S. HERNÁNDEZ-GONZÁLEZ & A. ANDRADE TORRES. 2014. Colonización y estructura de la comunidad de hongos micorrízicos arbusculares en Alsophila firma (Cyatheaceae) en bosque mesófilo de montaña en Veracruz, México. Rev. Biol. Trop. 62: 1609-1623. https://doi.org/10.15517/rbt.v62i4.13324
LEHNERT, M., I. KOTTKE, S. SETARO, L. F. PAZMIÑO & M. KESSLER. 2009. Mycorrhizal associations in ferns from Southern Ecuador. Am. Fern J. 99: 292-306.
LEHNERT, M. & M. KESSLER. 2016. Mycorrhizal relationships in lycophytes and ferns. Fern gazette. 20: 101-116.
LEHNERT, M., M. KRUG & M. KESSLER. 2017. A review of symbiotic fungal endophytes in lycophytes and ferns–a global phylogenetic and ecological perspective. Symbiosis 71: 77-89. htpps://doi.org/10.1007/s13199-016-0436-5
LIZARRAGA, S. V., G. A. PEREZ, A. I. RUIZ, S. M. SALAZAR & P. L. ALBORNOZ. 2018. Rendimiento frutal de tres variedades de Fragaria ananassa en relación con el grado de colonización por micorrizas arbusculares y otros endófitos fúngicos, Tucumán, Argentina. Respuesta histológica radical a la interacción. Rev. Agron. Noroeste arg. 38: 145-154.
MANDYAM, K. & A. JUMPPONEN. 2005. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol. 53: 173-189. https://doi.org/10.3114/sim.53.1.173
MARSCHNER, H. & B. DELL. 1994. Nutrient uptake in mycorrhizal symbiosis. Plant Soil. 159: 89-102. https://doi.org/10.1007/BF00000098
MCGONIGLE, T. P., M. H. MILLER, D. G. EVANS, G. L. FAIRCHILD & J. A. SWAN. 1990. A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol. 115: 495-501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
MENDOZA, E. A. & J. A. GONZÁLEZ. 2011. Las ecorregiones del noroeste argentino basadas en la clasificación climática de Köppen. Serie Conserv. Nat. 19: 3-41.
MORTE, A., C. LOVISOLO & A. SCHUBERT. 2000. Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almeriense - Terfezia claveryi. Mycorrhiza 10: 115-119. https://doi.org/10.1007/s005720000066
MUTHURAJA, R., T. MUTHUKUMAR, K. SATHIYADASH, E. UMA & P. PRIYADHARSINI. 2014. Arbuscular mycorrhizal (AM) and dark septate endophyte (DSE) fungal association in lycophytes and ferns of the Kolli Hills, Eastern Ghats, Southern India. Am. Fern J. 104: 67-102. https://doi.org/10.1640/0002-8444-104.2.67
NEUENKAMP, L., S. M. PROBER, J. N. PRICE, M. ZOBEL & R. J. STANDISH. 2019. Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. Fungal Ecol. 40: 140-149.
NEWSHAM, K. K., R. UPSON & D. J. READ. 2009. Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol. 2: 10-20. https://doi.org/10.1016/j.funeco.2008.10.005
PAGANO, M. C. & M. N. CABELLO. 2012. Mycorrhizas in Natural and Restored Riparian Zones. En: PAGANO, M. C. (ed.), Mycorrhiza: Occurrence and Role in Natural and Restored Environments, pp. 292-316. Nova Science Publishers, Hauppauge.
PHILLIPS, J. M. & D. S. HAYMAN. 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-IN18. https://doi.org/10.1016/S0007-1536(70)80110-3
PONCE, M. M. 1987. Revisión sistemática de las Thelypteridaceae (Pteridophyta) argentinas. Tesis Doctoral. Universidad de Buenos Aires. Argentina.
PONCE, M. M. 2016. Thelypteridaceae. En: PONCE, M. M & M. D. ARANA (coords.), Flora Vascular de la República Argentina, vol. 2: 353-384. Estudio Sigma S.R.L., Buenos Aires. https://doi.org/10.2307/j.ctt1p0vjr5.35
PPG I. 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54: 563-603. https://doi.org/10.1111/jse.12229
REDMAN, R. S., K. B. SHEEHAN, R. G. STOUT, R. J. RODRIGUEZ & J. M. HENSON. 2002. Thermo tolerance generated by plant/fungal symbiosis. Science 298: 1581-1584. https://doi.org/10.1126/science.1078055
ŘEZÁČOVÁ, V., A. CZAKÓ, M. STEHLÍK, M. MAYEROVÁ & M. MADARAS. 2021. Organic fertilization improves soil aggregation through increases in abundance of eubacteria and products of arbuscular mycorrhizal fungi. Sci Rep 11: 12548. https://doi.org/10.1038/s41598-021-91653-x
RILLIG, M. C. & D. L. MUMMEY. 2006. Mycorrhizas and soil structure. New Phytol. 171: 41-53.
ROMAGNOLI, G., P. ALBORNOZ & M. ARANA. 2023. Nuevas citas para la flora de helechos (Polypodiopsida) en las Yungas de Tucumán, Argentina. Lilloa 60: 97-104. https://doi.org/10.30550/j.lil/2023.60.1/2023.06.01
SÁNCHEZ BAIZABAL, E. M. S., R. MEDEL-ORTIZ & D. T. AGUILAR. 2020. Evidencia de asociaciones fúngicas en Phlegmariurus reflexus (Lycopodiaceae). Botanical Sciences 100: 345-352. https://doi.org/10.17129/botsci.2953
SIEVERDING, E., J. FRIEDRICHSEN & W. SUDEN. 1991. Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Sonderpublikation der GTZ, Eschborn .
SILVA, V. L. D., C. R. ORLANDI, L. FUNCK, M. C. WINHELMANN & E. M. D. FREITAS. 2019. Heterogeneity of fern communities in riparian forest remnants from the South Brazilian Campos (Pampa). Braz. J. Biol. 80: 803-813. https://doi.org/10.1590/1519-6984.221124
SIROMBRA, M. G. & L. M. MESA. 2010. Composición florística y distribución de los bosques ribereños subtropicales andinos del río Lules, Tucumán, Argentina. Rev. Biol. Trop. 58: 499-510. https://doi.org/10.15517/rbt.v58i1.5224
SMITH, S. E. & D. J. READ. 2008. Mycorrhizal symbiosis. Third ed. Academic Press, Londres.
VALDEZ NÚÑEZ, R. A., J. C. ROJAS GARCÍA & E. J. BEDMAR. 2022. Dark septate endophytes: A review. Mol 22: 1-13.
YAÑEZ, A., G. J. MARQUEZ, D. OCAMPO TERRAZA & M. PONCE. 2022. Amauropelta yabotiensis (Thelypteridaceae), A New Species from Biosphere Yabotí Reserve (Misiones, Argentina) and its Taxonomic Relationships. An. Acad. Bras. Cienc. 94: e20201870. https://doi.org/10.1590/0001-3765202220201870
ZHANG, Y., L. D. GUO & R. J. LIU. 2004. Arbuscular mycorrhizal fungi associated with common pteridophytes in Dujiangyan, southwest China. Mycorrhiza 14: 25-30. https://doi.org/10.1007/s00572-003-0272-3
ZAR, J. D. 1996. Bioestatistical analysis. Tercera edición. Prentice Hall Inc., New Jersey.
ZHAO, Y. J., S. X. GUO & W. W. GAO. 1999. The symbiosis of endophytic fungi with Cymbidium goeringii and its effects on the mineral nutrition absorption. Acta Horticulturae Sin. 26: 110-115.
ZUBEK, S., K. PIĄTEK, P. NAKS, W. HEISE & P. MLECZKO. 2010. Fungal root endophyte colonization of fern and lycophyte species from the Celaque National Park in Honduras. Am. Fern J. 100: 126-136. https://doi.org/10.1640/0002-8444-100.2.126
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Gabriela Romagnoli, Marcelo D. Arana, Patricia L. Albornoz
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Provides immediate and free OPEN ACCESS to its content under the principle of making research freely available to the public, which fosters a greater exchange of global knowledge, allowing authors to maintain their copyright without restrictions.
Material published in Bol. Soc. Argent. Bot. is distributed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International license.
