Arbuscular mycorrhizal fungi and dark septate endophytes in roots of native medicinal ferns from “Sierras Centrales de San Luis”, central-west Argentina

Authors

  • María Luz Torres Área de Ecología, Dpto. de Bioquímica y Ciencias Biológicas, Facultad de Química Bioquímica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina. MICODIF- Grupo de Micología, Diversidad e Interacciones Fúngicas https://orcid.org/0000-0002-3313-7471
  • Esteban M. Crespo Área de Ecología, Dpto. de Bioquímica y Ciencias Biológicas, Facultad de Química Bioquímica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina. MICODIF- Grupo de Micología, Diversidad e Interacciones Fúngicas https://orcid.org/0000-0002-4188-926X
  • M. Cecilia Carosio Área de Ecología, Dpto. de Bioquímica y Ciencias Biológicas, Facultad de Química Bioquímica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina
  • Mónica Lugo Área de Ecología, Dpto. de Bioquímica y Ciencias Biológicas, Facultad de Química Bioquímica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina. MICODIF- Grupo de Micología, Diversidad e Interacciones Fúngicas. IMIBIO-CONICET-UNSL https://orcid.org/0000-0002-7592-0528

DOI:

https://doi.org/10.31055/1851.2372.v59.n3.44533

Keywords:

Arbuscular mycorrhizae, Arum, Chaco District,, dark septate endophytes, ferns, Paris

Abstract

Background and aims: The plant´s roots and fungi establish symbiotic endophytic associations that can coexist: arbuscular mycorrhizae and “dark septate” endophytes. Ferns and lycophytes are vascular plants that can form both fungal symbioses. The objective of this work is to detect the presence of fungal root endosymbiosis, know the mycorrhizal status, and analyze the type of colonizationin in native and ornamental ferns from the “Sierras Centrales de San Luis”.

M&M: In three sites in the “Sierras Centrales de San Luis”, 9-10 individuals of each studied species were collected, their roots were processed to study these fungal. Characterization and quantification of their root colonization was evaluated.

Results: In the three sites studied, Anemia tomentosa var. anthriscifolia formed mycorrhizal associations, the colonization presented abundant hyphal and arbusculated intracellular coils. In addition, glomoid spores of mycorrhizal fungi were found in their rhizospheres. Dark septate endophytes were absent in all species analyzed, none hyphae neither microsclerotia were recorded in roots of these native medicinal ferns.

Conclusions: The mycorrhizal status of Anemia tomentosa var. anthriscifolia, one of the five medicinal fern species from the Sierras Centrales de San Luis studied, is presented. The arbuscular mycorrhizal colonization is described and quantified, and its type is determined as Paris. None of the fern species studied was associated with dark septate endophytes.

References

ABRAHAM, S. & T. THOMAS 2022. Ferns: A potential source of medicine and future prospects. En: MARIMUTHU, J., H. FERNÁNDEZ, A. KUMAR & S. THANGAIAH (eds.), Ferns, pp. 345-378. Springer, Singapore.

AHULU, M. E., M. NAKATA & M. NONAKA. 2005. Arum- and Paris-type arbuscular mycorrhizas in a mixed pine forest on sand dune soil in Niigata Prefecture, central Honshu, Japan. Mycorrhiza 15: 129-36. https://doi.org/10.1007/s00572-004-0310-9

ALBORNOZ, P. & M. HERNÁNDEZ. 2006. Anatomía y endomicorrizas en Pellaea ternifolia (Cav.) Link subsp. ternifolia (Pteridaceae) en Tucumán. Lilloa 43: 13-21.

ANDERSON, O.R. 2021. Physiological ecology of ferns: Biodiversity and conservation perspectives. Inter. J. Biodiv. Conserv. 13: 49-63. https://doi.org/10.5897/IJBC2021.1482

ANTONY R. & S. SURESH. 2022. Ethnobotanical uses of ferns and lycophytes of Kerala. En: MARIMUTHU, J., H. FERNÁNDEZ, A. KUMAR & S. THANGAIAH (eds.), Ferns, pp. 413-432. Springer, Singapore.

BARBOZA, G. E., J. J. CANTERO, C. O. NUÑEZ & L. ARIZA ESPINAR. 2006. Flora Medicinal de la Provincia de Córdoba (Argentina): Pteridófitas y Antófitas silvestres o naturalizadas. Museo Botánico de Córdoba, Córdoba.

BARBOZA, G. E., J. J. CANTERO, C. O. NUÑEZ, A. PACCIARONI & L. ARIZA ESPINAR. 2009. Medicinal plants: A general review and a phytochemical and ethnopharmacological screening of the native Argentine Flora. Kurtziana 34: 7-365.

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

BAYLIS, G. T. S. 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. En: SANDERS F. E., B. MOSSE & P. B. TINKER (eds.), Endomycorrhizas, Proceedings of a Symposium held at the University of Leeds, 22-25 July 1974, pp. 373-389. Academic Press, London.

BECERRA, A., M. CABELLO & F. CHIARINI. 2007. Arbuscular mycorrhizal colonization of vascular plants from the Yungas forests, Argentina. Ann. For. Sci. 64: 765-772.

BONFANTE, P. & A. GENRE. 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1: 48. https://doi.org/10.1038/ncomms1046

BRUNDRETT, M. C. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytol. 154: 275-304.

BRUNDRETT, M. C. 2004. Diversity and classification of mycorrhizal associations. Biol. Rev. 78: 473-495.

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 Soil 320: 37-77. https://doi.org/10.1007/s11104-008-9877-9

BRUNDRETT, M. & B. KENDRICK. 1990a. The roots and mycorrhizas of herbaceous woodland plants. I. Quantitative aspects of morphology. New Phytol. 114: 457-468.

BRUNDRETT, M. & B. KENDRICK. 1990b. The roots and mycorrhizas of herbaceous woodland plants. II. Structural aspects of morphology. New Phytol. 114: 469-479.

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

CHÁVEZ-HERNÁNDEZ, C. G., C. C. BARRERA AGUILAR, G. J. TÉLLEZ ESPINOSA, E. CHIMAL-SÁNCHEZ & R. GARCÍA-SÁNCHEZ. 2021. Colonización micorrízica y comunidades de hongos micorrizógenos arbusculares en plantas medicinales del bosque templado “Agua Escondida”, Taxco, Guerrero, México. Sci. Fungorum 51:e1325. https://doi.org/10.33885/sf.2021.51.1325

CAO, H., T.-T. CHAI, X. WANG, M. F. B. MORAIS-BRAGA, …, & H. D. M. COUTINHO. 2017. Phytochemicals from fern species: potential for medicine applications. Phytochem. Rev. 16: 379-440. https://doi.org/10.1007/s11101-016-9488-7

DE LA ROSA-MERA, C. J., R. FERRERA-CERRATO, A. ALARCÓN, M. J. SÁNCHEZ-COLÍN & A. FRANCO-RAMÍREZ. 2012. Aislamiento de consorcios de hongos micorrícicos arbusculares de plantas medicinales y su efecto en el crecimiento de vinca (Catharanthus roseus). Rev. Chil. Hist. Nat. 85: 187-198. http://dx.doi.org/10.4067/S0716-078X2012000200005

DE LA SOTA, E. R., M. M. PONCE & L. CASSA´ DE PAZOS. 1998. Pteridophyta. En: CORREA, M. N. (ed.), Flora patagónica, Parte I, Tomo I, pp. 282-371. Colección Científica del INTA, Buenos Aires.

DE LA SOTA, E. R, M. L. LUNA, G. E. GIUDICE & J. P. RAMOS GIACOSA. 2009. Sinopsis de las Pteridotifas de la Provincia de San Luis (Argentina). Bol. Soc. Argent. Bot. 44: 367-385.

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

EDWARDS, D. & U. FANNING. 1985. Evolution and environment in the late Silurian-early Devonian: the rise of the pteridophytes. Phil. Trans. Royal Soc. London B 309: 147-165. https://royalsocietypublishing.org/doi/epdf/10.1098/rstb.1985.0076

FERNÁNDEZ, N., M. I. MESSUTI & S. FONTENLA. 2008. Arbuscular mycorrhizas and dark septate fungi in Lycodium paniculatum (Lycopodiaceae) and Equisetum bogotense (Equisetaceae) in a Valdivian temperate forest of Patagonia, Argentina. Am. Fern J. 98: 117-127.

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.

FERNÁNDEZ, N. V., M. I. MESSUTI & S. B. FONTENLA. 2012a. Occurrence of arbuscular mycorrhizas and dark septate endophytes in pteridophytes from a Patagonian rainforest, Argentina. J. Basic Microbiol. 52: 1-11.

FERNÁNDEZ, N. V., S. B. FONTENLA & M. I. MESSUTI. 2012b. Co-ocurrence of arbuscular mycorrhizas and dark septate endophytes in pteridophytes from a Valdivian temperate rainforest in Patagonia, Argentina. En: PAGANO, M. C. (ed.), Mycorrhiza. Occurrence in natural and restored environments, pp. 99-125. NOVA Science Publishing Inc., New York.

FITTER, A. H. 2004. Magnolioid roots-hairs, architecture and mycorrhizal dependency. New Phytol. 164: 15-16. https://doi.org/10.1111/j.1469-8137.2004.01193.x

FONTENLA, S., R. GODOY, P. ROSSO & M. HAVRYLENKO. 1998. Root associations in Austrocedrus forests and seasonal dynamics of arbuscular mycorrhizas. Mycorrhizas 8: 29-33

FONTENLA, S., J. PUNTIERI & J. A. OCAMPO. 2001. Mycorrhizal associations in the Patagonia 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: Biodiversity, Conservation, and Sustainable Food Production, pp. 255-280. Springer, Cham. https://doi.org/10.1007/978-3-031-12994-0

FRACCHIA, S., A. ARANDA, A. GOPAR, V. SILVANI, L. FERNANDEZ & A. GODEAS. 2009. Mycorrhizal status of plant species in the Chaco Serrano Woodland from central Argentina. Mycorrhiza 19: 205-214.

GEMMA, J. N., R. E. KOSKE & T. FLYNN. 1992. Mycorrhizae in Hawaiian pteridophytes: occurrence and evolutionary significance. Am. J. Bot. 79: 843-852.

GODOY, R. & C. MARÍN. 2019. Mycorrhizal studies in temperate rainforests of Southern Chile. En: PAGANO, M. C. & M. A. LUGO (eds.), Mycorrhizal fungi in South America, pp. 315-341. Springer, Cham.

GUCWA-PRZEPIÓRA, E., D. CHMURA & K. SOKOŁOWSKA. 2016. AM and DSE colonization of invasive plants in urban habitat: a study of Upper Silesia (southern Poland). J. Plant Res. 129: 603-614. https://doi.org/10.1007/s10265-016-0802-7

HERNÁNDEZ, M., P. ALBORNOZ, F. RODRÍGUEZ & S. SERRANO. 2008. Anatomía de rizoma, raíz y micorrizas arbusculares en Cheilanthes pruinata Kaulf. y Cheilanthes myriophylla Desv. (Pteridaceae) en el Noroeste Argentino. Lilloa 45: 73-82.

HERNÁNDEZ, M., G. TERÁN & P. ALBORNOZ. 2010. Morfología, anatomía y endomicorrizas en el esporofito de Doryopteris concolor (Pteridaceae). Lilloa 47: 74-84.

HODGE, A., T. HELGASON & A. H. FITTER. 2010. Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol. 10: 267-273. https://doi.org/10.1016/j.funeco.2010.02.002

HODSON, E., F. SHAHID, J. BASINGER & S. KAMINSKYJ. 2009. Fungal endorhizal associates of Equisetum species from Western and Arctic Canada. Mycol. Progress 8: 19-27.

JANOS, D. P. 1980. Mycorrhizae influence tropical succession. Biotropica 12: 56-64.

JANOS, D. P. 1993. Vesicular-arbuscular mycorrhizae of epiphytes. Mycorrhiza 4: 1-4. https://doi.org/10.1007/BF00203242

JANOS, D. P. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17: 75-91.

JUMPPONEN, A. & J. M. TRAPPE. 1998. Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol. 140: 295-310.

KENRICK, P. 2017a. Changing expressions: a hypothesis for the origin of the vascular plant life cycle. Phil. Trans. R. Soc. B 373: 20170149. http://dx.doi.org/10.1098/rstb.2017.0149

KENRICK, P. 2017b. How land plant life cycles first evolved. Science 358: 1538-1539. https://www.science.org/doi/10.1126/science.aan2923

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.

KHOLIA, B. S. & A. BALKRISHNA. 2022. Pteridophytes used by peoples of Indian Himalayan Region and Northern India: An overview. En: MARIMUTHU, J., H. FERNÁNDEZ, A. KUMAR & S. THANGAIAH (eds.), Ferns, pp. 379-412. Springer, Singapore.

KNAPP, D. G., A. PINTYE & G. M. KOVÁCS. 2012. The dark side is not fastidious. Dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. Plos One 7: e32570.

LEHNERT, M., I. KOTTKE, S. SETARO, L. F. PAZMIÑO, J. P. SUÁREZ & M. KESSLER. 2009. Mycorrhizal associations in ferns from Southern Ecuador. Am. Fern J. 99: 292-306.

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.

LUGO, M. A. & M. N. CABELLO. 2002. Native arbuscular mycorrhizal fungi (AMF) from mountain grassland (Córdoba, Argentina) I. Seasonal variation of fungal spore diversity. Mycologia 94: 579-586.

LUGO, M. A., M. E. GONZÁLEZ MAZA & M. N. CABELLO. 2003. Arbuscular mycorrhizal fungi (AMF) from native Argentinian -South American- mountain grassland II. Seasonal variation of colonization and its relation with grazing and metabolic host type. Mycologia 95: 407-415.

LUGO, M. A. & E. MENOYO. 2019. Southern Highlands: Fungal endosymbiotic associations. En: PAGANO, M. C. & M. A. LUGO (eds.), Mycorrhizal Fungi in South America, pp. 217-255. Springer, Cham.

LUGO, M. A. & M. C. PAGANO. 2019. Overview of the mycorrhizal fungi in South America. En: PAGANO, M. C. & M. A. LUGO (eds.), Mycorrhizal Fungi in South America, pp. 1-27. Springer, Cham.

LUGO, M. A. & M. C. PAGANO. 2022. Overview of the biodiversity, conservation, and sustainable food production with mycorrhizal fungi in South America. En: LUGO, M.A. & M.C. PAGANO (eds.), Mycorrhizal Fungi in South America: Biodiversity, Conservation, and Sustainable Food Production, pp. 1-23. Springer, Cham.

LUJÁN, M. C, G. E. BARBOZA, S. WELER DE SERRA & L. ARIZA ESPINAR. 2000. Quality control in two medicinal ferns and its local market insertion. Stud. Bot. 19: 75-94.

MANDYAM, K. & A. JUMPPONEN. 2005. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies Mycol. 53: 173-189.

MANDYAM, K. & A. JUMPPONEN. 2015. Mutualism parasitism paradigm synthesized from results of root-endophyte models. Front. Microbiol. 5: 1-13.

MARIMUTHU, J., N. JANAKIRAMAN, J. CHANDRA SALERIDE, A. SIVARAMAN, … & K. PAULRAJ. 2022. Biopotency of Pteridophytes: A review. En: MARIMUTHU, J., H. FERNÁNDEZ, A. KUMAR & S. THANGAIAH (eds.), Ferns, pp. 481-520. Springer, Singapore.

MARÍN, C., R. GODOY & J. RUBIO. 2022. Gaps in South American mycorrhizal biodiversity and ecosystem function research. En: LUGO, M. A. & M.C. PAGANO (eds.), Mycorrhizal Fungi in South America: Biodiversity, Conservation, and Sustainable Food Production, pp. 445-461. Springer, Cham.

MARTÍNEZ, A. E., V. CHIOCCHIO, L. TAI EM, M. A. RODRIGUEZ & A. M. GODEAS. 2012. Mycorrhizal association in gametophytes and sporophytes of the fern Pteris vittata L. (Pteridaceae) with Glomus intraradices. Rev. Biol. Trop. 60: 857-865.

McGONIGLE, T. P., S. M. H. MILLERS, 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.

MEHLTRETER, K. 2010a. Fern conservation. En: MEHLTRETER K., L. R. WALKER & J. M. SHARPE (eds.), Fern ecology, pp. 323-359. Cambridge University Press, Cambridge.

MEHLTRETER, K. 2010b. Interactions of ferns with fungi and animals. En: MEHLTRETER K., L. R. WALKER & J. M. SHARPE (eds.), Fern ecology, pp. 220-254. Cambridge University Press, Cambridge.

MENOYO, E., A. BECERRA & D. RENISON. 2007. Mycorrhizal associations in Polylepis woodlands of Central Argentina. Can. J. Bot. 85: 526-531. https://doi.org/10.1139/B07-04

MOFOKENG, M. M., C. P. DU PLOOY, H. T. ARAYA, S. O. AMOO, S. N. MOKGEHLE, K. M. POFU & P. W. MASHELA. 2022. Medicinal plant cultivation for sustainable use and commercialisation of high-value crops. S. Afr. J. Sci. 118: Art. #12190. https://doi.org/10.17159/sajs.2022/12190

MONTOLIU-NERIN, M., M. SÁNCHEZ-GARCÍA, C. BERGIN, C. KUTSCHERA, …, & A. ROSLING. 2021. In-depth phylogenomic analysis of arbuscular mycorrhizal fungi based on a comprehensive set of de novo genome assemblies. Front. Fungal Biol. 2: 716385. https://doi.org/10.3389/ffunb.2021.716385

MORERO, R. E., M. A. GIORGIS, M. D. ARANA & G. BARBOZA. 2014. Helechos y licófitas del centro de Argentina, cultivo y especies ornamentales. Instituto Multidisciplinario de Biología Vegetal (CONICET-UNC), Córdoba.

MUTHUKUMAR, T. & S. PRAKASH. 2009. Arbuscular mycorrhizal morphology in crops and associated weeds in tropical agroecosystems. Mycoscience 50: 233-239.

MUTHUKUMAR, T., M. SENTHILKUMAR, M. RAJANGAM & K. UDAIYAN. 2007. Arbuscular mycorrhizal morphology and dark septate fungal associations in medicinal and aromatic plants of Western Ghats, Southern India. Mycorrhiza 17: 11-24. https://doi.org/10.1007/s00572-006-0077-2

NAGALINGUM, N. S. 2016. Evolution and diversification of seedless land plants En: KLIMAN, R. D. (ed.), Encyclopedia of Evolutionary Biology, vol. 4, pp. 16-21. Elsevier, Amsterdam. https://doi.org/10.1016/B978-0-12-800049-6.00255-9

NEWSHAM, K. K. 2011. A meta-analysis of plant responses to dark septate root endophytes. New Phytol. 190: 783-793.

NITTA, J. H., E. SCHUETTPELZ, S. RAMÍREZ-BARAHONA & W. IWASAKI. 2022. An open and continuously updated fern tree of life. Front. Plant. Sci. 24: 909768. https://doi.org/10.3389/fpls.2022.909768

OMAR, M. B., L. BOLLAND & W. A. HEATHER. 1979. P.V.A. (polivinil alcohol). A permanent mounting medium for fungi. Bull. Brit. Mycol. Soc. 13: 31-32.

PAGANO, M. C. & M. N. CABELLO. 2012. Mycorrhizas in natural and restored riparian zones. En: PAGANO, M. C. (ed.), Mycorrhiza. Occurrence in natural and restored environments, pp. 291-316. NOVA Science Publishing Inc., New York.

PINTO, S. C., G. G. LEITÃO, A. CASTELLAR, D. S. D’ELIA, …, & S. G. LEITÃO. 2013. Chemical composition of the volatile fractions from wild and in vitro plants of Anemia tomentosa var. anthriscifolia (Pteridophyta). J. Ess. Oil Res. 25:3: 198-202. https://doi.org/10.1080/10412905.2012.755477

POLANCO, M. & M. A. LUGO. 2005. Micorrizas arbusculares en plantas medicinales de la Reserva Provincial Floro-Faunística La Florida (San Luis, Argentina). Encuentro de Jóvenes Investigadores de Investigadores de las Universidades Nacionales. En: Libro de resúmenes Jóvenes Investigadores, pp. 114. Universidad Nacional de San Luis, San Luis.

PORWAL, O., S. K. SINGH, D. K. PATEL, S. GUPTA, … & S. KATEKHAYE. 2020. Cultivation, collection and processing of medicinal plants. En: AHMAD, J. (ed.), Bioactive phytochemicals: drug discovery to product development, pp. 14-30. Bentham Science Publishers, Sharjah.

PRESSEL, S., M. I. BIDARTONDO, K. J. FIEL, W. R. RIMINGTON & J. G. DUCKETT. 2016. Pteridophyte fungal associations: Current knowledge and future perspectives. J. Syst. Evol. 54: 666-678.

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. Brit. Mycol. Soc. 55: 158-161.

ROIG, F. A. 2002. Flora medicinal mendocina. Las plantas medicinales y aromáticas de la provincia de Mendoza (Argentina). Universidad Nacional de Cuyo, Mendoza.

SANTOS, M. G., L. M. ROCHA, E. S. CARVALHO & A. KELECOM. 2006. Isoafricanol, um sesquiterpeno incomum encontrado na pteridófita Anemia tomentosa var. anthriscifolia. Rev. Bras. Plant. Med. 8: 71-75.

SCHUETTPELZ, E. & K. M. PRYER. 2009. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc. Nat. Acad. Sc. 106: 11200-11205.

https://doi.org/10.1073/pnas.0811136106

SCHUETTPELZ, E., H. SCHNEIDER, A. R. SMITH, P. HOVENKAMP, ..., & X.-M. ZHOU. 2016. A community-derived classification for extant lycophytes and ferns. PPG I. J. Syst. Evol. 54: 563-603. https://doi.org/10.1111/jse.12229

SCHULZ, B. 2006. Mutualistic interactions with fungal root endophytes. En: SCHULZ, B. J. E., C. J. C. BOYLE & T. N. SIEBER (eds.), Microbial root endophytes, pp. 261-279. Springer, Berlin.

SHAH, M. A., Z. A. RESHI & D. P. KHASA. 2009. Arbuscular mycorrhizas: drivers or passengers of alien plant invasion. Bot. Rev. 75: 397-417.

SHARPE, J. M., K. MEHLTRETER & L. R. WALKER. 2010. Ecological importance of ferns. En: MEHLTRETER, K., L. R. WALKER & J. M. SHARPE (eds.), Fern ecology, pp. 1-21. Cambridge University Press, Cambridge.

SMITH, S. E. & D. J. READ. 2008. Mycorrhizal Symbiosis. 3rd Ed. Academic Press, London.

SMITH, F. A. & S. E. SMITH. 1997. Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol. 137: 373-388.

URCELAY, C., P. A. TECCO & F. CHIARINI. 2005. Micorrizas arbusculares del tipo Arum y Paris y endófitos radicales septados oscuros en Miconia ioneura y Tibouchina paratropica (Melastomataceae). Bol. Soc. Argent. Bot. 40: 151-155.

VELÁZQUEZ, M. S., F. BIGANZOLI & M. N. CABELLO. 2010. Arbuscular mycorrhizal fungi in El Palmar National Park (Entre Rios Province, Argentina)-a protected reserve. Sydowia 62: 149-163.

WANG, B. & Y. L. QIU. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299-363.

WANG, W., J. SHI, Q. XIE, Y. JIANG, … & E. WANG. 2017. Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol. Plant. 10: 1147-1158. http://dx.doi.org/10.1016/j.molp.2017.07.012

WANG, C. C., H. CAI, H. ZHAO, Y. YAN, …, & X. LIU. 2018. Distribution patterns for metabolites in medicinal parts of wild and cultivated licorice. J. Pharm. Biomed. Anal. 161: 464-473. https://doi.org/10.1016/j.jpba.2018.09.004

WIJAYAWARDENE, N. N., K. D. HYDE, D. Q. DAI, M. SÁNCHEZ-GARCÍA, ..., & M. THINES. 2022. Outline of fungi and fungus-like taxa. Mycosphere 13: 53-453.

YAMATO, M. & M. IWASAKI M. 2002. Morphological types of arbuscular mycorrhizal fungi in roots of understory plants in Japanese deciduous broadleaved forests. Mycorrhiza 12: 291-296.

YAMOTO, M. 2004. Morphological types of arbuscular mycorrhizal fungi in roots of weeds on vacant land. Mycorrhiza 14: 127-131. https://doi.org/10.1007/s00572-003-0246-5

YUAN, M.-L., M.-H. ZHANG, Z.-Y. SHI, S. YANG, …, & J.-K. GAO. 2023. Arbuscular mycorrhizal fungi enhance active ingredients of medicinal plants: a quantitative analysis. Front. Plant Sci. 14: 1276918. https://doi.org/10.3389/fpls.2023.1276918

ZENG, Y., L. P. GUO, B. D. CHEN, Z. P. HAO, …, & Y. ZHANG. 2013. Arbuscular mycorrhizal symbiosis and active ingredients of medicinal plants: current research status and prospectives. Mycorrhiza 23: 253-265. https://doi.org/10.1007/s00572-013-0484-0

ZHANG, Y., L. D. GUO & R. J. LIU. 2004. Arbuscular mycorrhizal fungi associated with common pteridophytes in Dujiangyan, southwest China. Mycorrhiza 14: 25-30.

ZHANG, M., Z. SHI, S. ZHANG & J. GAO. 2022. A Database on mycorrhizal traits of Chinese medicinal plants. Front. Plant Sci. 13: 840343. https://doi.org/10.3389/fpls.2022.840343

ZHAO, Y., A. CARTABIA, I. LALAYMIA & S. DECLERCK. 2022. Arbuscular mycorrhizal fungi and production of secondary metabolites in medicinal plants. Mycorrhiza 32: 221-256. https://doi.org/10.3389/fpls.2022.840343

ZHOU, X.-M., J.-J. YANG, Z.-L. LIANG, R. POLLAWATN, ..., & L.-B. ZHANG. 2023. A global phylogeny of grammitid ferns (Polypodiaceae) and its systematic implications. Taxon 72: 974-1018. https://doi.org/10.1002/tax.12992

ZUBEK, S. & J. BLASZKOWSKI. 2009. Medicinal plants as hosts of arbuscular mycorrhizal fungi and dark septate endophytes. Phytochem. Rev. 8: 571-580. doi 10.1007/s11101-009-9135-7

Published

2024-09-30

How to Cite

“Arbuscular Mycorrhizal Fungi and Dark Septate Endophytes in Roots of Native Medicinal Ferns from ‘Sierras Centrales De San Luis’, Central-West Argentina”. 2024. Boletín De La Sociedad Argentina De Botánica (Journal of the Argentine Botanical Society 59 (3). https://doi.org/10.31055/1851.2372.v59.n3.44533.

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