Keywords
Anemiaceae, esporogénesis, esporocitos, esporodermis, tapetum, ultraestructura
How to Cite
Abstract
Introduction: Research into the ontogeny of sporangia and sporogenesis of leptosporangiate ferns is scarce in the scientific literature. Objectives: To describe and analyze the ontogeny of sporangia, sporogenesis, micromorphology, and ultrastructure of mature spores of the fern Anemia hirsuta. Methods: Fertile fronds of A. hirsuta were processed according to standard protocols for sectioning and embedding samples in paraffin and resin. Sections in paraffin were stained with safranin-alcian blue, Toluidine Blue, and PAS/amidoblack. Sections in resin were stained with Toluidine Blue. The samples were prepared for observation under scanning electron microscopy (SEM) to yield detailed descriptions. Mature spores were analyzed by X-ray energy dispersion (XEDS). Ultrathin sections were obtained for transmission electron microscopy (TEM) observation. Results: The entire leptosporangium is formed from a basal and an apical cell derived from a single epidermal cell of the fertile pinna. The mature leptosporangia are globose, with a subapical ring and a short pedicel. During development, the tapetum is initially cellular, and then becomes plasmodial. The sporocytes undergo simultaneous meiotic division to form tetrads of spores in a tetrahedral arrangement. The exospore is formed first, with two layers, a very thin internal layer and a thick outer layer, followed by the endospore, and finally the perispore. The spores are trilete and muriform, with simple or branched siliceous microspines. The perispore associated with the muri and grooves appears to be highly organized with evident ultrastructural differences. Conclusions: The ontogeny of the sporangia and sporogenesis of A. hirsuta is similar to that previously described for leptosporangiate ferns and recorded in some related fossil species. The highly structured and organized perispore is observed. A high silica content in the microspines of the sporodermis is herein reported for the first time in this group.
References
Albornoz, P. L., Romagnoli, M. G., & Hernández, M. A. (2021). Anatomy of the sporophyte of Anemia phyllitidis var. phyllitidis (Anemiaceae) from a riparian forest (Tucumán, Argentina). Acta Botánica Mexicana, 128, e1830. https://doi.org/10.21829/abm128.2021.1830
Archangelsky, S., & Archangelsky, A. (2010). Revisión taxonómica y estratigráfica de esporas cicatricosas del Cretácico Inferior de Patagonia: 2. Géneros Cicatricosisporites Potonié & Gelletich y Ruffordiaspora Dettmann & Clifford. Revista del Museo Argentino de Ciencias Naturales, 12(2), 179–201.
Archangelsky, S., Archangelsky, A., & Cladera, G. (2012). Palinología y paleoambientes en el perfil de Bajo Comisión (Cretácico), provincia de Santa Cruz, Argentina. Revista del Museo Argentino de Ciencias Naturales, 14(1), 23–39.
Bhattacharya, R., Saha, S., Kostina, O., Muravnik, L., & Mitra, A. (2020). Replacing critical point drying with a low-cost chemical drying provides comparable surface image quality of glandular trichomes from leaves of Millingtonia hortensis L. f. in scanning electron micrograph. Applied Microscopy, 50, 15. https://doi.org/10.1186/s42649-020-00035-6
Chambi, C. J., & Martínez, O. G. (2020). Fase gametofítica de tres taxones de Anemia (Anemiaceae). Acta Botánica Mexicana, 127, e1631. https://doi.org/10.21829/abm127.2020.1631
Corrêa-Lopes, K. C., & Feio, A. C. (2020). Silica bodies in Selaginella (Selaginellaceae). American Fern Journal, 110(1), 29–41. https://doi.org/10.1640/0002-8444-110.1.29
Currie, H. A., & Perry, C. C. (2007). Silica in plants: biological, biochemical and chemical studies. Annals of Botany, 100(7), 1383–1389. https://doi.org/10.1093/aob/mcm247
Dettmann, M. E., & Clifford, H. T. (1991). Spore morphology of Anemia, Mohria, and Ceratopteris (Filicales). American Journal of Botany, 78(3), 303–325. https://doi.org/10.1002/j.1537-2197.1991.tb15194.x
Dias, E., & Branco, S. (2023). Experimental transport of Trichomanes speciosum spores on Azorean woodpigeon feathers as a possible explanation for interisland dispersal. Plant Species Biology, 38(3), 86–94. https://doi.org/10.1111/1442-1984.12401
Furness, C. A., Rudall, P. J., & Sampson, F. B. (2002). Evolution of microsporogenesis in angiosperms. International Journal of Plant Sciences, 163(2), 235–260. https://doi.org/10.1086/338322
Gifford, M. E., & Foster, S.A. (1989). Morphology and evolution of vascular plants. W. H. Freeman and Company.
Gómez‐Noguez, F., Domínguez‐Ugalde, C., Flores‐Galván, C., León‐Rossano, L. M., Pérez-García, B., Mendoza‐Ruiz, A., Rosas-Pérez, I., & Mehltreter, K. (2022). Terminal velocity of fern and lycopod spores is affected more by mass and ornamentation than by size. American Journal of Botany, 109(8), 1221–1229. https://doi.org/10.1002/ajb2.16041
Hernandez-Hernandez, V., Terrazas, T., Mehltreter, K., & Angeles, G. (2012). Studies of petiolar anatomy in ferns: structural diversity and systematic significance of the circumendodermal band. Botanical Journal of the Linnean Society, 169(4), 596–610. https://doi.org/10.1111/j.1095-8339.2012.01236.x
Hill, S. R. (1979). Spore morphology of Anemia subgenus Anemia. American Fern Journal, 69(3), 71–79. https://doi.org/10.2307/1546381
Kumar, S., Soukup, M., & Elbaum, R. (2017). Silicification in grasses: variation between different cell types. Frontiers in Plant Science, 8, 438. https://doi.org/10.3389/fpls.2017.00438
Labiak, P. H., Mickel, J. T., & Hanks, J. G. (2015). Molecular phylogeny and character evolution of Anemiaceae (Schizaeales). Taxon, 64(6), 1141–1158. https://doi.org/10.12705/646.3
Law, C., & Exley, C. (2011). New insight into silica deposition in horsetail (Equisetum arvense). BMC Plant Biology, 11, 112. https://doi.org/10.1186/1471-2229-11-112
Lellinger, D. B. (2002). A modern multilingual glossary for taxonomic pteridology (Vol. 3). American Fern Society. https://doi.org/10.5962/bhl.title.124209
Lin, C. H., Falk, R. H., & Stocking, C. R. (1977). Rapid chemical dehydration of plant material for light and electron microscopy with 2,2-dimethoxypropane and 2,2-diethoxypropane. American Journal of Botany, 64(5), 602–605. https://doi.org/10.1002/j.1537-2197.1977.tb11898.x
Llorens, C., Argentina, M., Rojas, N., Westbrook, J., Dumais, J., & Noblin, X. (2016). The fern cavitation catapult: mechanism and design principles. Journal of The Royal Society Interface, 13(114), 20150930. https://doi.org/10.1098/rsif.2015.0930
Macluf, C. C., Morbelli, M. A., & Giudice, G. E. (2003). Morphology and ultrastructure of megaspores and microspores of Isoetes savatieri Franchet (Lycophyta). Review of Palaeobotany and Palynology, 126(3–4), 197–209. https://doi.org/10.1016/S0034-6667(03)00086-1
Macluf, C., Meza-Torres, E. I., & Solís, S. M. (2010). Isoetes pedersenii, a new species from Southern South America. Anais da Academia Brasileira de Ciências, 82(2), 353–359. https://doi.org/10.1590/S0001-37652010000200011
Macluf, C., Morbelli, M., & Giudice, G. (2010). Morphology and ultrastructure of megaspores and microspores of Isoetes sehnemii Fuchs (Lycophyta). Anais da Academia Brasileira de Ciências, 82(2), 341–352. https://doi.org/10.1590/S0001-37652010000200010
Mazumdar, J. (2011). Phytoliths of pteridophytes. South African Journal of Botany, 77(1), 10–19. https://doi.org/10.1016/j.sajb.2010.07.020
Mickel, J. T. (1982). The genus Anemia (Schizaeaceae) in Mexico. Brittonia, 34, 388–413. https://doi.org/10.2307/2806495
Mickel, J. T. (2016). Anemia (Anemiaceae), flora neotropica monograph (Vol. 118). New York Botanical Garden Press.
Mickel, J. T., & Smith, R. A. (2004). The Pteridophytes of Mexico (Vol. 88). New York Botanical Garden Press.
Murillo-Aldana, J. M., & Murillo, M. T. (2017). Diversidad de los helechos y licófitos de Colombia. Acta Botánica Malacitana, 42(1), 23–32. https://doi.org/10.24310/abm.v42i1.2654
Murillo-Pulido, M. T., & Murillo, J. A. (2004). Pteridofitos de Colombia v. el género Anemia (Schizaeaceae) en Colombia. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 28(109), 471–480. https://doi.org/10.18257/raccefyn.28(109).2004.2106
Nadal, M., Brodribb, T. J., Fernández‐Marín, B., García‐Plazaola, J. I., Arzac, M. I., López‐Pozo, M., Perera-Castro, A. V., Gulías, J., Flexas, J., & Farrant, J. M. (2021). Differences in biochemical, gas exchange and hydraulic response to water stress in desiccation tolerant and sensitive fronds of the fern Anemia caffrorum. New Phytologist, 231(4), 1415–1430. https://doi.org/10.1111/nph.17445
Nester, J. E., & Schedlbauer, M. D. (1981). Gametophyte development in Anemia mexicana Klotzsch. Botanical Gazette, 142(2), 242–250. https://doi.org/10.1086/337219
Parkinson, B. M. (1987). Tapetal organization during sporogenesis in Psilotum nudum. Annals of Botany, 60(4), 353–360. https://doi.org/10.1093/oxfordjournals.aob.a087455
Parkinson, B. M. (1995). Development of the sporangia and associated structures in Schizaea pectinata (Schizaeaceae: Pteridophyta). Canadian Journal of Botany, 73(12), 1867–1877. https://doi.org/10.1139/b95-199
Polevova, S., & Moiseenko, A. (2023). Silicon in sporoderms of micro-and megaspores of Isoetes echinospora Durieu registered by EDS and EELS. Protoplasma, 260, 663–667. https://doi.org/10.1007/s00709-022-01791-w
Pteridophyte Phylogeny Group I. (2016). A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution, 54(6), 563–603. https://doi.org/10.1111/jse.12229
Ramos-Giacosa, J. P. (2014). Abnormal spore morphology and wall ultrastructure in Anemia tomentosa var. anthriscifolia and A. tomentosa var. tomentosa (Anemiaceae). Plant Systematics and Evolution, 300, 1571–1578. https://doi.org/10.1007/s00606-014-0983-2
Ramos-Giacosa, J. P., Morbelli, M. A., & Giudice, G. E. (2012). Spore morphology and wall ultrastructure of Anemia Swartz species (Anemiaceae) from Argentina. Review of Palaeobotany and Palynology, 174, 27–38. https://doi.org/10.1016/j.revpalbo.2012.02.004
Rincón-Barón, E. J., Forero-Ballesteros, H. G., Gélvez-Landazábal, L. V., Torres, G. A., & Rolleri, C. H. (2011). Ontogenia de los estróbilos, desarrollo de los esporangios y esporogénesis de Equisetum giganteum (Equisetaceae) en los Andes de Colombia. Revista de Biología Tropical, 59(4), 1845–1858. https://doi.org/10.15517/rbt.v59i4.33190
Rincón-Barón, E. J., Guerra-Sierra, B. E., Restrepo-Zuluaga, D. E., & Espinosa-Matías, S. (2019). Ontogenia e histoquímica de los esporangios y escamas receptaculares del helecho epífito Pleopeltis macrocarpa (Polypodiaceae). Revista de Biología Tropical, 67(6), 1292–1312. http://dx.doi.org/10.15517/rbt.v67i6.36984
Rincón-Barón, E. J., Guerra-Sierra, B. E., Sandoval-Meza, A. X., & Espinosa-Matías, S. (2020). Ontogeny of sporangia and sporogenesis of the fern Phymatosorus scolopendria (Polypodiaceae). Revista de Biología Tropical, 68(2), 655–668. http://dx.doi.org/10.15517/rbt.v68i2.39676
Rincón-Barón, E. J., Rolleri, C. H., Alzate-Guarin, F., & Dorado-Gálvez, J. M. (2014). Ontogenia de los esporangios, formación y citoquímica de esporas en licopodios (Lycopodiaceae) colombianos. Revista de Biología Tropical, 62(1), 282–307. https://doi.org/10.15517/rbt.v62i1.9795
Rincón-Barón, E. J., Rolleri, C. H., Passarelli, L. M., Espinosa-Matías, S., & Torres, A. M. (2014). Esporogénesis, esporodermo y ornamentación de esporas maduras en Lycopodiaceae. Revista de Biología Tropical, 62(3), 1161-1195. https://doi.org/10.15517/rbt.v62i3.12330
Rincón-Barón, E. J., Torres, G. A., & Rolleri, C. H. (2013). Esporogénesis y esporas de Equisetum bogotense (Equisetaceae) de las áreas montañosas de Colombia. Revista de Biología Tropical, 61(3), 1067–1081. https://doi.org/10.15517/rbt.v61i3.11786
Rincón-Barón, E. J., Torres-Rodríguez, G. A., Zarate, D. A., Cuarán, V. L., Santos-Heredia, C., & Passarelli, L. M. (2024). Microsporogénesis y ultraestructura de granos de polen de la mora andina Rubus glaucus (Rosaceae). Revista de Biología Tropical, 72(1), e55748. https://doi.org/10.15517/rev.biol.trop..v72i1.55748
Roshchina, V. V. (2008). Fluorescing World of Plant Secreting Cells. CRC Press.
Ruzin, S. E. (1999). Plant microtechnique and microscopy. Oxford University.
Sessa, B. E. (2018). Evolution and classification of ferns and Lycophytes. In H. Fernández (Ed.), Current advances in fern research (pp. 179–200). Springer. https://doi.org/10.1007/978-3-319-75103-0_9
Shih, M. C., Xie, P. J., Chen, J., Chesson, P., & Sheue, C. R. (2022). Size always matters, shape matters only for the big: potential optical effects of silica bodies in Selaginella. Journal of the Royal Society Interface, 19(192), 1–13. https://doi.org/10.1098/rsif.2022.0204
Smith, A. R., & Kessler, M. (2017). Prodromus of a fern flora for Bolivia. XIII. Anemiaceae. Phytotaxa, 329(1), 80–86. https://doi.org/10.11646/phytotaxa.329.1.5
Soukup, A. (2014). Selected simple methods of plant cell wall histochemistry and staining for light microscopy. In V. Žárský, & F. Cvrčková (Eds.), Plant cell morphogenesis: Methods and protocols, methods in molecular biology (pp. 25–40). Humana Press. https://doi.org/10.1007/978-1-62703-643-6_2
Sundue, M. (2009). Silica bodies and their systematic implications in Pteridaceae (Pteridophyta). Botanical Journal of the Linnean Society, 161(4), 422–435. https://doi.org/10.1111/j.1095-8339.2009.01012.x
Taylor, W. A. (1992). Megaspore wall development in Isoetes melanopoda: morphogenetic post-initiation changes accompanying spore enlargement. Review of Palaeobotany and Palynology, 72(1–2), 61–72. https://doi.org/10.1016/0034-6667(92)90176-H
Taylor, W. A. (1993). Megaspore wall ultrastructure in Isoetes. American Journal of Botany, 80(2), 165–171. https://doi.org/10.1002/j.1537-2197.1993.tb13785.x
Triana-Moreno, L. A. (2012). Desarrollo del esporangio en Pecluma eurybasis var. villosa (Polypodiaceae). Boletín Científico Centro de Museos Museo de Historia Natural, 16(2), 60–66.
Tryon, A. F., & Lugardon, B. (1991). Spores of the Pteridophyta: Surface, wall structure, and diversity based on electron microscope studies. Springer.
Tryon, R. M., & Tryon, A. F. (1982). Ferns and allied plants, with special reference to tropical America. Springer.
Uehara, K., & Kurita, O. (1991). Ultrastructural study on spore wall morphogenesis in Lycopodium clavatum (Lycopodiaceae). American Journal of Botany, 78(1), 24–36. https://doi.org/10.1002/j.1537-2197.1991.tb12568.x
Uehara, K., Kurita, S., Sahashi, N., & Ohmoto, T. (1991). Ultrastructural study on microspore wall morphogenesis in Isoetes japonica (Isoetaceae). American Journal of Botany, 78(9), 1182–1190. https://doi.org/10.1002/j.1537-2197.1991.tb11411.x
Volkov, V. V., Hickman, G. J., Sola-Rabada, A., & Perry, C. C. (2019). Distributions of silica and biopolymer structural components in the spore elater of Equisetum arvense, an ancient silicifying plant. Frontiers in Plant Science, 10, 210. https://doi.org/10.3389/fpls.2019.00210
Wallace, S., Fleming, A., Wellman, C. H., & Beerling, D. J. (2011). Evolutionary development of the plant and spore wall. AoB Plants, 2011, plr027. https://doi.org/10.1093/aobpla/plr027
Wilson, K. A. (1999). Ontogeny of the sporangia of Sphaeropteris cooperi. American Fern Journal, 89(3), 204–214.
Yang, N. Y., Jia, X. L., Sui, C. X., Shen, S. Y., Dai, X. L., Xue, J. S., & Yang, Z. N. (2022). Documenting the sporangium development of the polypodiales fern Pteris multifida. Frontiers in Plant Science, 13, 878693. https://doi.org/10.3389/fpls.2022.878693
Yao, X., Hu, W., & Yang, Z. N. (2022). The contributions of sporophytic tapetum to pollen formation. Seed Biology, 1, 5. https://doi.org/10.48130/SeedBio-2022-0005
##plugins.facebook.comentarios##
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2025 Revista de Biología Tropical