Ontogeny of sporangia and sporogenesis of the fern Phymatosorus scolopendria (Polypodiaceae)
DOI:
https://doi.org/10.15517/rbt.v68i2.39676Keywords:
epiphytic fern, Microsoroideae, sporangia development, sorus, ultrastructureAbstract
Introduction: Research about the ontogeny of sori, sporangia, receptacular paraphyses and sporogenesis of leptosporangiate ferns are scarce in the scientific literature. Objectives: To describe and analyze the ontogeny of sori, sporangia, receptacular paraphyses and sporogenesis of Phymatosorus scolopendria. Methods: Fertile fronds of P. scolopendria were collected in the campus of the Universidad de Antioquia, Medellín, Colombia, during the months March and May (annual rain season) of 2017. The fertile fronds of the samples at different developmental stages were fixed and processed according to the standard protocols for embedding and sectioning in paraffin and resin. Sections of 0.5 µm obtained in resin were stained with Toluidine blue, which differentially stains primary and secondary walls, highlights the cell nucleus and sporopolenin and secondarily stains polyphenols. For detailed descriptions, additional sections were processed with Safranin-Alcian blue, allowing the distinction of components of primary and secondary walls, nuclei, cuticle and polyphenols; Hematoxylin-Alcian blue to enhance nuclei and primary walls and Phloroglucinol-HCl for lignin. Observations and photographic records were done with a photonic microscope. For the observations and descriptions with scanning electron microscopy (SEM), the sori were dehydrated with 2,2-dimethoxypropane, critical point dried and coated with gold. Results: The sori are exindusiate, superficial, vascularized and have mixed development; they are associated with uniseriate and multicellular receptacle paraphyses. During the development of the sori, the epidermal cells of the receptacle that will form the sporangia are the first differentiated followed by those forming the receptacle paraphyses. The sporangium is leptosporangiate, with long stalks formed by one or two cell rows. The annulus of the sporangia displays secondary walls with U-shaped thickenings rich in lignin. The meiosis is simultaneous and the spore tetrads are arranged in a decussate or tetragonal shape. The cellular tapetum is initially unistratified but becomes bistratified after a periclinal division. The cells of the internal strata of the cellular tapetum loose structural integrity giving rise to a plasmodial tapetum that invades the meiotic sporocytes. During the sporoderm development, the sporopollenin-composed exospore is the first formed followed by the endospore, composed by cellulose, pectin and carboxylated polysaccharides; the process ends with the perispore. Polyphenols were mainly detected on vacuoles in cells of the sporangium, paraphysis and receptacle. When the time comes for the spore maturation, the remnants of cellular and the plasmodial tapeta have fully degenerated. Abundant orbicles are seen near the spores in the sporangial cavity. Conclusions: The ontogeny of the sporangia and sporogenesis of P. scolopendria are similar to the previously described for leptosporangiate ferns. Furthermore, in P. scolopendria, the receptacle paraphyses of the sori have a role protecting the sporangium during the early development stages.
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References
Bosman, M.T.M. (1991). A monograph of the fern genus Microsorum (Polypodiaceae) including an attempt towards a reconstruction of the phylogenetic history of the microsoroids. Leiden Botanical Series, 14(1), 1-161.
Bostock, P.D., & Spokes, T.M. (1998). Polypodiaceae. In P.M. McCarthy (ed.), Flora of Australia (Vol. 48, pp. 66-84). Melbourne, Australia: BRS and CSIRO.
Bowen, W., & Williams, D. (1977). Development of sporangia in Polypodium aureum var. undulatum: Initial scanning electron microscopical observations. Arkansas Academy of Science Proceedings, 31, 26-28.
Bower, F.O. (1963). The ferns (Filicales). Vols. I-III Reprint edn. New Delhi, India: Today and Tomorrow's Book Agency.
Brown, R.C., & Lemmon, B.E. (2001a). Sporogenesis in eusporangiate ferns: I. Monoplastidic meiosis in Angiopteris (Marattiales). Journal of Plant Research, 114(3), 223-23. DOI: https://doi.org/10.1007/PL00013986
Brown, R.C., & Lemmon, B.E. (2001b). Sporogenesis in eusporangiate ferns: II. Polyplastidic meiosis in Ophioglossum (Ophioglossales). Journal of Plant Research, 114(3), 237-246. DOI: https://doi.org/10.1007/PL00013987
Churchill, H., Tryon, R., & Barrington, D.S. (1998). Development of the sorus in tree ferns: Dicksoniaceae. Canadian Journal of Botany, 76, 1245-1252. DOI: https://doi.org/10.1139/b98-122
Christenhusz, M., Zhang, X.C., & Schneider, H. (2011). A linear sequence of extant families and genera of lycophytes and ferns. Phytotaxa, 19, 7-54. DOI: https://doi.org/10.11646/phytotaxa.19.1.2
Demarco, D. (2017). Histochemical analysis of plant secretory structures. En C. Pellicciari & M. Biggiogera (Eds.), Histochemistry of single molecules methods and protocols (pp. 313-330). New York, U.S.A.: Humana Press. DOI: https://doi.org/10.1007/978-1-4939-6788-9_24
Furness, C.A., Rudall, J.P., & Sampson, F.B. (2002). Evolution of microsporogenesis in angiosperms. International Journal of Plant Science, 163(2), 35-260. DOI: https://doi.org/10.1086/338322
Gabarayeva, N.I., Grigorjeva, V.V., & Márquez, G. (2011). Ultrastructure and development during meiosis and the tetrad period of sporogenesis in the leptosporangiate fern Alsophila setosa (Cyatheaceae) compared with corresponding stages in Psilotum nudum (Psilotaceae). Grana, 50, 235-261. DOI: https://doi.org/10.1080/00173134.2011.631759
Gifford, M.E., & Foster, S.A. (1989). Morphology and evolution of vascular plants. New York, U.S.A.: W. H. Freeman and Company.
González, G.E., Prada, C., & Rolleri, C.H. (2010). Nuevo recuento cromosómico para Blechnum hastatum (Blechnaceae-Pteridophyta), con un estudio de la ontogenia y tipos de leptoporangios adultos. Gayana Botanica, 67(1), 52-64. DOI: https://doi.org/10.4067/S0717-66432010000100006
Hennipman, E., Veldhoen, P., & Kramer, K.U. (1990). Polypodiaceae. En K.U. Kramer & P.S. Green (Eds.), The Families and Genera of Vascular Plants. I Pteridophytes and Gymnosperms (pp. 203-230). Berlin, Germany: Springer-Verlag. DOI: https://doi.org/10.1007/978-3-662-02604-5_41
Kreier, H.P., Zhang, X.C., Muth, H., & Schneider, H. (2008). The microsoroid ferns: Inferring the relationships of a highly diverse lineage of paleotropical epiphytic ferns (Polypodiaceae, Polypodiopsida). Molecular Phylogenetics and Evolution, 48(3), 1155-1167. DOI: https://doi.org/10.1016/j.ympev.2008.05.001
Kulbat, K. (2016). The role of phenolic compounds in plant resistance. Biotechnology and Food Science, 80(2), 97-108.
Kumar, K. (2001). Reproductive Biology of Pteridophytes. En B.M. Johri & P.S. Srivastava (Eds.), Reproductive Biology of Plants (pp. 175-214). New York, U.S.A.: Springer-Verlag. DOI: https://doi.org/10.1007/978-3-642-50133-3_9
Lattanzio, V., Lattanzio, M.T.V., & Cardinali, A. (2006). Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. En F. Imperato (Ed.), Phytochemistry: advances in research (pp. 23-67). Trivandrum, India: Research Signpost.
Lellinger, D.B. (2002). A modern multilingual glossary for taxonomic pteridology. Pteridologia, 3, 1-263. DOI: https://doi.org/10.5962/bhl.title.124209
Lehmann, H., Neidhart, K.M., & Schlenkermann, G. (1984). Ultrastructural investigations on sporogenesis in Equisetum fluviatile. Protoplasma, 123(1), 38-47. DOI: https://doi.org/10.1007/BF01283180
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. DOI: https://doi.org/10.1002/j.1537-2197.1977.tb11898.x
Lugardon, B. (1990). Pteridophyte sporogenesis: a survey of spore wall ontogeny and fine structure in a polyphyletic plant group. En S. Blackmore & R.B. Knox (Eds.), Microspores: evolution and ontogeny (pp. 95-120). London, England: Academic Press. DOI: https://doi.org/10.1016/B978-0-12-103458-0.50008-0
Morbelli, M.A. (1995). Megaspore wall in Lycophyta ultrastructure and function. Review of Palaeobotany and Palynology, 85, 1-12. DOI: https://doi.org/10.1016/0034-6667(94)00089-3
Nitta, J.H., Amer, S., & Davis, C.C. (2018). Microsorum × tohieaense (Polypodiaceae), a new hybrid fern from French Polynesia, with implications for the taxonomy of Microsorum. Systematic Botany, 43(2), 397-413. DOI: https://doi.org/10.1600/036364418X697166
Nooteboom, H.P. (1997). The microsoroid ferns (Polypodiaceae). Blumea, 42(2), 261-395.
Pacini, E. & Franchi, G.G. (1993). Role of the tapetum in pollen and spore dispersal. Plant Systematics and Evolution, 7, 1-11. DOI: https://doi.org/10.1007/978-3-7091-6661-1_1
Pal, N., & Pal, S. (1963). Studies on morphology and affinity of the Parkeriaceae. II. Sporo-genesis, development of the gametophyte, and cytology of Ceratopteris thalictroides. Botanical Gazette, 124, 405-412. DOI: https://doi.org/10.1086/336226
Parkinson, B.M. (1987). Tapetal organization during sporogenesis in Psilotum nudum. Annals of Botany, 60, 353-360. DOI: 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 Botany, 73, 1867-1877. DOI: https://doi.org/10.1139/b95-199
Parkinson, B.M., & Pacini, E. (1995). A comparison of tapetal structure and function in pteridophytes and angiosperms. Plant Systematics and Evolution, 198, 55-88. DOI: https://doi.org/10.1007/BF00985107
Passarelli, L.M., Gabriel, J.G., Prada, C., & Rolleri, C.H. (2010). Spore morphology and ornamentation in the genus Blechnum (Blechnaceae). Grana, 49(4), 243-262. DOI: https://doi.org/10.1080/00173134.2010.524245
Peterson, R.L., & Kott, L.S. (1974). The sorus of Polypodium virginianum: some aspects of the development and structure of paraphyses and sporangia. Canadian Journal of Botany, 52, 2283-2288. DOI: https://doi.org/10.1139/b74-297
Petchsri, S., & Boonkerd, T. (2014). The genera Microsorum and Phymatosorus (Polypodiaceae) in Thailand. Tropical Natural History, 14(2), 45-74. DOI: https://doi.org/10.58837/tnh.14.2.103021
PPG I. (2016). A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution, 54, 563-603. DOI: https://doi.org/10.1111/jse.12229
Possley, J., & Howell, P.L. (2015). Misidentification of "Microsorum scolopendria" in South Florida. American Fern Journal, 105(2), 127-130. DOI: https://doi.org/10.1640/amfj-105-02-127-130.1
Punt, W., Hoen, P.P., Blackmore, S., Nilsson, S., & Le Thomas, A. (2007). Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology, 143(1-2), 1-83. DOI: https://doi.org/10.1016/j.revpalbo.2006.06.008
Qiu, Y.J., White, R.A., & Turner, M.D. (1995). The developmental anatomy of Metaxya rostrata (Filicales: Metaxyaceae). American Journal of Botany, 82(8), 969-981. DOI: https://doi.org/10.1002/j.1537-2197.1995.tb11561.x
Rincón, B.E.J., Forero, B.H.G., Gélvez, L.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.
Rincón, B.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. DOI: https://doi.org/10.15517/rbt.v61i3.11786
Rincón, B.E.J., Rolleri, C.H., Alzate, G.F., & Dorado, G.J.M. (2014a). Ontogenia de los esporangios, formación y citoquímica de esporas en licopodios (Lycopodiaceae) colombianos. Revista de Biología Tropical, 62(1), 273-298. DOI: https://doi.org/10.15517/rbt.v62i1.9795
Rincón, B.E.J., Rolleri, C.H., Passarelli, M.L., Espinosa, M.S., & Torres, G.A.M. (2014b). Esporogénesis, esporodermo y ornamentación de esporas maduras en Lycopodiaceae. Revista de Biología Tropical, 62(3), 1161-1195. DOI: https://doi.org/10.15517/rbt.v62i3.12330
Rincón, B.E.J., Guerra, S.B.H., Restrepo, Z.D.E. & Espinosa, M.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. DOI: https://doi.org/10.15517/rbt.v67i6.36984
Ruzin, S.E. (1999). Plant microtechnique and microscopy. New York, U.S.A.: Oxford University.
Schölch., A. (2003). Relations between submarginal and marginal sori in ferns III. Superficial sori with emphasis on Pteridaceae and morphological relations to marginal sori. Plant Systematics and Evolution, 240, 21-233. DOI: https://doi.org/10.1007/s00606-003-0023-0
Sessa, B.E. (2018). Evolution and classification of ferns and Lycophytes. En H. Fernández (Ed.), Current advances in fern research (pp. 179-200). Cham, Switzerland: Springer. DOI: https://doi.org/10.1007/978-3-319-75103-0_9
Sheffield, E., & Bell, P.R. (1979). Ultrastructural aspects of sporogenesis in a fern, Pteridium aquilinum (L.) Kuhn. Annals of Botany, 44, 393-405. DOI: https://doi.org/10.1093/oxfordjournals.aob.a085748
Sheffield, E., Laird, S., & Bell, P.R. (1983). Ultrastructural aspects of sporogenesis in the apogamous fern Dryopteris borreri. Journal of Cell Science, 63, 125-134. DOI: https://doi.org/10.1242/jcs.63.1.125
Smith, A.R., Pryer, K.M., Schuettpelz, E., Korall, P., Schneider, H., & Wolf, P.G. (2006). A classification for extant ferns. Taxon, 55(3), 705-731. DOI: https://doi.org/10.2307/25065646
Soukup, A. (2014). Selected simple methods of plant cell wall histochemistry and staining for light microscopy. En V. Žárský, & F. Cvrčková (Eds.), Plant cell morphogenesis: methods and protocols, methods in molecular biology (pp. 25-40). New York, U.S.A.: Humana Press. DOI: https://doi.org/10.1007/978-1-62703-643-6_2
Tejero-Díez, J.D., & Torres-Díaz, A.N. (2012). Phymatosorus grossus (Polypodiaceae) en México y comentarios sobre otros pteridobiontes no-nativos. Acta Botánica Mexicana, 98, 111-124. DOI: https://doi.org/10.21829/abm98.2012.1143
Testo, W.L., Field, A.R., Sessa, E.B., & Sundue, M. (2019). Phylogenetic and morphological analyses support the resurrection of Dendroconche and the recognition of two new genera in Polypodiaceae subfamily Microsoroideae. Systematic Botany, 44(4), 1-16. DOI: https://doi.org/10.1600/036364419X15650157948607
Testo, W. & Sundue, M. (2016). A 4000-species dataset provides new insight into the evolution of ferns. Molecular Phylogenetics and Evolution, 105, 200-211. DOI: https://doi.org/10.1016/j.ympev.2016.09.003
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, R.M., & Tryon, A.F. (1982). Ferns and allied plants, with special reference to tropical America. New York, U.S.A.: Springer. DOI: https://doi.org/10.1007/978-1-4613-8162-4
Tryon, A.F., & Lugardon, B. (1991). Spores of the Pteridophyta: surface, wall structure, and diversity based on electron microscope studies. Nueva York, U.S.A.: Springer. DOI: https://doi.org/10.1007/978-1-4613-8991-0
Uehara, K., & Kurita, S. (1989). An ultrastructural study of spore wall morphogenesis in Equisetum arvense. American Journal of Botany, 76(7), 939-951. DOI: https://doi.org/10.1002/j.1537-2197.1989.tb15074.x
Uehara, K. & Kurita, S. (1991). Ultrastructural study on spore wall morphogenesis in Lycopodium clavatum (Lycopodiaceae). American Journal Botany, 78(1), 24-36. DOI: https://doi.org/10.1002/j.1537-2197.1991.tb12568.x
Uehara, K., Kurita, S., Sahashi, N., & Ohmoto, T. (1991). Ultrastructural study of microspore wall morphogenesis in Isoëtes japonica (Isoëtaceae). American Journal of Botany, 78, 1182-1190. DOI: https://doi.org/10.1002/j.1537-2197.1991.tb11411.x
Van Uffelen, G.A. (1990). Sporogenesis in Polypodiaceae (Filicales). I. Drynaria sparsisora (Desv.) Moore. Blumea, 35, 177-215.
Van Uffelen, G.A. (1992). Sporogenesis in Polypodiaceae (Filicales). II. The genera Microgramma Presl and Belvisia Mirbel. Blumea, 36, 515-540.
Van Uffelen, G.A. (1993). Sporogenesis in Polypodiaceae (Filicales). III. Species of several genera. Spore characters and their value in phylogenetic analysis. Blumea, 37, 529-561.
Wellman, C.H. (2004). Origin, function and development of the spore wall in early land plants. En A.R. Hemsley & I. Pole (Eds.), The evolution of plant physiology (pp. 43-63). Linnean Society Symposium, Number 21. San Diego, U.S.A.: Academic Press. DOI: https://doi.org/10.1016/B978-012339552-8/50004-4
Wilson, K.A. (1958). Ontogeny of the sporangium of Phlebodium (Polypodium) aureum. American Journal of Botany, 45(6), 483-491. DOI: https://doi.org/10.1002/j.1537-2197.1958.tb13155.x
Yeung, E.C.T., Stasolla, C., Sumner, M.J., & Huang, B.Q. (2015). Plant microtechniques and protocols. New York, U.S.A.: Springer. DOI: https://doi.org/10.1007/978-3-319-19944-3
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