Keywords
microspore;
palynology;
pollen ontogeny;
Rosaceae;
sporodermis;
tapetum
esporodermis;
microspora;
mora;
ontogenia del polen;
palinología;
Rosaceae;
tapete
How to Cite
Abstract
Introduction: Studies on the microsporogenesis of Rubus glaucus are non-existent and little is known about the ultrastructure of the pollen grains. Objectives: To describe the microsporogenesis process, and ultrastructural aspects of the pollen grains in Rubus glaucus. Methods: Flowers at different developmental stages were embedded in paraffin. Sections were stained with Safranin-Alcian Blue, PAS-Amidoblack and Lacmoid or included in resin and stained with toluidine blue. Ultrathin sections were examined by transmission electron microscopy (TEM). For scanning electron microscopy (SEM) observation, the material was fixed and dehydrated in 2.2 dimethoxypropane, then with Hexamethyldisilazane (HMDS), and the samples were coated with gold. Results: Anthers are differentiated by a cellular mass at the ends distal to the staminal filaments. During development, the anther wall presents several cellular layers and at maturity, they are reduced to the epidermis and the endothecium. Microsporocytes undergo simultaneous meiosis and form tetrahedral tetrads. The tapetum develops secretory activity until pollen grains are released, then the cellular content undergoes autolysis. During sporodermis formation, the exine is first deposited and then the intine in a centripetal form. The pollen grains are tricolporate, isopolar, oblate to peroblate, with radial simetry, circular in outline with blunt apices in polar view, ellipsoidal in equatorial view. The exine is thick, tectated, striate perforate. The sporodermis presents an ectexine formed by a tectum interrupted by perforations and thick columellae. Colpus membrane presents small exine granules and orbicules on the surface. The intine develops known structural patterns. Pollenkitt is inconspicuous. Conclusion: Anthers structure and development follows the known patterns of angiosperms. Simultaneous microsporogenesis and centripetal deposition of the sporodermis, as well as ornamentation patterns, have been previously described for the Rosaceae Family.
References
Akšić, M. F., Cerović, R., Ercişli, S., & Jensen, M. (2016). Microsporogenesis and meiotic abnormalities in different ‘Oblačinska’sour cherry (Prunus cerasus L.) clones. Flora, 219, 25–34.
Alice, L. A., & Campbell, C. S. (1999). Phylogeny of Rubus (Rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. American Journal of Botany, 86(1), 81–97.
Alice, L. A., Goldman, D. H., Macklin, J. A., Moore, G. (2014). Rubus. En: Flora of North America Editorial Committee (Ed.), Flora of North America north of Mexico (Vol. 9, pp 28–56). Oxford University Press.
The Angiosperm Phylogeny Group, Chase, M. W., Christenhusz, M. J., Fay, M. F., Byng, J. W., Judd, W. S., Soltis, D. E., Mabberley, D. J., Sennikov, A. N., Soltis, P. S., & Stevens, P.F. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181(1), 1–20.
Araque-Castellanos, D., Cancino-Escalante, G., Hernandez-Contreras, D. A., & Chinchilla-Cárdenas, D. (2021). Diversidad genética de Rubus glaucus Benth en el municipio de Pamplona (nororiente de Colombia). BISTUA Revista de la Facultad de Ciencias Básicas, 19(2), 8–14.
Aronne, G., Iovane, M., & Strumia, S. (2021). Temperature and humidity affect pollen viability and may trigger distyly disruption in threatened species. Annali Di Botanica, 11, 77–82.
Arozarena, I., Ortiz, J., Hermosín-Gutiérrez, I., Urretavizcaya, I., Salvatierra, S., Córdova, I., & Navarro, M. (2012). Color, ellagitannins, anthocyanins, and antioxidant activity of Andean blackberry (Rubus glaucus Benth.) wines. Journal of Agricultural and Food Chemistry, 60, 7463−7473.
Åstrand, J., Knight, C., Robson, J., Talle, B., & Wilson, Z. A. (2021). Evolution and diversity of the angiosperm anther: trends in function and development. Plant reproduction, 34(4), 307–319.
Bayer, C., & Kubitzki, K. (2003). Malvaceae. En K. Kubitzki (Ed.), The families and genera of vascular plants (pp. 225–31). Springer-Verlag.
Bhojvani, S. S., & Soh W. Y. (2010). Current trends in the embryology of Angiosperms. Springer.
Blackmore, S., Wortley, A. H., Skvarla, J. J., & Rowley, J. R. (2007). Pollen wall development in flowering plants. New Phytologist, 174(3), 483–498.
Bolaños, M. M., Cardona, W. A., García, M. C., Zapata, Y. A., Beltrán, C. R., Vásquez, R. E., Martínez, E. P., Clímaco, J., Ortega, N. C., Peña, A. C., Bautista, L. G., & López, D. A. (2020). Mora (Rubus glaucus Benth.): Manual de recomendaciones técnicas para su cultivo en el departamento de Cundinamarca. Corredor Tecnológico Agroindustrial CTA-2.
Cancino-Escalante, G. O., Sánchez-Montaño, L. R., Quevedo-García, E., & Díaz-Carvajal, C. (2011). Caracterización fenotípica de accesiones de especies de Rubus L. de los municipios de Pamplona y Chitagá, región Nororiental de Colombia. Universitas Scientiarum, 16(3), 219–233.
Carter, K. A., Liston, A., Bassil, N. V., Alice, L. A., Bushakra, J. M., Sutherland, B. L., Mockler, T. C., Bryant, D. W., & Hummer, K. E. (2019). Target capture sequencing unravels Rubus evolution. Frontiers in plant science, 10, 1–18.
Çetinbaş, A., & Ünal, M. (2015). Developmental and Cytochemical Features of Male Reproductive Organ in Crataegus tanacetifolia (Lam.) Pers. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 43(2), 507–514.
Chissoe, W. F., Vezey, E. L., & Skvarla, J. J. (1994). Hexamethyldisilazane as a drying agent for pollen scanning electron microscopy. Biotechnic & Histochemistry, 69(4), 192–198.
Clark, L. V., & Jasieniuk, M. (2012). Spontaneous hybrids between native and exotic Rubus in the Western United States produce offspring both by apomixis and by sexual recombination. Heredity, 109(5), 320–328.
Crang, R., Lyons-Sobaski, S., & Wise, R. (2018). Plant Anatomy: A Concept-Based Approach to the Structure of Seed Plants. Springer.
Davis, G. L. (1966). Systematic embryology of the angiosperms. John Wiley & Sons Inc.
De Storme, N., & Geelen, D. (2014). The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant, cell & environment, 37(1), 1–18.
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). Humana Press.
Dolferus, R., Ji, X., & Richards, R. A. (2011). Abiotic stress and control of grain number in cereals. Plant science, 181(4), 331–341.
Doyle, J. (2005). Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana, 44, 227–25.
Eide, F. Y. (1981). Key for northwest european rosaceae pollen. Grana, 20(2), 101–118.
Erdtman, G. (1969). Handbook of Palynology: An introduction to the study of pollen grains and spores. Munksgaard, Copenhagen.
Espinosa, B. N., Ligarreto, M. G. A., Barrero, M. L. S., & Medina, C. C. I. (2016). Variabilidad morfológica de variedades nativas de mora (Rubus sp.) en los Andes de Colombia. Revista Colombiana de Ciencias Hortícolas, 10(2), 211–221.
Fadón, E., Herrero, M., & Rodrigo, J. (2019). Anther and pollen development in sweet cherry (Prunus avium L.) in relation to winter dormancy. Protoplasma, 256, 733–744.
Feng, Y., Cai, Y., Zhang, X., Gao, T., Mu, X., & Liang, C. (2016). Microsporogenesis and male gametophyte development in Prunus mahaleb Linn. The Journal of Horticultural Science and Biotechnology, 91(5), 514–519.
Fernández, G. J., Talle, B., & Wilson, Z. A. (2015). Anther and pollen development: a conserved developmental pathway. Journal of Integrative Plant Biology, 57(11), 876–891.
Focke, W. O. (1910). Species Ruborum: Monographiae Generis Rubi Prodromus (Pars I). Bibliotheca Botanica.
Focke, W. O. (1911) Species Ruborum, Monographiae Generis Rubi Prodromus (Pars II). Bibliotheca Botanica.
Focke, W. O. (1914) Species Ruborum, Monographiae Generis Rubi Prodromus (Pars III). Bibliotheca Botanica.
Foster, T. M., Bassil, N.V., Dossett, M., Leigh Worthington, M., & Graham, J. (2019). Genetic and genomic resources for Rubus breeding: A roadmap for the future. Horticulture research, 6, 1–9.
Franco, G., & Bernal, J. A. (Comps.) (2020). Tecnología para el cultivo de la mora (Rubus glaucus Benth.). Corporación Colombiana de Investigación Agropecuaria AGROSAVIA.
Furness, C. A., Rudall, P. J., & Sampson, F. B. (2002). Evolution of microsporogenesis in angiosperms. International Journal of Plant Sciences, 163(2), 235–260.
Furness, C. A., & Rudall, P. J. (2004). Pollen aperture evolution–a crucial factor for eudicot success? Trends in Plant Science, 9(3), 154–158.
Galati, B. G. (2003). Ubisch bodies in Angiosperms. En A. K. Pandey & M. R. Dhakal (Eds.), Advances in Plant Reproductive Biology, Vol. II (pp. 1–21). Narendra Publishing House.
Galati, C., & Strittmatter, L. I. (1999). Correlation between pollen development and Ubisch bodies ontogeny in Jacaranda mimosifolia (Bignoniaceae). Beitrage zur Biologie der Pflanzen, 71(2), 249–260.
Garzón, G. A., Riedl, K. M., & Schwartz, S. J. (2009). Determination of anthocyanins, total phenolic content, and antioxidant activity in Andes berry (Rubus glaucus Benth). Journal of food science, 74(3), 227–232.
Graham, J., & Brennan, R. (2018). Introduction to the Rubus Genus. En Graham, J. & Brennan, R. (Eds.), Raspberry: breeding, challenges and advances (pp. 1–16). Springer.
Hajnal, V., Omid, Z., Ladanyi, M., Tóth, M., & Szalay, L. (2013). Microsporogenesis of Apricot Cultivars in Hungary. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 41(2), 434–439.
Halbritter, H., Ulrich, S., Grimsson, F., Weber, M., Zetter, R., Hesse, M., Buchner, R., Svojtka, M., & Frosch-Radivo, A. (2018). Illustrated pollen terminology (2nd Ed.). Springer.
Hanchana, K., Saensouk, S. & Saensouk, P. (2023). Pollen morphology and anatomy of Rubus L. (Rosaceae) in Thailand. Notulae Botanicae, Horti Agrobotanici, Cluj-Napoca, 51(1), 1–41.
Hebda, R. J. & Chinnappa, C. C. (1990). Studies on pollen morphology of Rosaceae in Canada. Review of Palaeobotany and Palynology, 64(1-4), 103–108.
Hebda, R. J., & Chinnappa, C. C. (1994). Studies on pollen morphology of Rosaceae. Acta Botanica Gallica, 141(2), 183–193.
Hedhly, A. (2011). Sensitivity of flowering plant gametophytes to temperature fluctuations. Environmental and Experimental Botany, 74, 9–16.
Hickey, L. J., & Wolfe, J. A. (1975). The bases of angiosperm phylogeny: vegetative morphology. Annals of the Missouri Botanical Garden, 62(3), 538–589.
Hummer, K. E. (2017). Blackberries: An introduction. En H. K. Hall & R. C. Funt (Eds), Blackberries and their hybrids (pp. 1–16). CAB International.
Iovane, M., & Aronne, G. (2022). High temperatures during microsporogenesis fatally shorten pollen lifespan. Plant Reproduction, 35, 9–17.
Julian, C., Rodrigo, J., & Herrero, M. (2011). Stamen development and winter dormancy in apricot (Prunus armeniaca). Annals of Botany, 108(4), 617–625.
Konzmann, S., Koethe, S., & Lunau, K. (2019). Pollen grain morphology is not exclusively responsible for pollen collectability in bumble bees. Scientific Reports, 9(1), 1–8.
Kostryco, M., & Chwil, M. (2021). Structure of anther epidermis and endothecium, production of pollen, and content of selected nutrients in pollen grains from six Rubus idaeus L. cultivars. Agronomy, 11(9), 1–44.
Kostryco, M., Chwil, M., & Matraszek-Gawron, R. (2020). Comparison of the micromorphology and ultrastructure of pollen grains of selected Rubus idaeus L. cultivars grown in commercial plantation. Plants, 9(9), 1–31.
Kumar, B., Smita, K., Cumbal, L., Debut, A., & Angulo, Y. (2017). Biofabrication of copper oxide nanoparticles using Andean blackberry (Rubus glaucus Benth.) fruit and leaf. Journal of Saudi Chemical Society, 21 (Supplement 1), 475–480.
Lechowicz, K., Bocianowski, J., & Wrońska-Pilarek, D. (2021). Pollen morphology and variability of species from the genus Rubus L. (Rosaceae) alien and invasive in Poland. Journal of Plant Taxonomy and Geography, 76(1), 109–121.
Lechowicz, K., Bocianowski, J., & Wrońska-Pilarsk, D. (2022). Pollen morphological Inter-and intraspecific variability in selected species of Rubus L. (Rosaceae). Forests, 13(11), 1–26.
Lechowicz, K., Wrońska-Pilarek, D., Bocianowski, J., & Maliński, T. (2020). Pollen morphology of Polish species from the genus Rubus L. (Rosaceae) and its systematic importance. Plos one, 15(5), 1–23.
López, G. A. M., Marulanda, A. M. L., Gómez, L. L. M., & Barrera S. C. F. (2019). Rubus glaucus Benth.: morphology and floral biology aimed at plant breeding processes. Revista Facultad Nacional de Agronomía Medellín, 72(3), 8909–8915.
Lu, L. T., & Bouford, D. E. (2003). Rubus. En: Wu, Z. Y., Raven P. H. & Hong, D. Y. (Eds) Flora of China, vol. 9 (pp 195–285). Science Press.
Mertz, C., Cheynier, V., Günata, Z., & Brat, P. (2007). Analysis of phenolic compounds in two blackberry species (Rubus glaucus and Rubus adenotrichus) by high-performance liquid chromatography with diode array detection and electrospray ion trap mass spectrometry. Journal of agricultural and food chemistry, 55(21), 8616–8624.
Monasterio-Huelin, E., & Pardo, C. (1995). Pollen morphology and wall stratification in Rubus L. (Rosaceae) in the Iberian Peninsula. Grana, 34, 229–236.
Ontivero, M. R., Radice, S., Giordani, E., & Bellini, E. (2005). Preliminary studies on microsporogenesis in Prunus salicina Lindl. The Journal of Horticultural Science and Biotechnology, 80(5), 599–604.
Osorio, C., Hurtado, N., Dawid, C., Hofmann, T., Heredia-Mira, F. J., & Morales, A. L. (2012). Chemical characterisation of anthocyanins in tamarillo (Solanum betaceum Cav.) and Andes berry (Rubus glaucus Benth.) fruits. Food Chemistry, 132(4), 1915–1921.
Pacini, E. (2010). Relationships between tapetum, loculus, and pollen during development. International Journal of Plant Sciences, 171(1), 1–11.
Pacini, E., & Dolferus, R. (2019). Pollen developmental arrest: maintaining pollen fertility in a world with a changing climate. Frontiers in Plant Science, 10(679), 1–15.
Pacini, E., & Hesse, M. (2005). Pollenkitt-its composition, forms and functions. Flora-Morphology, Distribution, Functional Ecology of Plants, 200(5), 399–415.
Pacini, E., & Hesse, M. (2012). Uncommon pollen walls: reasons and consequences. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Osterreich, 148, 291–306.
Padilla, F., Soria, N., Oleas, A., Rueda, D., Manjunatha, B., Kundapur, R. R., Maddela, N. R., & Rajeswari, B. (2017). The effects of pesticides on morphology, viability, and germination of Blackberry (Rubus glaucus Benth.) and Tree tomato (Solanum betaceum Cav.) pollen grains. Biotech, 7, 1–12.
Potter, D., Eriksson, T., Evans, R. C., Oh, S., Smedmark, J. E. E., Morgan, D. R., Kerr, M., Robertson K. R., Arsenault, M., Dickinson, T. A., & Campbell, C. S. (2007). Phylogeny and classification of Rosaceae. Plant systematics and evolution, 266, 5–43.
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.
Radice, S., & Galati, B. (2006). Development of pollen grains in Forastero peach cultivar (Prunus persica Batsch). Advances in Horticultural Science, 20(4), 275–280.
Rahmani, H., Ahmad, M., Sedigheh, A., Fariba, S., & Sedigheh, M. (2012). A study of microsporogenesis and pollen morphology in Crataegus babakhanloui (Rosaceae). Advances in Environmental Biology, 6(11), 2986–2991.
Ramírez, F. (2023). Latin American Blackberries Biology: Mora de Castilla (Rubus glaucus Benth.) Vol 1. Springer Nature.
Rincón-Barón, E. J., Grisales, E. C., Cuaran, V. L., & Cardona, N. L. (2020). Alteraciones anatómicas e histoquímicas ocasionadas por la oidiosis en hojas de Hydrangea macrophylla (Hydrangeaceae). Revista de Biología Tropical, 68(3), 959–976.
Rincón-Barón, E. J., Torres-Rodríguez, G. A., Cuarán, V. L., Carreño-Olejua, R., & Passarelli, L. M. (2023). Microsporogénesis y ultraestructura de los granos de polen en la planta del cacao, Theobroma cacao (Malvaceae). Revista de Biología Tropical, 71(1), 1–13.
Rincón-Barón, E. J., Torres-Rodríguez, G. A., Passarelli, L. M., Zárate, D. A., Cuarán, V. L., & Plata-Arboleda, S. (2021b). Microsporogénesis y micromorfología del polen de la planta Alcea rosea (Malvaceae). Revista de Biología Tropical, 69(3), 852–864.
Rincón-Barón, E. J., Zarate, D. A., Castañeda, G. A. A., Cuarán, V. L., & Passarelli, L. M. (2021a). Micromorfología y ultraestructura de las anteras y los granos de polen en diez genotipos élite de Theobroma cacao (Malvaceae). Revista de Biología Tropical, 69(2), 403–421.
Rosbakh, S., Pacini, E., Nepi, M., & Poschlod, P. (2018). An unexplored side of regeneration niche: seed quantity and quality are determined by the effect of temperature on pollen performance. Frontiers in Plant Science, 9, (1036), 1–17.
Ruggiero, F., & Bedini, G. (2020). Phylogenetic and morphologic survey of orbicules in angiosperms. Taxon, 69(3), 543–566.
Ruzin, S. E. (1999). Plant microtechnique and microscopy. Oxford University.
Samaniego, I., Brito, B., Viera, W., Cabrera, A., Llerena, W., Kannangara, T., Vilcacundo, R., Angós, I., & Carrillo, W. (2020). Influence of the maturity stage on the phytochemical composition and the antioxidant activity of four Andean blackberry cultivars (Rubus glaucus Benth) from Ecuador. Plants, 9(8), 1–16.
Song, J. H., Moon, H. K., & Hong, S. P. (2016). Pollen morphology of the tribe Sorbarieae (Rosaceae). Plant Systematics and Evolution, 302, 853–869.
Song, J. H., Oak, M. K., Roh, H. S., & Hong, S. P. (2017). Morphology of pollen and orbicules in the tribe Spiraeeae (Rosaceae) and its systematic implications. Grana, 56(5), 351–367.
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). Humana Press.
Sumner, M. J., & Remphrey, W. R. (2005). Microsporogenesis in Amelanchier alnifolia: sporogenous cells, microsporocytes, and tetrads. Botany, 83(9), 1106–1116.
Szalay, L., Timon, B., Szabó, Z., & Papp, J. (2002). Microsporogenesis of peach (Prunus persica L. Batsch) varieties. International Journal of Horticultural Science, 8(3–4), 7–10.
Thakur, P., Kumar, S., Malik, J. A., Berger, J. D., & Nayyar, H. (2010). Cold stress effects on reproductive development in grain crops: an overview. Environmental and Experimental Botany, 67(3), 429–443.
Tomlik-Wyremblewska, A., Van Der Ham, R. W. & Kosinski, P. (2004). Pollen morphology of genus Rubus L. Part III. Studies on the Malesian species of subgenera Chamaebatus L. and Idaeobatus L. Acta societatis botanicorum Poloniae, 73(3), 207–227.
Verstraete, B., Moon, H. K., Smets, E., & Huysmans, S. (2014). Orbicules in flowering plants: a phylogenetic perspective on their form and function. The Botanical Review, 80(2), 107–134.
Wang, Y., Chen, Q., Chen, T., Tang, H., Liu, L., & Wang, X. (2016). Phylogenetic insights into Chinese Rubus (Rosaceae) from multiple chloroplast and nuclear DNAs. Frontiers in plant science, 7, 1–13.
Watson, L., & Dallwitz, M. J. (1991). The families of angiosperms: automated descriptions, with interactive identification and information retrieval. Australian Systematic Botany, 4(4), 681–695.
Weber, H. E. (1996). Former and modern taxonomic treatment of the apomictic Rubus complex. Folia Geobotanica, 31, 373–380.
Wrońska-Pilarek, D., Jagodzińsk, A. M., Malińsk, T. (2012). Morphological studies of pollen grains of the Polish endemic species of the genus Rubus (Rosaceae) Biologia, 67(1), 87–96.
Xiong, X. H., Zhou, X. M., Li, M., Xu, B., Deng, H. N., Yu, Q., & Gao, X. F. (2019). Pollen morphology in Rubus (Rosaceae) and its taxonomic implications. Plant Systematics and Evolution, 305, 705–716.
Ye, Z., Su, M., Li, L., & Zhang, S. (2010). Effects of high temperature on the microsporogenesis and pollen development of peach. Acta Horticulturae Sinica, 37(3), 355–362.
Zini, L. M., Galati, B. G., Zarlavsky, G., & Ferrucci, M. S. (2017). Developmental and ultrastructural characters of the pollen grains and tapetum in species of Nymphaea subgenus Hydrocallis. Protoplasma, 254, 1777–1790.
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