Keywords
microornamentation
sporopollenin
histochemistry
palynology
pollenkitt
cacao
microornamentación
esporopolenina
histoquímica
palinología
polenkit
How to Cite
Abstract
Introduction: Despite the fact that T. cacao is an important species worldwide for cocoa production, little is known about the micromorphology and structure of anthers and pollen grains. Objectives: To describe and analyze the structure and micromorphology of the anthers and pollen grains of 10 elite genotypes of this important tropical species. Methods: More than 30 anthers of flowers in anthesis were taken of the 10 elite genotypes of T. cacao from the ex situ germplasm bank of the Suiza-Agrosavia Research Center (Rionegro, Santander-Colombia). The anthers with the pollen grains were fixated and processed according to the standard protocols for embedding and sectioning in paraffin. Sections obtained (3 μm thick) were stained with Safranin-Alcian blue to discriminate structures with primary and secondary walls and total polyphenols. Additionally, the samples were also stained with the PAS-Amidoblack technique was used to differentiate between structural and reserve polysaccharides as well as proteins. Toluidine blue staining was used for the determination of sporopollenin and polyphenols and finally Alcian blue-PAS-Hematoxylin staining was applied for additional descriptions. Observations were made using photonic microscopy and epifluorescence microscopy. For observation with scanning electron microscopy (SEM) the anthers with the pollen grains were fixed and dehydrated in 2.2 Dimethoxypropane, then desiccated to critical point and finally coated with gold. Results: the anthers are dithecal and supported by a long filament made up of an epidermal stratum, parenchymal tissue, and a vascular bundle. The dehiscence occurs longitudinally through the stomium. The anther wall is made up of a monostratified epidermal layer, followed by a layer of endothecial cells with lignified fibrillar thickenings, cellular remnants of tapetum and abundant orbicules can be seen covering the cavity of the microsporangia. The epidermal and parenchymal tissues of the anthers are abundant in polyphenols. Orbicules are generally spherical, psilated, and these exhibit the same staining and fluorescence reactions as exine from pollen grains. The pollen grains are monades, isopolar, small (16-19 µm) with circular amb, spheroidal, tricolpate with medium or short colpi (5-10 µm) with sculptured membrane, semitectate, reticulated, heterobrochate, sculptured or non- sculptured walls, with microgranules of different size or scabrate. The statistical analyzes showed that there are significant differences in the size of the pollen grains (P ˂ 0.05). It is observed that the smallest pollen grains are those of the TCS 19 genotype (16.890 µm) and are different from the other genotypes, and among these there are no significant differences. Only two genotypes (SCC 19 and SCA 6) Observable pollenkitt and only one has perforated walls (SCA 6). Conclusions: The structure and micromorphology of the anthers of T. cacao are similar to those described for other Malvaceae. Likewise, the pollen grains showed variations in size, ornamentation of the sporoderm and the lumen of the reticulum and the presence of pollenkitt. However, no relationship was observed between the micromorphological characters analyzed in the pollen grains and the pollen compatibility models reported for these genotypes.
References
Adjaloo, M.K., & Oduro, W. (2013). Insect assemblage and the pollination system in cocoa ecosystems. Journal of Applied Biosciences, 62, 4582-4594.
Agudelo, C.G.A., Palencia, C.P.G.E., Antolinez, S.E.Y.E., & Báez, D.E.Y. (2017). Nuevas variedades de cacao TCS (Theobroma Corpoica La Suiza) 13 y 19. Colombia: Corporación Colombiana de Investigación Agropecuaria, Minagriculatura. Recuperado de http://hdl.handle.net/20.500.12324/11536
Aime, M.C., & Phillips-Mora, W. (2005). The causal agents of witches’ broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia, 97(5), 1012-1022.
Alean, J., Chejne, F., Ramírez, S., Rincón, E., Alzate-Arbelaez, A.F., & Rojano, B. (2020). Proposal of a method to evaluate the in-situ oxidation of polyphenolic during the cocoa drying. Drying Technology, 1-12. DOI: 10.1080/07373937.2020.1817933
Amirul-Aiman, A.J., Noraini, T., Nurul-Aini, C.A.C., Chung, R., Phupumirat, W., Ruzi, A., ... Suhaniza, R. (2019). Pollen morphology and harmomegathic characters of Byttneria Löfl. Species (Sterculiaceae s.s subfam. Byttnerioideae). Malaysian Applied Biology, 48(3), 19-26.
Aoun, M. (2017). Host defense mechanisms during fungal pathogenesis and how these are overcome in suscepti¬ble plants: A review. International Journal of Botany, 13, 82-102.
Aoun, M., Rioux, D., Simard, M., & Bernier, L. (2009). Fungal colonization and host defense reactions in Ulmus americana callus cultures inoculated with Ophiostoma novo-ulmi. Phytopathology, 99, 642-650.
Baker, H.G. & Baker, I. (1979). Starch in Angiosperm pollen grains and its evolutionary significance. American Journal of Botany, 66(5), 591-600.
Bartley, B.G.D. (2005) The genetic diversity of cacao and its utilization. Wallingford, UK: CABI Publishing.
Bayer, C., Fay, M.F., De bruijn, A.Y., Savolainen, V., Morton, C.M., Kubitzki, K., ... Chase, M.W. (1999). Support for an expanded family concept of Malvaceae within a recircumscribed order Malvales: A combined analysis of plastid atp B and rbc L DNA sequences. Botanical Journal of the Linnean Society, 129(4), 267-303.
Bayer, C., & Kubitzki, K. (2003). Malvaceae. In K. Kubitzki (Ed.), The families and genera of vascular plants (pp. 225-31). Germany: Springer-Verlag.
Beg, M.S., Ahmad, S., Jan, K., & Bashir, K. (2017). Status, supply chain and processing of Cocoa-a review. Trends in Food Science & Technology, 66, 108-116.
Bhattacharjee, R. (2018). Taxonomy and classification of cacao. In P. Umaharan (Ed.), Achieving sustainable cultivation of cocoa (pp. 1-16). London, England: Burleigh Dodds Science Publishing.
Bibi, N., Naveed, A., Manzoor, H., & Ajab, K.M. (2010). Systematic implications of pollen morphology in the family Malvaceae from North West frontier province, Pakistan. Pakistan Journal of Botany, 42, 2205-2214.
Bridgemohan, P., Singh, K., Cazoe, E., Perry, G., Mohamed, A., & Bridgemohan, S.H.R. (2017). Cocoa floral phenology and pollination: Implications for productivity in Caribbean Islands. Journal of Plant Breeding and Crop Science, 9(7), 106-117.
Carrizo, C.C. (2002). An approach to the diversity of endothecial thickenings in Solanaceae. Flora-Morphology, Distribution, Functional Ecology of Plants, 197(3), 214-223.
Corporación Colombiana de Investigación Agropecuaria. (2014a). Clon de Cacao TCS 01: Theobroma Corpoica La Suiza 01. Recuperado de https://repository.agrosavia.co/handle/20.500.12324/34650
Corporación Colombiana de Investigación Agropecuaria. (2014b). Clon de Cacao TCS 06: Theobroma Corpoica La Suiza 06. Recuperado de http://hdl.handle.net/20.500.12324/34651
Counet, C., Ouwerx, C., Rosoux, D., & Collin, S. (2004). Relationship between procyanidin and flavor contents of cocoa liquors from different origins. Journal of Agricultural and Food Chemistry, 52(20), 6243-6249.
Chumacero de Schawe, C.C., Kessler, M., Hensen, I., & Tscharntke, T. (2018). Abundance and diversity of flower visitors on wild and cultivated cacao (Theobroma cacao L.) in Bolivia. Agroforestry Systems, 92(1), 117-125.
Crang, R., Lyons-Sobaski, S., & Wise, R. (2018). Plant Anatomy: A Concept-Based Approach to the Structure of Seed Plants. Cham, Switzerland: Springer.
Dawson, J., Sözen, E., Vizir, I., Van Waeyenberge, S., Wilson, Z.A., & Mulligan, B.J. (1999). Characterization and genetic mapping of a mutation (ms35) which prevents anther dehiscence in Arabidopsis thaliana by affecting secondary wall thickening in the endothecium. New Phytologist, 144(2), 213-222.
de Almeida, A.A., & Valle, R.R. (2010). Cacao: ecophysiology of growth and production. In F. Damatta (Ed.), Ecophysiology of Tropical Tree Crops (pp. 37-70). New York, USA: Nova Science Publishers, Inc. ed. Soil Science Society of America.
de Jesus Branco, S.M., da Silva, D.V., Lopes, U.V., & Corrêa, R.X. (2018). Characterization of the sexual self-and cross-compatibility in genotypes of cacao. American Journal of Plant Sciences, 9(9), 1794-1806.
de Souza, A.P., Moreira, F.L., Sarmento, H.A.D., & da Costa, B.F. (2018). Cacao-Theobroma cacao. In S. Rodrigues, E.S. de Oliveira, & E.S. de Brito (Eds.), Exotic Fruits reference guide (pp. 69-76). London, UK: Academic Press.
Demarco, D. (2017). Histochemical analysis of plant secretory structures. In C. Pellicciari & M. Biggiogera (Eds.), Histochemistry of single molecules methods and protocols (pp. 313-330). New York, USA: Humana Press.
Elwers, S., Zambrano, A., Rohsius, C., & Lieberei, R. (2010). Histological features of phenolic compounds in fine and bulk cocoa seed (Theobroma cacao L.). Journal of Applied Botany and Food Quality, 83(2), 182-188.
Enríquez, G.A. (1985). Curso sobre el cultivo del cacao. Turrialba, Costa Rica: Centro Agronómico Tropical de Investigación y Enseñanza (CATIE).
Erdtman, G. (1986) Pollen Morphology and Plant Taxonomy. Angiosperms. Amsterdam, Netherlands: Brill Verlag.
Ford, C.S., & Wilkinson, M.J. (2012). Confocal observations of late-acting self-incompatibility in Theobroma cacao L. Sexual Plant Reproduction, 25(3), 169-183.
French, J.C. (1985). Patterns of endothecial wall thickenings in Araceae: subfamilies Pothoideae and Monsteroideae. American Journal of Botany, 72(3), 472-486.
Frimpong-Anin, K., Adjaloo, M.K., Kwapong, P.K., & Oduro, W. (2014). Structure and stability of cocoa flowers and their response to pollination. Journal of Botany, 2014, 1-6.
Furness, C.A., & Rudall, P.J. (2001). The tapetum in basal angiosperms: early diversity. International Journal of Plant Sciences, 162(2), 375-392.
Galati, B.G. (2003). Ubisch bodies in Angiosperms. Advance Plant Reproduction Biology, 2, 1-20.
Galati, B.G., Gotelli, M.M., Dolinko, A.E., & Rosenfeldt, S. (2019). Could microechinate orbicules be related to the release of pollen in anemophilous and ‘buzz pollination’species? Australian Journal of Botany, 67(1), 16-35.
Galati, B.G., Gotelli, M.M., Rosenfeldt, S., Torretta, J.P., & Zarlavsky, G. (2011). Orbicules in relation to the pollination modes. In B.J. Kaiser (Ed.), Pollen: structure, y types and effects (pp. 1-15). New York, USA: Nova Science Publisher.
Galati, B.G., Monacci, F., Gotelli, M.M., & Rosenfeldt, S. (2007). Pollen, tapetum and orbicule development in Modiolastrum malvifolium (Malvaceae). Annals of Botany, 99(4), 755-763.
Galati B.G., & Rosenfeldt, S. (1998). The pollen development in Ceiba insignis (Kunth) Gibbs and Semir ex Chorisia speciosa St Hil. (Bombacaceae). Phytomorphology, 48, 121-129.
Gallego, R.A.M., Henao, R.A.M., Urrea, T.A.I., & Atehortua, G.L. (2016). Polyphenols distribution and reserve substances analysis in cacao somatic embryogenesis. Acta Biológica Colombiana, 21(2), 335-345.
García, T.B., Bazurto, Z.A., García, C.L., & Zambrano, G.F. (2019). Morphology, viability, and longevity of pollen of National Type and Trinitarian (CCN-51) clones of cocoa (Theobroma cacao L.) on the coast of Ecuador. Brazilian Journal of Botany, 42(3), 441-448.
Garcia, T.B., Potiguara, R.C.D.V., Kikuchi, T.Y.S., Demarco, D., & Aguiar-Dias, A.C.A.D. (2014). Leaf anatomical features of three Theobroma species (Malvaceae sl) native to the Brazilian Amazon. Acta Amazonica, 44(3), 291-300.
García, C.L.C., Vera, P.L., Zambrano, G.F., Zamora, M.A., & Cedeño, O.J. (2020). Pollen production in Theobroma cacao L. genotypes national type and CCN-51 and its relationship with climatic factors on the ecuadorian coast. Acta Agrobotanica, 73(2), 1-9.
Gotelli, M.M., Galati, B.G., & Medan, D. (2008). Embryology of Helianthus annuus (Asteraceae). Annales Botanici Fennici, 45(2), 81-96.
Gotelli, M.M., Galati, B.G., & Zarlavsky, G. (2016). Pollen development and anther morphology in 14 species of Rhamnaceae. Plant Systematics and Evolution, 302(10), 1433-1444.
Ha, L.T.V., Hang, P.T., Everaert, H., Rottiers, H., Anh, L.P.T., Dung, T.N., ... Messens, K. (2016). Characterization of leaf, flower, and pod morphology among Vietnamese cocoa varieties (Theobroma cacao L.). Pakistan Journal Botany, 48(6), 2375-2383.
Halbritter, H. (1998). Preparing living pollen material for scanning electron microscopy using 2,2-dimethoxypropane (DMP) and critical-point drying. Biotechnic & Histochemistry, 73(3), 137-143.
Halbritter, H., & Buchner, R. (2016). Theobroma cacao. In: PalDat - A palynological database. Recuperado de https://www.paldat.org/pub/Theobroma_cacao/301733
Halbritter, H., Ulrich, S., Grimsson, F., Weber, M., Zetter, R., Hesse, M., … Frosch-Radivo, A. (2018). Illustrated pollen terminology. Cham, Switzerland: Springer.
Hamdy, R., & Shamso, E. (2010). Pollen morphology of Sterculiaceae (s. str.) in Egypt and its taxonomic significance. Egyptian Journal of Botany, 50, 103-117.
Heslop-Harrison, J. (1968). Pollen wall development. Science, 161(3838), 230-237.
Huysmans, S., El-Ghazaly, G., Nilsson, S., & Smets, E. (1997). Systematic value of tapetal orbicules: a preliminary survey of the Cinchonoideae (Rubiaceae). Canadian Journal of Botany, 75, 815-826.
Huysmans, S., El-Ghazaly, G., & Smets, E. (1998). Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. The Botanical Review, 64(3), 240-272.
Ioannone, F., Di Mattia, C.D., De Gregorio, M., Sergi, M., Serafini, M., & Sacchetti, G. (2015). Flavanols, proanthocyanidins and antioxidant activity changes during cocoa (Theobroma cacao L.) roasting as affected by temperature and time of processing. Food Chemistry, 174, 256-262.
Kaufmann, T. (1975). Ecology and behavior of cocoa pollinating Ceratopogonidae in Ghana, W. Africa. Environmental Entomology, 4(2), 347-351.
Konyar, S.T., Dane, F., & Tütüncü, S. (2013). Distribution of insoluble polysaccharides, neutral lipids, and proteins in the developing anthers of Campsis radicans (L.) Seem. (Bignoniaceae). Plant Systematics and Evolution, 299(4), 743-760.
Lanaud, C., Fouet, O., Legavre, T., Lopes, U., Sounigo, O., Eyango, M.C., ... Gyapay, G. (2017). Deciphering the Theobroma cacao self-incompatibility system: from genomics to diagnostic markers for self-compatibility. Journal of Experimental Botany, 68(17), 4775-4790.
Lattanzio, V., Lattanzio, M.T.V., & Cardinali, A. (2006). Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In F. Imperato (Ed.), Phytochemistry: Advances in Research (pp. 23-67). India: Research Signpost.
Lattar, E., Galati, B.G., & Ferrucci, M.S. (2014). Comparative study of anther development, microsporogenesis and microgametogenesis in species of Corchorus, Heliocarpus, Luehea and Triumfetta (Malvaceae: Grewioideae) from South America. New Zealand Journal of Botany, 52(4), 429-445.
López, H.J.G., López, H.L.E., Avendaño, A.C.H., Aguirre, M.J.F., Espinosa, Z.S., Moreno, M.J.L., ... Suárez, V.G.M. (2018). Biología floral de cacao (Theobroma cacao L.); criollo, trinitario y forastero en México. Agroproductividad, 11(9), 129-136.
Magrone, T., Russo, M.A., & Jirillo, E. (2017). Cocoa and dark chocolate polyphenols: from biology to clinical applications. Frontiers in Immunology, 8, 677-690.
Mambrín, M.V., Avanza, M.M., & Ferrucci, M.S. (2010). Análisis morfológico y morfométrico del polen de Corchorus, Heliocarpus, Luehea, Mollia y Triumfetta (Malvaceae, Grewioideae) en la región austral de América del Sur. Darwiniana, 48(1), 45-58.
Manning, J.C. (1996). Diversity of endothecial patterns in the angiosperms. In W.G.D. Arcy, & R.C. Keating (Eds.), The anther: form, function and phylogeny (pp. 136-158). Cambridge, England: University of Cambridge Press Syndicate.
Manning, J.C., & Linder, H.P. (1990). Cladistic analysis of patterns of endothecial thickenings in the Poales/Restionales. American Journal of Botany, 77(2), 196-210.
Martini, M.H., Figueira, A., Lenci, C.G., & Tavares, D.D.Q. (2008). Polyphenolic cells and their interrelation with cotyledon cells in seven species of Theobroma (Sterculiaceae). Brazilian Journal of Botany, 31(3), 425-431.
Moon, H.K. (2018). The phylogenetic potential of orbicules in angiosperms. Korean Journal of Plant Taxonomy, 48(1), 9-23.
Motamayor, J.C., Lachenaud, P., Mota, J.W.D.S., Loor, R., Kuhn, D.N., Brown, J.S., & Schnell, R.J. (2008). Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L). PloS One, 3(10), 1-8.
Motamayor, J.C., Lachenaud, P., Da Silva e Mota, J.W., Loor, R.G., Martinez, W.J., Graham, J., ... Schnell, R.J. (2010). No mas forastero: a new protocol for meaningful cacao germplasm classification. In Proceedings of the 16th international cocoa research conference (pp. 179-185). Nigeria: COPAL.
Nair, K.P. (2010). The agronomy and economy of important tree crops of the developing world. Burlington, USA: Elsevier.
Nakamura, A.T., Longhi-Wagner, H.M., & Scatena, V.L. (2010). Anther and pollen development in some species of Poaceae (Poales). Brazilian Journal of Biology, 70(2), 351-360.
Narayanapur, V.B., Suma, B., & Minimol, J.S. (2018). Self-incompatibility: a pollination control mechanism in plants. International Journal of Plant Sciences (Muzaffarnagar), 13(1), 201-212.
Niemenak, N., Rohsius, C., Elwers, S., Ndoumou, D.O., & Lieberei, R. (2006). Comparative study of different cocoa (Theobroma cacao L.) clones in terms of their phenolics and anthocyanins contents. Journal of Food Composition and Analysis, 19(6-7), 612-619.
N’Zi, J.C., Kahia, J., Diby, L., & Kouamé, C. (2017). Compatibility of ten elite cocoa (Theobroma cacao L.) clones. Horticulturae, 3(3), 1-8.
Oracz, J., Zyzelewicz, D., & Nebesny, E. (2015). The content of polyphenolic compounds in cocoa beans (Theobroma cacao L.), depending on variety, growing region, and processing operations: a review. Critical Reviews in Food Science and Nutrition, 55(9), 1176-1192.
Osorio, G.J.A., Berdugo, C.J., Coronado, R.A., Zapata, Y.P., Quintero, C., Gallego, S.G., & Yockteng, R. (2017). Colombia a source of cacao genetic diversity as revealed by the population structure analysis of germplasm bank of Theobroma cacao L. Frontiers in Plant Science, 8, 1-13.
Pacini, E. (2010). Relationships between tapetum, loculus, and pollen during development. International Journal of Plant Sciences, 171(1), 1-11.
Pacini, E., & Franchi, G.G. (1988). Amylogenesis and amylolysis during pollen grain development. In M. Cresti, P. Gori, & E. Pacini (Eds.), Sexual Reproduction in Higher Plant (pp. 181-186). Germany: Springer-Verlag.
Pacini, E., Franchi, G.G., & Hesse, M. (1985). The tapetum: Its form, function, and possible phylogeny in Embryophyta. Plant Systematics and Evolution, 149(3-4), 155-185.
Pacini, E., Guarnieri, M., & Nepi, M. (2006). Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma, 228(1-3), 73.
Pacini, E., & Hesse, M. (2005). Pollenkitt-its composition, forms and functions. Flora-Morphology, Distribution, Functional Ecology of Plants, 200(5), 399-415.
Parkinson, B.M., & Pacini, E. (1995). A comparison of tapetal structure and function in pteridophytes and angiosperms. Plant Systematics and Evolution, 198(1-2), 55-88.
Passarelli, L., & Cocucci, A.A. (2006). Morphological and functional aspects of anthers from species of Solanum sect. Cyphomandropsis. Phytomorphology, 56(1-2), 1-8.
Perveen, A., Grafström, E., & El-Ghazaly, G. (2004). World Pollen and Spore Flora 23. Malvaceae Adams. Pp. Subfamilies: Grewioideae, Tilioideae, Brownlowioideae. Grana, 43(3), 129-155.
Perveen, A., & Qaiser, M. (2009). Pollen flora of Pakistan-Malvaceae: Dombeyoideae-Lxii. Pakistan Journal of Botany, 41(2), 491-494.
Pipitone, L. (2016). Overview of cocoa supply and demand. In International Cocoa Organization (ICCO). ICCO Cocoa Market Outlook Conference September. England: International Cocoa Organization (ICCO).
Porter, L.J., Ma, Z., & Chan, B.G. (1991). Cacao procyanidins: major flavanoids and identification of some minor metabolites. Phytochemistry, 30(5), 1657-1663.
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.
Rangel, F.M.A., Zavaleta, M.H.A., Córdova, T.L., López, A.A.P., Delgado, A.A., Vidales, F.I., & Villegas, M.Á. (2012). Anatomía e histoquímica de la semilla del cacao (Theobroma cacao L.) criollo mexicano. Revista Fitotecnia Mexicana, 35(3), 189-197.
Richardson, J.E., Whitlock, B.A., Meerow, A.W., & Madriñán, S. (2015). The age of chocolate: a diversification history of Theobroma and Malvaceae. Frontiers in Ecology and Evolution, 3, 1-14.
Rincón, B.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.
Rojas, L.F., Londoño, J., Gallego, A.M., Herrera, A.L., Aguilera, C., & Atehortúa, L. (2008). Total polyphenols analysis of mature seeds and tissue cultures of some Colombian cocoa varieties. Actualidades Biológicas, 30(89), 117-123.
Roth, I., & Lindorf, H. (1971). Desarrollo y anatomía del fruto y de la semilla de Theobroma cacao L. Acta Botánica Venezuélica, 6(1), 261-295.
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. Nueva York, USA: Oxford University.
Saba, M.D., & dos Santos, F.D.A.R. (2015). Pollen morphology and exine ultrastructure of selected species of Waltheria L. (Byttnerioideae-Malvaceae). Review of Palaeobotany and Palynology, 221, 204-210.
Santos, R.C., Pires, J.L., & Correa, R.X. (2012). Morphological characterization of leaf, flower, fruit and seed traits among Brazilian Theobroma L. species. Genetic Resources and Crop Evolution, 59(3), 327-345.
Santos de Oliveira, J.M., Martins, M.S., Dorneles, M.P., & Carvalho de Freitas, C. (2015). Starch distribution in anthers, microspores and pollen grains in Aechmea recurvata (Klotzsch.) LB Sm., Dyckia racinae LB Sm. and Tillandsia aeranthos (Loisel.) LB Sm. (Bromeliaceae). Acta Botanica Brasilica, 29(1), 103-112.
Shamrov, I.I., Anisimova, M.G., & Babro, A.A. (2020). Early stages of anther development in flowering plants. Botanica Pacifica, 9(2), 1-10.
Silveira Júnior, C.E.A, Lima, L.L.C., & Saba, M.D. (2017). Pollen morphology of Waltheria L. (Malvaceae-Byttnerioideae) from Bahia, Brazil. Acta Botanica Brasilica, 31(4), 597-612.
Simpson, M.G. (2010). Plant systematics. San Diego, USA: Academic Press.
Sivachandran, R., Gnanam, R., Sudhakar, D., Suresh, J., & Ram, S.G. (2017). Influence of genotypes, stages of microspore, pre-treatments and media factors on induction of callus from anthers of cocoa (Theobroma cacao L.). Journal of Plantation Crops, 45(3),162-172.
Squicciarini, M.P., & Swinnen, J. (2016) The Economics of Chocolate. Oxford, UK: Oxford University Press.
Strittmatter, L.I., & Galati, B.G. (2001). Development of anthers, microsporogenesis and
microgametogenesis of Myosotis azorica and M. laxa (Boraginaceae). Phytomorphology, 51(1), 1-10.
Strittmatter, L.I, Galati, B.G., & Monacci, F. (2000). Ubisch bodies in the peritapetal membrane of Abutilon pictum Gill (Malvaceae). Beiträge zur Biologie der Pflanzen, 71, 1-10.
Swanson, J.D., Carlson, J.E., & Guiltinan, M.J. (2008). Comparative flower development in Theobroma cacao based on temporal morphological indicators. International Journal of Plant Sciences, 169(9), 1187-1199.
Tang, Y.A., Gao, H.U.I., Wang, C.M., & Chen, J.Z. (2006). Microsporogenesis and microgametogenesis of Excentrodendron hsienmu (Malvaceae sl) and their systematic implications. Botanical Journal of the Linnean Society, 150(4), 447-457.
Tang, Y., Gao, H., & Xie, J.S. (2009). An embryological study of Eriolaena candollei Wallich (Malvaceae) and its systematic implications. Flora-Morphology, Distribution, Functional Ecology of Plants, 204(8), 569-580.
Tebbitt, M.C., & Maciver, C.M. (1999). The systematic significance of the endothecium in Begoniaceae. Botanical Journal of the Linnean Society, 131(3), 203-221.
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.
Wei, D., Xu, H., & Li, R. (2015). Dynamics of polysaccharides and neutral lipids during anther development in castor (Ricinus communis). Journal of the American Society for Horticultural Science, 140(4), 356-361.
Wickramasuriya, A.M., & Dunwell, J.M. (2018). Cacao biotechnology: current status and future prospects. Plant Biotechnology Journal, 16(1), 4-17.
Wilson, Z.A., Song, J., Taylor, B., & Yang, C. (2011). The final split: the regulation of anther dehiscence. Journal of Experimental Botany, 62(5), 1633-1649.
Yeung, E.C.T., Stasolla, C., Sumner, M.J., & Huang, B.Q. (2015). Plant microtechniques and protocols. New York, USA: Springer.
Young, A.M., Erickson, E.H., Strand, M.A., & Erickson, B.J. (1987). Pollination biology of Theobroma and Herrania (Sterculiaceae)- 1. Floral biology. International Journal of Tropical Insect Science, 8(2), 151-164.
Young, A.M., Schaller, M., & Strand, M. (1984). Floral nectaries and trichomes in relation to pollination in some species of Theobroma and Herrania (Sterculiaceae). American Journal of Botany, 71(4), 466-480.
Young, A.M., & Severson, D.W. (1994). Comparative analysis of steam distilled floral oils of cacao cultivars (Theobroma cacao L., Sterculiaceae) and attraction of flying insects: Implications for a Theobroma pollination syndrome. Journal of Chemical Ecology, 20(10), 2687-2703.
Yun, Z., & Huiqiao, T. (2015). The distribution features of polysaccharides and lipids in the development of tomato anthers. Horticultural Plant Journal, 1(1), 35-40.
Zhang, D., Martínez, W.J., Johnson, E.S., Somarriba, E., Phillips-Mora, W., Astorga, C., ... Meinhardt, L.W. (2012). Genetic diversity and spatial structure in a new distinct Theobroma cacao L. population in Bolivia. Genetic Resources and Crop Evolution, 59(2), 239-252.
Zhang, D., & Motilal, L. (2016). Origin, dispersal, and current global distribution of cacao genetic diversity. In B.A. Bailey & L.W. Meinhardt (Eds.), Cacao diseases a history of old enemies and new encounters (pp. 3-32). Switzerland: Springer International Publishing.
Zheng, R., Su, S., Xiao, H., & Tian, H. (2017). Polysaccharides and lipids in the developing anthers of Hong Kong orchid tree (Bauhinia blakeana). Trees, 31(4), 1295-1301.
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright (c) 2021 Edgar Javier Rincón Barón, Diego Alejandro Zarate, Genaro Andrés Agudelo Castañeda, Viviana Lucia Cuarán, Lilian M. Passarelli