Skip to main content
Log in

Orbicules in Flowering Plants: A Phylogenetic Perspective on their Form and Function

  • Published:
The Botanical Review Aims and scope Submit manuscript

Abstract

Next to pollen, stamens of flowering plants often produce microstructures, called orbicules, lining the locules. Although the existence of orbicules has been known since 1865, their function still remains enigmatic. This paper surveys orbicule distribution throughout angiosperms, including +1,500 entries. We show that orbicules are found all over of flowering plants with an evolutionary trend towards orbicule absence in more derived clades. Orbicules are common in the ANITA-grade and 85 % of the monocots studied produce orbicules, with Orchidaceae, Commelinales and Zingiberales as notable exceptions. Within eudicots, asterids are most densely sampled with 61 % orbicule presence. Asteraceae and the majority of Lamiaceae lack orbicules. For 17 angiosperm orders orbicule distribution data are lacking entirely. We demonstrate that the hypothesized correlation of orbicule presence with non-amoeboid tapetum types holds true. The presence of orbicules is therefore a convenient proxy for tapetum characterization. The potential of orbicules as an a-cellular model system for patterned sporopollenin polymerization is discussed and suitable model plants for future functional orbicule-research are identified.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. Rowley (1962) coined the term to acknowledge Gerta von Ubisch (1882–1965), a German biologist who did pioneering work on orbicules in the 1920’s. She was, however, not the first scientist to describe orbicules; to our knowledge Rosanoff (1865) was the first to discover orbicules.

Literature Cited

  • Alarid, K. M., R. D. Bray & L. J. Musselman. 2005. Morphology, ultrastructure and typology of orbicules in Isoetes (Isoetaceae, Lycophyta). Botany 2005: Annual Meeting of the Botanical Society of America in Austin, Texas, USA. [online abstract, www.2005.botanyconference.org/engine/search/index.php?func=detail&aid=267].

  • Amelia Garcia, M. T., B. G. Galati & A. M. Anton. 2002. Microsporogenesis, microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae). Botanical Journal of the Linnean Society 139: 383–394.

    Google Scholar 

  • Anger, E. M. & M. Weber. 2006. Pollen-wall formation in Arum alpinum. Annals of Botany 97: 239–244.

    PubMed Central  PubMed  Google Scholar 

  • APG. 2009. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105–121.

    Google Scholar 

  • Ariizumi, T., K. Hatakeyama, K. Hinata, R. Inatsugi, I. Nishida, S. Sato, T. Kato, S. Tabata & K. Toriyama. 2004. Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant Journal 39: 170–181.

    CAS  PubMed  Google Scholar 

  • Audran, J.-C. 1981. Pollen and tapetum development in Ceratozamia mexicana (Cycadaceae): sporal origin of the exinic sporopollenin in Cycads. Review of Palaeobotany and Palynology 33: 315–346.

    Google Scholar 

  • Bhandari, N. N. & R. Kishori. 1971. Ubisch granules on tapetal membranes in anthers; rapid selective staining by spirit blue. Stain Technology 46: 15–17.

    CAS  PubMed  Google Scholar 

  • Blackmore, S. & S. H. Barnes. 1985. Cosmos pollen ontogeny: a scanning electron microscope study. Protoplasma 126: 91–99.

    Google Scholar 

  • ——— & ———. 1990. Pollen wall development in angiosperms. Pp 173–192. In: S. Blackmore & R. B. Knox (eds). Microspores: evolution and ontogeny. Academic, London, UK.

    Google Scholar 

  • ———, M. Takahashi & K. Uehara. 2000. A preliminary phylogenetic analysis of sporogenesis in Pteridophytes. Pp 109–124. In: M. M. Harley, C. M. Morton, & S. Blackmore (eds). Pollen Spores: Morphology and Biology. Royal Botanic Gardens, Kew, UK.

    Google Scholar 

  • ———, A. H. Wortley, J. J. Skvarla & J. R. Rowley. 2007. Pollen wall development in flowering plants. New Phytologist 174: 483–498.

    CAS  PubMed  Google Scholar 

  • Buss, P. A. & N. R. Lersten. 1975. Survey of tapetal nuclear number as a taxonomic character in Leguminosae. Botanical Gazette 136: 388–395.

    Google Scholar 

  • Canini, A., J. Giovinazzi, P. Iacovacci, C. Pini & M. Grilli Caiola. 2004. Localisation of a carbohydrate epitope recognised by human IgE in pollen of Cupressaceae. Journal of Plant Research 117: 147–153.

    CAS  PubMed  Google Scholar 

  • Carniel, K. 1966. Über die Körnchen-Schicht in den Pollensäcken von Gnetum gnemon. Österreichische Botanische Zeitschrift 113: 368–374.

    Google Scholar 

  • Chatin, A. 1870. De l’anthère. Recherches sur le développement, la structure et les fonctions de ses tissus. Baillière, Paris, France.

  • Chen, S.-H., J.-P. Liao, M.-Z. Luo & B. K. Kirchoff. 2008. Calcium distribution and function during anther development of Torenia fournieri (Linderniaceae). Annales Botanici Fennici 45: 195–203.

    Google Scholar 

  • Chichiricco, G. 1999. Developmental stages of pollen wall and tapetum in some Crocus species. Grana 38: 31–41.

    Google Scholar 

  • Christensen, J. E., H. T. Jr. Horner & N. R. Lersten. 1972. Pollen wall and tapetal orbicular wall development in Sorghum bicolor (Gramineae). American Journal of Botany 59: 43–58.

  • Clément, C. & J. C. Audran. 1993. Orbicule wall surface characteristics in Lilium (Liliaceae). An ultrastructural and cytochemical approach. Grana 32: 348–353.

    Google Scholar 

  • Cortès-B., R. 2003. Systematics and biogeography of Retiniphyllum (Rubiaceae). Ph.D. dissertation, City University of New York, New York, New York, USA.

  • Davis, G. L. 1966. Systematic embryology of the angiosperms. Wiley, New York, New York, USA.

    Google Scholar 

  • Dessein, S., H. Ochoterena, P. De Block, F. Lens, E. Robbrecht, P. Schols, E. Smets, S. Vinckier & S. Huysmans. 2005. Palynological characters and their phylogenetic signal in Rubiaceae. Botanical Review 71: 354–414.

    Google Scholar 

  • D’Hondt, C., P. Schols, S. Huysmans & E. Smets. 2004. Systematic relevance of pollen and orbicule characters in the tribe Hillieae (Rubiaceae). Botanical Journal of the Linnean Society 146: 303–321.

    Google Scholar 

  • Dinis, A. M., F. Baptista & A. P. Coutinho. 2007. Is the quantity of orbicules released by Dactylis glomerata and Cynosurus echinatus (Poaceae) big enough to play an allergenic role? Grana 46: 140–147.

    Google Scholar 

  • Doores, A. S., J. M. Osborn & G. El-Ghazaly. 2007. Pollen ontogeny in Ephedra americana (Gnetales). International Journal of Plant Sciences 168: 985–997.

    Google Scholar 

  • Dunbar, A. 1973. Pollen development in the Eleocharis palustris group (Cyperaceae): 1. Ultrastructure and ontogeny. Botaniska Notiser 126: 197–254.

    Google Scholar 

  • Echlin, P. & H. Godwin. 1968. The ultrastructure and ontogeny of pollen in Helleborus foetidus L. I. The development of the tapetum and Ubisch bodies. Journal of Cell Science 3: 161–174.

    CAS  PubMed  Google Scholar 

  • El-Ghazaly, G. 1999. Tapetum and orbicules (Ubisch bodies): development, morphology and role of pollen grains and tapetal orbicules in allergenicity. Pp 157–173. In: M. Cresti, G. Cai, & A. Moscatelli (eds). Fertilization in higher plants. Springer, Berlin, Germany.

    Google Scholar 

  • ——— & S. Huysmans. 2001. Re-evaluation of a neglected layer in pollen wall development with comments on its evolution. Grana 40: 3–16.

    Google Scholar 

  • ———, ——— & E. Smets. 2001. Pollen wall development of Rondeletia odorata (Rubiaceae). American Journal of Botany 88: 14–30.

    PubMed  Google Scholar 

  • ——— & W. A. Jensen. 1986. Studies of the development of wheat (Triticum aestivum) pollen. I. Formation of the pollen wall and Ubisch bodies. Grana 25: 1–29.

    Google Scholar 

  • ——— & S. Nilsson. 1991. Development of tapetum and orbicules of Catharanthus roseus (Apocynaceae). Pp 317–329. In: S. Blackmore & S. H. Barnes (eds). Pollen Spores: Patterns of Diversity. Oxford University Press, Oxford, UK.

    Google Scholar 

  • ——— & J. R. Rowley. 1997. Pollen wall of Ephedra foliata. Palynology 21: 7–18.

    Google Scholar 

  • Fernando, D. D. & D. D. Cass. 1994. Plasmodial tapetum and pollen wall development in Butomus umbellatus (Butomaceae). American Journal of Botany 81: 1592–1600.

    Google Scholar 

  • Foreman, D. B. 1984. The morphology and phylogeny of the Monimiaceae (sensu lato). Ph.D. dissertation, University of New England, Armindale, Australia.

  • Furness, C. A. 2008a. A review of the distribution of plasmodial and invasive tapeta in eudicots. International Journal of Plant Sciences 169: 207–223.

    Google Scholar 

  • ——— 2008b. Successive microsporogenesis in eudicots, with particular reference to Berberidaceae (Ranunculales). Plant Systematics and Evolution 273: 211–223.

    Google Scholar 

  • ——— 2011. Comparative structure and development of pollen and tapetum in Malpighiales, with a focus on the parietal clade. International Journal of Plant Sciences 172: 980–1011.

    Google Scholar 

  • ——— & P. J. Rudall. 1998. The tapetum and systematics in monocotyledons. Botanical Review 64: 201–239.

    Google Scholar 

  • ——— & ———. 1999. Microsporogenesis in monocotyledons. Annals of Botany 84: 475–499.

    Google Scholar 

  • ——— & ———. 2001a. The tapetum in basal angiosperms: early diversity. International Journal of Plant Sciences 162: 375–392.

    Google Scholar 

  • ——— & ———. 2001b. Pollen and anther characters in monocot systematics. Grana 40: 17–25.

    Google Scholar 

  • ——— & ———. 2006. Comparative structure and development of pollen and tapetum in Pandanales. International Journal of Plant Sciences 167: 331–348.

    Google Scholar 

  • ———, ——— & A. Eastman. 2002. Contribution of pollen and tapetal characters to the systematics of Triuridaceae. Plant Systematics and Evolution 235: 209–218.

    Google Scholar 

  • Gabarayeva, N. I. 1995. Pollen wall and tapetum development in Anaxagorea brevipes (Annonaceae): sporoderm substructure, cytoskeleton, sporopollenin precursor particles, and the endexine problem. Review of Palaeobotany and Palynology 85: 123–152.

    Google Scholar 

  • ——— & G. El-Ghazaly. 1997. Sporoderm development in Nymphaea mexicana (Nymphaeaceae). Plant Systematics and Evolution 204: 1–19.

    Google Scholar 

  • ———, V. V. Grigorjeva & J. R. Rowley. 2010a. A new look at sporoderm ontogeny in Persea americana and the hidden side of development. Annals of Botany 105: 939–955.

    CAS  PubMed Central  PubMed  Google Scholar 

  • ———, ——— & ———. 2010b. Sporoderm development in Acer tataricum (Aceraceae): an interpretation. Protoplasma 247: 65–81.

    PubMed  Google Scholar 

  • ———, ———, ——— & A. R. Hemsley. 2009. Sporoderm development in Trevesia burckii (Araliaceae). II. Post-tetrad period: further evidence for the participation of self-assembly processes. Review of Palaeobotany and Palynology 156: 233–247.

    Google Scholar 

  • ——— & A. R. Hemsley. 2006. Merging concepts: the role of self-assembly in the development of pollen wall structure. Review of Palaeobotany and Palynology 138: 121–139.

    Google Scholar 

  • Galati, B. G. 2003. Ubisch bodies in angiosperms. Advances in Plant Reproductive Biology 2: 1–20.

    Google Scholar 

  • ———, F. Monacci, M. M. Gotelli & S. Rosenfeldt. 2007. Pollen, tapetum and orbicule development in Modiolastrum malvifolium (Malvaceae). Annals of Botany 99: 755–763.

    PubMed Central  PubMed  Google Scholar 

  • ——— & S. Rosenfeldt. 1998. The pollen development in Ceiba insignis (Kunth) Gibbs & Semir ex Chorisia speciosa St.Hil. (Bombacaceae). Phytomorphology 48: 121–129.

    Google Scholar 

  • ——— & L. I. Strittmatter. 1999a. Correlation between pollen development and Ubisch bodies ontogeny in Jacaranda mimosifolia (Bignoniaceae). Beiträge zur Biologie der Pflanzen 71: 249–260.

    Google Scholar 

  • ——— & ———. 1999b. Microsporogenesis and microgametogenesis in Jacaranda mimosifolia (Bignoniaceae). Phytomorphology 49: 67–74.

    Google Scholar 

  • ———, G. Zarlavsky, S. Rosenfeldt & M. M. Gotelli. 2012. Pollen ontogeny in Magnolia liliflora Desr. Plant Systematics and Evolution 298: 527–534.

    Google Scholar 

  • Geeraerts, A., J. A. M. Raeymaekers, S. Vinckier, A. Pletsers, E. Smets & S. Huysmans. 2009. Systematic palynology in Ebenaceae with focus on Ebenoideae: morphological diversity and character evolution. Review of Palaeobotany and Palynology 153: 336–353.

    Google Scholar 

  • Goebel, K. 1901. Organographie der Pflanzen, ed. 1st. Gustav Fischer Verlag, Jena, Germany.

    Google Scholar 

  • Goldberg, R. B., T. P. Beals & P. M. Sanders. 1993. Anther development: basic principles and practical applications. Plant Cell 5: 1217–1229.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gonzalez, F. 1999. A phylogenetic analysis of the Aristolochioideae (Aristolochiaceae). Ph.D. dissertation, The City University of New York, New York, New York, USA.

  • ———, P. J. Rudall & C. A. Furness. 2001. Microsporogenesis and systematics of Aristolochiaceae. Botanical Journal of the Linnean Society 137: 221–242.

    Google Scholar 

  • Gotelli, M., B. G. Galati & D. Medan. 2012. Pollen, tapetum, and orbicule development in Colletia paradoxa and Discaria americana (Rhamnaceae). The Scientific World Journal 2012: ID 948469.

  • Gupta, S. C. & K. Nanda. 1972. Occurrence and histochemistry of the anther tapetal membrane. Grana 12: 99–104.

    Google Scholar 

  • Halbritter, H. & M. Hesse. 2005. Specific ornamentation of orbicular walls and pollen grains, as exemplified by Acanthaceae. Grana 44: 308–312.

    Google Scholar 

  • ———, ——— & M. Weber. 2012. The unique design of pollen tetrads in Dionaea and Drosera. Grana 51: 148–157.

    Google Scholar 

  • Hansson, T. & G. El-Ghazaly. 2000. Development and cytochemistry of pollen and tapetum in Mitriostigma axillare (Rubiaceae). Grana 39: 65–89.

    Google Scholar 

  • Harley, R. M., S. Atkins, A. L. Budantsev, P. D. Cantino, B. J. Conn, R. Grayer, M. M. Harley, R. de Kok, T. Krestovskaja, R. Morales, A. J. Paton, O. Ryding & T. Upson. 2004. Labiatae. Pp 167–275. In: J. W. Kadereit (ed). The Families and Genera of Vascular Plants, vol. 7, Flowering plants: Dicotyledons (Lamiales except Acanthaceae including Avicenniaceae). Springer, Berlin, Germany.

    Google Scholar 

  • Hermann, P. M. & B. F. Palser. 2000. Stamen development in the Ericaceae. I. Anther wall, microsporogenesis, inversion and appendages. American Journal of Botany 87: 934–957.

    CAS  PubMed  Google Scholar 

  • Heslop-Harrison, J. 1968. Tapetal origin of pollen-coat substances in Lilium. New Phytologist 67: 779–786.

    CAS  Google Scholar 

  • Hesse, M. 1986. Orbicules and the ektexine are homologous sporopollenine concretions in Spermatophyta. Plant Systematics and Evolution 153: 37–48.

    CAS  Google Scholar 

  • ——— 1999. Electron-translucent angular areas in developing tapetum cell walls and pollen grains of Tilia platyphyllos. Protoplasma 207: 169–173.

    Google Scholar 

  • ——— 2001. Pollen characters of Amborella trichopoda (Amborellaceae): a reinvestigation. International Journal of Plant Sciences 162: 201–208.

    Google Scholar 

  • ———, H. Halbritter, R. Zetter, M. Weber, R. Buchner, A. Frosch-Radivo & S. Ulrich. 2009. Pollen terminology. An illustrated handbook. Springer, Vienna, Austria.

    Google Scholar 

  • Hosoo, Y., E. Yoshii, K. Negishi & H. Taira. 2005. A histological comparison of the development of pollen and female gametophytes in fertile and sterile Cryptomeria japonica. Sexual Plant Reproduction 18: 81–89.

    Google Scholar 

  • Huysmans, S., S. Dessein, E. Smets & E. Robbrecht. 2003. Pollen morphology of NW European representatives confirms monophyly of Rubieae (Rubiaceae). Review of Palaeobotany and Palynology 127: 219–240.

    Google Scholar 

  • ———, G. El-Ghazaly, S. Nilsson & E. Smets. 1997. Systematic value of tapetal orbicules: a preliminary survey of the Cinchonoideae (Rubiaceae). Canadian Journal of Botany 75: 815–826.

    Google Scholar 

  • ———, ——— & E. Smets. 1998. Orbicules in angiosperms. Morphology, function, distribution, and relation with tapetum types. Botanical Review 64: 240–272.

    Google Scholar 

  • ———, ——— & ———. 2000. Orbicules: still a well hidden secret of the anther. Pp 201–212. In: B. Nordenstam, G. El-Ghazaly, & M. Kassas (eds). Plant Systematics for the 21st Century. Portland Press, London, UK.

    Google Scholar 

  • ———, E. Robbrecht, P. Delprete & E. Smets. 1999. Pollen morphological support for the Catesbaeeae-Chiococceae-Exostema-complex (Rubiaceae). Grana 38: 325–338.

    Google Scholar 

  • ———, B. Verstraete, E. Smets & L. W. Chatrou. 2010. Distribution of orbicules in Annonaceae mirrors evolutionary trend in angiosperms. Plant Ecology and Evolution 143: 199–211.

    Google Scholar 

  • Inamuddin, M., B. Were & M. Saquib. 2009. A contribution to the embryology of Rhynchelytrum repens (Willd.) C.E. Hubbard. Scientific World 7: 37–40.

    Google Scholar 

  • Jacobs, B., K. Geuten, N. Pyck, S. Huysmans, S. Jansen & E. Smets. 2011. Unraveling the phylogeny of Heptacodium and Zabelia (Caprifoliaceae): an interdisciplinary approach. Systematic Botany 36: 231–252.

    Google Scholar 

  • Jäger-Zürn, I., R. N. Novelo & C. T. Philbrick. 2006. Microspore development in Podostemaceae-Podostemoideae, with implications on the characterization of the subfamilies. Plant Systematics and Evolution 256: 209–216.

    Google Scholar 

  • Janssens, S., S. Dessein & E. Smets. 2011. Portrayal of Impatiens nzabiana (Balsaminaceae): a morphological, molecular and biogeographic study of a new Gabonese species. Systematic Botany 36: 440–448.

    Google Scholar 

  • ———, E. Knox, S. Dessein & E. Smets. 2009. Impatiens msisimwanensis (Balsaminaceae): Description, pollen morphology and phylogenetic position of a new East African species. South African Journal of Botany 75: 104–109.

    Google Scholar 

  • ———, F. Lens, S. Dressler, K. Geuten, E. Smets & S. Vinckier. 2005. Palynological variation in balsaminoid Ericales. II. Balsaminaceae, Tetrameristaceae, Pellicieraceae and general conclusions. Annals of Botany 96: 1061–1073.

    PubMed  Google Scholar 

  • ———, Y. Song Wilson, Y.-M. Yuan, A. Nagels, E. F. Smets & S. Huysmans. 2012. A total evidence approach using palynological characters to infer the complex evolutionary history of the Asian Impatiens (Balsaminaceae). Taxon 61: 355–367.

    Google Scholar 

  • Jato, V., F. J. Rodríguez-Rajo, Z. González-Parrado, B. Elvira-Rendueles, S. Moreno-Grau, A. Vega-Maray, D. Fernández-González, J. A. Asturias & M. Suárez-Cervera. 2010. Detection of airborne Par j 1 and Par j 2 allergens in relation to Urticaceae pollen counts in different bioclimatic areas. Annals of Allergy, Asthma & Immunology 105: 50–56.

    Google Scholar 

  • Jung, K.-H., M.-J. Han, D.-Y. Lee, Y.-S. Lee, L. Schreiber, R. Franke, A. Faust, A. Yephremov, H. Saedler, Y.-W. Kim, I. Hwang & G. An. 2006. Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18: 3015–3032.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johri, B. M. & S. P. Bhatnagar. 1955. A contribution to the morphology and life history of Aristolochia. Phytomorphology 3: 123–137.

    Google Scholar 

  • Kapoor, S., A. Kobayashi & H. Takatsuji. 2002. Silencing of the tapetum-specific Zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in Petunia. Plant Cell 14: 2353–2367.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kenrick, J. & R. B. Knox. 1979. Pollen development and cytochemistry in some Australian species of Acacia. Australian Journal of Botany 27: 413–427.

    Google Scholar 

  • von Kosmath, L. 1927. Studien über das Antherentapetum. Österreichische Botanische Zeitschrift 76: 235–241.

    Google Scholar 

  • Kress, W. J. 1986. Exineless pollen structure and pollination systems of tropical Heliconia (Heliconiaceae). Pp 329–345. In: S. Blackmore & I. K. Ferguson (eds). Pollen and Spores: Form and Function. Academic, London, UK.

    Google Scholar 

  • Kreunen, S. S. & J. M. Osborn. 1999. Pollen and anther development in Nelumbo (Nelumbonaceae). American Journal of Botany 86: 1662–1676.

    CAS  PubMed  Google Scholar 

  • Krjatchenko, M. D. 1925. De l’activité des chondriosomes pendant le développement des grains de pollen et des cellules nourricières du pollen dans Lilium croceum Chaix. Revue Générale de Botanique 37: 193–211.

    Google Scholar 

  • Lens, F., S. Dressler, S. Vinckier, S. Janssens, S. Dessein, L. Van Evelghem & E. Smets. 2005. Palynological variation in balsaminoid Ericales. I. Marcgraviaceae. Annals of Botany 96: 1047–1060.

    PubMed  Google Scholar 

  • Le Thomas, A., M. Suàrez-Cervera & P. Goldblatt. 2001. Ontogeny of the exine in pollen of Aristea (Iridaceae). Grana 40: 35–44.

    Google Scholar 

  • Li, T. & H. Cao. 1986. Microsporogensis and development of male gametophyte of Camellia chrysantha (Hu) Tuyama. Journal of Beijing Forestry University.

  • Li, H., Z. Yuan, G. Vizcay-Barrena, C. Yang, W. Liang, J. Zong, Z. A. Wilson & D. Zhang. 2011. PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiology 156: 615–630.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liang, X., Y. Zhang, S. Liu & B. Yu. 1994. Studies on the infrastructure of the development of anther tapetum in Sesame (Sesamum indicum L.). Journal of Agricultural Biotechnology.

  • Lombardo, G. & L. Carraro. 1976. Tapetal ultrastructural changes during pollen development. III. Studies on Gentiana acaulis. Caryologia 29: 345–349.

    Google Scholar 

  • Lugardon, B. 1981. Les globules des Filicinées, homologues des corps d’Ubisch des Spermatophytes. Pollen Spores 23: 93–124.

    Google Scholar 

  • Mascré, M. 1922. Sur l’étamine des Boraginées. Comptes Rendus de l’Académie des Sciences de Paris 175: 987–988.

    Google Scholar 

  • McNeil, K. J. & A. G. Smith. 2010. A glycine-rich protein that facilitates exine formation during tomato pollen development. Planta 231: 793–808.

    CAS  PubMed  Google Scholar 

  • Merckx, V., P. Schols, K. Geuten, S. Huysmans & E. Smets. 2008. Phylogenetic relationships in Nartheciaceae (Dioscoreales) with focus on pollen and orbicule morphology. Belgian Journal of Botany 141: 64–77.

    Google Scholar 

  • ———, ———, H. Maas-van de Kamer, P. Maas, S. Huysmans & E. Smets. 2006. Phylogeny and evolution of Burmanniaceae (Dioscoreales) based on nuclear and mitochondrial data. American Journal of Botany 93: 1684–1698.

    PubMed  Google Scholar 

  • Moon, H.-K., S. Vinckier, E. Smets & S. Huysmans. 2008a. Comparative pollen morphology and ultrastructure of Mentheae subtribe Nepetinae (Lamiaceae). Review of Palaeobotany and Palynology 149: 174–186.

    Google Scholar 

  • ———, ———, ——— & ———. 2008b. Palynological evolutionary trends within the tribe Mentheae with special emphasis on subtribe Menthinae (Nepetoideae: Lamiaceae). Plant Systematics and Evolution 275: 93–108.

    Google Scholar 

  • ———, ———, J. B. Walker, E. Smets & S. Huysmans. 2008c. A search for phylogenetically informative pollen characters in the subtribe Salviinae (Mentheae: Lamiaceae). International Journal of Plant Sciences 169: 455–471.

    Google Scholar 

  • Mu, X., F. Wang & W. Wang. 1988. Development and histochemical observations of tapetum and peritapetal membrane in anther of Pulsatilla chinensis. Acta Botanica Sinica 30: 6–13.

    Google Scholar 

  • Muasya, A. M., P. M. Musili & A. Vrijdaghs. 2010. Kyllinga mbitheana (Cyperaceae)-Description, floral ontogeny and pollen micromorphology of a new species from Kenya. Journal of East African Natural History 99: 65–75.

    Google Scholar 

  • Murgia, M., M. Charzynska, M. Rougier & M. Cresti. 1991. Secretory tapetum of Brassica oleracea L.: polarity and ultrastructural features. Sexual Plant Reproduction 4: 28–35.

    Google Scholar 

  • Murphy, D. J. 2006. The extracellular pollen coat in members of the Brassicaceae: composition, biosynthesis, and functions in pollination. Protoplasma 228: 31–39.

    CAS  PubMed  Google Scholar 

  • Nagels, A., A. M. Muasya, S. Huysmans, A. Vrijdaghs, E. Smets & S. Vinckier. 2009. Palynological diversity and major evolutionary trends in Cyperaceae. Plant Systematics and Evolution 277: 117–142.

    Google Scholar 

  • Nilsson, S. & A. Robyns. 1974. Pollen morphology and taxonomy of the genus Quararibea s.l. (Bombacaceae). Bulletin du Jardin Botanique National de Belgique 44: 77–99.

    Google Scholar 

  • Pacini, E. 1996. Tapetum types in the Compositae: forms and function. Pp 21–28. In: D. J. N. Hind & H. J. Beentje (eds). Proceedings of the International Compositae Conference in Kew, 1994, vol. 1. Kew Publishing, Kew, UK.

    Google Scholar 

  • ——— 1997. Tapetum character states: analytical keys for tapetum types and activities. Canadian Journal of Botany 75: 1448–1459.

    Google Scholar 

  • ——— 2009. Orchids pollen dispersal units and reproductive consequences. Pp 185–218. In: T. Kull, J. Arditti, & S. M. Wong (eds). Orchid Biology: reviews and perspectives. Springer, Berlin, Germany.

    Google Scholar 

  • ———, G. G. Franchi & M. Hesse. 1985. The tapetum: its form, function and possible phylogeny in Embryophyta. Plant Systematics and Evolution 149: 155–185.

    Google Scholar 

  • ——— & ———. 1993. Role of the tapetum in pollen and spore dispersal. Plant Systematics and Evolution Supplement 7: 1–11.

    Google Scholar 

  • ——— & B. E. Juniper. 1979. The ultrastructure of pollen-grain development in the olive (Olea europaea). II. Secretion by the tapetal cells. New Phytologist 83: 165–174.

    Google Scholar 

  • ——— & ———. 1983. The ultrastructure of the formation and development of the amoeboid tapetum in Arum italicum Miller. Protoplasma 117: 116–129.

    Google Scholar 

  • Papini, A., S. Mosti & L. Brighigna. 1999. Programmed-cell-death events during tapetum development of angiosperms. Protoplasma 207: 213–221.

    Google Scholar 

  • Parish, R. W. & S. F. Li. 2010. Death of a tapetum: A programme of developmental altruism. Plant Science 178: 73–89.

    CAS  Google Scholar 

  • Parkinson, B. M. & E. Pacini. 1995. A comparison of tapetal structure and function in pteridophytes and angiosperms. Plant Systematics and Evolution 198: 55–88.

    Google Scholar 

  • Parulekar, N. K. 1970. Annonaceae. Bulletin of Indian National Academy of Sciences 41: 38–41.

    Google Scholar 

  • Passarelli, L. M., S. B. Girarde & N. M. Tur. 2002. Palynology of South American Podostemaceae. Grana 41: 10–15.

    Google Scholar 

  • Periasamy, K. & B. G. Swamy. 1959. Studies in the Annonaceae I: microsporogenesis in Cananga odorata and Miliusa wightiana. Phytomorphology 9: 251–263.

    Google Scholar 

  • Piffanelli, P. & D. J. Murphy. 1998. Novel organelles and targeting mechanisms in the anther tapetum. Trends in Plant Science 3: 250–253.

    Google Scholar 

  • ———, J. H. E. Ross & D. J. Murphy. 1998. Biogenesis and function of the lipidic structures of pollen grains. Sexual Plant Reproduction 11: 65–80.

    CAS  Google Scholar 

  • Prakash, N., D. B. Foreman & S. J. Griffith. 1984. Gametogenesis in Galbulimima belgraveana (Himantandraceae). Australian Journal of Botany 32: 605–612.

    Google Scholar 

  • Radice, S., M. Ontivero, E. Giordani & E. Bellini. 2008. Anatomical differences on development of fertile and sterile pollen grains of Prunus salicina Lindl. Plant Systematics and Evolution 273: 63–69.

    Google Scholar 

  • Raghavan, V. 1988. Anther and pollen development in rice (Oryza sativa). American Journal of Botany 75: 183–196.

    Google Scholar 

  • Ray, B. & G. El-Ghazaly. 1987. Morphology and taxonomic application of orbicules (Ubisch bodies) in Chloanthaceae. Pollen Spores 29: 151–166.

    Google Scholar 

  • Risueño, M. C., G. Giménez-Martín, J. F. López-Sáez & M. I. R. García. 1969. Origin and development of sporopollenine bodies. Protoplasma 67: 361–374.

    Google Scholar 

  • Ronse De Craene, L. P. 2002. Floral development and anatomy of Pentadiplandra (Pentadiplandraceae): a key genus in the identification of floral morphological trends in the core Brassicales. Canadian Journal of Botany 80: 443–459.

    Google Scholar 

  • ——— 2005. Floral developmental evidence for the systematic position of Batis (Bataceae). American Journal of Botany 92: 752–760.

    PubMed  Google Scholar 

  • ———, T. A. Yang, P. Schols & E. Smets. 2002. Flower anatomy and systematics of Bretschneidera (Bretschneideraceae). Botanical Journal of the Linnean Society 139: 29–45.

    Google Scholar 

  • ——— & A. G. Miller. 2004. Floral development and anatomy of Dirachma socotrana (Dirachmaceae): a controversial member of the Rosales. Plant Systematics and Evolution 249: 111–127.

    Google Scholar 

  • ——— & L. Wanntorp. 2008. Morphology and evolution of the flower of Meliosma (Sabiaceae): implications for pollination biology. Plant Systematics and Evolution 271: 79–91.

    Google Scholar 

  • Rosanoff, S. 1865. Zur Kenntnis des Baues und der Entwicklungsgeschichte des Pollens der Mimoseae. Jahrbuch für wissenschaftliche Botanik 4: 441–450.

    Google Scholar 

  • Rosenfeldt, S. & B. G. Galati. 2005. Ubisch bodies and pollen ontogeny in Oxalis articulata Savigny. Biocell 29: 271–278.

    PubMed  Google Scholar 

  • ——— & ———. 2008. Orbicules diversity in Oxalis species from the province of Buenos Aires (Argentina). Biocell 32: 41–47.

    PubMed  Google Scholar 

  • ——— & ———. 2012. Embryological studies of Oxalis debilis Kunth. Plant Systematics and Evolution 298: 1567–1573.

    Google Scholar 

  • Rowley, J. R. 1962. Nonhomogeneous sporopollenin in microcspores of Poa annua L. Grana Palynologica 3: 3–19.

    Google Scholar 

  • ——— 1993. Cycles of hyperactivity in tapetal cells. Plant Systematics and Evolution Supplement 7: 23–37.

    Google Scholar 

  • ——— & N. I. Gabarayeva. 2004. Microspore development in Quercus robur (Fagaceae). Review of Palaeobotany and Palynology 132: 115–132.

    Google Scholar 

  • ———, ——— & B. Walles. 1992. Cyclic invasion of tapetal cells into loculi during microspore development in Nymphaea colorata (Nymphaceae). American Journal of Botany 79: 801–808.

    Google Scholar 

  • ———, K. Mühlethaler & A. Frey-Wyssling. 1959. A route for the transfer of materials through the pollen grain wall. Journal of Biophysical and Biochemical Cytology 6: 537–538.

    CAS  PubMed Central  PubMed  Google Scholar 

  • ——— & B. Walles. 1987. Origin and structure of Ubisch bodies in Pinus sylvestris. Acta Societatis Botanicorum Poloniae 56: 215–227.

    Google Scholar 

  • Rudall, P. J., E. M. Engleman, L. Hanson & M. W. Chase. 1998. Embryology, cytology and systematics of Hemiphylacus, Asparagus and Anemarrhena (Asparagales). Plant Systematics and Evolution 211: 181–199.

    Google Scholar 

  • Sajo, M. G., C. A. Furness, C. J. Prychid & P. J. Rudall. 2005. Microsporogenesis and anther development in Bromeliaceae. Grana 44: 65–74.

    Google Scholar 

  • Santos, R. P. & J. F. A. Mariath. 1999. Ultrastructure of the orbicules (Ubisch bodies) in Ilex paraguariensis St.Hil. (Aquifoliaceae). Acta Microscopica 8 Supplement C: 773–774.

  • Schäppi, G. F., P. E. Taylor, I. A. Staff, C. Suphioglu & R. B. Knox. 1997. Source of Bet v 1 loaded inhalable particles from birch revealed. Sexual Plant Reproduction 10: 315–323.

    Google Scholar 

  • Schnarf, K. 1923. Kleine Beiträge zur Entwicklungsgeschichte der Angiospermen. IV. Über das Verhalten des Antherentapetums einiger Pflanzen. Österreichische Botanische Zeitschrift 72: 242–245.

    Google Scholar 

  • Schols, P., C. A. Furness, V. Merckx, P. Wilkin & E. Smets. 2005a. Comparative pollen development in Dioscoreales. International Journal of Plant Sciences 166: 909–924.

    Google Scholar 

  • ———, ———, P. Wilkin, S. Huysmans & E. Smets. 2001. Morphology of pollen and orbicules in some Dioscorea species and its systematic implications. Botanical Journal of the Linnean Society 136: 295–311.

    Google Scholar 

  • ———, ———, ———, E. Smets, V. Cielen & S. Huysmans. 2003. Pollen morphology of Dioscorea (Dioscoreaceae) and its relation to systematics. Botanical Journal of the Linnean Society 143: 375–390.

    Google Scholar 

  • ———, P. Wilkin, C. A. Furness, S. Huysmans & E. Smets. 2005b. Pollen evolution in yams (Dioscorea: Dioscoreaceae). Systematic Botany 30: 750–758.

    Google Scholar 

  • Scott, R. J. 1994. Pollen exine – the sporopollenin enigma and the physics of pattern. Pp 49–81. In: R. J. Scott & M. A. Stead (eds). Molecular and Cellular Aspects of Plant Reproduction. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Staehelin, L. A. 1997. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant Journal 11: 1151–1165.

    CAS  PubMed  Google Scholar 

  • Staiger, D., S. Kappeler, M. Müller & K. Apel. 1994. The proteins encoded by two tapetum-specific transcripts, Satap35 and Satap44, from Sinapis alba L. are localized in the exine cell wall layer of developing microspores. Planta 192: 221–231.

    CAS  PubMed  Google Scholar 

  • Stevens, P. F. 2001 onwards. Angiosperm Phylogeny Website. Version 12, July 2012 [and more or less continuously updated since].

  • Stone, D. E., S. C. Sellers & W. J. Kress. 1979. Ontogeny of exineless pollen in Heliconia, a banana relative. Annals of the Missouri Botanical Garden 66: 701–730.

    Google Scholar 

  • Strittmatter, L. & B. G. Galati. 2000. Embryological study in Oziroe acaulis (Hyacinthaceae). Phytomorphology 50: 161–171.

    Google Scholar 

  • ——— & ———. 2001. Pollen development in Myosotis azorica and M. laxa (Boraginaceae). Phytomorphology 54: 1–9.

    Google Scholar 

  • ———, ——— & F. Monacci. 2000. Ubisch bodies in the peritapetal membrane of Abutilon pictum Gill (Malvaceae). Beiträge zur Biologie der Pflanzen 71: 393–402.

    Google Scholar 

  • Su, Y. C. F. & R. M. K. Saunders. 2003. Pollen structure, tetrad cohesion and pollen-connecting threads in Pseuduvaria (Annonaceae). Botanical Journal of the Linnean Society 143: 69–78.

    Google Scholar 

  • Suàrez-Cervera, M., Y. Takahashi, A. Vega-Maray & J. A. Seoane-Camba. 2003. Immunocytochemical localization of Cry j 1, the major allergen of Cryptomeria japonica (Taxodiaceae) in Cupressus arizonica and Cupressus sempervirens (Cupressaceae) pollen grains. Sexual Plant Reproduction 16: 9–15.

    Google Scholar 

  • Suzuki, T., K. Masaoka, M. Nishi, K. Nakamura & S. Ishiguro. 2008. Identification of kaonashi mutants showing abnormal pollen exine structure in Arabidopsis thaliana. Plant Cell Physiology 49: 1465–1477.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Taylor, M. L., B. L. Gutman, N. A. Melrose, A. M. Ingraham, J. A. Schwartz & J. M. Osborn. 2008. Pollen and anther ontogeny in Cabomba caroliniana (Cabombaceae, Nymphaeales). American Journal of Botany 95: 399–413.

    PubMed  Google Scholar 

  • ———, P. J. Hudson, J. M. Rigg, N. Julie, J. Schwartz Green, T. C. Thiemann & J. M. Osborn. 2012. Tapetum structure and ontogeny in Victoria (Nymphaeaceae). Grana 51: 107–118.

    Google Scholar 

  • ——— & J. M. Osborn. 2006. Pollen ontogeny in Brasenia (Cabombaceae, Nymphaeales). American Journal of Botany 93: 344–356.

    PubMed  Google Scholar 

  • Taylor, T. N. 1976. The ultrastructure of Schopfipollenites: orbicules and tapetal membranes. American Journal of Botany 63: 857–862.

    Google Scholar 

  • Teppner, H. & E. Stabentheiner. 2007. Anther opening, polyad presentation, pollenkitt and pollen adhesive in four Calliandra species (Mimosaceae-Ingeae). Phyton 47: 291–320.

    Google Scholar 

  • Thom, I., M. Grote, J. Abraham-Peskir & R. Wiermann. 1998. Electron and X-ray microscopic analyses of reaggregated materials obtained after fractionation of dissolved sporopollenin. Protoplasma 204: 13–21.

    Google Scholar 

  • Tiwari, S. C. & B. E. S. Gunning. 1986a. Development of tapetum and microspores in Canna L.: an example of an invasive but non-syncytial tapetum. Annals of Botany 57: 557–563.

    Google Scholar 

  • ——— & ———. 1986b. Cytoskeleton, cell surface and the development of invasive plasmodial tapetum in Tradescantia virginiana L. Protoplasma 133: 89–99.

    Google Scholar 

  • ——— & ———. 1986c. An ultrastructural, cytochemical and immunofluorescence study of postmeiotic development of plasmodial tapetum in Tradescantia virginiana L. and its relevance to the pathway of sporopollenin secretion. Protoplasma 133: 100–114.

    Google Scholar 

  • ——— & ———. 1986d. Colchicine inhibits plasmodium formation and disrupts pathways of sporopollenin secretion in the anther tapetum of Tradescantia virginiana L. Protoplasma 133: 115–128.

    CAS  Google Scholar 

  • Tsou, C.-H. & Y.-L. Fu. 2007. Octad pollen formation in Cymbopetalum (Annonaceae): the binding mechanism. Plant Systematics and Evolution 263: 13–23.

    Google Scholar 

  • ——— & D. M. Johnson. 2003. Comparative development of aseptate and septate anthers of Annonaceae. American Journal of Botany 90: 832–848.

    PubMed  Google Scholar 

  • von Ubisch, G. 1927. Zur Entwicklungsgeschichte der Antheren. Planta 3: 490–495.

    Google Scholar 

  • Van der Ham, R. W. J. M. 1991. Pollen morphology of the Stemonaceae. Blumea 36: 127–159.

    Google Scholar 

  • ———, Y.-M. Zimmermann, S. Nilsson & A. Igersheim. 2001. Pollen morphology and phylogeny of the Alyxieae (Apocynaceae). Grana 40: 169–191.

    Google Scholar 

  • Verellen, J., S. Dessein, S. G. Razafimandimbison, E. Smets & S. Huysmans. 2007. Pollen morphology of the tribes Naucleeae and Hymenodictyeae (Rubiaceae-Cinchonoideae) and its phylogenetic significance. Botanical Journal of the Linnean Society 153: 329–341.

    Google Scholar 

  • ———, E. Smets & S. Huysmans. 2004. The remarkable genus Coptosapelta (Rubiaceae): pollen and orbicule morphology and systematic implications. Journal of Plant Research 117: 57–68.

    CAS  PubMed  Google Scholar 

  • Verstraete, B. 2009. Orbicules in angiospermen: distributie en relatie met tapetum. Casestudies in Annonaceae, Rubiaceae en modelplanten. MSc Thesis, KU Leuven, Belgium. [Dutch]

  • ———, I. Groeninckx, E. Smets & S. Huysmans. 2011. Phylogenetic signal of orbicules at family level: Rubiaceae as case study. Taxon 60: 742–757.

    Google Scholar 

  • Vinckier, S., S. Huysmans & E. Smets. 2000. Morphology and ultrastructure of orbicules in the subfamily Ixoroideae (Rubiaceae). Review of Palaeobotany and Palynology 108: 151–174.

    PubMed  Google Scholar 

  • ———, S. Janssens, S. Huysmans, A. Vandevenne & E. Smets. 2012. Pollen ontogeny linked to tapetal cell maturation in Impatiens parviflora (Balsaminaceae). Grana 52: 10–24.

    Google Scholar 

  • ——— & E. Smets. 2001a. A survey of the presence and morphology of orbicules in European allergenic angiosperms. Background information for allergen research. Canadian Journal of Botany 79: 757–766.

    Google Scholar 

  • ——— & ———. 2001b. The potential role of orbicules as a vector of allergens. Allergy 56: 1129–1136.

    CAS  PubMed  Google Scholar 

  • ——— & ———. 2002a. Morphology, ultrastructure and typology of orbicules in Loganiaceae s.l. and related genera, in relation to systematics. Review of Palaeobotany and Palynology 119: 161–189.

    Google Scholar 

  • ——— & ———. 2002b. Systematic importance of orbicule diversity in Gentianales. Grana 41: 158–182.

    Google Scholar 

  • ——— & ———. 2002c. Morphological and ultrastructural diversity of orbicules in relation to evolutionary tendencies in Apocynaceae s.l. Annals of Botany 90: 647–662.

    CAS  PubMed  Google Scholar 

  • ——— & ———. 2003. Morphological and ultrastructural diversity of orbicules in Gentianaceae. Annals of Botany 92: 657–672.

    PubMed  Google Scholar 

  • ——— & ———. 2005. A histological study of microsporogenesis in Tarenna gracilipes (Rubiaceae). Grana 44: 30–44.

    Google Scholar 

  • ———, P. Cadot, M. Grote, J. L. Ceuppens & E. Smets. 2006. Orbicules do not significantly contribute to the allergenic micro-aerosol emitted from birch trees. Allergy 61: 1243–1244.

    CAS  PubMed  Google Scholar 

  • ———, ——— & E. Smets. 2005. The manifold characters of orbicules: structural diversity, systematic significance, and vectors for allergens. Grana 44: 300–307.

    Google Scholar 

  • von Balthazar, M., K. Raunsgaard Pedersen & E. M. Friis. 2005. Teixeiraea lusitanica, a new fossil flower from the early Cretaceous of Portugal with affinities to Ranunculales. Plant Systematics and Evolution 255: 55–75.

    Google Scholar 

  • Wang, A. M., Q. Xia, W. S. Xie, R. Datla & G. Selvaraj. 2003. The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proceedings of the National Academy of Sciences, USA 100: 14487–14492.

    CAS  Google Scholar 

  • Weber, M., H. Halbritter & M. Hesse. 1998. The spiny pollen wall in Sauromatum (Araceae) - With special reference to the endexine. International Journal of Plant Science 159: 744–749.

    Google Scholar 

  • Wilson, Z. A. & D.-B. Zhang. 2009. From Arabidopsis to rice: pathways in pollen development. Journal of Experimental Biology 60: 1479–1492.

    CAS  Google Scholar 

  • Wolter, M., C. Seuffert & R. Schill. 1988. The ontogeny of pollinia and elastoviscin in the anther of Doritis pulcherrima (Orchidaceae). Nordic Journal of Botany 8: 77–88.

    Google Scholar 

  • Wu, S. S. H., K. A. Platt, C. Ratnayake, T.-W. Wang, J. T. L. Ting & A. H. C. Huang. 1997. Isolation and characterization of neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum. Proceedings of the National Academy of Sciences, USA 94: 12711–12716.

    CAS  Google Scholar 

  • Wu, S., S. J. B. O’Leary, S. Gleddie, F. Eudes, A. Laroche & L. S. Robert. 2008. A chalcone synthase-like gene is highly expressed in the tapetum of both wheat (Triticum aestivum L.) and triticale (x Triticosecale Wittmack). Plant Cell Reports 27: 1441–1449.

    CAS  PubMed  Google Scholar 

  • Yui, R., S. Iketani, T. Mikami & T. Kubo. 2003. Antisense inhibition of mitochondrial pyruvate dehydrogenase E1α subunit in anther tapetum causes male sterility. Plant Journal 34: 57–66.

    CAS  PubMed  Google Scholar 

  • Zavada, M. S. & N. Gabarayeva. 1991. Comparative pollen wall development of Welwitschia mirabilis and selected primitive angiosperms. Bulletin of the Torrey Botanical Club 118: 292–302.

    Google Scholar 

  • Zetter, R., M. Weber, M. Hesse & M. Pingen. 2002. Pollen, pollenkitt, and orbicules in Craigia bronnii flower buds (Tilioideae, Malvaceae) from the Miocene of Hambach, Germany. International Journal of Plant Sciences 163: 1067–1071.

    Google Scholar 

  • Zhang, D., W. Liang, C. Yin, J. Zong, F. Gu & D. Zhang. 2010. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiology 154: 149–162.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, X.-H., Y. Ren & X.-H. Tian. 2012. Microsporogenesis and megasporogenesis in Sinofranchetia (Lardizabalaceae). Flora 207: 197–202.

    Google Scholar 

Download references

Acknowledgments

The authors gratefully thank N. Geerts (KU Leuven) and F. Christie (RBG Edinburgh) for technical assistance, A. Wortley and A. Poulsen for hospitality and sampling assistance to the last author at Royal Botanic Gardens Edinburgh, and A. Worberg for drawing an updated and tailor-made bubble diagram of angiosperms. Special thanks are due to all whom kindly shared personal observations of orbicules with special mention of L. Ronse De Craene, F. Gonzalez and G. Prenner, and to all students at the Laboratory of Plant Systematics who contributed to the dense asterid and monocots sampling. S. Blackmore, M. Hesse, and the late J. Rowley are gratefully acknowledged by the last author for stimulating discussions on orbicules. A visit to RBG Edinburgh by the last author was funded by the European Commission’s Research Infrastructure Action via the Synthesys Project (GB-TAF-5561). The Research Foundation - Flanders (FWO, G.0268.04, G.0250.05) and the KU Leuven (OT/05/35) financially supported our research. This work is dedicated to Gamal El-Ghazaly (1947–2001) and John Rowley (1926–2010).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brecht Verstraete.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Appendix S1

Orbicule distribution data for flowering plants including tapetum characterisation if available. Note that in literature, orbicule data is obtained from observations at species level, while tapetum data is often extrapolated at generic level. Classification of families in higher order taxa follows APG III (2009) except for the recognition of Taccaceae and Thismiaceae as separate families in Dioscoreales (Merckx et al., 2006), the recognition of the monotypic order Dilleniales for Dilleniaceae, and the inclusion of Rafflesiaceae in Euphorbiaceae (with recognition of Peraceae to maintain monophyly of Euphorbiaceae). The assignment of taxa to families is according to Stevens (2001 onwards). At order level, families are arranged alphabetically. To allow cross-reference to Huysmans et al. (1998, 2000), taxa included in those two papers are repeated with the respective reference. Note that in these cases, family designation was updated according to Stevens (2001 onwards). Notes: O = orbicules; T = tapetum; + = presence; − = absence; A = amoeboid tapetum; I = invasive tapetum; P = parietal tapetum. (DOC 2358 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Verstraete, B., Moon, HK., Smets, E. et al. Orbicules in Flowering Plants: A Phylogenetic Perspective on their Form and Function. Bot. Rev. 80, 107–134 (2014). https://doi.org/10.1007/s12229-014-9135-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12229-014-9135-1

Keywords

Navigation