Could microechinate orbicules be related to the release of pollen in anemophilous and ‘buzz pollination’ species?
Beatriz G. Galati A E , Marina M. Gotelli A B , Andrés E. Dolinko B C D and Sonia Rosenfeldt C
+ Author Affiliations
- Author Affiliations
A Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Recursos Naturales y Ambiente, Cátedra de Botánica General, Buenos Aires, Argentina.
B Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Godoy Cruz 2290 (C1425FQB) Buenos Aires, Argentina.
C Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Buenos Aires, Argentina.
D Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Ingeniería Agrícola y Uso de la Tierra, Cátedra de Física, Buenos Aires, Argentina.
E Corresponding author. Email: galati@agro.uba.ar
Australian Journal of Botany 67(1) 16-35 https://doi.org/10.1071/BT18169
Submitted: 28 August 2018 Accepted: 17 December 2018 Published: 11 February 2019
Abstract
The function of orbicules has been a matter of speculation for a long time and until now no satisfactory answer has been put forward. We propose two hypotheses that could contribute to the elucidation of their function: (1) that anemophilous and ‘buzz pollination’ species have microechinate orbicules; and (2) that microechinate orbicules are advantageous for pollen release in both pollination modes. To test the first hypothesis, orbicule morphology of species in which the pollen is released by anther shaking (20 anemophilous and three with buzz-pollination) was analysed. We also conducted a literature review, noting the orbicule surface type and the presence of floral traits suggesting that pollen is released by anther shaking. Ninety-two percent of the species with microechinate orbicules are anemophilous or present ‘buzz pollination’. Orbicules without spinules are present in species that lack floral traits linked to anther shaking for pollen release. To test the second hypothesis, a computational simulation that reveals the electric field produced by electrostatically charged orbicules was used. Results showed that the field is increased at the tip of each orbicule spinule. Therefore, an anther loculus surface coated by pointed structures increases the repulsion force of the pollen grains. This is an advantage when pollen is released by shaking the anther.
Additional keywords: anemophilous pollination mode, electrostatic field, microechinate orbicule.
References
Abadie M, Hideux M (1979) L’anthère de Saxifraga cymbalaria L. ssp. huetiana (Boiss.) Engl. et Iemsch en microscopie électronique (M.E.B. et M.E.T). 1. Généralités. Ontogenèse des orbicules. Annales des Sciences Naturelles Botanique 13, 199–233.Amela García MT, Galati BG, Anton AM (2002) Microsporogenesis, microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae). Botanical Journal of the Linnean Society 139, 383–394.
| Microsporogenesis, microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae).Crossref | GoogleScholarGoogle Scholar |
Audran JC, Batcho M (1980) Aspects infrastructuraux des alterations antheres de Silene dioica parasitees par Ustilago violacea. Canadian Journal of Botany 58, 405–415.
| Aspects infrastructuraux des alterations antheres de Silene dioica parasitees par Ustilago violacea.Crossref | GoogleScholarGoogle Scholar |
Buchmann SL (1983) Buzz pollination in angiosperms. In ‘Handbook of experimental pollination biology’. (Eds CE Jones, RJ Little) pp. 73–113. (Van Nostrand Reinhold: New York)
Cardoso CC de, Oliveira PEAM de, Pimentel RM de M (2008) Reproductive biology of the herkogamous vine Chiococca alba (L.) Hitchc. (Rubiaceae) in the Atlantic rain forest, SE Brazil. Revista Brasileira de Botanica. Brazilian Journal of Botany 31, 317–321.
| Reproductive biology of the herkogamous vine Chiococca alba (L.) Hitchc. (Rubiaceae) in the Atlantic rain forest, SE Brazil.Crossref | GoogleScholarGoogle Scholar |
Chen SH (1988) A scanning electron microscope survey of common airborne pollen grains in Taipei, Taiwan. Taiwania 33, 75–108.
Chen SK, Wang FH, Zhou F (1988) On the origin, development and ultrastructure of the orbicuies and pollenkitt in the tapetum of Anemarrhena asphodeloides (Liliaceae). Grana 27, 273–282.
| On the origin, development and ultrastructure of the orbicuies and pollenkitt in the tapetum of Anemarrhena asphodeloides (Liliaceae).Crossref | GoogleScholarGoogle Scholar |
Christensen JE, Horner HT, Lersten NR (1972) Pollen wall and tapetal orbicular wall development in Sorghum bicolor (Gramineae). American Journal of Botany 59, 43–58.
| Pollen wall and tapetal orbicular wall development in Sorghum bicolor (Gramineae).Crossref | GoogleScholarGoogle Scholar |
Clement C, Audran JC (1993) Cytochemical and ultrastructural evolution of orbicules in Lilium. Plant Systematics and Evolution 7, 63–74.
Coetzee H, Robbertse PJ (1985) Pollen and tapetum development in Securidaca longipedunculata. South African Journal of Botany 51, 111–124.
| Pollen and tapetum development in Securidaca longipedunculata.Crossref | GoogleScholarGoogle Scholar |
Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollination in angiosperms. Trends in Ecology & Evolution 17, 361–369.
| The evolution of wind pollination in angiosperms.Crossref | GoogleScholarGoogle Scholar |
D’Hondt C, Schols P, Huysmans S, Smets E (2004) Systematic relevance of pollen and orbicule characters in the tribe Hillieae (Rubiaceae). Botanical Journal of the Linnean Society 146, 303–321.
| Systematic relevance of pollen and orbicule characters in the tribe Hillieae (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |
de Figueiredo RA, Sazima M (2000) Pollination biology of Piperaceae species in southeastern Brazil. Annals of Botany 85, 455–460.
| Pollination biology of Piperaceae species in southeastern Brazil.Crossref | GoogleScholarGoogle Scholar |
Dinis AM, Baptista F, Pereira Coutinho A (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.
| Is the quantity of orbicules released by Dactylis glomerata and Cynosurus echinatus (Poaceae) big enough to play an allergenic role?Crossref | GoogleScholarGoogle Scholar |
Dolinko AE (2008) Non-destructive visualization of defect borders in flawed plates inspected by thermal load. Journal of Physics. D, Applied Physics 41, 205503
| Non-destructive visualization of defect borders in flawed plates inspected by thermal load.Crossref | GoogleScholarGoogle Scholar |
Dolinko AE (2009) From Newton’s second law to Huygens’s principle: visualizing waves in a large array of masses joined by springs. European Journal of Physics 30, 1217–1228.
| From Newton’s second law to Huygens’s principle: visualizing waves in a large array of masses joined by springs.Crossref | GoogleScholarGoogle Scholar |
Dolinko AE (2018) Kirchhoff and Ohm in action: solving electric currents in continuous extended media. European Journal of Physics 39, 025201
| Kirchhoff and Ohm in action: solving electric currents in continuous extended media.Crossref | GoogleScholarGoogle Scholar |
Dolinko A, Losinno B, Zunni N, Lemeillet F (2016) Analysis of the response of the electrical resistivity tomography method to soil cracks. In ‘Near Surface Geoscience. The 22nd European Meeting of Enviromental and Engineering Geophysics’. Barcelona, Spain.
Doores AS, Osborn JM, El-Ghazaly G (2007) Pollen ontogeny in Ephedra americana (Gnetales). International Journal of Plant Sciences 168, 985–997.
| Pollen ontogeny in Ephedra americana (Gnetales).Crossref | GoogleScholarGoogle Scholar |
Doria MG, Pabón-Mora N, González F (2012) Reassessing inflorescence and floral morphology and development in Hedyosmum (Chloranthaceae). International Journal of Plant Sciences 173, 735–750.
| Reassessing inflorescence and floral morphology and development in Hedyosmum (Chloranthaceae).Crossref | GoogleScholarGoogle Scholar |
Echlin P, Godwin H (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.
El-Ghazaly G (1989) Pollen and orbicule morphology of some Euphorbia species. Grana 28, 243–259.
| Pollen and orbicule morphology of some Euphorbia species.Crossref | GoogleScholarGoogle Scholar |
El-Ghazaly G, Chaudhary R (1993) Morphology and taxonomic application of orbicules (Ubisch bodies) in the genus Euphorbia. Grana 32, 26–32.
| Morphology and taxonomic application of orbicules (Ubisch bodies) in the genus Euphorbia.Crossref | GoogleScholarGoogle Scholar |
El-Ghazaly G, Jensen WA (1986) Studies of the development of wheat (Triticum aestivum) pollen. I. Formation of the pollen wall and Ubisch bodies. Grana 25, 1–29.
| Studies of the development of wheat (Triticum aestivum) pollen. I. Formation of the pollen wall and Ubisch bodies.Crossref | GoogleScholarGoogle Scholar |
El-Ghazaly G, Jensen WA (1987) Development of wheat (Triticum aestivum) pollen. II. Histochemical differentiation of wall and Ubisch bodies during development. American Journal of Botany 74, 1396–1418.
| Development of wheat (Triticum aestivum) pollen. II. Histochemical differentiation of wall and Ubisch bodies during development.Crossref | GoogleScholarGoogle Scholar |
El-Ghazaly G, Nilsson S (1991) Development of tapetum and orbicules of Catharanthus roseus (Apocynaceae). In ‘Pollen and spores’. (Eds S Blackmore, SH Barnes) pp. 317–329. (Clarendon Press: Oxford, UK)
El-Ghazaly G, Takahashi Y, Nilsson S, Grafstrom E, Berggren B (1995) Orbicules in Betula pendula and their possible role in allergy. Grana 34, 300–304.
| Orbicules in Betula pendula and their possible role in allergy.Crossref | GoogleScholarGoogle Scholar |
Endress PK (1998) ‘Diversity and evolutionary biology of tropical flowers.’ (Cambridge University Press: Cambridge, UK)
Fernando DD, Cass DD (1994) Plasmodial tapetum and pollen wall development in Butomus umbellatus (Butomaceae). American Journal of Botany 81, 1592–1600.
| Plasmodial tapetum and pollen wall development in Butomus umbellatus (Butomaceae).Crossref | GoogleScholarGoogle Scholar |
Furness CA (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.
| Comparative structure and development of pollen and tapetum in Malpighiales, with a focus on the parietal clade.Crossref | GoogleScholarGoogle Scholar |
Furness CA, Rudall PJ (2001) The tapetum in basal angiosperms: early diversity. International Journal of Plant Sciences 162, 375–392.
| The tapetum in basal angiosperms: early diversity.Crossref | GoogleScholarGoogle Scholar |
Furness CA, Rudall PJ (2006) Comparative structure and development of the tapetum and pollen in Pandanales. International Journal of Plant Sciences 167, 331–348.
| Comparative structure and development of the tapetum and pollen in Pandanales.Crossref | GoogleScholarGoogle Scholar |
Furness CA, Gregory T, Rudall PJ (2015) Pollen structure and diversity in Liliales. International Journal of Plant Sciences 176, 697–723.
| Pollen structure and diversity in Liliales.Crossref | GoogleScholarGoogle Scholar |
Gabarayeva NI (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.
| Pollen wall and tapetum development in Anaxagorea brevipes (Annonaceae): sporoderm substructure, cytoskeleton, sporopollenin precursor particles, and the endexine problem.Crossref | GoogleScholarGoogle Scholar |
Gabarayeva N, Grigorjeva V (2012) Sporoderm development and substructure in Magnolia sieboldii and other Magnoliaceae: an interpretation. Grana 51, 119–147.
| Sporoderm development and substructure in Magnolia sieboldii and other Magnoliaceae: an interpretation.Crossref | GoogleScholarGoogle Scholar |
Gabarayeva NI, Grigorjeva VV, Rowley JR (2010) Sporoderm development in Acer tataricum (Aceraceae): an interpretation. Protoplasma 247, 65–81.
| Sporoderm development in Acer tataricum (Aceraceae): an interpretation.Crossref | GoogleScholarGoogle Scholar | 20431899PubMed |
Galati BG (2003) Ubisch bodies in angiosperms. In ‘Advances in plant reproductive biology’. (Eds AK Pandey, MR Dhakal) pp. 1–21. (Narendra Publishing House: Delhi, India)
Galati BG, Strittmatter LI (1999) Correlation between pollen development and Ubisch bodies ontogeny in Jacaranda mimosifolia (Bignoniaceae). Beitrage zur Biologie der Pflanzen 71, 1–12.
Galati BG, Monacci F, Gotelli MM, Rosenfeldt S (2007) Pollen, tapetum and orbicule development in Modiolastrum malvifolium (Malvaceae). Annals of Botany 99, 755–763.
| Pollen, tapetum and orbicule development in Modiolastrum malvifolium (Malvaceae).Crossref | GoogleScholarGoogle Scholar | 17353203PubMed |
Galati BG, Zarlavsky G, Rosenfeldt S, Gotelli MM (2012) Pollen ontogeny in Magnolia liliflora Desr. Plant Systematics and Evolution 298, 527–534.
| Pollen ontogeny in Magnolia liliflora Desr.Crossref | GoogleScholarGoogle Scholar |
Gaudeul M, Till-Bottraud I (2003) Low selfing in a mass-flowering, endangered perennial, Eryngium alpinum L. (Apiaceae). American Journal of Botany 90, 716–723.
| Low selfing in a mass-flowering, endangered perennial, Eryngium alpinum L. (Apiaceae).Crossref | GoogleScholarGoogle Scholar | 21659167PubMed |
Geeraerts A, Raeymaekers JAM, Vinckier S, Pletsers A, Smets E, Huysmans S (2009) Systematic palynology in Ebenaceae with focus on Ebenoideae: morphological diversity and character evolution. Review of Palaeobotany and Palynology 153, 336–353.
| Systematic palynology in Ebenaceae with focus on Ebenoideae: morphological diversity and character evolution.Crossref | GoogleScholarGoogle Scholar |
González F, Rudall PJ, Furness CA (2001) Microsporogenesis and systematics of Aristolochiaceae. Botanical Journal of the Linnean Society 137, 221–242.
| Microsporogenesis and systematics of Aristolochiaceae.Crossref | GoogleScholarGoogle Scholar |
Gori P, Ferri S (1982) Ultrastructural study of the microspore development in Allium sativum, cl. Piemonte. Journal of Ultrastructure Research 79, 341–349.
| Ultrastructural study of the microspore development in Allium sativum, cl. Piemonte.Crossref | GoogleScholarGoogle Scholar | 7086951PubMed |
Gotelli MM, Galati BG, Medan D (2008) Embryology of Helianthus annuus (Asteraceae). Annales Botanici Fennici 45, 81–96.
| Embryology of Helianthus annuus (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Gotelli MM, Galati BG, Medan D (2012) Pollen, tapetum and orbicule development in Colletia paradoxa and Discaria americana (Rhamnaceae). Scientific World Journal 2012, 948469
| Pollen, tapetum and orbicule development in Colletia paradoxa and Discaria americana (Rhamnaceae).Crossref | GoogleScholarGoogle Scholar |
Gotelli MM, Galati BG, Zarlavsky G (2016) Pollen development and anther morphology in 14 species of Rhamnaceae. Plant Systematics and Evolution 302, 1433–1444.
| Pollen development and anther morphology in 14 species of Rhamnaceae.Crossref | GoogleScholarGoogle Scholar |
Halbritter Halbritter (2005) Specific ornametation of orbicular walls and pollen grains, as exemplified by Acanthaceae. Grana 44, 308–313.
Halbritter H, Hesse M, Weber M (2012) The unique design of pollen tetrads in Dionaea and Drosera. Grana 51, 148–157.
| The unique design of pollen tetrads in Dionaea and Drosera.Crossref | GoogleScholarGoogle Scholar |
Hall JA, Walter GH (2018) Pollination of the Australian cycad Cycas ophiolitica (Cycadaceae): the limited role of wind pollination in a cycad with beetle pollinator mutualists, and its ecological significance. Journal of Tropical Ecology 34, 121–134.
| Pollination of the Australian cycad Cycas ophiolitica (Cycadaceae): the limited role of wind pollination in a cycad with beetle pollinator mutualists, and its ecological significance.Crossref | GoogleScholarGoogle Scholar |
Herich R, Lux A (1985) Lytic activity of Ubisch bodies (orbicles). Cytologia 50, 563–569.
| Lytic activity of Ubisch bodies (orbicles).Crossref | GoogleScholarGoogle Scholar |
Heslop-Harrison J (1968a) Pollen wall development. Science 161, 230–237.
| Pollen wall development.Crossref | GoogleScholarGoogle Scholar | 5657325PubMed |
Heslop-Harrison J (1968b) Tapetal origin of pollen-coat substances in Lilium. New Phytologist 67, 779–786.
| Tapetal origin of pollen-coat substances in Lilium.Crossref | GoogleScholarGoogle Scholar |
Hesse M (1984) Pollenkitt is lacking in Gnetatae: Ephedra and Welwitschia; further proof for its restriction to the angiosperms. Plant Systematics and Evolution 144, 9–16.
| Pollenkitt is lacking in Gnetatae: Ephedra and Welwitschia; further proof for its restriction to the angiosperms.Crossref | GoogleScholarGoogle Scholar |
Hesse M (1986) Orbicules and the ektexine are homologous sporopollenin concretions in Spermatophyta. Plant Systematics and Evolution 153, 37–48.
| Orbicules and the ektexine are homologous sporopollenin concretions in Spermatophyta.Crossref | GoogleScholarGoogle Scholar |
Hesse M (2000) Pollen wall stratification and pollination. Plant Systematics and Evolution 222, 1–17.
| Pollen wall stratification and pollination.Crossref | GoogleScholarGoogle Scholar |
Hesse M (2001) Pollen characters of Amborella trichopoda (Amborellaceae): a reinvestigation. International Journal of Plant Sciences 162, 201–208.
| Pollen characters of Amborella trichopoda (Amborellaceae): a reinvestigation.Crossref | GoogleScholarGoogle Scholar |
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.
| Systematic value of tapetal orbicules: a preliminary survey of the Cinchonoideae (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |
Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. Botanical Review 64, 240–272.
| Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types.Crossref | GoogleScholarGoogle Scholar |
Huysmans S, El-Ghazaly G, Smets E (2000) Orbicules: still a well-hidden secret of the anther. In ‘Plant systematics for the 21st century’. (Eds B Nordenstam, G El-Ghazaly, M Kassas) pp. 201–212. (Portland Press: London)
Huysmans S, Verstraete B, Smets E, Chatrou LW (2010) Distribution of orbicules in Annonaceae mirrors evolutionary trend in angiosperms. Plant Ecology and Evolution 143, 199–211.
| Distribution of orbicules in Annonaceae mirrors evolutionary trend in angiosperms.Crossref | GoogleScholarGoogle Scholar |
Keijzer CJ (1984) Pollen dispersal and the function of the orbicules. Acta Botanica Neerlandica 33, 244
Kreunen SS, Osborn JM (1999) Pollen and anther development in Nelumbo (Nelumbonaceae). American Journal of Botany 86, 1662–1676.
| Pollen and anther development in Nelumbo (Nelumbonaceae).Crossref | GoogleScholarGoogle Scholar | 10602759PubMed |
Lattar EC, Galati BG, Ferrucci MS (2012) Ultrastructural study of pollen and anther development in Luehea divaricata (Malvaceae, Grewioideae) and its systematic implications: Role of tapetal transfer cells, orbicules and male germ unit. Flora 207, 888–894.
| Ultrastructural study of pollen and anther development in Luehea divaricata (Malvaceae, Grewioideae) and its systematic implications: Role of tapetal transfer cells, orbicules and male germ unit.Crossref | GoogleScholarGoogle Scholar |
Le Thomas A, Suàrez-Cervera M, Goldblatt P (2001) Ontogeny of the exine in pollen of Aristea (Iridaceae). Grana 40, 35–44.
| Ontogeny of the exine in pollen of Aristea (Iridaceae).Crossref | GoogleScholarGoogle Scholar |
Lens F, Dressler S, Vinckier S, Janssens S, Dessein S, Van Evelghem L, Smets E (2005) Palynological variation in balsaminoid Ericales. I. Marcgraviaceae. Annals of Botany 96, 1047–1060.
| Palynological variation in balsaminoid Ericales. I. Marcgraviaceae.Crossref | GoogleScholarGoogle Scholar | 16157628PubMed |
Lombardo G, Carraro L (1976) Tapetal ultrastructural changes during pollen development. III. Studies on Gentiana acaulis. Caryologia 29, 345–349.
| Tapetal ultrastructural changes during pollen development. III. Studies on Gentiana acaulis.Crossref | GoogleScholarGoogle Scholar |
Lovisolo M, Galati BG (1999) Pollen development in Deyeuxia viridiflavescens (Poir) Kunth (Gramineae: Poaceae). Phytomorphology 49, 411–418.
Lovisolo M, Galati BG (2012) Diversidad de orbículas en Poaceae. Boletín de la Sociedad Argentina de Botánica 47, 87–96.
Maheshwari P (1950) ‘Introduction to the embryology of angiosperms.’ (McGraw-Hill: New York)
Mariotti Lippi M, Cimoli F, Maugini E, Tani G (1994) A comparative study of the tapetal behaviour in male fertile and male sterile Iris pallida Lam. during microsporogenesis. Caryologia 47, 109–120.
| A comparative study of the tapetal behaviour in male fertile and male sterile Iris pallida Lam. during microsporogenesis.Crossref | GoogleScholarGoogle Scholar |
Merckx V, Schols P, Geuten K, Huysmans S, Smets E (2008) Phylogenetic relationships in Nartheciaceae (Dioscoreales) with focus on pollen and orbicule morphology. Belgian Journal of Botany 141, 64–77.
Mi-Mi L, Qin-Qin Y, Xiao-Qin S, Ya-Mei Z, Yi-Feng Z, Yue-Yu H (2014) A preliminary study on pollination biology of three species in Dioscorea (Dioscoreaceae). Life Science Journal 11, 436–444.
Mu X, Wang F, Wang W (1988) Development and histochemical observations of tapetum and peritapetal membrane in anther of Pulsatilla chinensis. Acta Botanica Sinica 30, 6–13.
Nagels A, Muasya AM, Huysmans S, Vrijdaghs A, Smets E, Vinckier S (2009) Palynological diversity and major evolutionary trends in Cyperaceae. Plant Systematics and Evolution 277, 117–142.
| Palynological diversity and major evolutionary trends in Cyperaceae.Crossref | GoogleScholarGoogle Scholar |
Nitiu DS (2006) Aeropalynologic analysis of La Plata City (Argentina) during a 3-year period. Aerobiologia 22, 79–87.
| Aeropalynologic analysis of La Plata City (Argentina) during a 3-year period.Crossref | GoogleScholarGoogle Scholar |
O’Brien TP, McCully ME (1981) ‘The study of plant structure: principles and selected methods.’ (Termarcarphi Pty Ltd: Melbourne)
Pacini E (1997) Tapetum character states: analytical keys for tapetum types and activities. Canadian Journal of Botany 75, 1448–1459.
| Tapetum character states: analytical keys for tapetum types and activities.Crossref | GoogleScholarGoogle Scholar |
Pacini E, Franchi GG (1993) Role of the tapetum in pollen and spore dispersal. Plant Systematics and Evolution 7, 1–11.
Pacini E, Franchi GG, Hesse M (1985) The tapetum: its form, function and possible phylogeny in Embryophyta. Plant Systematics and Evolution 149, 155–185.
| The tapetum: its form, function and possible phylogeny in Embryophyta.Crossref | GoogleScholarGoogle Scholar |
Proctor M, Yeo P, Lack A (1996) ‘The natural history of pollination.’ (Timber Press: Portland, OR, USA)
Ronse De Craene LP, Yang TA, Schols P, Smets E (2002) Flower anatomy and systematics of Bretschneidera (Bretschneideraceae). Botanical Journal of the Linnean Society 139, 29–45.
| Flower anatomy and systematics of Bretschneidera (Bretschneideraceae).Crossref | GoogleScholarGoogle Scholar |
Rosenfeldt S, Galati BG (2005) Ubisch bodies and pollen ontogeny in Oxalis articulata Savigny. Biocell 29, 271–278.
Rosenfeldt S, Galati BG (2008) Orbicules diversity in Oxalis species from Buenos Aires province (Argentina). Biocell 32, 41–47.
Rowley JR, Erdtman G (1967) Sporoderm in Populus and Salix. Grana 7, 518–567.
Rowley JR, Gabarayeva NI (2004) Microspore development in Quercus robur (Fagaceae). Review of Palaeobotany and Palynology 132, 115–132.
| Microspore development in Quercus robur (Fagaceae).Crossref | GoogleScholarGoogle Scholar |
Rowley JR, Walles B (1987) Origin and structure of Ubisch bodies in Pinus sylvestris. Acta Societatis Botanicorum Poloniae 56, 215–227.
| Origin and structure of Ubisch bodies in Pinus sylvestris.Crossref | GoogleScholarGoogle Scholar |
Ruggiero F, Bedini G (2018) Free orbicules of Cupressaceae detected in daily aerobiological samples by optical and confocal microscopy. Aerobiologia 34, 55
| Free orbicules of Cupressaceae detected in daily aerobiological samples by optical and confocal microscopy.Crossref | GoogleScholarGoogle Scholar |
Sajo MG, Furness CA, Prychid CJ, Rudall PJ (2005) Microsporogenesis and anther development in Bromeliaceae. Grana 44, 65–74.
| Microsporogenesis and anther development in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Schols P, Furness CA, Wilkin P, Huysmans S, Smets E (2001) Morphology of pollen and orbicules in some Dioscorea species and its systematic implications. Botanical Journal of the Linnean Society 136, 295–311.
| Morphology of pollen and orbicules in some Dioscorea species and its systematic implications.Crossref | GoogleScholarGoogle Scholar |
Schols P, Furness CA, Wilkin P, Smets E, Cielen V, Huysmans S (2003) Pollen morphology of Dioscorea (Dioscoreaceae) and its relation to systematics. Botanical Journal of the Linnean Society 143, 375–390.
Schols P, Wilkin P, Furness CA (2005) Pollen evolution in yams (Dioscorea: Dioscoreaceae). Systematic Botany 30, 750–758.
Skarby A, Morbelli MA, Rowley JR (2009) Structure of the pollen exine of Rhoiptelea chiliantha. Taiwania 54, 101–112.
Strittmatter LI, Galati BG (2000) Embryological study in Oziroë acaulis (Baker) Speta (Hyacinthaceae). Phytomorphology 50, 161–171.
Strittmatter LI, Galati BG (2001) Development of anthers, microsporogenesis and microgametogenesis of Myosotis azorica and M. laxa (Boraginaceae). Phytomorphology 51, 1–10.
Strittmatter LI, Galati BG, Monacci F (2000) Übisch bodies in the peritapetal membrane of Abutilon pictum Gill (Malvaceae). Beitrage zur Biologie der Pflanzen 71, 1–10.
Sun S-G, Lu Y, Huang S-Q (2006) Floral phenology and sex expression in functionally monoecious Rhoiptelea chiliantha (Rhoipteleaceae). Botanical Journal of the Linnean Society 152, 145–151.
| Floral phenology and sex expression in functionally monoecious Rhoiptelea chiliantha (Rhoipteleaceae).Crossref | GoogleScholarGoogle Scholar |
Taylor ML, Hudson PJ, Rigg JM, Julie N, Schwartz Green J, Thiemann TC, Osborn JM (2012) Tapetum structure and ontogeny in Victoria (Nymphaeaceae). Grana 51, 107–118.
| Tapetum structure and ontogeny in Victoria (Nymphaeaceae).Crossref | GoogleScholarGoogle Scholar |
Teppner H, Stabentheiner E (2007) Anther opening, polyad presentation, pollenkitt and pollen adhesive in four Calliandra species (Mimosaceae-Ingeae). Phyton 47, 291–320.
Ubisch G von (1927) Kurze mitteilungen zur entwicklungsgeschiehte der antheren. Planta 3, 490–495.
| Kurze mitteilungen zur entwicklungsgeschiehte der antheren.Crossref | GoogleScholarGoogle Scholar |
Verellen J, Smets E, Huysmans S (2004) The remarkable genus Coptosapelta (Rubiaceae): pollen and orbicule morphology and systematic implications. Journal of Plant Research 117, 57–68.
| The remarkable genus Coptosapelta (Rubiaceae): pollen and orbicule morphology and systematic implications.Crossref | GoogleScholarGoogle Scholar | 14999514PubMed |
Verstraete B, Groeninckx I, Smets E, Huysmans S (2011) Phylogenetic signal of orbicules at family level: Rubiaceae as case study. Taxon 60, 742–757.
Verstraete B, Moon HK, Smets E, Huysmans S (2014) Orbicules in flowering plants: a phylogenetic perspective on their form and function. Botanical Review 80, 107–134.
| Orbicules in flowering plants: a phylogenetic perspective on their form and function.Crossref | GoogleScholarGoogle Scholar |
Vinckier S, Smets E (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.
| A survey of the presence and morphology of orbicules in European allergenic angiosperms. Background information for allergen research.Crossref | GoogleScholarGoogle Scholar |
Vinckier S, Smets E (2001b) The potential role of orbicules as a vector of allergens. Allergy 56, 1129–1136.
| The potential role of orbicules as a vector of allergens.Crossref | GoogleScholarGoogle Scholar | 11736741PubMed |
Vinckier S, Smets E (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.
| Morphology, ultrastructure and typology of orbicules in Loganiaceae s.l. and related genera, in relation to systematics.Crossref | GoogleScholarGoogle Scholar |
Vinckier S, Smets E (2002b) Morphological and ultrastructural diversity of orbicules in relation to evolutionary tendencies in Apocynaceae s.l. Annals of Botany 90, 647–662.
| Morphological and ultrastructural diversity of orbicules in relation to evolutionary tendencies in Apocynaceae s.l.Crossref | GoogleScholarGoogle Scholar | 12466106PubMed |
Vinckier S, Smets E (2002c) Systematic importance in orbicule diversity in Gentianales. Grana 41, 158–182.
| Systematic importance in orbicule diversity in Gentianales.Crossref | GoogleScholarGoogle Scholar |
Vinckier S, Smets E (2003) Morphological and ultrastructural diversity of orbicules in Gentianaceae. Annals of Botany 92, 657–672.
| Morphological and ultrastructural diversity of orbicules in Gentianaceae.Crossref | GoogleScholarGoogle Scholar | 14500324PubMed |
Vinckier S, Huysmans S, Smets E (2000) Morphology and ultrastructure of orbicules in the subfamily Ixoroideae (Rubiaceae). Review of Palaeobotany and Palynology 108, 151–174.
| Morphology and ultrastructure of orbicules in the subfamily Ixoroideae (Rubiaceae).Crossref | GoogleScholarGoogle Scholar | 10704642PubMed |
Vinckier S, Cadot P, Smets E (2005) The manifold characters of orbicules: structural diversity, systematic significance, and vectors for allergens. Grana 44, 300–307.
| The manifold characters of orbicules: structural diversity, systematic significance, and vectors for allergens.Crossref | GoogleScholarGoogle Scholar |
Zavada MS (1984) Pollen wall development of Austrobaileya maculata. Botanical Gazette 145, 11–21.
| Pollen wall development of Austrobaileya maculata.Crossref | GoogleScholarGoogle Scholar |
Zini LM, Galati BG, Zarlavsky G, Ferrucci MS (2017) Developmental and ultrastructural characters of the pollen grains and tapetum in species of Nymphaea subgenus Hydrocallis. Protoplasma 254, 1777–1790.
| Developmental and ultrastructural characters of the pollen grains and tapetum in species of Nymphaea subgenus Hydrocallis.Crossref | GoogleScholarGoogle Scholar | 28083653PubMed |
