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

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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.

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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.

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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).

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Authors and Affiliations

  1. Laboratory of Plant Systematics, KU Leuven, Kasteelpark Arenberg 31, PO Box 2435, 3001, Leuven, Belgium

    Brecht Verstraete, Hye-Kyoung Moon, Erik Smets & Suzy Huysmans

  2. Botanic Garden Meise, Domein van Bouchout, 1850, Meise, Belgium

    Brecht Verstraete

  3. Naturalis Biodiversity Center, Leiden University, PO Box 9517, 2300 RA, Leiden, The Netherlands

    Erik Smets

  4. Faculty of Science, University of Antwerp, Groenenborgerlaan 171, 2020, Antwerp, Belgium

    Suzy Huysmans

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Correspondence to Brecht Verstraete.

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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)

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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

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