Skip to main content

Flower and fruit anatomy of Cordia nodosa Lam. and Varronia bonplandii Desv. (Cordiaceae, Boraginales) with phylogenetic implications

Abstract

Despite their ecological importance and wide distribution, Cordiaceae have not been subject to detailed anatomical study yet. We examined flower and fruit anatomies of Cordia nodosa and Varronia bonplandii (using paraffin sectioning and light microscopy) in comparison with other woody members of Boraginales. The internal architecture of the superior bicarpellate ovary resulted from the development of secondary septa including apical, basal and false septa, as reported also from other Boraginales. Novel characters of Cordiaceae were identified such as an extensive tissue surrounding the gynoecium of C. nodosa and a lignified cap on top of the endocarp in V. bonplandii. Fruits containing a single seed may have originated several times independently in Cordiaceae deriving from the four-seeded condition present today in most other non-capsular Boraginales. Distyly of V. bonplandii does not appear genetically fixed but may result from different ecological conditions. Hemianatropous ovules are now considered the derived character state in Cordiaceae, originating from anatropous ovules present in other Boraginales. Studies like this improve the knowledge about generative organs in general and identify phylogenetically informative characters. However, better knowledge of functional morphology and ecological importance regarding many traits identified require further investigations on the diversity of Cordiaceae.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Baillon, H. (1863). Organogénie florale des Cordiacées. Adansonia, 3, 1–7.

    Google Scholar 

  • Borhidi, A., Gondár, E., & Orosz-Kovács, Z. (1988). The re-consideration of the genus Cordia L. Acta Botanica Hungaria, 34, 375–423.

    Google Scholar 

  • Bouman, F. (1984). The ovule. In B. M. Johri (Ed.), Embryology of angiosperms (pp. 122–157). Berlin: Springer.

    Google Scholar 

  • Candolle, A. P. D. (1845). Ordo CXXXIX. Borraginaceæ. In A. L. P. P. D. Candolle (Ed.), Prodromus Systematis Naturalis Regni Vegetabilis (pp. 466–513). Paris: Treuttel & Würtz.

    Google Scholar 

  • Desvaux, N.A. (1808). Mémoire sur le genre Varronia. Journal de Botanique, 1, 257–281.

  • Diane, N., Hilger, H. H., & Gottschling, M. (2002). Transfer cells in the seeds of Boraginales. Botanical Journal of the Linnean Society, 140, 155–164.

    Google Scholar 

  • Diane, N., Hilger, H. H., Förther, H., Weigend, M., & Luebert, F. (2016). Heliotropiaceae. In J. W. Kadereit & V. Bittrich (Eds.), Flowering plants. Eudicots, the families and genera of vascular plants 14 (pp. 203–211). Berlin: Springer.

    Google Scholar 

  • Don, G. (1838). Order CLXVII. Cordiaceae. In A general history of the dichlamydeous plants 4. Corollifloræ (pp. 374–393). London: Rivington.

  • Endress, P. K. (1994). Diversity and evolutionary biology of tropical flowers. Cambridge: Cambridge University Press.

    Google Scholar 

  • Fathima, T. (1966). Sporogenesis and the development of gametophytes in Cordia alba L. Current Science, 35, 73–74.

    Google Scholar 

  • Friesen, C. V. (1933). Les caractères essentiels de la famille des Sebestenaceae et revision du genre Varronia. Geneva: Société Genevoise d'éditions et impressions.

    Google Scholar 

  • Gaviria, J. C. (1987). Die Gattung Cordia in Venezuela. Mitteilungen der Botanischen Staatssammlung München, 23, 1–279.

    Google Scholar 

  • Gilg, E. (1908). Die systematische Stellung der Gattung Hoplestigma und einiger anderer zweifelhafter Gattungen. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie, 40, 76–84.

    Google Scholar 

  • Gottschling, M. (2003). Phylogenetic analysis of selected Boraginales. Doctoral thesis (http://www.diss.fu-berlin.de/diss/receive/FUDISS_thesis_000000001181), Freie Universität Berlin: Berlin.

  • Gottschling, M. (2004). Floral ontogeny in Bourreria (Ehretiaceae, Boraginales). Flora, 199, 409–423.

    Google Scholar 

  • Gottschling, M., & Hilger, H. H. (2004). Characterisation of a novel fruit type found in Ehretia (Ehretiaceae, Boraginales). Blumea, 49, 145–153.

    Google Scholar 

  • Gottschling, M., & Miller, J. S. (2006). Clarification of the taxonomic position of Auxemma, Patagonula, and Saccellium (Cordiaceae, Boraginales). Systematic Botany, 31, 361–367.

    Google Scholar 

  • Gottschling, M., Miller, J. S., Weigend, M., & Hilger, H. H. (2005). Congruence of a phylogeny of Cordiaceae (Boraginales) inferred from ITS1 sequence data with morphology, ecology, and biogeography. Annals of the Missouri Botanical Garden, 92, 425–437.

    Google Scholar 

  • Gottschling, M., Nagelmüller, S., & Hilger, H. H. (2014). Generative ontogeny in Tiquilia (Ehretiaceae: Boraginales) and phylogenetic implications. Biological Journal of the Linnean Society, 112, 520–534.

    Google Scholar 

  • Gottschling, M., Weigend, M., & Hilger, H. H. (2016). Ehretiaceae. In J. W. Kadereit & V. Bittrich (Eds.), Flowering plants. Eudicots, the families and genera of vascular plants (pp. 165–178). Berlin: Springer.

    Google Scholar 

  • Gürke, M. (1893). Borraginaceae. In A. Engler & K. Prantl (Eds.), Die natürlichen Pflanzenfamilien IV 3a (pp. 71–131). Leipzig: Engelmann.

    Google Scholar 

  • Hamilton, M.A. (2016). Boraginaceae. Varronia rupicola (Urb.) Britton: Biogeography, systematic placement and conservation genetics of a threatened species endemic to the Caribbean. PhD thesis, University of London: London.

  • Hartl, D. (1962). Die morphologische Natur und die Verbreitung des Apicalseptums. Analyse einer bisher unbekannten Gestaltungsmöglichkeit des Gynoeceums. Beiträge zu Biologie der Pflanzen, 37, 241–330.

    Google Scholar 

  • Heubl, G. R., Gaviria, J. C., & Wanner, G. (1990). A contribution to the taxonomy and evolution of Cordia (Boraginaceae) and allied genera. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie, 112, 129–165.

    Google Scholar 

  • Hilger, H. H. (1985). Ontogenie, Morphologie und systematische Bedeutung geflügelter und glochidientragender Cynoglosseae- und Eritricheae-Früchte (Boraginaceae). Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie, 105, 323–378.

    Google Scholar 

  • Hilger, H. H. (1987). Fruchtbiologische Untersuchungen an Heliotropioideae (Boraginaceae). I. Die Ontogenie der monospermen Früchte von Heliotropium supinum L. Flora, 179, 291–303.

    Google Scholar 

  • Hilger, H. H. (1992). Morphology of Heliotropium (Boraginaceae) dispersal units. Botanica Acta, 105, 387–393.

    Google Scholar 

  • Hilger, H. H. (2014). Ontogeny, morphology, and systematic significance of glochidiate and winged fruits of Cynoglosseae and Eritrichieae (Boraginaceae). Plant Diversity and Evolution, 131, 167–214.

    Google Scholar 

  • Hoeltgebaum, M. P., Montagna, T., Lando, A. P., Puttkammer, C., Orth, A. I., Guerra, M. P., et al. (2018). Reproductive biology of Varronia curassavica Jacq. (Boraginaceae). Anais da Academia Brasileira de Ciências, 90, 59–71.

    PubMed  Google Scholar 

  • Hofmann, M. (1994). Untersuchungen zur Gynoecealentwicklung in der Tribus Eritrichieae (Boraginaceae – Boraginoideae). Doctoral thesis, Freie Universität Berlin: Berlin.

  • Jeiter, J., Staedler, Y. M., Schönenberger, J., Weigend, M., & Luebert, F. (2018). Gynoecium and fruit development in Heliotropium sect. Heliothamnus (Heliotropiaceae). International Journal of Plant Sciences, 179, 275–286.

    Google Scholar 

  • Johnston, I. M. (1930). Studies in the Boraginaceae, VIII. Contributions from the Gray Herbarium of Havard University, 92, 3–95.

    Google Scholar 

  • Johnston, I. M. (1951). Studies in the Boraginaceae. XX. Representatives of three subfamilies on Eastern Asia. Journal of the Arnold Arboretum, 32, 1–26.

    Google Scholar 

  • Johri, B. M., & Vasil, I. K. (1956). The embryology of Ehretia laevis Roxb. Phytomorphology, 6, 134–143.

    Google Scholar 

  • Johri, B. M., Ambegaokar, K. B., & Srivastava, P. S. (1992). Comparative embryology of angiosperms. Berlin: Springer.

    Google Scholar 

  • Khaleel, T. F. (1975). Embryology of Cordia. Botanical Gazette, 136, 380–387.

    Google Scholar 

  • Khaleel, T. F. (1977). Embryology of Ehretia acuminata R. Br. Proceedings of the Montana Academy of Sciences, 37, 35–53.

    Google Scholar 

  • Khaleel, T. F. (1982). Embryology of Cordia sebestena (Boraginaceae). Plant Systematics and Evolution, 139, 303–311.

    Google Scholar 

  • Khaleel, T. F. (1985). A review of endosperm and the taxonomic position of Boraginaceae. Journal of Plant Science Research, 1, 117–133.

    Google Scholar 

  • Lamarck, J.-B. (1792). Tableau encyclopédique et méthodique. Botanique. Paris: Panckoucke.

  • Lawrence, J. R. (1937). A correlation of the taxonomy and the floral anatomy of certain of the Boraginaceae. American Journal of Botany, 24, 433–444.

    Google Scholar 

  • Leinfellner, W. (1950). Der Bauplan des synkarpen Gynözeums. Österreichische Botanische Zeitschrift, 97, 403–436.

    Google Scholar 

  • Luebert, F., Cecchi, L., Frohlich, M. W., Gottschling, M., Guilliams, C. M., Hasenstab-Lehman, K. E., et al. (2016). Familial classification of the Boraginales. Taxon, 65, 502–522.

    Google Scholar 

  • Martins, E.S. (1990). 116. Boraginaceae. In E. Launert & G.V. Pope (Eds), Flora Zambesiaca. Managing Committee on behalf of the Contributors to Flora Zambesiaca.

  • Mez, C. (1890). Morphologische und anatomische Studien über die Gruppe der Cordieae. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie, 12, 526–586.

    Google Scholar 

  • Miers, J. (1869). XLVIII. — On the comparative carpical structure of the Ehretiaceæ and Cordiaceæ. The Annals and Magazine of Natural History, Including Zoology, Botany, and Geology, 3, 383–388.

    Google Scholar 

  • Miers, J. (1875). II: On the Auxemmeæ, a new tribe of the Cordiaceæ. Transactions of the Linnean Society, 12, 23–36.

    Google Scholar 

  • Miller, J.S. (1985). Systematics of the genus Cordia (Boraginaceae) in Mexico and Central America. PhD thesis, Saint Louis University: Saint Louis.

  • Miller, J. S., & Gottschling, M. (2007). Generic classification in the Cordiaceae (Boraginales): Resurrection of the genus Varronia P.Br. Taxon, 56, 163–169.

    Google Scholar 

  • Nowicke, J. W., & Ridgway, J. E. (1973). Pollen studies in the genus Cordia (Boraginaceae). American Journal of Botany, 60, 584–591.

    Google Scholar 

  • Opler, P. A., Baker, H. G., & Frankie, G. W. (1975). Reproductive biology of some Costa Rican Cordia species (Boraginaceae). Biotropica, 7, 234–247.

    Google Scholar 

  • Paria, N., Kamilya, P., & Bhattacharya, B. (1995). Seedling morphology in taxonomic study of some members of Boraginaceae. Journal of the National Botanical Society, 49, 75–81.

    Google Scholar 

  • Rao, B. H., & Rani, S. S. (1987). Floral anatomy of Ehretia. Acta Botanica Indica, 15, 50–54.

    Google Scholar 

  • Renner, S. S. (2014). The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany, 101, 1588–1596.

    PubMed  Google Scholar 

  • Stutzman, J. K., Lickey, E. B., Weeks, A., & McMullen, C. K. (2012). A taxonomic study of the Galapagos endemic Varronia (Cordiaceae) species with nomenclatural notes. Journal of the Botanical Research Institute of Texas, 6, 75–99.

    Google Scholar 

  • Svensson, H.G. (1925). Zur Embryologie der Hydrophyllaceen, Borraginaceen und Heliotropiaceen mit besonderer Rücksicht auf die Endospermbildung. PhD thesis, Uppsala Universitets Ã…rsskrift: Uppsala.

  • Uhlarz, H., & Weberling, F. (1977). Ontogenetische Untersuchungen an Cordia verbenacea DC. (Boraginaceae), ein Beitrag zur Kenntnis der Syndesmien. Berichte der Deutschen Botanischen Gesellschaft, 90, 127–134.

    Google Scholar 

  • Vasil, I. K. (1955). 47. Morphology and embryology of Ehretia laevis Roxb. Proceedings of the Annual Session of the Indian Congress Association, 42, 239.

    Google Scholar 

  • Venkateswarlu, J., & Atchutaramanurti, B. (1955). Embryological studies in Boraginaceæ. I. — Coldenia procumbens Linn. Journal of the Indian Botanical Society, 34, 235–247.

    Google Scholar 

  • Watanabe, M. T. C., Hiura, A. L., & Nogueira, M. G. C. (2017). Flora das cangas da Serra dos Carajás, Pará, Brasil: Cordiaceae. Rodriguésia, 68, 955–960.

    Google Scholar 

  • Weberling, F. (1981). Morphologie der Blüten und der Blütenstände. Stuttgart: Ulmer.

    Google Scholar 

  • Weberling, F. (1989). Morphology of flowers and inflorescences. Cambridge: Cambridge University Press [translation of Weberling (1981) by R. Pankhurst].

    Google Scholar 

  • Weeks, A., Baird, K. E., & McMullen, C. K. (2010). Origin and evolution of endemic Galápagos Varronia species (Cordiaceae). Molecular Phylogenetics and Evolution, 57, 948–954.

    CAS  PubMed  Google Scholar 

  • Weigend, M., Luebert, F., Gottschling, M., Couvreur, T. L. P., Hilger, H. H., & Miller, J. S. (2014). From capsules to nutlets—phylogenetic relationships in the Boraginales. Cladistics, 30, 508–518.

    Google Scholar 

Download references

Acknowledgments

We thank Peter K. Endress (Zurich) and Michael W. Frohlich (Richmond) for critical reading of our manuscript and Harald Loose with his team (Munich), who devotedly cares for the living plants at the Botanical Garden.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marc Gottschling.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Heigl, H.M., Kretschmann, J., Hilger, H.H. et al. Flower and fruit anatomy of Cordia nodosa Lam. and Varronia bonplandii Desv. (Cordiaceae, Boraginales) with phylogenetic implications. Org Divers Evol 20, 9–24 (2020). https://doi.org/10.1007/s13127-019-00420-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-019-00420-4

Keywords