Different ways to obtain similar results: the development of the corolla and epipetaly in Rubieae (Rubioideae, Rubiaceae)


corolla tube sensu stricto
floral ontogeny
herbaceous Rubiaceae
stamen-corolla tube

How to Cite

Vrijdaghs, A., Smets, E. and De Block, P. (2020) “Different ways to obtain similar results: the development of the corolla and epipetaly in Rubieae (Rubioideae, Rubiaceae)”, Plant Ecology and Evolution, 153(3), pp. 466-486. doi: 10.5091/plecevo.2020.1764.


Background and aims – Rubieae is a tribe in the subfamily Rubioideae characterised by herbaceous plants with verticillate leaves and flowers with a rudimentary or absent calyx and a short, cup-shaped corolla. This is in contrast to the flowers of most other Rubiaceae, in which the tubular corolla is longer than the corolla lobes. Also, the description by Payer, a French 19th century pioneer of floral ontogenetic research, of the floral development in Asperula, Galium, and Rubia deviates from recent insights about the development of tubular corollas, which are based on investigations of flowers of tropical Rubiaceae. Tubular corollas are currently considered as resulting from the development of underlying annular intercalary meristems, whereas Payer explained the tubular corollas in the three taxa by postgenital fusion. We therefore tested both hypotheses in six Rubieae genera, including the three taxa studied by Payer.
Methods – Floral ontogeny of ten species in six Rubieae genera based on scanning electron (SEM) and light microscopy (LM).
Conclusions – Our results suggest that, in all species studied, the mature phenotype of the corolla as well as the epipetaly of the stamens is caused by a combination of three developmental processes (the development of a stamen-corolla tube, the development of a corolla tube sensu stricto, and postgenital fusion), and the relative moment of activation of each of these processes during floral development (plastochron variation or heterochrony).



Bernardello G. (2007) Nectary structure and ultrastructure. In: Nicolson S.W., Nepi M., Pacini E. (eds) Nectaries and nectar: 129–166. Dordrecht, Springer.

Bremer B., Eriksson T. (2009) Time tree of Rubiaceae: phylogeny and dating the family subfamilies, and tribes. International Journal of Plant Sciences 170(6): 766–793. https://doi.org/10.1086/599077

Davis A., Govaerts R., Bridson D.M., Ruhsam M., Moat J., Brummitt N. (2009) A global assessment of distribution, diversity, endemism, and taxonomic effort in the Rubiaceae. Annals of the Missouri Botanical Garden 96(1): 68–78. https://doi.org/10.3417/2006205

De Block P., Vrijdaghs A. (2013) Development of reproductive organs in Canephora madagascariensis (Octotropideae-Rubiaceae). Plant Ecology and Evolution 146(3): 310–327. https://doi.org/10.5091/plecevo.2013.844

Ehrendorfer F., Barfuss M.H.J., Manen J.-F., Schneeweiss G.M. (2018) Phylogeny, character evolution and spatiotemporal diversification of the species-rich and world-wide distributed tribe Rubieae (Rubiaceae). Plos One 13(12): e0207615. https://doi.org/10.1371/journal.pone.0207615

Endress P.K. (2006) Angiosperm floral evolution: morphological developmental framework. Advances in Botanical Research 44: 1–61. https://doi.org/10.1016/S0065–2296(06)44001–5

Endress P.K. (2019) The morphological relationship between carpels and ovules in angiosperms: pitfalls of morphological interpretation. Botanical Journal of the Linnean Society 189(3): 201–227. https://doi.org/10.1093/botlinnean/boy083

Erbar C. (1991) Sympetaly: a systematic character? Botanische Jahrbücher fur Systematik, Pflanzengeschichte und Pflanzengeographie 112(4): 417–451.

Erbar C., Leins P. (1996) The formation of corolla tubes in Rubiaceae and presumably related families. Opera Botanica Belgica 7: 103–112.

Govaerts R., Ruhsam M., Andersson L., Robbrecht E., Bridson D., Davis A., Schanzer I., Sonké B. (2020) World Checklist of Rubiaceae. Facilitated by the Royal Botanic Gardens, Kew. Available at http://apps.kew.org/wcsp/ [accessed 24 Jan. 2020].

Groeninckx I., Vrijdaghs A., Huysmans S., Smets E., Dessein S. (2007) Floral ontogeny of the Afro-Madagascan genus Mitrasacmopsis with comments on the development of superior ovaries in Rubiaceae. Annals of Botany 100(1): 41–49. https://doi.org/10.1093/aob/mcm085

Heywood V.H., Brummit R.K., Culham A., Seberg O. (2007) Flowering plant families of the world. Royal Botanical Gardens, Kew.

Lawrence E. (1996) Henderson’s dictionary of biological terms, 11th edition. Singapore, Longman Singapore Editions Ltd.

Leins P., Erbar C. (2010) Flower and fruit. Morphology, ontogeny, phylogeny, function and ecology. Stuttgart, Schweizerbart Science Publishers.

Lens F., Groeninckx I., Smets E., Dessein S. (2009) Woodiness within the Spermacoceae-Knoxieae alliance (Rubiaceae): retention of the basal woody condition in Rubiaceae or recent innovation? Annals of Botany 103(7): 1049–1064. https://doi.org/10.1093/aob/mcp048

Naghiloo S., Classen-Bockhoff R. (2016) Developmental analysis of merosity and sexual morphs in Rubiaceae: a case study in Rubia and Cruciata. Flora 222: 52–59. https://doi.org/10.1016/j.flora.2016.03.010

Naghiloo S., Classen-Bockhoff R. (2017) Developmental changes in time and space promote evolutionary diversification of flowers: a case study in Dipsacoideae. Frontiers in Plant Science 8: 1665. https://doi.org/10.3389/fpls.2017.01665

Ochoterena H., Vrijdaghs A., Smets E., Classen-Bockhoff R. (2019) The search for common origin: Homology revisited. Systematic Biology 68(5): 767–780. https://doi.org/10.1093/sysbio/syz013

Payer J.B. (1857) Traité d’organogénie comparée de la fleur. Paris, Masson, Paris, France.

Pötter K., Klopfer K. (1987) Untersuchungen zur Blatt- und Blütenentwicklung bei Galium aparine L. (Rubiaceae). Flora 179(4): 305–314. https://doi.org/10.1016/S0367-2530(17)30256-6

Puff C., Robbrecht E., Buchner R., De Block P. (1996) A survey of secondary pollen presentation in the Rubiaceae. Opera Botanica Belgica 7: 369–402.

Robbrecht E. (1988) Tropical woody Rubiaceae. Opera Botanica Belgica 1: 1–271.

Robbrecht E. (1993) On the delimitation of the Rubiaceae. In Robbrecht E. (ed.) Advances in Rubiaceae macrostystematics. Opera Botanica Belgica 6: 19–30.

Robbrecht E., Manen J.-F. (2006) The major evolutionary lineages of the coffee family (Rubiaceae, angiosperms). Combined analysis (nDNA and cpDNA) to infer the position of Coptosapelta and Luculia, and supertree construction based on rbcL, rps16, trnL-trnF and atpB-rbcL data. A new classification in two subfamilies, Cinchonoideae and Rubioideae. Systematics and Geography of Plants 76(1): 85–146. https://www.jstor.org/stable/20649700

Ronniger K. (1931) Floristische Ergebnisse einer Reise nach Bulgarien. Feddes Repertorium Specierum Novarum Regni Vegetabilis 29: 142–149.

Ronse Decraene L.P., Smets E. (2000) Floral development of Galopina tomentosa with a discussion of sympetaly and placentation in the Rubiaceae. Systematics and Geography of Plants 70(1): 155–170. https://doi.org/10.2307/3668619

Rutishauser R., Ronse Decraene L.P., Smets E., Mendoza-Heuer I. (1998) Theligonum cynocrambe: developmental morphology of a peculiar rubiaceous herb. Plant Systematics and Evolution 210: 1–24. https://doi.org/10.1007/BF00984724

Rutishauser R. (1999) Polymerous leaf whorls in vascular plants: developmental morphology and fuzziness of organ identity. International Journal of Plant Sciences 160 (6 Suppl.): S81–S103. https://doi.org/10.1086/314221

Schönbeck-Temesy E., Ehrendorfer F. (1989) The perennial taxa of Crucianella (Rubiaceae) in SW. Asia and their eco-geographical differentiation. Plant Systematics and Evolution 165: 101–136. https://doi.org/10.1007/BF00936040

Smets E. (1988) La présence des “nectaria persistentia” chez les Magnoliophytina (Angiospermes). Candollea 43: 709–716.

Smets E., Cresens E. (1988) Types of floral nectaries and the concepts “character” and “character-state” – a reconsideration. Acta Botanica Neerlandica 37: 121–128.

Smith K. (2001) Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society 73(2): 169–186. https://doi.org/10.1111/j.1095-8312.2001.tb01355.x

Stevens P.F. (2001 onwards) Angiosperm Phylogeny Website. Version 14, July 2017. Available at http://www.mobot.org/MOBOT/Research/APweb/ [accessed 1 Jul. 2017].

Tao C., Ehrendorfer F. (2011) 50. Microphysa Schrenk. In: Zhengyi W., Raven P.H., Deyuan H. (eds) Flora of China 19: 216–217.

Van der Meulen A. (1939) Over den bouw en de periodieke ontwikkeling der bloemknoppen bij Coffea-soorten. PhD thesis, Wageningen University, the Netherlands. Available at https://edepot.wur.nl/173736 [accessed 2 Sep. 2020].

Von Faber F.C. (1912) Morphologisch-physiologische Untersuchungen an Blüten von Coffea-Arten. Annales du Jardin Botanique de Buitenzorg, 2nd ser. 25(10): 59–160.

Vrijdaghs A., De Block P., Verstraete B., Groeninckx I., Smets E., Dessein S. (2015) A developmental model for the corolla in Rubiaceae. Cryptic character states in corollas of the Spermacoceae alliance. Plant Ecology and Evolution 148(2): 237–255. https://doi.org/10.5091/plecevo.2015.1088

Weberling F. (1992) Morphology of flowers and inflorescences. Cambridge, UK, Cambridge University Press.

Yang L.-E., Meng Y., Peng D.-L., Nie Z.-L., Sun H. (2018) Molecular phylogeny of Galium L. of the tribe Rubieae (Rubiaceae) – Emphasis on Chinese species and recognition of a new genus Pseudogalium. Molecular Phylogenetics and Evolution 126: 221–232. https://doi.org/10.1016/j.ympev.2018.04.004

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.