Skip to main content
Log in

Floral ontogeny in Passiflora lobata (Malpighiales, Passifloraceae) reveals a rare pattern in petal formation and provides new evidence for interpretation of the tendril and corona

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Passiflora lobata differs from most other passion flowers in that it has a tetramerous gynoecium and dorsiventral flowers. A detailed ontogenetic analysis using scanning electron microscopy revealed the following characters: tendril formation starts late, indicating an axial nature. The paired flowers show mirror symmetry, which is manifested very early in ontogeny. Five sepals initiate in a spiral followed by five petals, which are formed successively adjacent to each other. This is a rare pattern and the first report in Passifloraceae. Frequently a sixth petal primordium was found, which never develops and which could be interpreted as the first outgrowth or frill of the corona (which therefore might be interpreted as derived from the perianth). The abaxial carpel forms always in front of the first-formed sepal. The remaining three carpels are alternate with the stamens. This means that a positional change took place from the typical trimerous ovary with two carpels in front of stamens to only one antestaminal carpel in P. lobata. This shift might have opened up space for a fourth carpel. Together with the analysis of other tetramerous Passifloraceae, this study will foster the understanding of flower morphology in this family and its systematic relationships among Malpighiales.

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

Access this article

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • APG (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121

    Article  Google Scholar 

  • Bell AD (2008) Plant form. An illustrated guide to flowering plant morphology, 2nd edn. Timber Press, London

    Google Scholar 

  • Bello MA, Hawkins JA, Rudall PJ (2007) Floral morphology and development in Quillajaceae and Surianaceae (Fabales), the species-poor relatives of Leguminosae and Polygalaceae. Ann Bot 100:1491–1505

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bernhard A (1999) Flower structure, development, and systematics in Passifloraceae and in Abatia (Flacourtiaceae). Int J Plant Sci 160:135–150

    Article  Google Scholar 

  • Buzato S, Franco ALM (1992) Tetrastylis ovalis: a second case of bat pollinated passionflower (Passifloraceae). Plant Syst Evol 181:261–267

    Article  Google Scholar 

  • Calonje M, Cubas P, Martinez-Zapater JM, Carmona MJ (2004) Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiol 135:1491–1501

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cardoso MZ (2008) Herbivore handling of a plant’s trichome: the case of Heliconius chrithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora lobata (Killip) Hutch. (Passifloraceae). Neotrop Entomol 37:247–252

    Article  PubMed  Google Scholar 

  • Caze ALR, Mäder G, Bonatto SL, Freitas LB (2013) A molecular systematic analysis of Passiflora ovalis and Passiflora contracta (Passifloraceae). Phytotaxa 132:39–46

    Article  Google Scholar 

  • De Candolle AP (1813) Théorie élémentaire de la botanique. Paris

  • De Wilde WJJO (1974) The genera of tribe Passifloreae (Passifloraceae) with special reference to flower morphology. Blumea 22:37–50

    Google Scholar 

  • Drinnan A, Carrucan A (2005) The ontogenetic basis for floral diversity in Agonis, Leptospermum and Kunzea (Myrtaceae). Plant Syst Evol 251:71–88

    Article  Google Scholar 

  • Eichler AW (1878) Blüthendiagramme. 2. Teil. W. Engelmann, Leipzig

    Google Scholar 

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

    Google Scholar 

  • Endress PK (1999) Symmetry in flowers: diversity and evolution. Int J Plant Sci 160:S3–S23

    Article  PubMed  Google Scholar 

  • Endress PK, Matthews ML (2006) Elaborate petals and staminodes in eudicots: diversity, function and evolution. Org Div Evol 6:257–293

    Article  Google Scholar 

  • Endress PK, Davis CC, Matthews ML (2013) Advances in the floral structural characterization of the major subclades of Malpighiales, one of the largest orders of flowering plants. Ann Bot 111:969–985

    Article  PubMed Central  PubMed  Google Scholar 

  • Feuillet C (2011) Two new species of Dilkea subgenus Dilkea (Passifloraceae) from Loreto, Peru. PhytoKeys 2:1–8

    PubMed  Google Scholar 

  • Feuillet C, MacDougal JM (2004) A new infrageneric classification of Passiflora L. (Passifloraceae). Passiflora 13:34–38

    Google Scholar 

  • Feuillet C, MacDougal JM (2007) Passifloraceae. In: Kubizki K (ed) The families and genera of vascular plants. Springer, Berlin, pp 270–281

    Google Scholar 

  • Gentry AH (1976) Additional Panamanian Passifloraceae. Ann Missouri Bot Gard 63:341–345

    Article  Google Scholar 

  • Hansen AK, Gilbert LE, Simpson BB, Downie SR, Cervi AC, Jansen RK (2006) Phylogenetic relationships and chromosome number evolution in Passiflora. Syst Bot 31:138–150

    Article  Google Scholar 

  • Harms H (1893) Passifloraceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien. W. Engelmann, Leipzig, pp 69–94

    Google Scholar 

  • Harms H (1897) Zur Morphologie der Ranken und Blütenstände bei den Passifloraceen. Bot Jahrb 24:163–178

    Google Scholar 

  • Harms H (1931) Eine neue Gattung der Flacourtiaceae. Notizbl königl bot Gart Berlin 11:146–149

    Article  Google Scholar 

  • Harms H (1932) Zur Kenntnis der Gattung Ancistrothyrsus. Notizbl königl bot Gart Berlin 11:598–600

    Article  Google Scholar 

  • Hemingway CA, Christensen AR, Malcomber ST (2011) B- and C-class gene expression during corona development of the blue passionflower (Passiflora caerulea, Passifloraceae). Am J Bot 98:923–934

    Article  CAS  PubMed  Google Scholar 

  • Hofmeister W (1868) Allgemeine Morphologie der Gewächse. W. Engelmann, Leipzig

    Google Scholar 

  • Killip EP (1926) Tetrastylis, a genus of Passifloraceae. J Wash Acad Sci 16:365–369

    Google Scholar 

  • Killip EP (1938) The American species of Passifloraceae. Bot Ser Field Mus Nat Hist 19:1–613

    Google Scholar 

  • Kirchoff BK (2003) Shape matters: Hofmeister’s rule, primordium shape, and flower orientation. Int J Plant Sci 164:505–517

    Article  Google Scholar 

  • Krosnick SE, Freudenstein JV (2005) Monophyly and floral character homology of old world Passiflora (subgenus Decaloba: supersection Disemma). Syst Bot 30:139–152

    Article  Google Scholar 

  • Krosnick SE, Harris EM, Freudenstein JV (2006) Patterns of anomalous floral development in the Asian Passiflora (subgenus Decaloba: supersection Disemma). Am J Bot 93:620–636

    Article  PubMed  Google Scholar 

  • Krosnick SE, Ford AJ, Freudenstein JV (2009) Taxonomic revision of Passiflora subgenus Tetrapathea including the monotypic genera Hollrungia and Tetrapathea (Passifloraceae), and a new species of Passiflora. Syst Bot 34:375–385

    Article  Google Scholar 

  • Krosnick SE, Porter-Utley KE, Macdougal JM, Jorgensen PM, McDade LA (2013) New insights into the evolution of Passiflora subgenus Decaloba (Passifloraceae): phylogenetic relationships and morphological synapomorphies. Syst Bot 38:692–713

    Article  Google Scholar 

  • Levin DA (1973) The role of trichomes in plant defense. Quart Rev Biol 48:3–15

    Article  Google Scholar 

  • Lindman CAM (1906) Zur Kenntnis der Corona einiger Passifloren. Botaniska Studier, tellägnade F.R. Kjellman den 4 November 1906. Almquist & Wiksells Boktryckerei-A.-B., Uppsala

    Google Scholar 

  • MacDougal JM (1986) A new combination in Passifloraceae. Phytologia 60:446

    Google Scholar 

  • MacDougal JM (1994) Revision of Passiflora subgenus Decaloba section Pseudodysosmia (Passifloraceae). Syst Bot Monogr 41:1–446

    Article  Google Scholar 

  • Masters MT (1869) Vegetable teratology. Ray Society, London

    Google Scholar 

  • Masters MT (1871) Contribution to the natural history of the Passifloraceae. Trans Linn Soc Lond Bot 27:593–645

    Article  Google Scholar 

  • Muschner VC, Lorenz AP, Cervi AC, Bonatto SL, Souza-Chies TT, Salzano FM, Freitas LB (2003) A first molecular phylogenetic analysis of Passiflora (Passifloraceae). Am J Bot 90:1229–1238

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Prenner G, Klitgaard BB (2008) Towards unlocking the deep nodes of Leguminosae: floral development and morphology of the enigmatic Duparquetia orchidacea (Leguminosae, Caesalpinioideae). Am J Bot 95:1349–1365

    Article  PubMed  Google Scholar 

  • Prenner G, Deutsch G, Harvey P (2002) Floral developmet and morphology in Cuscuta reflexa Roxb. (Convolvulaceae). Stapfia 80:311–322

    Google Scholar 

  • Prenner G, Vergara-Silva F, Rudall PJ (2009) The key role of morphology in modelling inflorescence architecture. Trends Plant Sci 14:302–309

    Article  CAS  PubMed  Google Scholar 

  • Prenner G, Bateman RM, Rudall PJ (2010) Floral formulae updated for routine inclusion in formal taxonomic descriptions. Taxon 59:241–250

    Google Scholar 

  • Puri V (1948) Studies in floral anatomy, V. On the structure and nature of the corona in certain species of the Passifloraceae. J Indian Bot Soc 27:130–149

    Google Scholar 

  • Ronse De Craene LP (2010) Floral diagrams. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Sajo G, de Mello-Silva R, Rudall PJ (2010) Homologies of floral structures in Velloziaceae with particular reference to the corona. Int J Plant Sci 171:595–606

    Article  Google Scholar 

  • Sazima M, Buzato S, Sazima I (1999) Bat-pollinated flower assemblages and bat visitors at two Atlantic forest sites in Brazil. Ann Bot 83:705–712

    Article  Google Scholar 

  • Schleiden JM (1849) Principles of scientific botany. Longman, Brown, Green and Longmans, London

    Google Scholar 

  • Schönenberger J, Grenhagen A (2005) Early floral development and androecium organization in Fouquieriaceae (Ericales). Plant Syst Evol 254:233–249

    Article  Google Scholar 

  • Schwabe WW, Clewer AG (1984) Phyllotaxis—a simple computer model based on the theory of a polarly-translocated inhibitor. J Theor Biol 109:595–619

    Article  CAS  Google Scholar 

  • Shah JJ, Dave YS (1970) Tendrils of Passiflora foetida: histogenesis and morphology. Am J Bot 57:786–793

    Article  Google Scholar 

  • Snow N, MacDougal JM (1993) New chromosome reports in Passiflora (Passifloraceae). Syst Bot 18:261–273

    Article  Google Scholar 

  • Thury M (1897) Observations sur la morphologie et l’organogénie florales des Passiflores. Bull Herb Boissier 5:494–503

    Google Scholar 

  • Tokuoka T (2012) Molecular phylogenetic analysis of Passifloraceae sensu lato (Malpighiales) based on plastid and nuclear DNA sequences. J Plant Res 125:489–497

    Article  PubMed  Google Scholar 

  • Traas J (2013) Phyllotaxis. Development 140:249–253

    Article  CAS  PubMed  Google Scholar 

  • Vitta FA, Bernacci LC (2004) A new species of Passiflora in section Tetrastylis (Passifloraceae) and two overlooked species of Passiflora from Brazil. Brittonia 56:89–95

    Article  Google Scholar 

  • von Mohl H (1827) Über den Bau und das Winden der Ranken und Schlingpflanzen. Heinrich Laupp, Tübingen

    Book  Google Scholar 

  • Waters MT, Tiley AMM, Kramer EM, Meerow AW, Langdale JA, Scotland RW (2013) The corona of the daffodil Narcissus bulbocodium shares stamen-like identity and is distinct from the orthodox floral whorls. Plant J 74:615–625

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Many thanks to John Longino (The Evergreen State College, Olympia, WA, USA) for identifying the captured ant to genus level (further determination not possible based on the evidence provided), Felicitas and Veronika Kollman (B-Rainforest, Costa Rica) for their generous hospitability during two visits to their finca, Paula Rudall and two anonymous reviewers for their valuable comments on the manuscript and the Office of International Relations (Karl-Franzens University Graz, Austria) for a travel grant to visit Costa Rica in 2002.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerhard Prenner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prenner, G. Floral ontogeny in Passiflora lobata (Malpighiales, Passifloraceae) reveals a rare pattern in petal formation and provides new evidence for interpretation of the tendril and corona. Plant Syst Evol 300, 1285–1297 (2014). https://doi.org/10.1007/s00606-013-0961-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-013-0961-0

Keywords

Navigation