Abstract
The development of inflorescences and flowers of three species of Ranunculus and three allied genera (Ceratocephala, Halerpestes, and Oxygraphis) (Ranunculeae, Ranunculaceae) was studied comparatively using scanning electron microscopy (SEM). Our results showed that both the inflorescence branching patterns and the floral morphogenesis in Ranunculeae are extremely labile. Inflorescences range from a thyrsoid to a solitary flower, with intermediate branching patterns in which sometimes only the terminal flower of the inflorescence main axis fully develops, such as in Ceratocephala and Halerpestes. Only in Oxygraphis is the flower truly solitary. In all species, sepal primordia are broad, crescent-shaped, and truncate, and the primordia of petals, stamens, and carpels are rather small and hemispherical, and very similar to each other. The plastochron between the last sepal and the first petal is relatively long. At the onset of androecium or gynoecium development, the regular spiral pattern of the perianth may become irregular in Ceratocephala and Oxygraphis, whereas spiral and whorled patterns may co-occur in Ranunculus and Halerpestes. The development of the petals is delayed with regard to that of the other floral organs in all species studied here, except for Oxygraphis. Our study confirms that, for solitary flowers, increased number of petals and the shape of the ventral nectary may have evolved independently many times, as suggested by earlier molecular phylogenetic studies and ancestral character reconstructions. With respect to the remainder of the tribe, Oxygraphis displays several autapomorphies, such as nondelayed development and increased number of petals, which will be of interest for comparative molecular developmental studies.
Similar content being viewed by others
References
Benson L (1940) The North American subdivisions of Ranunculus. Am J Bot 27:799–807
Bentham G, Hooker JD (1862) Genera plantarum I. Reeves, London
Chang H-L, Ren Y, Lu A-M (2005) Floral morphogenesis of Anemone rivularis Buch.-Ham. ex DC. var. flore-minore Maxim. (Ranunculaceae) with special emphasis on androecium developmental sequence. J Integr Plant Biol 47:257–263
Cook CDK (1966) A monographic study of Ranunculus subgenus Batrachium (DC.) A. Gray. Mitt Bot Staatssamml München 6:47–237
Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, de Pamphilis CW (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749
Dahlgren G (1992) Ranunculus subgens Batrachium on the Aegean islands and adjacent areas: nectary types and breeding system. Nord J Bot 12:299–310
Damerval C, Nadot S (2007) Evolution of perianth and stamen characteristics with respect to floral symmetry in Ranunculales. Ann Bot 100:631–640
De Candolle AP (1818) Regni vegetabilis systema naturale I. Treuttel and Würtz, Paris
De Candolle AP (1824) Prodromus systematis naturalis regni vegetabilis I. Treuttel and Würtz, Paris
Di Stilio VS, Kramer EM, Baum DA (2005) Floral MADS box genes and homeotic gender dimorphism in Thalictrum dioicum (Ranunculaceae)—a new model for the study of dioecy. Plant J 41:755–766
Emadzade K, Lehnebach C, Lockhart P, Hörandl E (2010) A molecular phylogeny, morphology and classification of genera of Ranunculeae (Ranunculaceae). Taxon 59:809–828
Endlicher S (1839) Genera plantarum. 2. Beck, Vienna
Endress PK (1987) Floral phyllotaxis and floral evolution. Bot Jahrb Syst 108:417–438
Endress PK (1995) Floral structure and evolution in Ranunculanae. Plant Syst Evol 9(Suppl):47–61
Endress PK (2006) Angiosperm floral evolution: morphological developmental framework. Adv Bot Res 44:1–61
Endress PK (2010a) Flower structure and trends of evolution in eudicots and their major subclades. Ann Missouri Bot Gard 97:541–583
Endress PK (2010b) Disentangling confusions in inflorescence morphology: patterns and diversity of reproductive shoot ramification in angiosperms. J Syst Evol 48:225–239
Endress PK, Doyle JA (2007) Floral phyllotaxis in basal angiosperms-development and evolution. Curr Opin Plant Biol 10:52–57
Endress PK, Doyle JA (2009) Reconstructing the ancestral flower and its initial specializations. Am J Bot 96:22–66
Erbar CS, Kusma S, Leins P (1998) Development and interpretation of nectary organs in Ranunculaceae. Flora 194:317–332
Feng M, Fu D-Z, Liang H-X, Lu A-M (1995) Floral morphogenesis of Aquilegia L. (Ranunculaceae). Acta Bot Sin 37:791–794
Gregory WC (1941) Phylogenetic and cytological studies in the Ranunculaceae. Trans Am Philos Soc 31:443–521
Gu T-Q, Ren Y (2007) Floral morphogenesis of Coptis (Ranunculaceae). Chin Bull Bot 24:80–86
Gupta D, Singh V (1983) Floral organogenesis of Ranunculus sceleratus L. Proc Indian Nat Sci Acad B 49:273–277
Hammond HD (1952) Serology applied to systematic studies in the Ranunculaceae. University of Pennsylvania, Dissertation
Hiepko P (1965) Vergleichend-morphologische und entwicklungsgeschichtliche Untersuchungen über das Perianth bei den Polycarpicae. Bot Jahrb Syst 84:359–426
Hileman LC, Irish VF (2009) More is better: the uses of developmental genetic data to reconstruct perianth evolution. Am J Bot 96:83–95
Hirmer M (1931) Zur Kenntnis der Schraubenstellungen im Pflanzenreich. Planta 14:132–206
Hoot SB (1995) Phylogeny of the Ranunculaceae based on preliminary atpB, rbcL and 18S nuclear ribosomal DNA sequence data. Plant Syst Evol 9(Suppl):241–251
Hoot SB, Kramer J, Arroyo MTK (2008) Phylogenetic position of the South American dioecious genus Hamadryas and related Ranunculeae (Ranunculaceae). Int J Plant Sci 169:433–443
Hörandl E, Paun O, Johansson JT, Lehnebach C, Armstrong T, Chen L, Lockhart PJ (2005) Phylogenetic relationships and evolutionary traits in Ranunculus s. l. (Ranunculaceae) inferred from ITS sequence analysis. Mol Phyl Evol 36:305–327
Hutchinson J (1923) Contributions towards a phylogenetic classification of flowering plants. I. Bull Misc Inform Kew Bull 1923:65–89
Irish VF (2006) Duplication, diversification, and comparative genetics of angiosperm MADS-box genes. Adv Bot Res 44:129–161
Irish VF (2009) Evolution of petal identity. J Exp Bot 60:2517–2527
Jabbour F, Ronse De Craene LP, Nadot S, Damerval C (2009) Establishment of zygomorphy on an ontogenic spiral and evolution of perianth in the tribe Delphinieae (Ranunculaceae). Ann Bot 104:809–822
Janchen E (1949) Die systematische Gliederung der Ranunculaceen und Berberidaceen. Denkschr Akad Wiss Wien Math-Naturw Kl 108:1–82
Jensen U, Hoot SB, Johansson JT, Kosuge K (1995) Systematics and phylogeny of the Ranunculaceae-a revised family concept on the basis of molecular data. Plant Syst Evol 9(Suppl):273–280
Johansson JT (1995) A revised chloroplast DNA phylogeny of the Ranunculaceae. Plant Syst Evol 9(Suppl):253–261
Johansson JT (1998) Chloroplast DNA restriction site mapping and the phylogeny of Ranunculus (Ranunculaceae). Plant Syst Evol 213:1–19
Kosuge K (1994) Petal evolution in Ranunculaceae. Plant Syst Evol 8(Suppl):185–191
Kosuge K, Tamura M (1989) Ontogenetic studies on petal of the Ranunculaceae. J Jap Bot 64:65–74
Kramer EM (2009) Aquilegia: a new model for plant development, ecology, and evolution. Annu Rev Plant Biol 60:261–277
Kramer EM, Irish VF (1999) Evolution of genetic mechanisms controlling petal development. Nature 399:144–148
Kramer EM, Zimmer EA (2006) Gene duplication and floral developmental genetics of basal eudicots. Adv Bot Res 44:353–384
Kramer EM, Di Stilio VS, Schluter P (2003) Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Int J Plant Sci 164:1–11
Kramer EM, Su HJ, Wu CC, Hu JM (2006) A simplified explanation for the frameshift mutation that created a novel C-terminal motif in the APETALA3 gene lineage. BMC Evol Biol 6:30
Kramer EM, Holappa L, Gould B, Jaramillo MA, Setnikov D, Santiago PM (2007) Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. Plant Cell 19:750–766
Langlet O (1932) Uber Chromosomenverhältnisse und Systematik der Ranunculaceae. Svensk Bot Tidskr 26:381–400
Lee JY, Baum SF, Oh SH, Jiang CZ, Chen JC, Bowman JL (2005) Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132:5021–5032
Lehmann NL, Sattler R (1994) Floral development and homeosis in Actaea rubra (Ranunculaceae). Int J Plant Sci 155:658–671
Lehnebach CA, Cano A, Monsalve C, McLenachan P, Hörandl E, Lockhart P (2007) Phylogenetic relationships of the monotypic Peruvian genus Laccopetalum (Ranunculaceae). Plant Syst Evol 264:109–116
Leinfellner W (1958) Beiträge zur Kronblattmorphologie. VIII. Der peltate Bau der Nektarblätter von Ranunculus, dargelegt an Hand jener von Ranunculus pallasii Schlecht. Plant Syst Evol 105:184–192
Liou L (1980) Ranunculeae. In: Wang WC (ed) Flora Reipublicae Popularis Sinicae, vol 28. Science, Beijing, pp 241–345
Lockhart P, McLenachan PA, Havell D, Glenny D, Huson D, Jensen U (2001) Phylogeny, dispersal and radiation of New Zealand alpine buttercups: molecular evidence under split decomposition. Ann Missouri Bot Gard 88:458–477
Ovczinnikov PN (1937) Ranunculus. In: Komarow WA (ed) Flora URSS, vol VII., Ranales and RhoeadalesBotanicheskii Institut Akademii Nauk USSR, Moscow, pp 351–509
Paun O, Lockhart P, Hörandl E, Lehnebach C, Johansson JT (2005) Phylogenetic relationships and biogeography of Ranunculus and allied genera (Ranunculaceae) in the Mediterranean region and in the European Alpine system. Taxon 54:911–930
Payer JB (1857) Traité d’organogénie comparée de la fleur. Masson, Paris
Prantl K (1887) Beiträge zur Morphologie und Systematik der Ranunculaceen. Bot Jahrb Syst 9:225–273
Prantl K (1891) Ranunculaceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien III(2). Engelmann, Leipzig, pp 43–66
Rasmussen DA, Kramer EM, Zimmer EA (2009) One size fits all? Molecular evidence for a commonly inherited petal identity program in the Ranunculales. Am J Bot 96:96–109
Ren Y, Chang HL, Tian XH, Song P, Endress PK (2009) Floral development in Adonideae (Ranunculaceae). Flora 204:506–517
Ren Y, Chang HL, Endress PK (2010) Floral development in Anemoneae (Ranunculaceae). Bot J Linn Soc 162:77–100
Ren Y, Gu T-Q, Chang H-L (2011) Floral development of Dichocarpum, Thalictrum, and Aquilegia (Thalictroideae, Ranunculaceae). Plant Syst Evol 292:203–213
Ro KE, Keener CS, Mcpheron BA (1997) Molecular phylogenetic study of the Ranunculaceae: utility of the nuclear 26S Ribosomal DNA in inferring intrafamilial relationships. Mol Phylogenet Evol 8:117–127
Ronse De Craene LP, Smets EF (1995) Evolution of the androecium in the Ranunculiflorae. Plant Syst Evol 9(Suppl):63–70
Ruijgrok HWL (1966) The distribution of ranunculin and cyanogenic compounds in the Ranunculaceae. In: Swain T (ed) Comparative phytochemistry. London and New York, pp 175–186
Sattler R (1973) Organogenesis of flowers: a photographic text-atlas. University of Toronto Press, Toronto
Schöffel K (1932) Untersuchungen über den Blütenbau der Ranunculaceae. Planta 17:315–371
Song P, Tian X-H, Ren Y (2007) Floral morphogenesis of Caltha and Trollius (Ranunculaceae) and the systematic significance. Acta Bot Sin 45:769–782
Staedler YM, Endress PK (2009) Diversity and lability of floral phyllotaxis in the pluricarpellate families of core Laurales (Gomortegaceae, Atherospermataceae, Siparunaceae, Monimiaceaea). Int J Plant Sci 170:522–550
Stevens PF (2001) (onwards) Angiosperm phylogeny website. Version 9, June 2008 (and more or less continuously updated since). http://www.mobot.org/MOBOT/research/APweb/
Tamura M (1962) Taxonomical and phylogenetical consideration of the Ranunculaceae. Acta Phytotax Geobot 20:71–81
Tamura M (1967) Morphology, ecology and phylogeny of the Ranunculaceae. VII. Sci Rep Osaka Univ 16:35–42
Tamura M (1972) Morphology and phyletic relationship of the Glaucidiaceae. Bot Mag Tokyo 85:29–41
Tamura M (1984) Phylogenetical consideration of the Ranunculaceae. Korean J Plant Tax 14:33–42
Tamura M (1993) Ranunculaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants, vol 2. Springer, Berlin, pp 563–583
Tamura M (1995) Ranunculaceae. In: Hiepko P (ed) Die natürlichen Pflanzenfamilien, vol 17a (4), 2nd edn. Duncker und Humblot, Berlin, pp 1–555
Tepfer SS (1953) Floral anatomy and ontogeny in Aquilegia formosa var. truncata and Ranunculus repens. Univ California Publ Bot 25:513–648
The Angiosperm Phylogeny Group (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
Tucker SC, Hodges SC (2005) Floral ontogeny of Aquilegia, Semiaquilegia, and Enemion (Ranunculaceae). Int J Plant Sci 166:557–574
Tutin TG, Cook CDK (1993) Ranunculus. In: Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea I: Psilotaceae to Platanaceae, 2nd edn. Cambridge University Press, Cambridge, pp 269–290
van Heel WA (1981) A SEM-investigation on the development of free carpels. Blumea 27:499–522
van Heel WA (1984) Variation in the development of ascidiform carpels, a SEM-investigation. Blumea 29:443–452
Wang W, Lu AM, Ren Y, Endress ME, Chen ZD (2009) Phylogeny and classification of Ranunculales: evidence from four molecular loci and morphological data. Perspect Plant Ecol Evol Syst 11:81–110
Whittemore A (1997) Ranunculus. In: Flora of North America Committee (ed) Flora of North America North of Mexico, vol 3. Magnoliophyta: Magnoliidae and Hamamelidae, Oxford University Press, New York, pp 88–135
Wu HY, Sun K, Cai ZW, Su X, Pang HL (2008) Floral organogenesis and development of Clematis fruticosa Turcz. (Ranunculaceae). Bull Bot Res 28:273–277
Zhao L, Liu P, Che XF, Wang W, Ren Y (2011) Floral organogenesis of Helleborus and Nigella (Ranunculaceae) and its systematic significance. Bot J Linn Soc 166:431–443
Zhao L, Wang W, Ren Y, Bachelier JB (2012) Floral development in Asteropyrum (Ranunculaceae): implication for its systematic position. Ann Bot Fenn 49
Acknowledgments
We sincerely thank Dr. Dun-yan Tan, Xinjiang Agriculture University, China, for collecting valuable material and taking the picture of the anthetic flower of Ceratocephala orthoceras; Dr. Quan-ru Liu, Beijing Normal University, China, for assistance in field collection of Ranunculus bungei; Dr. Jeremy Lundholm, Saint Mary’s University, Canada, and Dr. Xin-wei Li, Wuhan Botanical Garden, China, for critically reading the earlier versions of the manuscript. We also sincerely thank Dr. Robert L. Baker, University of Colorado at Boulder, USA, for editing the English, and Dr. Peter K. Endress and an anonymous reviewer for their helpful comments on the manuscript. This project was supported by the National Nature Science Foundation of China (Nos. 30370095, 31170215, and 31100141) and Doctoral Foundation of Northwest A & F University (No. Z109021118).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhao, L., Bachelier, J.B., Chang, Hl. et al. Inflorescence and floral development in Ranunculus and three allied genera in Ranunculeae (Ranunculoideae, Ranunculaceae). Plant Syst Evol 298, 1057–1071 (2012). https://doi.org/10.1007/s00606-012-0616-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-012-0616-6