Abstract
Nymphaea and Nuphar (Nymphaeaceae) share an extra-axillary mode of floral inception in the shoot apical meristem (SAM). Some leaf sites along the ontogenetic spiral are occupied by floral primordia lacking a subtending bract. This pattern of flower initiation in leaf sites is repeated inside branching flowers of Nymphaea prolifera (Central and South America). Instead of fertile flowers this species usually produces sterile tuberiferous flowers that act as vegetative propagules. N. prolifera changes the meristem identity from reproductive to vegetative or vice versa repeatedly. Each branching flower first produces some perianth-like leaves, then it switches back to the vegetative meristem identity of the SAM with the formation of foliage leaves and another set of branching flowers. This process is repeated up to three times giving rise to more than 100 vegetative propagules. The developmental morphology of the branching flowers of N. prolifera is described using both microtome sections and scanning electron microscopy.
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References
APG II (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Bot J Linn Soc 141:399–436
Arber A (1946) Goethe’s botany. Chron Bot 10:63–126
Baum DA, Donoghue MJ (2002) Transference of function, heterotopy and the evolution of plant development. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor and Francis, London, pp 52–69
Borsch T, Hilu KW, Wilde V, Bartlott W (1998) Inferring the phylogeny of Nymphaea: evidence from the trnT–trnF region of the chloroplast genome. Am J Bot 86:116–117
Bose RB (1961) A note on an abnormal Nymphaea pubescens Willd. Bull Bot Surv India 3:41
Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52
Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20
Chassat JF (1962) Recherches sur la ramification chez les Nymphaeacées. Mém Soc Bot Fr 42:72–95
Conard HS (1905) The water lilies. A monograph of the genus Nymphaea. The Carnegie Institution of Washington, Washington
Cornejo X, Bonifaz C (2003) Nymphaeaceae. Flora Ecuador 70:5–24
Cutter EG (1957a) Studies of morphogenesis in the Nymphaeaceae. I. Introduction: some aspects of the morphology of Nuphar lutea (L.) Sm. and Nymphaea alba L. Phytomorphology 7:45–56
Cutter EG (1957b) Studies of morphogenesis in the Nymphaeaceae. II. Floral development in Nuphar and Nymphaea: bracts and calyx. Phytomorphology 7:57–73
Cutter EG (1961) The inception and distribution of flowers in the Nymphaeaceae. Proc Linn Soc Bot 172:93–100
Debbarman PM (1934) A case of axial floral prolification of the flower of Nymphaea rubra Roxb. Indian Bot Soc 3:66–67
Dornelas MC, Rodriguez APM (2006) The tropical cedar tree (Cedrela fissilis Vell., Meliaceae) homolog of the Arabidopsis LEAFY gene is expressed in reproductive tissues and can complement Arabidopsis leafy mutants. Planta 223:306–314
Gandolfo MA, Nixon KC, Crepet WL (2004) Cretaceous flowers of Nymphaeaceae and implications for complex insect entrapment pollination mechanisms in early angiosperms. Proc Natl Acad Sci USA 101:8056–8060
Goto K, Kyozuka J, Bowman JL (2001) Turning floral organs into leaves, leaves into floral organs. Curr Opin Genet Dev 11:449–456
Igersheim A, Cichocki O (1996) A simple method for microtome sectioning of prehistoric charcoal specimens embedded in 2-hydroxyethyl methacrylate (HEMA). Rev Palaeobot Palynol 92:389–393
Kim S, Koh J, Yoo MJ, Kong H, Hu Y, Ma H, Soltis PS, Soltis DE (2005) Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J 43:724–744
Lacroix C, Jeune B, Barabé D (2005) Encasement in plant morphology: an integrative approach from genes to organisms. Can J Bot 83:1207–1221
Les DH, Schneider EL (1995) The Nymphaeales, Alismatidae and the theory of an aquatic monocotyledon origin. In: Rudall PJ, Cribb P, Cuttler DF, Humphries CJ (eds) Monocotyledons: systematics and evolution. Royal Botanic Gardens Kew, Kew, pp 23–42
Les DH, Schneider EL, Padgett DJ, Soltis PS, Soltis DE, Zanis M (1999) Phylogeny, classification and floral evolution of water lilies (Nymphaeaceae: Nymphaeales): a synthesis of non-molecular, rbcL, matK, and 18s rDNA data. Syst Bot 24:28–46
Löhne C, Borsch T (2005) Molecular evolution and phylogenetic utility of the petD Group II intron: a case study in basal angiosperms. Mol Biol Evol 22:317–332
Meyerowitz EM, Smyth DR, Bowman JL (1989) Abnormal flowers and pattern formation in floral development. Development 106:209–217
Mitra RL, Subramanyam K (1982) Is Nymphaea rubra Roxb. ex Andrews an apomict? Bull Bot Surv India 24:83–86
Mohan Ram HY, Nayyar VL (1974) A case of reversion of flower of Nymphaea mexicana to vegetative condition. Curr Sci 43:290–291
Olvera M, Lot A (1991) New record of Nymphaea prolifera in Mexico. Bol Soc Bot Mex 51:93–94
Pott VJ (1998) A Fámilia Nymphaeaceae no Pantanal, Mato Grosso e Mato Grosso do Sul, Brasil. Acta Bot Bras 12:183–194
Qiu YL, Dombrovska O, Lee J, Li L, Whitlock BA, Bernasconi-Quadroni F, Rest JS, Davis CC, Borsch T, Hilu KW, Renner SS, Soltis DE, Soltis PS, Zanis MJ, Cannone JJ, Gutell RR, Powell M, Savolainen V, Chatrou LW, Chase MW (2005) Phylogenetic analyses of basal angiosperms based on nine plastid, mitochondrial and nuclear genes. Int J Plant Sci 166:815–842
Ritter NP, Crow GE, Wiersema JH (2001) Nymphaea (Nymphaeaceae) in Bolivia: notes on several species, three new country records, and a key to species. Rhodora 103:326–331
Ronse De Craene LP, Louis P, Soltis PS, Soltis DE (2003) Evolution of floral structure in basal angiosperms. Int J Plant Sci 164:S329–S363
Rutishauser R, Isler B (2001) Fuzzy Arberian Morphology: Utricularia, developmental mosaics, partial shoot hypothesis of the leaf and other FAMous ideas of Agnes Arber (1879–1960) on vascular plant bauplans. Ann Bot 88:1173–1202
Rutishauser R, Moline P (2005) Evo-devo and the search for homology (“sameness”) in biological systems. Theory Biosci 124:213–241
Rutishauser R, Ronse Decraene LP, Smets E, Mendoza-Heuer I (1998) Theligonum cynocrambe: the developmental morphology of a peculiar rubiaceous herb. Plant Syst Evol 210:1–24
Schneider EL, Tucker SC, Williamson PS (2003) Floral development in the Nymphaeales. Int J Plant Sci 164:S279–S292
Soltis PS, Soltis DE (2004) The origin and diversification of angiosperms. Am J Bot 91:1614–1626
Soltis DE, Albert VA, Kim S, Yoo MJ, Soltis PS, Frohlich MW, Leebens-Mack J, Kong H, Wall K, dePamphilis C, Ma H (2005) Evolution of the flower. In: Henry RJ (eds) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CAB International, Wallingford, pp 165–200
Stevenson DW (1976) Observations on phyllotaxis, stelar morphology, the shoot apex and gemmae of Lycopodium lucidulum Michaux (Lycopodiaceae). Bot J Linn Soc 72:81–100
Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85
Theissen G (2005) Birth, life and death of developmental control genes: new challenges for the homology concept. Theory Biosci 124:199–212
Uimari A, Kotilainen M, Elomaa P, Yu D, Albert VA, Teeri TH (2004) Integration of meristem fates by a SEPALLATA-like MADS-box gene. Proc Natl Acad Sci USA 101:15817–15822
Venugopala Reddy G, Heisler MG, Erhardt DW, Meyerowitz EM (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131:4225–4237
Weber M, Igersheim A (1994) ‘Pollen buds’ in Ophiorrhiza (Rubiaceae) and their role in Pollenkitt release. Bot Acta 107:257–262
Weidlich WH (1976a) The organization of the vascular system in the stems of the Nymphaeaceae. I. Nymphaea subgenera Castalia and Hydrocallis. Am J Bot 63:499–509
Weidlich WH (1976b) The organization of the vascular system in the stems of the Nymphaeaceae. I. Nymphaea subgenera Anechya, Lotos and Brachyceras. Am J Bot 63:1365–1379
Weidlich WH (1980) The organization of the vascular system in the stems of the Nymphaeaceae. III. Victoria and Euryale. Am J Bot 67:790–803
Wiersema JH (1984) Systematics of Nymphaea subgenus Hydrocallis (Nymphaeaceae). I. Four new species from the neotropics. Brittonia 36:213–232
Wiersema JH (1987) A monograph of Nymphaea subgenus Hydrocallis (Nymphaeaceae). Syst Bot Monogr 16:1–112
Yoo MJ, Bell CD, Soltis PS, Soltis DE (2005) Divergence times and historical biogeography of Nymphaeales. Syst Bot 30:693–704
Yoon HS, Baum DA (2004) Transgenic study of parallelism in plant morphological evolution. Proc Natl Acad Sci USA 101:6524–6529
Zahn LM, Leebens-Mack J, Arrington JM, Hu Y, Landherr LL, DePamphilis CW, Becker A, Theissen G, Ma H (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 8:30–45
Zanis MJ, Soltis DE, Soltis PS, Mathews S, Donoghue MJ (2002) The root of the angiosperms revisited. Proc Natl Acad Sci USA 99:6848–6853
Acknowledgements
We thank G. Theissen (Jena) and two anonymous reviewers for valuable comments on the manuscript. The last two authors also wish to thank Biol. J. C. Romero (Director of the Reserva de la Biosphera “Pantanos de Centla,” Estado de Tabasco, Mexico) for permission to collect plant material. The technical assistance (scanning electron microscopy) of U. Jauch (Institute of Plant Biology, University of Zurich) is gratefully acknowledged. This paper is part of a research project supported by the Swiss National Science Foundation (grant no. 3100AO-105974/1). We dedicate this publication to Matthias Wolf (†), an inspiring young biologist and lover of water lilies. He provided the SEM graphs for N. alba (Fig. 5).
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Grob, V., Moline, P., Pfeifer, E. et al. Developmental morphology of branching flowers in Nymphaea prolifera . J Plant Res 119, 561–570 (2006). https://doi.org/10.1007/s10265-006-0021-8
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DOI: https://doi.org/10.1007/s10265-006-0021-8