Flower-like heads from flower-like meristems: pseudanthium development in Davidia involucrata (Nyssaceae)
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Abstract
Flower-like inflorescences (pseudanthia) have fascinated botanists for a long time. They are explained as condensed inflorescences implying that the pseudanthium develops from an inflorescence meristem (IM). However, recent developmental studies identified a new form of reproductive meristem, the floral unit meristem (FUM). It differs from IMs by lacking acropetal growth and shares fractionation, expansion and autonomous space filling with flower meristems (FM). The similarity among FUMs and FMs raises the question how far flower-like heads originate from flower-like meristems. In the present paper, pseudanthium development in Davidia involucrata is investigated using scanning electron microscopy. D. involucrata has pincushion-shaped heads composed of densely aggregated, perianthless flowers and associated with two large showy bracts. Early developmental stages show a huge naked FUM. The FMs appear almost simultaneously and lack subtending bracts. With ongoing FUM expansion new space is generated which is immediately used by further FM fractionation. The heads have only staminate flowers or are andromonoecious with staminate and a single perfect flower in oblique position. All FMs lack perianth structures and fractionate a variable number of stamen primordia. The perfect FM is much larger than the staminate FMs and forms a syncarpous gynoecium with inferior ovary. Pseudanthium development in D. involucrata confirms the morphogenetic similarity to FMs as to acropetal growth limitation, meristem expansion and fractionation. It thus should not be interpreted as a condensed inflorescence, but as a flower equivalent. Furthermore as the FUM develops inside a bud, its development is considered to be influenced by mechanical pressure. The oblique position of the perfect flower, the developmental delay of the proximal flowers, and the variable number of stamens which were observed in the pseudanthium development, can be caused by mechanical pressure. Next to the Asteraceae, D. involucrata offers a further example of a pseudanthium originating from a FUM. More knowledge on FUMs is still needed to understand diversification and evolution of flower-like inflorescences.
Keywords
Extrafloral bracts Floral unit meristem (FUM) Flower meristem (FM) Inflorescence meristem (IM) Mechanical pressure Utilization of spaceNotes
Acknowledgements
We thank Akitoshi Iwamoto (Tokyo) and Kester Bull-Hereñu (Santiago de Chile) for initiating this special issue on flowers. The first author is very grateful to the Botanical Society of Japan for the invitation and financial support to participate at its annual congress at Okinawa 2016. We thank Bernd Mengel (BG Mainz) for collecting Davidia buds throughout the year, Madeleine Junginger (Mainz) for measuring the primordia at the SEM pictures and Maria Geyer (Mainz) for working over the illustrations. Special thanks go to Margerita Remizowa (Moscow) and an unknown reviewer for stimulating discussion.
References
- Albert VA, Gustafson MHG, Di Laurenzio L (1998) Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants. II. DNA sequencing. Kluwer, Boston, pp 1–25Google Scholar
- Bäurle I, Laux T (2003) Apical meristems: the plant’s fountain of youth. Bioassays 25:96–970CrossRefGoogle Scholar
- Bello MA, Álvarez I, Torices R, Fuertes-Aguilar J (2013) Floral development and evolution of capitulum structure in Anacyclus (Anthemideae Asteraceae). Ann Bot 112:1597–1612CrossRefPubMedPubMedCentralGoogle Scholar
- Bello MA, Cubas P, Álvarez I, Sanjuanbenito G, Fuertes-Aguilar J (2017) Evolution and expression patterns of CYC/TB1 genes in Anacyclus: Phylogenetic insights for floral symmetry genes in Asteraceae. Front Plant Sci 8:589. https://doi.org/10.3389/fpls.2017.00589 CrossRefPubMedPubMedCentralGoogle Scholar
- Broholm SK, Teeri TH, Elomaa P (2014) Molecular control of inflorescence development in Asteraceae. Adv Bot Res 27:297–334CrossRefGoogle Scholar
- Bull-Hereñu K, Claßen-Bockhoff R (2010) Developmental conditions for terminal flower production in apioid umbellets. Plant Div Evol 128:221–232CrossRefGoogle Scholar
- Bull-Hereñu K, Claßen-Bockhoff R (2011a) Open and closed inflorescences: more than simple opposites. J Exp Bot 62:79–88CrossRefPubMedGoogle Scholar
- Bull-Hereñu K, Claßen-Bockhoff R (2011b) Ontogenetic course and spatial constraints in the appearance and disappearance of the terminal flower in inflorescences. Int J Plant Sci 172:471–498CrossRefGoogle Scholar
- Burr B, Barthlott W (1993) Untersuchungen zur Ultraviolettreflexion von Angiospermenblüten.II. Magnoliidae, Ranunculidae, Hamamelididae, Caryophyllidae, Rosidae. Trop subtrop Pflanzenwelt 87, Akad Wiss Lit Mainz. Steiner, StuttgartGoogle Scholar
- Claßen Bockhoff R (1996) A survey of flower-like inflorescences in the Rubiaceae. Opera Bot Belg 7:329–367Google Scholar
- Claßen-Bockhoff R (1990) Pattern analysis in pseudanthia. Plant Syst Evol 171:57–88CrossRefGoogle Scholar
- Claßen-Bockhoff R (1991) Anthodien, Pseudanthien und Infloreszenzblumen. Beitr Biol Pfl 66:221–224Google Scholar
- Claßen-Bockhoff R (2016) The shoot concept of the flower: Still up to date? Flora 221:46–53CrossRefGoogle Scholar
- Claßen-Bockhoff R, Bull-Hereñu K (2013) Towards an ontogenetic understanding of inflorescence diversity. Ann Bot 112:1523–1542CrossRefPubMedPubMedCentralGoogle Scholar
- Claßen-Bockhoff R, Meyer C (2016) Space matters: meristem expansion triggers corona formation in Passiflora. Ann Bot 117:277–290PubMedGoogle Scholar
- Claßen-Bockhoff R, Ruonala R, Bull-Hereñu K, Marchant N, Albert VA (2013) The unique pseudanthium of Actinodium (Myrtaceae) - morphological reinvestigation and possible regulation by CYCLOIDEA-like genes. EvoDevo 4:8. https://doi.org/10.1186/2041-9139-4-8 CrossRefPubMedPubMedCentralGoogle Scholar
- Diggle PK (2003) Architectural effects on floral form and function: a review. In: Stuessy T, Hörandl E, Mayer V (eds) Deep morphology: toward a renaissance of morphology in plant systematics. Koeltz, Konigstein, pp 63–80Google Scholar
- Douady S, Couder Y (1996) Phyllotaxis as a dynamic self organizing process. J Theor Biol 139:178–312Google Scholar
- Eyde RH (1963) Morphological and paleobotanical studies in Nyssaceae. J Arnold Arboretum 44:1–54Google Scholar
- Fang WP, Chang CY (1983) Flora Republicae Popularis Sinicae, vol 52. Science, BejingGoogle Scholar
- Feng CM, Liu X, Yu Y, Xie D, Franks RG, Xiang QJ (2012) Evolution of bract development and B-class MADS box gene expression in petaloid bracts of Cornus s.l. (Cornacese). New Phytol 196:631–643CrossRefPubMedGoogle Scholar
- Froebe HA, Ulrich G (1978) Pseudanthien bei Umbelliferen. Beitr Biol Pfl 54:175–206Google Scholar
- Good R (1956) Features of evolution in the flowering plants. Longman, Green & Co, LondonGoogle Scholar
- Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz WM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322:1650–1655CrossRefPubMedGoogle Scholar
- Harris E (1995) Inflorescence and floral ontogeny in Asteraceae: a synthesis of historical and current concepts. Bot Rev 61:93–278CrossRefGoogle Scholar
- Harris EM, Tucker SC, Urbatsch LE (1991) Floral initiation and early development in Erigeron philadelphicus (Asetarcaeae). Am J Bot 78:108–121CrossRefGoogle Scholar
- Hempel FD, Feldman LJ (1994) Bi-directional inflorescence development in Arabidopsis thaliana: acropetal initiation of flowers and basipetal initiation of paraclades. Planta 192:276–286CrossRefGoogle Scholar
- Horne AS (1909) The structure and affinities of Davidia involucrata Baill. Trans Linn Soc Bot 2 Ser 7:303.367Google Scholar
- Hu Y, Zhang SL, Su ZX, Liao YM (2007) Pollinator attraction by Davidia involucrata. I. Color. J Plant Ecol 31:166–171 (Chinese with English abstract) CrossRefGoogle Scholar
- Jahnke C (1986) Der Infloreszenzbau der Cornaceen sensu lato und seine systematischen Konsequenzen. Trop subtrop Pflanzenwelt 57, Akad Wiss Lit Mainz. Steiner, StuttgartGoogle Scholar
- Jerominek M, Bull-Hereñu K, Arndt M, Claßen-Bockhoff R (2014) Live imaging of developmental processes in a living meristem of Davidia involucrata (Nyssaceae). Front Plant Sci 5:613. https://doi.org/10.3389/fpls.2014.00613 CrossRefPubMedPubMedCentralGoogle Scholar
- Johow F (1884) Zur Biologie der floralen und extrafloralen Schauapparate. Jb Kgl Bot Gart Berlin 3:47–68Google Scholar
- Kubitzki K (2004) Cornaceae. In: Kubitzki K (ed) The families and genera of vascular plants. VI. Flowering plants dicotyledons. Celastrales, Oxalidales, Rosales, Cornales, Ericales. Heidelberg. Springer, Heidelberg, pp 82–90Google Scholar
- Kwiatkowska D (2008) Flowering and apical meristem growth dynamics. J Exp Bot 59:187–201CrossRefPubMedGoogle Scholar
- Leppik EE (1969) Morphogenetic classification of flower types. Phytomorphology 18:451–466Google Scholar
- Manchester SR (2003) Leaves and fruits of Davidia (Cornales) from the Paleocene of North America. Syst Bot 27:368–382Google Scholar
- Mizzotti C, Fambrini M, Caporali E, Masiero S, Pugliesi C (2015) A CYCLOIDEA-like gene mutation in sunflower determines an unusual floret type able to produce filled achenes at the periphery of the pseudanthium. Botany 93:171–181CrossRefGoogle Scholar
- Moser V (1968) Der Blütenbau der angeblich verwandten Gattungen Davidia und Camptotheca. Vierteljahrsschr Nat forsch Ges Zür 113:157–184Google Scholar
- Naghiloo S, Claßen-Bockhoff R (2017) Understanding the unique flowering dequence in Dipsacus fullonum: Evidence from geomertrical changes during head development. PLoS One. https://doi.org/10.1371/journal.pone.0174091 Google Scholar
- Owens A, Cieslak M, Hart J, Classen-Bockhoff R, Prusinkiewicz P (2016) Modeling dense inflorescences. ACM Trans Graph 35:4. https://doi.org/10.1145/2897824.2925982 CrossRefGoogle Scholar
- Pozner R, Zanotti C, Johnson LA (2012) Evolutionary origin of the Asteraceaen capitulum: insights from Calyceraceae. Am J Bot 99:1–13CrossRefPubMedGoogle Scholar
- Prenner G, Rudall PJ (2007) Comparative ontogeny of the cyathium in Euphorbia (Euphorbiaceae) and its allies: exploring the organ–flower–inflorescence boundary. Am J Bot 94:1612–1629CrossRefPubMedPubMedCentralGoogle Scholar
- Prenner G, Hopper SD, Rudall PJ (2008) Pseudanthium development in Calycopeplus paucifolius, with particular reference to the evolution of the cyathium in Euphorbieae (Euphorbiaceae-Malpighiales). Austr Syst Bot 21:153–161CrossRefGoogle Scholar
- Prenner G, Cacho NI, Baum D, Rudall PJ (2011) Is LEAFY a useful marker gene for the flower–inflorescence boundary in the Euphorbia cyathium? J Exp Bot 62:345–350CrossRefPubMedGoogle Scholar
- Prusinkiewicz P, Barbier de Reuille P (2010) Constraints of space in plant development. J Exp Bot 61:2117–2129CrossRefPubMedGoogle Scholar
- Prusinkiewicz P, Runions A (2012) Computational models of pklant development and form. New Phytol 193:549–569CrossRefPubMedGoogle Scholar
- Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M. Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260CrossRefPubMedGoogle Scholar
- Reuther K, Claßen-Bockhoff R (2010) Diversity behind uniformity - inflorescence architecture and flowering sequence in Apioideae. Plant Div Evol 128:181–220CrossRefGoogle Scholar
- Ronse de Craene L, Smets E (1992) Complex polyandry in the Magnoliateae: definition, distribution and systematic value. Nord J Bot 12:621–649CrossRefGoogle Scholar
- Rudall PJ (2003) Monocot pseudanthia revisited: floral structure of the mycoheterotrophic family Triuridaceae. Int J Plant Sci 164(S5):307–320CrossRefGoogle Scholar
- Rudall PJ (2010) All in a spin: centrifugal organ formation and floral patterning. Curr Opin Plant Biol 13:108–114CrossRefPubMedGoogle Scholar
- Rudall PJ, Bateman RM (2010) Defining the limits of flowers: the challenge of distinguishing between the evolutionary products of simple versus compound strobili. Philos Trans R Soc B Biol Sci 365:397–409CrossRefGoogle Scholar
- Runions A, Smith RS, Prusinkiewicz P (2014) Computational models of auxin-driven development. In: Zažímalová E, Petrášek J, Benkova E (eds) Auxin and its role in plant development. Springer, Heidelberg, pp 315–357CrossRefGoogle Scholar
- Sokoloff D, Rudall PJ, Remizowa M (2006) Flower-like terminal structures in racemose inflorescences: a tool in morphogenetic and evolutionary research. J Exp Bot 57:3517–3530CrossRefPubMedGoogle Scholar
- Stützel T, Trovó M (2013) Inflorescences in Eriocaulaceae: taxonomic relevance and practical implications. Ann Bot 112:1505–1522CrossRefPubMedPubMedCentralGoogle Scholar
- Sun JF, Gong YB, Renner SS, Huang SQ (2008) Multifunctional bracts in the dove tree Davidia involucrata (Nyssaceae: Cornales): rain protection and pollinator attraction. Am Nat 171:119–124CrossRefPubMedGoogle Scholar
- Troll W (1928) Organisation und Gestalt im Bereich der Blüte. Springer, BerlinGoogle Scholar
- Tucker SC, Grimes J (1999) The inflorescence: introduction. Bot Rev 65:303–316CrossRefGoogle Scholar
- van Tunen AJ, Eikelboom W, Angenent GC (1993) Floral organogenesis in Tulipa. Flower Newsl 116:33–38Google Scholar
- Vekemans D, Viaene T, Caris P, Geuten K (2012) Transference of function shapes organ identity in the dove tree inflorescence. New Phytol 193:216–228CrossRefPubMedGoogle Scholar
- Xiang QY, Thomas DT, Xiang QP (2011) Resolving and dating the phylogeny of Cornales—effects of taxon sampling, data partitions, and fossil calibrations. Mol Phyl Evol 59:123–128CrossRefGoogle Scholar
- You H, Liu Y, Fujiwara K (2013) Effects of life-history components on population dynamics of the rare endangered plant Davidia involucrate. Nat Sci 5:62–70. https://doi.org/10.4236/ns.2013.51011 Google Scholar
- You H, Fujiwara K, Liu Y (2014) A preliminary vegetation-ecological study of Davidia involucrata forest. Nat Sci 6:1012–1029Google Scholar
- Zhao Y, Zhang T, Broholm SK, Tähtiharju S, Mouhu K, Albert VA, Teeri TH, Elomaa P (2016) Evolutionary co-option of floral meristem identity genes for patterning of the flower-like Asteraceae inflorescence. Plant Physiol Preview. https://doi.org/10.1104/pp.16.00779 Google Scholar