Abstract
Mapanioideae (besides Cyperoideae the other subfamily of Cyperaceae) is divided in two tribes (Hypolytreae and Chrysitricheae) in which the reproductive units (spicoids) are interpreted either as flowers or as inflorescences. Little is known about the ontogenetic factors operating during the spicoid development and how they may contribute to the spicoid final morphology. In this context, we studied the spicoid development in the monotypic genus Diplasia and compared it with other developmental studies in Mapanioideae. Our results show that the main developmental variations are related to the sequence of organ formation, the size and shape of the spicoid primordium and the influence of the subtending bract constraints in different sides of such primordium. Our hypotheses to explain the spicoid’s morphological variation in Mapanioideae are: that size and shape of the spicoid primordium contribute to changes in the number and position of organs to be formed, and spatial constraints of the subtending bracts influence the reduction of adaxial parts. Developmental features of the spicoids showed to be stable within the tribe. Our observations of the nature of spicoids in Diplasia give arguments for both, floral and inflorescence interpretations, sustaining the uncertainty towards a satisfactory definition. The difficulty in distinguishing the boundaries of flower and inflorescence nature in the spicoids raised a third hypothesis where the spicoid could be interpreted as a de novo structure, due to a reorganisation of regulatory genes resulting in a single unit with flower and inflorescence features combined, considered a synapomorphy of Mapanioideae.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bentham G (1877) On the distribution of the monocotyledonous orders into primary groups, more especially in reference to the Australian Flora, with notes on some points of terminology. Bot J Linn Soc 15:490–520. https://doi.org/10.1111/j.10958339.1877.tb00261.x
Bruhl JJ (1995) Sedge genera of the world: relationships and a new classification of the Cyperaceae. Austral Syst Bot 8:125–305. https://doi.org/10.1071/SB9950125
Chandler JW (2014) Patterns and polarity in floral meristem and floral organ initiation. Crit Rev Pl Sci 33:457–469. https://doi.org/10.1080/07352689.2014.917531
Chartier M, Jabbour F, Gerber S, Mitteroecker P, Sauquet H, von Balthazar M, Staedler Y, Crane PR, Schönenberger J (2014) The floral morphospace—a modern comparative approach to study angiosperm evolution. New Phytol 204:841–853. https://doi.org/10.1111/nph.12969
Clarke CB (1909) Illustrations of Cyperaceae. Williams and Norgate, London
Claßen-Bockhoff R, Frankenhäuser H (2020) The ‘Male Flower’ of Ricinus communis (Euphorbiaceae) Interpreted as a Multi-Flowered Unit. Frontiers Cell Dev Biol 8:313. https://doi.org/10.3389/fcell.2020.00313
Claßen-Bockhoff R, Meyer C (2016) Space matters: meristema expansion triggers corona formation in Passiflora. Ann Bot (Oxford) 117:277–290. https://doi.org/10.1093/aob/mcv177
Dahlgren R, Clifford H, Yeo P (1985) The families of the monocotyledons: evolution and taxonomy. Springer, Berlin
De Bruijn S, Angenent GC, Kaufmann K (2012) Plant ‘evo-devo’ goes genomic: from candidate genes to regulatory networks. Trends Pl Sci 17:441–447. https://doi.org/10.1016/j.tplants.2012.05.002
Dos Santos P, Ronse De Craene LP (2016) Floral development of Lewisia (Montiaceae): investigating patterns of perianth and stamen diversity. Flora 221:4–13. https://doi.org/10.1016/j.flora.2015.11.011
Doust AN (2001) The development basis of floral variation in Drimys winteri (Winteraceae). Int J Pl Sci 162:697–717. https://doi.org/10.1086/320790
Doust AN, Drinnan AN (2004) Floral development and molecular phylogeny support the generic status of Tasmannia (Winteraceae). Amer J Bot 91:321–331
Eiten LT (1976) Inflorescence units in the Cyperaceae. Ann Missouri Bot Gard 63:81–112. https://doi.org/10.2307/2395224
Endress PK (2006) Angiosperm floral evolution: morphological developmental framework. Advances Bot Res 44:1–61. https://doi.org/10.1016/S0065-2296(06)44001-5
Gagliardi KB, Cordeiro I, Demarco D (2018) Structure and development of flowers and inflorescences in Peraceae and Euphorbiaceae and the evolution of pseudanthia in Malpighiales. PLoS ONE 13:e0203954. https://doi.org/10.1371/journal.pone.0203954
Goetghebeur P (1998) Cyperaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol. 4. Springer, Berlin, pp 141–190
Guarise NJ, Vegetti AC (2008) Processes responsible of the structural diversity of the Cyperaceae synflorescence: hypothetical evolutionary trends. Flora 203:640–647. https://doi.org/10.1016/j.flora.2007.08.007
Hinchliff CE, Roalson EH (2013) Using supermatrices for phylogenetic inquiry: an example using the sedges. Syst Biol 62:205–219. https://doi.org/10.1093/sysbio/sys088
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York
Kern JH (1974) Cyperaceae. In: van Steenis CGGJ (ed) Flora Malesiana. Noordhoff, Leyden, pp 435–753
Koyama T (1971) Systematic interrelationships among Sclerieae, Lagenocarpeae and Mapanieae (Cyperaceae). Mitt Bot Staatssamml München 10:604–617
Lucero LE, Vegetti AC, Reinheimer R (2014) Evolution and development of the spikelet and flower of Rhynchospora (Cyperaceae). Int J Pl Sci 175:186–201. https://doi.org/10.1086/674317
Mesterhazy A, Browning J (2014) A rare enigmatic sedge rediscovered: principina grandis (Cyperaceae) newly recorded from Sao Tome. Kew Bull 69:9523. https://doi.org/10.1007/s12225-014-9532-y
Monteiro MM, Scatena VL, Oriani A (2016) Anatomy and development of the reproductive units of Mapania pycnostachya and Hypolytrum schraderianum (Mapanioideae, Cyperaceae). Austral J Bot 64:389–400. https://doi.org/10.1071/BT15281
Monteiro MM, Scatena VL, Oriani A (2017) Comparative floral anatomy of Rhynchospora consanguinea and Rhynchospora pubera (Cyperoideae, Cyperaceae). Pl Syst Evol 303:283–297. https://doi.org/10.1007/s00606-016-1371-x
Mora-Osejo JE (1967) Consideraciones sobre la naturaleza morfológica de las flores de algunos gêneros de las Cyperaceae. Revista Acad Colomb Ci Exact Fis Nat 16:23–35
Muasya AM, Simpson DA, Verboom GA, Goetghebeur P, Naczi RFC, Chase MC, Smets E (2009) Phylogeny of Cyperaceae based on DNA sequence data: current progress and future prospects. Bot Rev 75:2–21. https://doi.org/10.1007/s12229-008-9019-3
Prenner G, Rudall PJ (2007) Comparative ontogeny of the cyathium in Euphorbia (Euphorbiaceae) and its allies: exploring the organ-flower-inflorescence boundary. Amer J Bot 94:1612–1629. https://doi.org/10.3732/ajb.94.10.1612
Prenner G, Vergara-Silva F, Rudall PJ (2009) The key role of morphology in modelling inflorescence architecture. Trends Pl Sci 14:302–309. https://doi.org/10.1016/j.tplants.2009.03.004
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 62:345–350. https://doi.org/10.1093/jxb/erq275
Prychid CJ, Bruhl JJ (2013) Floral ontogeny and gene protein location rules out euanthial interpretation of reproductive units in Lepironia (Cyperaceae, Mapanioideae, Chrysitricheae). Ann Bot (Oxford) 112:161–177. https://doi.org/10.1093/aob/mct111
Remizowa MV, Sokoloff DD, Rudall PJ (2010) Evolutionary history of the monocot flower. Ann Missouri Bot Gard 97:617–645. https://doi.org/10.3417/2009142
Reyes E, Nadot S, Balthazar MV, Schönenberger J, Sauquet H (2018) Testing the impact of morphological rate heterogeneity on ancestral state reconstruction of five floral traits in angiosperm. Sci Rep 8:9473. https://doi.org/10.1038/s41598-018-27750-1
Richards JH, Bruhl JJ, Wilson KL (2006) Flower or spikelet? Understanding the morphology and development of reproductive structures in Exocarya (Cyperaceae, Mapanioideae, Chrysitricheae). Amer J Bot 93:1241–1250
Ronse De Craene LP (2010) Floral Diagrams: A aid to understanding flower morphology and evolution. Cambridge University Press, Cambridge
Ronse De Craene LP (2013) Reevaluation of the perianth and androecium in Caryophyllales: implications for flower evolution. Pl Syst Evol 99:1599–1636. https://doi.org/10.1007/s00606-013-0910-y
Ronse De Craene LP (2016) Meristic changes in flowering plants: how flowers play with number. Flora 221:22–37. https://doi.org/10.1016/j.flora.2015.08.005
Ronse De Craene LP (2018) Understanding the role of floral development in the evolution of angiosperm flowers: a clarification from different perspectives. J Pl Res 131:367–393. https://doi.org/10.1007/s10265-018-1021-1
Ronse De Craene LP, Smets EF (1994) Merosity in flowers: definition, origin, and taxonomic significance. Pl Syst Evol 191:83–104
Ronse De Craene LP, Linder HP, Smets EF (2002) Ontogeny and evolution of the flowers of South African Restionaceae with special emphasis on the gynoecium. Pl Syst Evol 231:225–258. https://doi.org/10.1007/s006060200021
Ronse De Craene LP, Soltis PS, Soltis DE (2003) Evolution of floral structures in basal Angiosperms. Int J Pl Sci 164:329–363. https://doi.org/10.1086/377063
Rosin FM, Kramer EM (2009) Old dogs, new tricks: regulatory evolution in conserved genetic modules leads to novel morphologies in plants. Developm Biol 332:25–35. https://doi.org/10.1016/j.ydbio.2009.05.542
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 Roy Soc B Biol Sci 365:397–409. https://doi.org/10.1098/rstb.2009.0234
Sauquet H, von Balthazar M, Magallon S, Doyle JA, Endress PK, Bailes EJ, de Morais EB, BullHerenu K, Carrive L, Chartier M, Chomicki G, Coiro M, Cornette R, El Ottra JHL, Epicoco C, Foster CSP, Jabbour F, Haevermans A, Haevermans T, Hernandez R, Little SA, Loefstrand S, Luna JA, Massoni J, Nadot S, Pamperl S, Prieu C, Reyes E, dos Santos P, Schoonderwoerd KM, Sontag S, Soulebeau A, Staedler Y, Tschan GF, Leung AW-S, Schoenenberger J (2017) The ancestral flower of angiosperms and its early diversification. Nat Commun 8:16047. https://doi.org/10.1038/ncomms16047
Semmouri I, Bauters K, Léveille-Bourret E, Starr JR, Goetghebeur P, Larridon I (2019) Phylogeny and systematics of Cyperaceae, the evolution and importance of embryo morphology. Bot Rev 85:1–39. https://doi.org/10.1007/s12229-018-9202-0
Simpson DA (1992) A revision of the genus Mapania. Royal Botanic Gardens, Kew, Publishing, London
Simpson DA (2006) Flora da Reserva Ducke—Cyperaceae. Rodriguesia 57:171–188
Simpson DA, Muasya AM, Alves M, Bruhl JJ, Dhooge S, Chase MW, Furness A, Ghamkhar K, Goetghebeur P, Hodkinson TR, Marchant AD, Reznicek AA, Nieuwborg R, Roalson EH, Smets E, Starr JR, Thomas WW, Wilson KL, Zhang X (2007) Phylogeny of Cyperaceae based on DNA sequence data: a new rbcL analysis. Aliso 23:72–83. https://doi.org/10.1007/s12229-008-9019-3
Sokoloff DD, Rudall P, Remizowa M (2006) Flower-like terminal structures in racemose inflorescences: a tool in morphogenetic and evolutionary research. J Exp Bot 57:3517–3530. https://doi.org/10.1093/jxb/erl126
Spalink D, Drew BT, Pace MC, Zaborsky JG, Starr JR, Cameron KM, Givnish TJ, Sytsma KJ (2016) Biogeography of the cosmopolitan sedges (Cyperaceae) and the area-richness correlation in plants. J Biogeogr 43:1893–1904. https://doi.org/10.1111/jbi.12802
Vegetti AC (2003) Synflorescence typology in Cyperaceae. Ann Bot Fenn 40:35–46
Vrijdaghs A, Smets E (2017) Spatial constraints influence the shape of spikelets and flowers in Cyperoideae (Cyperaceae). In: XIX International Botanical Congress (IBC 2017), Shenzhen, China, 23 - 29 July 2017, Abstract Book I. Curran Associates Inc., Red Hook, p 159
Vrijdaghs A, Caris P, Goetghebeur P, Smets E (2005) Floral ontogeny in Scirpus, Eriophorum and Dulichium (Cyperaceae), with special reference to the perianth. Ann Bot (Oxford) 95:1199–1209. https://doi.org/10.1093/aob/mci132
Vrijdaghs A, Goetghebeur P, Smets E, Muasya AM (2006) The floral scales in Hellmunthia (Cyperaceae, Cyperoideae) and Paramapania (Cyperaceae Mapanioideae): an ontogenetic study. Ann Bot (Oxford) 98:619–630. https://doi.org/10.1093/aob/mcl138
Vrijdaghs A, Goetghebeur P, Smets E, Caris P (2007) The Schoenus spikelet: a rhipidium? A floral ontogenetic answer. Aliso 23:204–209. https://doi.org/10.5642/aliso.20072301.15
Vrijdaghs A, Muasya AM, Goetghebeur P, Caris P, Nagels A, Smets E (2009) A floral ontogenetic approach to homology questions within the Cyperoideae (Cyperaceae). Bot Rev 75:30–51. https://doi.org/10.1007/s12229-008-9021-9
Vrijdaghs A, Reynders M, Larridon I, Muasya AM, Smets E, Goetghebeur P (2010) Spikelet structure and development in Cyperoideae, Cyperaceae: a monopodial general model based on ontogenetic evidence. Ann Bot (Oxford) 105:555–571. https://doi.org/10.1093/aob/mcq010
Vrijdaghs A, Reynders M, Muasya AM, Larridon I, Goetghebeur P, Smets E (2011) Spikelet and floral ontogeny in Cyperus and Pycreus (Cyperaceae). Pl Ecol Evol 144:44–63. https://doi.org/10.1093/aob/mcq010
Acknowledgments
The authors thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the PhD grant for MM and to CAPES-PRINT/USP (EDITAL No 01/2019-88887.368005/2019-00) for the scholarship that allowed MM to develop SEM analysis at the Royal Botanic Gardens, Kew. We thank Royal Botanic Gardens, Kew for providing the facilities and to Maria Conejero for her support with the SEM. We appreciate the valuable input of Dr Alex Vrijdaghs and Dr Louis Ronse De Craene on the manuscript.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES)-Finance Code 001 and by CAPES-PRINT/USP (EDITAL No 01/2019-88887.368005/2019-00).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Handling Editor: Louis P. Ronse De Craene.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Monteiro, M.M., Demarco, D., Oriani, A. et al. Spicoid ontogeny in Diplasia (Mapanioideae, Cyperaceae): an approach on the developmental processes operating in Mapanioideae spicoids. Plant Syst Evol 306, 91 (2020). https://doi.org/10.1007/s00606-020-01720-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-020-01720-5