Abstract
Thurniaceae are positioned at the base of the cyperids, in Poales, as a sister group of Cyperaceae + Juncaceae. However, Rapateaceae + Mayacaceae have emerged related to these families in a recent phylogenetic study. Although Thurniaceae are morphologically similar to Juncaceae, studies are needed to evaluate characters with systematic value and that may help comprehend the reproductive biology in the family. In this regard, we investigate the floral morphology and anatomy of Prionium serratum and Thurnia sphaerocephala using standard techniques of scanning electron microscopy and light microscopy. The flowers of both species are trimerous, pentacyclic, with diplostemonous androecium and tricarpellate syncarpous gynoecium. Nevertheless, dimerous flowers with an inconsistent number of stamens also occur in T. sphaerocephala. Most floral traits of Thurniaceae are shared with Juncaceae and indicate putative plesiomorphies in the cyperids. However, no consistent data corroborates a link between Rapateaceae and Mayacaceae and the cyperids. The perigonium of Thurniaceae has diagnostic characters for the family, but also for each one of the species studied. The androecium is similar in P. serratum and T. sphaerocephala. In the gynoecium, the number of ovules, the length of the ovary zones, and the occurrence of ovary wall intrusions distinguish P. serratum from T. sphaerocephala and may have a correlation in the cyperids. Furthermore, the type of inflorescence, the color of flowers, and the type of stigma suggest that P. serratum is wind-pollinated and that T. sphaerocephala is insect-pollinated.
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References
Alves M (2003) Hypolytrum Rich. (Cyperaceae) nos Neotrópicos. PhD Thesis, Universidade de São Paulo, São Paulo
Azad AK, Sawa Y, Ishikawa T, Shibata H (2007) Temperature-dependent stomatal movement in tulip petals controls water transpiration during flower opening and closing. Ann Appl Biol 150:81–87. https://doi.org/10.1111/j.1744-7348.2006.00111.x
Baillon H (1894) Histoire des plantes. Librairie Hachette, Paris
Balslev H (1998) Juncaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Flowering plants - Monocotyledons Alismatanae and Commelinanae (except Gramineae). Springer, Berlin, pp 252–260
Bentham G (1883) Juncaceae. In: Bentham G, Hooker JD (eds) Genera Plantarum, vol. 3. Reeve & Co., London, pp 861–869
Bouchenak-Khelladi Y, Muasya AM, Linder HP (2014) A revised evolutionary history of Poales: origins and diversification. Bot J Linn Soc 175:4–16. https://doi.org/10.1111/boj.12160
Bremer K (2002) Gondwanan evolution of the grass alliance of families (Poales). Evolution 56:1374–1387. https://doi.org/10.1554/0014-3820(2002)056[1374:GEOTGA]2.0.CO;2
Bremer B, Bremer K, Chase MW, Reveal JL, Soltis DE, Soltis PS, Stevens PF, Fay MF, Goldblatt P, Judd WS, Källersjö M, Kårehed J, Kron KA, Lundberg J, Nickrent DL, Olmstead RG, OxelmanB CPJ, Rodman JE, Rudall PJ, Savolainen V, Sytsma KJ, van der Bank M, Wurdack K, Xiang JQ-Y, Zmarzty S (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141:399–436. https://doi.org/10.1046/j.1095-8339.2003.t01-1-00158.x
Campbell LM, Stevenson DW (2007) Inflorescence architecture and floral morphology of Aratitiyopea lopezii (Xyridaceae). Aliso 23:227–233. https://doi.org/10.5642/aliso.20072301.17
Carvalho MLS, Nakamura AT, Sajo MG (2009) Floral anatomy of Neotropical species of Mayacaceae. Flora 204:220–227. https://doi.org/10.1016/j.flora.2008.02.003
Chase MW, Soltis DE, Soltis PS, Rudall PJ, Fay MF, Hahn WJ, Sullivan S, Joseph J, Molvray M, Kores PJ, Givnish TJ, Sytsma KJ, Pires JC (2000) Higher-level systematics of the monocotyledons: an assessment of current knowledge and a new classification. In: Wilson KL, Morrison DA (eds) Monocots: systematics and evolution. CSIRO, Melbourne, pp 3–16
Coan AI, Alves MV, Scatena VL (2008) Comparative study of ovule and fruit development in species of Hypolytrum and Rhynchospora (Cyperaceae, Poales). Pl Syst Evol 272:181–195. https://doi.org/10.1007/s00606-007-0636-9
Coan AI, Alves MV, Scatena VL (2010) Evidence of pseudomonad pollen formation in Hypolytrum (Mapanioideae, Cyperaceae). Austral J Bot 58:663–672. https://doi.org/10.1071/BT10149
Costa ACG, Thomas WW, Machado IC (2017) Comparative floral biology of Rhynchospora ciliata (Vahl) Kukenth and R. pubera (Vahl) Boeckeler (Cyperaceae): the role of white involucral bracts in attracting pollinating insects. Plant Sp Biol 32:403–411. https://doi.org/10.1111/1442-1984.12173
Culley TM, Weller SG, Sakai AK, Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollination in angiosperms. Trends Ecol Evol 17:361–369
Cutler DF (1963) Inverted vascular bundles in the leaf of the Thurniaceae. Nature 198:1111–1112
Cutler DF (1965) Vegetative anatomy of Thurniaceae. Kew Bull 19:431–441. https://doi.org/10.2307/4108191
Cutler DF (1969) Juncales. In: Metcalfe CR (ed) Anatomy of the monocotyledons IV. Clarendon Press, Oxford, pp 1–357
Dahlgren RMT, Clifford HT (1982) The monocotyledons: a comparative study. Academic Press, London
Dahlgren RMT, Clifford HT, Yeo PF (1985) The families of the monocotyledons: structure, evolution, and taxonomy. Springer, Berlin
Dobson HE, Bergström G (2000) The ecology and evolution of pollen odors. Pl Syst Evol 222:63–87. https://doi.org/10.1007/BF00984096
Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, New York
Engler A (1907) Syllabus der Pflanzenfamilien. Borntraeger, Berlin
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Amer J Bot 55:123–142. https://doi.org/10.2307/2440500
Ferrari RC, Oriani A (2017) Floral anatomy and development of Saxofridericia aculeata (Rapateaceae) and its taxonomic and phylogenetic significance. Pl Syst Evol 303:187–201. https://doi.org/10.1007/s00606-016-1361-z
Givnish TJ, Pires JC, Graham SW, Mcpherson MA, Prince LM, Patterson TB, Rai HS, Roalson EH, Evans TM, Hahn WJ, Hall C, Kress WJ, Sytsma KJ (2006) Phylogenetic relationships of monocots based on the highly informative plastid gene ndhF: evidence for widespread concerted convergence. Aliso 22:28–51. https://doi.org/10.5642/aliso.20062201.04
Givnish TJ, Ames M, McNeal JR, McKain MR, Steele PR, DePamphilis CW, Graham SW, Pires JC, Stevenson DW, Zomlefer WB, Briggs BG, Duvall MR, Moore MJ, Heaney JM, Soltis DE, Soltis PS, Thiele K, Leebens-Mack JH (2010) Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales. Ann Missouri Bot Gard 97:584–616. https://doi.org/10.3417/2010023
Givnish TJ, Zuluaga A, Spalink D, Gomez MS, Lam VKY, Saarela JM, Sass C, Iles WJD, Souza DJL, Leebens-Mack J, Pires JC, Zomlefer WB, Gandolfo MA, Davis JI, Stevenson DW, DePamphilis C, Specht CD, Graham SW, Barret CF, Ané C (2018) Monocot plastid phylogenomics, timeline, net rates of species diversification, the power of multi-gene analyses, and a functional model for the origin of monocots. Amer J Bot 105:1888–1910. https://doi.org/10.1002/ajb2.1178
Goetghebeur P (1998) Cyperaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Flowering plants – Monocotyledons. Alismatanae and Commelinanae (except Gramineae). Springer, Berlin, pp 141–189
Huang SQ, Xiong YZ, Barrett SCH (2013) Experimental evidence of insect pollination in Juncaceae, a primarily wind-pollinated family. Int J Pl Sci 174:1219–1228. https://doi.org/10.1086/673247
Ickert-Bond S, Gerrath J, Wen J (2014) Gynoecial structure of Vitales and implications for the evolution of placentation in the Rosids. Int J Pl Sci 175:998–1032. https://doi.org/10.1086/678086
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, London
Jones E, Simpson DA, Hodkinson TR, Chase MW, Parnell JAN (2007) The Juncaceae-Cyperaceae interface: a combined plastid sequence analysis. Aliso 23:55–61
Kubitzki K (1998) Thurniaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Flowering plants – Monocotyledons. Alismatanae and Commelinanae. (except Gramineae), Springer, Berlin, pp 455–457
Leinfellner W (1950) Der Bauplan des synkarpen Gynözeums. Pl Syst Evol 97:403–436. https://doi.org/10.1007/BF01763317
Linder HP, Rudall PJ (2005) Evolutionary history of Poales. Annual Rev Ecol Evol Syst 36:107–124. https://doi.org/10.1146/annurev.ecolsys.36.102403.135635
Lorougnon G (1973) Le vecteurpollinique chez les Mapania et les Hypolytrum, Cypéracées du sous-bois des forêtstropicales ombrophiles. Bull Jard Bot Natl Belg/Bull Natl Plantentuin Belg 43:33–36. https://doi.org/10.2307/3667561
Magalhães AF, Ruiz ALTG, Flach A, Faria AD, Magalhães EG, Amaral MDCE (2005) Floral scent of Eleocharis elegans (Kunth) Roem. & Schult. (Cyperaceae). Biochem Syst Ecol 33:675–679. https://doi.org/10.1016/j.bse.2004.12.004
Maheshwari P (1950) An introduction to the embryology of the angiosperms. McGraw-Hill, New York
Makde KH (1981) Endothecium in Cyperaceae. Curr Sci 50:98–99
Manning J, Goldblatt P (2012) Plants of the Greater Cape Floristic Region. 1. The Core Cape flora. South African National Biodiversity Institute, Pretoria
Mucina L, Rutherford, MC (2006) The vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19. South African National Biodiversity Institute, Pretoria
Munro SL, Linder HP (1998) The phylogenetic position of Prionium (Juncaceae) within the order Juncales based on morphological and rbcL sequence data. Syst Bot 23:43–55. https://doi.org/10.2307/2419573
Munyai R (2013) A systematic study of the South African genus Prionium (Thurniaceae). MScThesis, University of Cape Town, Cape Town
Nijalingappa BHM (1976) Sporogenesis and gametogenesis in some Cyperaceae. Proc Indian Acad Sci 83:66–72. https://doi.org/10.1007/BF03045461
Oriani A, Scatena VL (2012) Floral anatomy of Xyrids (Poales): contributions to their reproductive biology, taxonomy, and phylogeny. Int J Pl Sci 173:767–779. https://doi.org/10.1086/666664
Oriani A, Scatena VL (2013) The taxonomic value of floral characters in Rapateaceae (Poales-Monocotyledons). Pl Syst Evol 299:291–303. https://doi.org/10.1007/s00606-012-0721-6
Oriani A, Scatena VL (2019) Floral organogenesis and vasculature in Mayacaceae, an enigmatic family of Poales. Pl Syst Evol 7:549–562. https://doi.org/10.1007/s00606-019-01592-4
Oriani A, Stützel T, Scatena VL (2012) Contributions to the floral anatomy of Juncaceae (Poales - Monocotyledons). Flora 207:334–340. https://doi.org/10.1016/j.flora.2012.03.001
Plunkett G, Soltis D, Soltis P, Brooks R (1995) Phylogenetic relationships between Juncaceae and Cyperaceae: insights from rbcL sequence data. Amer J Bot 82:520–525. https://doi.org/10.1002/j.1537-2197.1995.tb15673.x
Porsch O (1956) Windpollen und Blumeninsekt. Österr Bot Z 103:1–18
Roddy AB, Brodersen CR, Dawson TE (2016) Hydraulic conductance and the maintenance of water balance in flowers. Pl Cell Environm 39:2123–2132. https://doi.org/10.1111/pce.12761
Ronse De Craene L (2016) Meristic changes in flowering plants: how flowers play with numbers. Flora 221:22–37. https://doi.org/10.1016/j.flora.2015.08.005
Sajo MG, Oriani A, Scatena VL, Rudall PJ (2017) Floral ontogeny and vasculature in Xyridaceae, with particular reference to staminodes and stylar appendages. Pl Syst Evol 303:1293–1310. https://doi.org/10.1007/s00606-017-1438-3
Swain T (2003) Secondary Compounds as Protective Agents. Annual Rev Pl Physiol 28:479–501. https://doi.org/10.1146/annurev.pp.28.060177.002403
Thimm U (1985) ZurEmbryologie, Blüten- und Fruchtanatomie der isolierten Juncales-Gattungen Prionium and Thurnia. MSc Thesis, Ruhr-Universität Bochum, Bochum
Vrijdaghs A, Caris P, Goetghebeur P, Smets E (2005a) 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, Muasya AM, CarisP S, E, (2005b) Floral ontogeny in Ficinia and Isolepis (Cyperaceae), with focus on the nature and origin of the gynophore. Ann Bot (Oxford) 96:1247–1264. https://doi.org/10.1093/aob/mci276
Vrijdaghs A, Muasya AM, Goetghebeur P, Caris P, Nagels A, Smets E (2009) A floral ontogenetic approach to questions of homology 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
Whitehead DR (1969) Wind pollination in the angiosperms: evolutionary and environmental considerations. Evolution 23:28–35. https://doi.org/10.1111/j.1558-5646.1969.tb03490.x
Wolowski M, Freitas L (2015) An overview on pollination of the Neotropical Poales. Rodriguésia 66:329–336. https://doi.org/10.1590/2175-7860201566204
Wragg PD, Johnson SD (2011) Transition from wind pollination to insect pollination in sedges: experimental evidence and functional traits. New Phytol 191:1128–1140. https://doi.org/10.1111/j.1469-8137.2011.03762.x
Acknowledgements
We thank Prof. Dr. Thomas Stützel (Ruhr-Universität Bochum, Germany) and Prof. Dr. Muthama Muasya (University of Cape Town, South Africa) for supplying the material of Prionium serratum. Financial support was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq to A.L. Silva (Ph.D. Scholarship/proc. 140014/2017–9) and to A.I. Coan (Research Scholarship Pq-2/proc. 308504/2018–0).
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Silva, A.d.L., Alves, M.V.S. & Coan, A.I. Comparative floral morphology and anatomy of Thurniaceae, an early-diverging family in the cyperids (Poales, Monocotyledons). Plant Syst Evol 306, 53 (2020). https://doi.org/10.1007/s00606-020-01681-9
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DOI: https://doi.org/10.1007/s00606-020-01681-9