Abstract
Non-papilionate and actinomorphic flowers have evolved independently in Papilionoideae, and few ontogeny studies are available about them. The objective of the present study was to better understand the ontogenetic processes that result in papilionate and non-papilionate flowers in a sister group of the Pterocarpus clade. Inflorescences, flower buds and flowers of Discolobium pulchellum and Riedeliella graciliflora were analyzed by scanning electron microscopy, light microscopy and histochemistry of the secretory structures of floral organs. The differentiation of the petals is initiated by the petal standard followed by the keel petals and finally by the wing petals in Discolobium, in contrast to a unidirectional development of the petals in the corolla of Riedeliella. The order of sepals and antesepalous stamen is unidirectional in D. pulchellum and modified unidirectional in R. graciliflora; however, the order of petal and antepetalous stamen initiation, stamen symmetry and early appearance of carpel are similar in both species. Hypanthium and floral nectary are present only in D. pulchellum and colleters in R. graciliflora. Glandular trichomes and idioblasts are present in both species. The presence of secretory structures is possibly related to the protection against herbivores, to pollination and pollinator’s attraction since different secondary compounds are present in reproductive structures. The development of the actinomorphic corolla of Riedeliella graciliflora has no similarity in terms of floral development to the other representatives of actinomorphic symmetry in Papilionoideae.
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References
Azani N, Babineau M, Bailey CD, Banks H, Barbosa AR, Pinto RB, Zimmerman E (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: the Legume Phylogeny Working Group (LPWG). Taxon 66:44–77. https://doi.org/10.12705/661.3
Barros TCD, Marinho CR, Pedersoli GD, Paulino JV, Teixeira SP (2017) Beyond pollination: diversity of secretory structures during flower development in different legume lineages. Acta Bot Brasil 31:358–373. https://doi.org/10.1590/0102-33062016abb0291
Barroso GM, Morim MP, Peixoto AL, Ichaso CLF (2004) Frutos e sementes: Morfología aplicada à Sistemática de Dicotiledôneas. Editora UFV, Viçosa
Beckman CH (2000) Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defence responses in plants? Physiol Molec Pl Pathol 57:101–110. https://doi.org/10.1006/pmpp.2000.0287
Bérgamo LM (2017) Modo de Polinização em espécies papilionadas e não-papilionadas de Faboideae: Discolobium pulchellum e Riedeliella graciliflora. MSc Thesis, Fundação Universidade Federal do Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul
Beyra Matos A, Lavin MT (1999) Monograph of Pictetia (Leguminosae-Papilionoideae) and review of the Aeschynomeneae. Syst Bot Monogr 56:1–93
Cardoso D, De Queiroz LP, Pennington RT, De Lima HC, Fonty E, WojciechowskI MF, Lavin M (2012a) Revisiting the phylogeny of papilionoid legumes: new insights from comprehensively sampled early-branching lineages. Amer J Bot 99:1991–2013. https://doi.org/10.3732/ajb.1200380
Cardoso D, De Lima HC, Rodrigues RS, De Queiroz LP, Pennington RT, Lavin M (2012b) The realignment of Acosmium sensu stricto with the Dalbergioid clade (Leguminosae: Papilionoideae) reveals a proneness for independent evolution of radial floral symmetry among early-branching papilionoid legumes. Taxon 61:1057–1073. https://doi.org/10.1002/tax.615011
Cardoso D, Pennington RT, De Queiroz LP, Boatwright JS, Van Wyk BE, Wojciechowski MF, Lavin M (2013) Reconstructing the deep-branching relationships of the papilionoid legumes. S African J Bot 89:58–75. https://doi.org/10.1016/j.sajb.2013.05.001
Cardoso D, São-Mateus WM, Da Cruz DT, Zartman CE, Komura DL, Kite G, Prenner G, Wieringa JJ, Clark A, Lewis G, Penningto RT, De Queiroz LP (2015) Filling in the gaps of the papilionoid legume phylogeny: the enigmatic Amazonian genus Petaladenium is a new branch of the early-diverging Amburaneae clade. Molec Phylogen Evol 84:112–124. https://doi.org/10.1016/j.ympev.2014.12.015
Citerne HL, Pennington RT, Cronk QC (2006) An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. Proc Natl Acad Sci USA 103:12017–12020. https://doi.org/10.1073/pnas.0600986103
Coutinho ÍAC, Francino DMT, Meira RMSA (2015) New records of colleters in Chamaecrista (Leguminosae, Caesalpinioideae SL): structural diversity, secretion, functional role, and taxonomic importance. Int J Pl Sci 176:72–85. https://doi.org/10.1086/679016
Cutter E (2002) Anatomia vegetal: parte I: células e tecidos. Roca, São Paulo
Davis AR, Gunning BES (1992) The modified stomata of the floral nectary of Vicia faba L. 1. Development, anatomy and ultrastructure. Protoplasma 166:134–152
Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, Oxford
De Lima HC, Studart AM, Vaz F (1984) Revisão Taxonômica do gênero Riedeliella Harms. Rodriguésia 36:9–16. https://doi.org/10.1590/2175-78601984365802
De Vargas W, Sartori AL, Dias ES (2015) Novelties in secretory structures and anatomy of Rhynchosia (Leguminosae). Anais Acad Brasil Civil 87:83–87. https://doi.org/10.1590/0001-3765201520130373
De Vargas W, Fortuna-Perez AP, Lewis GP, Piva TC, Vatanparast M, Machado SR (2019) Ultrastructure and secretion of glandular trichomes in species of subtribe Cajaninae Benth (Leguminosae, Phaseoleae). Protoplasma 256:431–445. https://doi.org/10.1007/s00709-018-1307-0
Endress PK (1996) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge
Erickson EH, Garment MB (1979) Soya-bean flowers: nectary ultrastructure, nectar guides, and orientation on the flower by foraging honeybees. J Apic Res 18:3–11. https://doi.org/10.1080/00218839.1979.11099935
Esau K (1960) Anatomy of seed plants. Wiley, New York
Evert RF (2006) Esau’s plant anatomy: Meristems, cells and tissues of the plant body—their structure, function and development, 3rd edn. Wiley, Hoboken
Fahn A (1979) Secretory tissues in plants. Academic Press, New York
Feng X, Zhao Z, Tian Z, Xu S, Luo Y, Cai Z, Wang Y, Yang J, Wang Z, Weng L, Chen J, Zheng L, Guo X, Luo J, Sato S, Tabata S, Ma W, Cao X, Hu X, Sun C, Luo D (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci USA 103:4970–4975. https://doi.org/10.1073/pnas.0600681103
Gerlach D (1969) A rapid safranin-crystal violet-light green staining sequence for paraffin sections of plant materials. Stain Technol 44:210–211
Gregory M, Baas P (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Israel J Bot 38:125–174. https://doi.org/10.1080/0021213X.1989.10677119
Haslam E (2007) Vegetable tannins–Lessons of a phytochemical lifetime. Phytochemistry 68:2713–2721. https://doi.org/10.1016/j.phytochem.2007.09.009
Horner HT, Healy RA, Cervantes-Martinez T, Palmer RG (2003) Floral nectary fine structure and development in Glycine max L. (Leguminosae). Int J Pl Sci 164:675–690. https://doi.org/10.1086/377060
Huchelmann A, Boutry M, Hachez C (2017) Plant glandular trichomes: natural cell factories of high biotechnological interest. Pl Physiol 175:6–22. https://doi.org/10.1104/pp.17.00727
Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253. https://doi.org/10.2307/1936841
Jensen WA (1962) Botanical histochemistry: principles and practice. Freeman, San Francisco
Johansen D (1940) Plant microtechnique, 3rd ed. Paul B. Hoeber, New York
Ireland HE (2005) Tribe Swartzieae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Royal Botanic Gardens, Kew, pp 215–225
Klitgaard BB (1999) Floral ontogeny in tribe Dalbergieae (Leguminosae : Papilionoideae): Dalbergia brasiliensis, Machaerium villosum s. I. Platymiscium floribundum, and Pterocarpus rotundifolius. Pl Syst Evol 219:1–25. https://doi.org/10.1007/BF01090296
Klitgaard BB, Lavin M (2005) Dalbergieae s.l. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Royal Botanic Gardens, Kew, pp 307–335
Klitgaard BB, Forest F, Booth TJ, Saslis-Lagoudakis CH (2013) A detailed investigation of the Pterocarpus clade (Leguminosae: Dalbergieae): Etaballia with radially symmetrical flowers is nested within the papilionoid-flowered Pterocarpus. S African J Bot 89:128–142. https://doi.org/10.1016/j.sajb.2013.07.006
Konarska A (2020) Microstructure of floral nectaries in Robinia viscosa var. hartwigii (Papilionoideae, Fabaceae)—a valuable but little-known melliferous plant. Protoplasma 257:421–437. https://doi.org/10.1007/s00709-019-01453-4
Lackey JA (1978) Leaflet anatomy of Phaseoleae (Leguminosae: Papilionoideae) and its relation to taxonomy. Bot Gaz 139:436–446. https://doi.org/10.1086/337019
Lackey JA (1981) Phaseoleae DC. (1825) In: Polhill RM, Raven PH (eds) Advances in legume systematics, part 1. Royal Botanic Gardens, Kew, pp 301–327
Lavin M, Pennington RT, Klitgaard BB, Sprent JI, De Lima HC, Gasson PE (2001) The dalbergioid legumes (Leguminosae): delimitation of a pantropical monophyletic clade. Amer J Bot 88:503–533. https://doi.org/10.2307/2657116
Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 54:575–594. https://doi.org/10.1080/10635150590947131
Leite VG, Mansano VF, Teixeira SP (2014) Floral ontogeny in Dipterygeae (Leguminosae) reveals new insights into one of the earliest branching tribes in papilionoid legumes. Bot J Linn Soc 174:529–550. https://doi.org/10.1111/boj.12158
Leite VG, Teixeira SP, Mansano VF, Prenner G (2015) Floral Development of the Early-Branching Papilionoid Legume Amburana cearensis (Leguminosae) Reveals Rare and Novel Characters. Int J Pl Sci 176:94–106. https://doi.org/10.1086/678468
Leite VG, Teixeira SP, Godoy F, Paulino JV, Mansano VF (2021) Resolving the non-papilionaceous flower of Camoensia scandens, a papilionoid legume of the core genistoid clade: development, glands and insights into the pollination and systematics of the group. J Plant Res 134:823–839. https://doi.org/10.1007/s10265-021-01293-5
Mair O (1977) Zur Entwicklungsgeschichte monosymmetrischer Dicotylen-Blüten
Mansano VF, Teixeira SP (2008) Floral anatomy of the Lecointea clade (Leguminosae, Papilionoideae, Swartzieae sensu lato). Pl Syst Evol 273:201–209. https://doi.org/10.1007/s00606-008-0018-y
Mansano VF, Tucker SC, Tozzi AMGA (2002) Floral ontogeny of Lecointea, Zollernia, Exostyles, and Harleyodendron (Leguminosae: Papilionoideae: Swartzieae s.l.). Amer J Bot 89:1553–1569. https://doi.org/10.3732/ajb.89.10.1553
Matthews ML, Endress PK (2006) Floral structure and systematics in four orders of rosids, including a broad survey of floral mucilage cells. Pl Syst Evol 260:199–221. https://doi.org/10.1007/s00606-006-0443-8
Mcmahon M, Hufford L (2005) Evolution and development in the Amorphoid clade (Amorpheae: Papilionoideae: Leguminosae): Petal loss and dedifferentiation. Int J Pl Sci 166:383–396. https://doi.org/10.1086/428633
Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons. Leaves, stem, and wood in relation to taxonomy with notes on economic uses, vol 1–2, 1st edn. Clarendon Press, Oxford
Meira RMSA, Martins FM (2003) Inclusão de material herborizado em metacrilato para estudos de anatomia vegetal. Rev Árv 27:109–112. https://doi.org/10.1590/S0100-67622003000100015
Moço MCM, Mariath JEA (2009) Comparative floral ontogeny in Adesmia (Leguminosae: Papilionoideae: Dalbergieae). Austral J Bot 57:65–75. https://doi.org/10.1071/BT07092
Movafeghi A, Dadpour MR, Naghiloo S, Farabi S, Omidi Y (2010) Floral development in Astragalus caspicus Bieb. (Leguminosae: Papilionoideae: Galegeae). Flora 205:251–258. https://doi.org/10.1016/j.flora.2009.04.001
Naghiloo S, Dadpour MR (2010) Floral ontogeny in Wisteria sinensis (Leguminosae: Papilionoideae: Millettieae) and its systematic implications. Austral Syst Bot 23:393–400. https://doi.org/10.1071/SB10027
Naghiloo S, Dadpour MR, Movafeghi A (2012) Floral ontogeny in Astragalus compactus (Leguminosae: Papilionoideae: Galegeae): variable occurrence of bracteoles and variable patterns of sepal initiation. Planta 235:793–805. https://doi.org/10.1007/s00425-011-1538-1
Nicolson SW, Nepi M, Pacini E (2007) Nectaries and nectar, vol 4. Springer, Dordrecht
O’Brien TP, McCully ME (1981) The study of plant structure. Principles and selected methods. Termacarphi Pty LTT, Melbourne
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373
Paulino JV, Mansano VF, Teixeira SP (2013a) Elucidating the unusual floral features of Swartzia dipetala (Leguminosae). Bot J Linn Soc 173:303–320. https://doi.org/10.1111/boj.12089
Paulino JV, Prenner G, Mansano VF, Teixeira SP (2013b) Comparative development of rare cases of a polycarpellate gynoecium in an otherwise monocarpellate family, Leguminosae. Amer J Bot 101:572–586. https://doi.org/10.3732/ajb.1300355
Pennington RT, Klitgaard BB, Ireland H, Lavin M (2000) New insights into floral evolution of basal Papilionoideae from molecular phylogenies. In: Herendeen PS, Bruneau A (eds) Advances in legume systematics, part 9. Royal Botanic Gardens, Kew, pp 233–248
Polhill RM (1981a) Dalbergieae Bronn ex DC. (1825). In: Polhill RM, Raven PH (eds) Advances in legume systematics. Royal Botanic Gardens, Kew, pp 233–342
Polhill RM (1981b) Advances in legume systematics, parts 1 & 2. Royal Botanic Gardens, Kew
Polhill RM (1994) Classification of the Leguminosae. In: Bisby FA, Buckingham J, Harborne JB (eds) Phytochemical dictionary of the Leguminosae, vol. 1, plants and their constituents. Chapman and Hall, London, pp xxv–xlvii
Prenner G (2003) A developmental analysis of the inflorescence and the flower of Lotus corniculatus (Leguminosae-Loteae). Mitt Naturwiss Vereines Steiermark 133:99–107
Prenner G (2004a) New aspects in floral development of Papilionoideae: Initiated but suppressed bracteoles and variable initiation of sepals. Ann Bot (Oxford) 93:537–545. https://doi.org/10.1093/aob/mch076
Prenner G (2004b) Floral ontogeny in Lespedeza thunbergii (Leguminosae: Papilionoideae: Desmodieae): variations from the unidirectional mode of organ formation. J Pl Res 117:297–302. https://doi.org/10.1007/s10265-004-0158-2
Prenner G (2004c) The asymmetric androecium in Papilionoideae (Leguminosae): definition, occurrence, and possible systematic value. Int J Pl Sci 165:499–510. https://doi.org/10.1086/386377
Prenner G (2013) Flower development in Abrus precatorius (Leguminosae: Papilionoideae: Abreae) and a review of androecial characters in Papilionoideae. S African J Bot 89:210–218. https://doi.org/10.1016/j.sajb.2013.06.008
Prenner G, Bateman RM, Rudall PJ (2010) Floral formulae updated for routine inclusion in formal taxonomic descriptions. Taxon 59:241–250. https://doi.org/10.1002/tax.591022
Prenner G, Cardoso D, Zartman CE, Queiroz LP (2015) Flowers of the early-branching papilionoid legume Petaladenium urceoliferum display unique morphological and ontogenetic features. Amer J Bot 102:1780–1793. https://doi.org/10.3732/ajb.1500348
Rodriguez-Riano T, Ortega-Olivencia A, Devesa JA (1999) Types of androecium in the Leguminosae of SW Europe. Ann Bot (Oxford) 83:109–116. https://doi.org/10.1006/anbo.1998.0808
Rodrigues RS, de Azevedo Tozzi AMG (2006) Guianodendron, a new genus of Leguminosae (Papilionoideae) from South America. Novon 16:129–132. https://doi.org/10.3417/1055-3177(2006)16[129:GANGOL]2.0.CO;2
Rodrigues RS, de Azevedo Tozzi AMG (2012) Revisão taxonômica de Leptolobium (Papilionoideae, Leguminosae). Acta Bot Brasil 26:146–164. https://doi.org/10.1590/S0102-33062012000100016
Sampaio DS, de Chiara Moço MC, Mariath JEA (2013) Floral ontogeny of Aeschynomene falcata and A. sensitiva (Leguminosae: Papilionoideae) supports molecular phylogenetic data. Pl Syst Evol 299:499–513. https://doi.org/10.1007/s00606-012-0739-9
Sartori ÂLB, Neves IM, Seleme EP, Mansano VF (2017) A taxonomic revision of the south american genus Discolobium (Leguminosae, Papilionoideae). Phytotaxa 308:1–19. https://doi.org/10.11646/phytotaxa.308.1.1
Schirire BD (2005) Tribe Abreae. In: Lewis G, Schrire B, Mackinder B, Lock M (eds) Legumes of the world. Royal Botanic Gardens, Kew, pp 388–391
Sinjushin AA (2018) Floral ontogeny in Cordyla pinnata (A. rich.) Milne-Redh. (Leguminosae, Papilionoideae): away from stability. Flora 241:8–15. https://doi.org/10.1016/j.flora.2018.02.005
Solereder H (1908) Systematic anatomy of the dicotyledons, 2 vols. Clarendon Press, Oxford
Spears EE (1983) A direct measure of pollinator effectiveness. Oecologia 57:196–199
Stpiczyńska M (1995) The structure of floral nectaries of some species of Vicia L. (Papilionaceae). Acta Soc Bot Poloniae 64:327–334. https://doi.org/10.5586/asbp.1995.042
Teixeira SP, Ranga NT, Tucker SC (2009) Inflorescence and floral development of Dahlstedtia species (Leguminosae: Papilionoideae: Millettieae). Flora 204:769–781. https://doi.org/10.1016/j.flora.2008.10.006
Thomas V (1991) Structural, functional and phylogenetic aspects of the colleter. Ann Bot (Oxford) 68:287–305. https://doi.org/10.1093/oxfordjournals.aob.a088256
Tucker SC (1984) Unidirectional organ initiation in leguminous flowers. Amer J Bot 71:1139–1148. https://doi.org/10.1002/j.1537-2197.1984.tb11967.x
Tucker SC (1987) Floral initiation and development in legumes. In: Stirton CH (ed) Advances in legume systematics, part 3. Royal Botanic Gardens, Kew, pp 183–239
Tucker SC (1990) Loss of floral organs in Ateleia (Leguminosae: Papilionoideae: Sophoreae). Amer J Bot 77:750–761. https://doi.org/10.1002/j.1537-2197.1990.tb14465.x
Tucker SC (1993) Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae). I. Myroxylon (Myroxylon Group) and Castanospermum (Angylocalyx Group). Amer J Bot 80:65–75. https://doi.org/10.1002/j.1537-2197.1993.tb13768.x
Tucker SC (1994) Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae): II. Sophora Sensu Lato (Sophora Group). Amer J Bot 81:1576–1581. https://doi.org/10.1002/j.1537-2197.1994.tb15456.x
Tucker SC (1997) Floral evolution, development, and convergence: the hierarchical-significance hypothesis. Int J Pl Sci 158:143–161. https://doi.org/10.1086/297514
Tucker SC (2002) Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae). III. Radial symmetry and random petal aestivation in Cadia purpurea. Amer J Bot 89:748–757. https://doi.org/10.3732/ajb.89.5.748
Tucker SC (2003a) Floral development in legumes. Pl Physiol 131:911–926. https://doi.org/10.1104/pp.102.017459
Tucker SC (2003b) Floral ontogeny in Swartzia (Leguminosae: Papilionoideae: Swartzieae): distribution and role of the ring meristem. Amer J Bot 90:1271–1292. https://doi.org/10.3732/ajb.90.9.1271
Tucker SC (2006) Floral ontogeny of Hardenbergia violacea (Leguminosae: Papilionoideae: Phaseoleae) and taxa of tribes Bossiaeeae and Mirbelieae, with emphasis on presence of pseudoraceme inflorescences. Austral Syst Bot 19:193–210. https://doi.org/10.1071/SB05004
Vidal CB (1970) Dichroism in collagen bundles stained with Xylidine-Ponceau 2R. Ann Histochim 15:289–296
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The authors would like to thank the Brazilian agency Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 for financing, in part, this study and for a scholarship to JPSPB, the Fundação Universidade Federal de Mato Grosso do Sul—UFMS for logistic support, the Laboratório Multiusuário de Análises de Materiais (MULTILAM), Physics Institute, UFMS, and the Laboratório de Microscopia Eletrônica Aplicada à Pesquisa Agropecuária (NAP/MEPA), Escola Superior de Agricultura “Luiz de Queiroz”/Universidade de São Paulo—ESALQ/USP for supervision and assistance with the use of the scanning electron microscope.
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Bento, J.P.S.P., Kochanovski, F.J. & Sartori, Â.L.B. Floral ontogeny and secretory structures of Discolobium pulchellum and Riedeliella graciliflora (Leguminosae: Papilionoideae: Dalbergieae): two closely related genera with diverging floral morphology. Plant Syst Evol 307, 67 (2021). https://doi.org/10.1007/s00606-021-01791-y
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DOI: https://doi.org/10.1007/s00606-021-01791-y