Research Paper

Floral development in Biancaea decapetala and Albizia julibrissin (Fabaceae: Caesalpinioideae), and its systematic significance

Shabir A. Rather, Arjun Adit, Zhou Jing, Josphat K. Saina, Hongmei Liu, Zhaoyang Chang, Harald Schneider

Published on: 06 July 2023

Page: 281 - 293

DOI: 10.6165/tai.2023.68.281

Abstract

This study investigates the floral morphology and development of two legume species from the subfamily Caesalpinioideae, Biancaea decapetala (a caesalpinioid), and Albizia julibrissin (a mimosoid), using scanning electron microscopy. The floral organ initiation in A. julibrissin involved the helical orientation of sepals’ formation, simultaneous initiation of petals, and formation of the ring meristem in place of stamens. Whereas in B. decapetala, organ whorls grow unidirectionally, from abaxial to adaxial, a characteristic found in the subfamily Papilionoideae. However, the floral development sequence in B. decapetala differs from papilionaceous flowers, as it lacks petal specialization and features a fused staminal tube. While fused sepal tube, free stamens, and short style were observed in flowers of B. decapetala; fused petals, fused staminal tube, and long style occurred in flowers of A. julibrissin. The petal aestivation is valvate in A. julibrissin, compared to ascending cochleate in B. decapetala. The observations during the initiation and developmental stages of floral whorls are essential to unravel the functional specificity of appendages. A. julibrissin belongs to the Mimosoid clade, which was until recently placed outside the Caesalpinioideae subfamily (of which B. decapetala was always been a part of) due to its floral architecture. There has been significant number of discussions and deliberations in the botanical community about the placement of this clade in the subfamily. Understanding of floral development in the subfamily and comparison of caesalpinioids with mimosoids can be crucial in evaluating the phylogenetic placement of the mimosoid clade. While most changes in the developmental sequence may appear subtle and minute, these are imperative for the remarkable disparity in the floral morphology of legumes.

Keyword: Floral ontogeny, legumes, morphogenesis, primordia, scanning electron microscopy, unidirectional initiation

Literature Cited

Adit, A., Koul, M., Choudhary, A.K., Tandon, R. 2022 Interaction between Cymbidium aloifolium and Apis cerana: incidence of an outlier in modular pollination network of oil flowers. Ecol. Evol. 12(3): e8697.
DOI: 10.1002/ece3.8697View Article Google Scholar

Broome, R., Sabir, K., Carrington, S. 2007 Plants of the Eastern Caribbean. Online database. Barbados: University of the West Indies.http://ecflora.cavehill.uwi.edu/index.html. Accessed 25 Mar. 2023

Choo, L.M. 2021 Biancaea scabrida, a new species of the Caesalpinia group (Fabaceae) from Peninsular Malaysia. Phytotaxa 525(4):251–257
DOI: 10.11646/phytotaxa.525.4.1View Article Google Scholar

Classen-Bockhoff, R. 2000 Inflorescences in Bruniaceae: With general comments on inflorescences in woody plants. Opera Bot. Belgica 12: 5–310.

De Barros, T.C., Pedersoli, G.D., Paulino, J.V., Teixeira, S.D.P. 2017 In the interface of caesalpinioids and mimosoids: Comparative floral development elucidates shared characters in Dimorphandra mollis and Pentaclethra macroloba (Leguminosae). Am. J. Bot. 104(2): 218–232.
DOI: 10.3732/ajb.1600308View Article Google Scholar

De Craene, L.R. 2018 Understanding the role of floral development in the evolution of angiosperm flowers: clarifications from a historical and physicodynamic perspective. J. Plant Res. 131(3): 367–393.
DOI: 10.1007/s10265-018-1021-1View Article Google Scholar

de Queiroz, L.P., Lewis, G.P., Allkin, R. 1999 A revision of the genus Moldenhawera Schrad. (Leguminosae-Caesalpinioideae). Kew Bull. 54(4): 817–852.
DOI: 10.2307/4111163View Article Google Scholar

Derstine, K.S., Tucker, S.C. 1991 Organ initiation and development of inflorescences and flowers of Acacia baileyana. Am. J. Bot. 78(6): 816–832.
DOI: 10.1002/j.1537-2197.1991.tb14484.xView Article Google Scholar

Endress, P.K. 1994 Diversity and Evolutionary Biology of Tropical Flowers, Cambridge University Press, Cambridge, UK.

Endress, P.K. 2011 Angiosperm ovules: diversity, development, evolution. Ann. Bot. 107(9): 1465–1489.
DOI: 10.1093/aob/mcr120View Article Google Scholar

Falcao, M.J.A., Paulino, J.V., Kochanovski, F.J., Figueiredo, R.C., Basso-Alves, J.P., Mansano, V.F. 2020 Development of inflorescences and flowers in Fabaceae subfamily Dialioideae: an evolutionary overview and complete ontogenetic series for Apuleia and Martiodendron. Bot. J. of the Linn. 193(1): 19–46.
DOI: 10.1093/botlinnean/boz098View Article Google Scholar

Foerste, A.F. 1888 Notes on structures adapted to cross-fertilization. Int. J. Plant Sci. 13(6): 151–156.
DOI: 10.1086/326286View Article Google Scholar

Frank, A.B. 1876 Uber die Entwicklung einiger Bliiten, mit besonderer Berucksichtigung der Theorie der Interponirung. Jahrb Wiss Bot. 10: 204–243

Gagnon, E., Bruneau, A., Hughes, C.E., De Queiroz, L.P., Lewis, G.P. 2016 A new generic system for the pantropical Caesalpinia group (Leguminosae). PhytoKeys 71: 1–160.
DOI: 10.3897/phytokeys.71.9203View Article Google Scholar

Hartog, M.M. 1888 On the floral ontogeny and anatomy of Brownea and Saraca. Ann. Bot. 2: 309–331.
DOI: 10.1093/aob/os-2.3.309View Article Google Scholar

Hopkins, H.C.F. 1986 Parkia (Leguminosae: Mimosoideae). Flora Neotropica, 43. New York Botanical Garden, Bronx, New York, USA.

Huang, L.J., Fu, W.L., Wang, X.F. 2014 Floral Development at Multiple Spatial Scales in Polygonum jucundum (Polygonaceae), a Distylous Species with Broadly Open Flowers. PLoS ONE 9(7): e102802.
DOI: 10.1371/journal.pone.0102802View Article Google Scholar

ILDIS 2014 International Legume Database and Information Service. Reading, UK: School of Plant Sciences, University of Reading. http://www.ildis.org/. Accessed 25 March 2023

Johansen, D.A. 1940 Plant Microtechnique, McGraw-Hill Book Co, New York, USA.

Khodaverdi, M., Movafeghi, A., Dadpour, M.R., Naghiloo, S., Ranjbar, M., Prenner, G. 2014 Comparative study of floral development in Onobrychis melanotricha, Hedysarum varium and Alhagi persarum (Leguminosae: Papilionoideae: Hedysareae). Flora 209(1): 23–33.
DOI: 10.1016/j.flora.2013.11.004View Article Google Scholar

Klitgaard, B.B. 1999 Floral ontogeny in tribe Dalbergieae (Leguminosae: Papilionoideae): Dalbergia brasiliensis, Machaerium villosum s.l. Platymiscium floribundum, and Pterocarpus rotundifolius. Plant Syst. Evol. 219(1-2): 1–25.
DOI: 10.1007/BF01090296View Article Google Scholar

Lang, W. 1906 Zur Bliitenentwicklung der Labiaten, Verbenaceen und Plantaginaceen. Bibl. Bot. 64: 1–40.

Lewis, G.P., Rico Arce, L. 2005 Tribe Ingeae. In: Lewis. G. et al. (eds.), Legumes of the World, 577, Royal Botanic Gardens, Kew, UK.

Lewis, G.P., Schrire, B.D., Mackinder, B.A., Rico, L., Clark, R. 2013 A 2013 linear sequence of legume genera set in a phylogenetic context: A tool for collections management and taxon sampling. S. African J. Bot. 89: 76–84.
DOI: 10.1016/j.sajb.2013.06.005View Article Google Scholar

LPWG (Legume Phylogeny Working Group) 2013 Legume phylogeny and classification in the 21st century: Progress, prospects and lessons for other species-rich clades. Taxon 62(2): 217–248.LPWG (Legume Phylogeny Working Group) 2017 A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66(1): 44–77.
DOI: 10.12705/622.8View Article Google Scholar

LPWG (Legume Phylogeny Working Group) 2017 A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66(1): 44–77.
DOI: 10.12705/661.3View Article Google Scholar

Luo, Z.L., Gu, L., Zhang, D.X. 2009 Intrafloral differentiation of stamens in heterantherous flowers. J. Syst. Evol. 47(1): 43–56.
DOI: 10.1111/j.1759-6831.2009.00002.xView Article Google Scholar

Mair, O. 1977 Zur Entwicklungsgeschichte monosymmetrischer Dicotylen-Bluten. Diss. Bot. 38: 1–274.

Marazzi, B., Endress, P.K. 2008 Patterns and development of floral asymmetry in Senna (Leguminosae, Cassiinae). Am. J. Bot. 95(1): 22–40.
DOI: 10.3732/ajb.95.1.22View Article Google Scholar

Masoumeh, K., Reza, D.M., Somayeh, N., Ali, M. 2013 A study on the floral ontogeny in Caesalpinia gilliesii (Hook) Dietr and its comparision with other species of Caesalpinia. J. Tax. Biosyst. 15(5): 67–74.

Movafeghi, A., Dadpour, M.R., Naghiloo, S., Farabi, S., Omidi, Y. 2010 Floral development in Astragalus caspicus Bieb. (Leguminosae: Papilionoideae: Galegeae). Flora 205(4): 251–258.
DOI: 10.1016/j.flora.2009.04.001View Article Google Scholar

Movafeghi, A., Naghiloo, S., Dadpour, M.R. 2011 Inflorescence and floral development in Astragalus lagopoides Lam. (Leguminosae: Papilionoideae: Galegeae). Flora 206(3): 219–226.
DOI: 10.1016/j.flora.2010.04.023View Article Google Scholar

Naghiloo, S., Dadpour, M.R. 2010 Floral ontogeny in Wisteria sinensis (Fabaceae: Faboideae: Millettieae) and its systematic implications. Aust. Syst. Bot. 23(6): 393–400.
DOI: 10.1071/SB10027View Article Google Scholar

Naghiloo, S., Dadpour, M.R., Movafeghi, A. 2012 Floral ontogeny in Astragalus compactus (Leguminosae: Papilionoideae: Galegeae): variable occurrence of bracteoles and variable patterns of sepal initiation. Planta 235(4): 793–805.
DOI: 10.1007/s00425-011-1538-1View Article Google Scholar

Paulino, J.V., Prenner, G., Mansano, V.F., Teixeira, S.P. 2014 Comparative development of rare cases of a polycarpellate gynoecium in an otherwise monocarpellate family, Leguminosae. Am. J. Bot. 101(4): 1–15.
DOI: 10.3732/ajb.1300355View Article Google Scholar

Phukela, B., Adit, A., Tandon, R. 2020 A Snapshot of Evolutionary History of Floral Nectaries Across Angiosperm Lineages. In: Tandon R, Shivanna KR, Koul M (eds), Reproductive Ecology of Flowering Plants: Patterns and Processes. Springer, Singapore.
DOI: 10.1007/978-981-15-4210-7_6View Article Google Scholar

Pinto, R.B., Torke, B.M., Mansano, V.F. 2012 Updates to the taxonomy of Swartzia (Leguminosae) in extra-Amazonian Brazil, with descriptions of five new species and a regional key to the genus. Brittonia 64(2): 119–138.
DOI: 10.1007/s12228-011-9219-8View Article Google Scholar

Polhill, R.M., Raven, P.H., Stirto, C.H. 1981 Evolution and Systematics of the Leguminosae. In: Polhill, R.M., Raven, P.H. (eds.), Advances in Legume Systematics, Part I: 1-26. Royal Botanic Garden, Kew, UK.

Prenner, G. 2004a New aspects in floral development of Papilionoideae: initiated but suppressed bracteoles and variable initiation of sepals. Ann. Bot. 93(5): 537–545.
DOI: 10.1093/aob/mch076View Article Google Scholar

Prenner, G. 2004b The asymmetric androecium in Papilionoideae (Leguminosae): definition, occurrence, and possible systematic value. Int. J. Plant Sci. 165(4): 499–510.
DOI: 10.1086/386377View Article Google Scholar

Prenner, G. 2004c Floral ontogeny in Calliandra angustifolia (Leguminosae: Mimosoideae: Ingeae) and its systematic implications. Int. J. Plant Sci. 165(3): 417–426.
DOI: 10.1086/382804View Article Google Scholar

Prenner, G. 2004d Floral development in Daviesia cordata (Leguminosae: Papilionoideae: Mirbelieae) and its systematic implications. Aust. J. Bot. 52(3): 285–291.
DOI: 10.1071/BT03155View Article Google Scholar

Prenner, G. 2004e Floral ontogeny in Lespedeza thunbergii (Leguminosae: Papilionoideae: Desmodieae): variations from the unidirectional mode of organ formation. J. Plant Res. 117(4): 297–302.
DOI: 10.1007/s10265-004-0158-2View Article Google Scholar

Prenner, G. 2011 Floral ontogeny of Acacia celastrifolia: an enigmatic mimosoid legume with pronounced polyandry and multiple carpels. In: Wanntorp L, Ronse DeCraene LP (eds.). Flowers on the tree of life, 256–278, Cambridge University Press, London, UK.
DOI: 10.1017/CBO9781139013321.011View Article Google Scholar

Prenner, G. 2013 Floral development in Abrus precatorius (Leguminosae: Papilionoideae: Abreae) and a review of androecial characters in Papilionoideae. S. Afr. J. Bot. 89: 210–218.
DOI: 10.1016/j.sajb.2013.06.008View Article Google Scholar

Prenner, G., Cardoso, D. 2017 Flower development of Goniorrhachis marginata reveals new insights into the evolution of the florally diverse detarioid legumes. Ann. Bot. 119(3): 417–432.
DOI: 10.1093/aob/mcw223View Article Google Scholar

Prenner, G., Klitgaard, B.B. 2008 Towards unlocking the deep nodes of Leguminosae: floral development and morphology of the enigmatic Duparquetia orchidacea (Leguminosae, Caesalpinioideae). Am. J. Bot. 95(11): 1349–1365.
DOI: 10.3732/ajb.0800199View Article Google Scholar

Prenner, G., Cardoso, D., Zartman, C.E., Queiroz, L.P. 2015 Flowers of the early-branching papilionoid legume Petaladenium urceoliferum display unique morphological and ontogenetic features. Am. J. Bot. 102(11): 1780–1793.
DOI: 10.3732/ajb.1500348View Article Google Scholar

Ram?rez?Domenech, J.I., Tucker, S.C. 1990 Comparative ontogeny of the perianth in mimosoid legumes. Am. J. Bot. 77(5): 624–635.
DOI: 10.1002/j.1537-2197.1990.tb14448.xView Article Google Scholar

Rohrbach, P. 1870 Beitrage zur Morphologie der Leguminosen. Bot. Zeit. 28: 817–82

Rather, S.A., Wei, Y., Wang, J., Zhao, L., Chang, Z. 2021 Comparative study of floral developments and its systematic importance in the genus Astragalus L. and Oxytropis DC. (Fabaceae, Leguminosae: Papilionoideae). Biologia 76(3): 865–888.
DOI: 10.1007/s11756-021-00688-yView Article Google Scholar

Sattler, R. 1973 Organogenesis of Flowers: A Photographic Text-Atlas, University of Toronto Press, Toronto, Canada

Singh, V. 1979 Early floral development in Digitalis purpurea. Phytomorphology 29: 239–245.

Son, H.D., Im, H.T. 2015 Pollination biology of Caesalpinia decapetala (Leguminosae) in Korea. J. Sp. Res. 4(2): 145–151.
DOI: 10.12651/JSR.2015.4.2.145View Article Google Scholar

Stebbins, G.L. 1974 Flowering Plants. Belknap Press, Cambridge, UK.
DOI: 10.4159/harvard.9780674864856View Article

Stergios, B.D., Aymard, G.A.C. 2008 A Striking New Species of Aldina (Fabaceae-Swartzieae-Aldininae) from the Venezuelan Guayana Highlands. Harv. Pap. Bot. 13(1): 29–33.
DOI: 10.3100/1043-4534(2008)13[29:ASNSOA]2.0.CO;2View Article Google Scholar

Takeda, S., Iwasaki, A., Matsumoto, N., Uemura, T., Tatematsu, K., Okada, K. 2013 Physical Interaction of Floral Organs Controls Petal Morphogenesis in Arabidopsis. Plant Physiol. 161(3): 1242–1250.
DOI: 10.1104/pp.112.212084View Article Google Scholar

Thomson, B., Zheng, B., Wellmer, F. 2017 Floral Organogenesis: When Knowing Your ABCs Is Not Enough. Plant Physiol. 173(1): 56–64.
DOI: 10.1104/pp.16.01288View Article Google Scholar

Torke, B.M., Mansano, V.F. 2009 A phylogenetically based sectional classification of Swartzia (Leguminosae-Papilionoidea). Taxon 58(3): 913–924.
DOI: 10.1002/tax.583019View Article Google Scholar

Tucker, S.C. 1984 Unidirectional organ initiation in leguminous flowers. Am. J. Bot. 71(8): 1139–1148.
DOI: 10.2307/2443390View Article Google Scholar

Tucker, S.C. 1987 Floral initiation and development in legumes. In: Stirton, C.H. (ed), Advances in legume systematics, Part 3: 183-239. Royal Botanic Gardens, Kew, UK.

Tucker, S.C. 1988a Loss versus suppression of floral organs. In: Leins, P. et al. (eds.), Aspects of floral development, 69-82. J Cramer, Berlin, Germany.

Tucker, S.C. 1988b Heteromorphic flower development in Neptunia pubescens, a mimosoid legume. Am. J. Bot. 75(2): 205–224.
DOI: 10.2307/2443887View Article Google Scholar

Tucker, S.C. 1989 Overlapping organ initiation and common primordia in flowers of Pisum sativum (Leguminosae: Papilionoidea). Am. J. Bot. 76(5): 714–729.
DOI: 10.1002/j.1537-2197.1989.tb11366.xView Article Google Scholar

Tucker, S.C. 1990 Loss of floral organs in Ateleia (Leguminosae: Papilionoideae: Sophoreae). Am. J. Bot. 77(6): 750–761.
DOI: 10.2307/2444367View Article Google Scholar

Tucker, S.C. 1991 Helical floral organogenesis in Gleditsia, a primitive Caesalpinioid Legume. Am. J. Bot. 78(8): 1130–1149.
DOI: 10.2307/2444901View Article Google Scholar

Tucker, S.C. 1993 Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae). I. Myroxylon (Myroxylon group) and Castanospermum (Angylocalyx group). Am. J. Bot. 80(1): 65–75.
DOI: 10.2307/2445121View Article Google Scholar

Tucker, S.C. 1996 Trends in evolution of floral ontogeny in Cassia sensu stricto, Senna, and Chamaecrista (Leguminosae: Caesalpinioideae: Cassieae: Cassiineae): a study in convergence. Am. J. Bot. 83(6): 687–711.
DOI: 10.2307/2445846View Article Google Scholar

Tucker, S.C. 1997 Floral evolution, development, and convergence: the hierarchical-significance hypothesis. Int. J. Plant Sci. 158(S6): S143-S161.
DOI: 10.1086/297514View Article Google Scholar

Tucker, S.C. 1998 Floral ontogeny in legume genera Petalostylis, Labichea, and Dialium (Caesalpinioideae: Cassieae), a series in floral reduction. Am. J. Bot. 85(2): 184–208.
DOI: 10.2307/2446307View Article Google Scholar

Tucker, S.C. 2003 Floral development in legumes. Plant Physiol. 131(3): 911–926.
DOI: 10.1104/pp.102.017459View Article Google Scholar

Tucker, S.C., Douglas, A.W. 1994 Ontogenetic evidence and phylogenetic relationships among basal taxa of legumes. In: Ferguson, I.K., Tucker, S.C. (eds.), Advances in legume systematics, part 6: 11-32. Royal Botanic Gardens, Kew, UK.

Tucker, S.C., Kantz, K.E. 2001 Open carpels with ovules in Fabaceae. Int. J. Plant Sci. 162(5): 1065–1073.
DOI: 10.1086/321923View Article Google Scholar

Tucker, S.C., Stein, O.L., Derstine, K.S. 1985 Floral development in Caesalpinia (Leguminosae). Am. J. Bot. 72(9): 1424–1434.
DOI: 10.2307/2443515View Article Google Scholar

Venkatesh, C.S. 1951 The inflorescence and flowers of Dichrostachys cinerea, W & A. Proc. Indian Acad. Sci. 4: 183–187von Arx, M. 2013 Floral humidity and other indicators of energy rewards in pollination biology. Commun. Integr. Biol. 6(1): e22750.
DOI: 10.4161/cib.22750View Article Google Scholar

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. 95(7): 1199–1209.
DOI: 10.1093/aob/mci132View Article Google Scholar

Weber, E. 2003. Invasive plant species of the world: a reference guide to environmental weeds, CABI Publishing, Cambridge, UK

Wojciechowski, M.F., Lavin, M., Sanderson, M.J. 2004 A Phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well supported subclades within the family. Am. J. Bot. 91(11): 1846–1862.
DOI: 10.3732/ajb.91.11.1846View Article Google Scholar

Wyatt, R., Lipow, S.R. 2021 Reproductive biology of Mimosa microphylla and Albizia julibrissin (Fabaceae: Caesalpinioideae) with a new explanation for the evolution of polyads, restricted stigmas, and polycarpelly in the mimosoid clade. J. Torrey Bot. 148(2): 97–108.
DOI: 10.3159/TORREY-D-20-00042.1View Article Google Scholar

Yahara, T., Javadi, F., Onoda, Y., Queiroz, L.P., Faith, D., Prado, D.E., Akasaka, M., Kadoya, T., Ishihama, F., Davies, S., Slik, J.W.F., Yi, T., Ma, K., Bin, C., Darnaedi, D., Pennington, R.T., Tuda, M., Shimada, M., Ito, M., Egan, A.N., Buerki, S., Raes, N., Kajita, T., Vatanparast, M., Mimura, M., Tachida, H., Iwasa, Y., Smith, G.F., Victor, J.E., Nkonki, T. 2013 Global legume diversity assessment: Concepts, key indicators, and strategies. Taxon 62(2): 249–266.
DOI: 10.12705/622.12View Article Google Scholar

Young, D.J., Watson, L. 1970 The classification of dicotyledons: a study of the upper levels of the hierarchy. Aust. J. Bot. 18(3): 387–433.
DOI: 10.1071/BT9700387View Article Google Scholar