Skip to main content
SpringerLink
Log in

Evolutionary History of the Leguminous Flower

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

The contemporary evolutionary developmental biology includes molecular phylogeny, studies on morphology and morphogenesis, genetics, and genomics. The most reliable conclusions about main trends of floral evolution can result from investigations of highly polymorphic group, which is precisely characterized from the positions of both modern systematics and molecular developmental biology. The legume family, Leguminosae, is a group of such kind. It demonstrates an outstanding variation in flower structure. The ancestral floral structure in this family includes monosymmetry, pentacycly, pentamerous perianth and androecium, and a monomerous gynoecium. However, distinct evolutionary lineages resulted in origin of polysymmetric perianth, different patterns of staminal reduction or polymerization, as well as multicarpellate gynoecium. A strikingly high level of homoplasy is found in Leguminosae. Besides the existing evolutionary tendency to stabilize floral structure, the exact “instability syndrome” evolved repeatedly, associated with a polysymmetry and characterized with a highly variable number and position of floral organs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.

Similar content being viewed by others

Notes

  1. Interestingly, the adaxial stamen of inner whorl is reduced most often in Leguminosae, while the opposed adaxial petal is reduced least often.

  2. The inflorescences of Apuleia are interpreted as cymose (Falcão et al., 2020), but their terminal flowers have clearly zygomorphic position of stamens, thus casting doubts on the existing interpretation. Terminal flowers in Ceratonia most probably emerge via fusion of several meristems of uppermost lateral flowers (Tucker, 1992).

REFERENCES

  1. Azani, N., Babineau, M., Donovan Bailey, C., Banks, H., Barbosa, A.R., Barbosa, P.R., Boatwright, J.S., Borges, L.M., Brown, G.K., Bruneau, A., and Legume Phylogeny Working Group, A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny, Taxon, 2017, vol. 66, pp. 44–77.

    Article  Google Scholar 

  2. Bauchet, G.J., Bett, K.E., Cameron, C.T., et al., The future of legume genetic data resources: challenges, opportunities, and priorities, Legume Sci., 2019, vol. 1, p. e16.

    Article  Google Scholar 

  3. Bello, M.A., Rudall, P.J., and Hawkins, J.A., Combined phylogenetic analyses reveal interfamiliar relationships and patterns of floral evolution in the eudicot order Fabales, Cladistics, 2012, vol. 28, pp. 393–421.

    Article  PubMed  Google Scholar 

  4. Bernardello, G., A systematic survey of floral nectaries, in Nectaries and Nectar, Nicolson, S.W., Nepi, M., and Pacini E., Eds., Dordrecht: Springer-Verlag, 2007, pp. 19–128.

    Google Scholar 

  5. Bowman, J.L., Brüggemann, H., Lee, J.Y., and Mummenhoff, K., Evolutionary changes in floral structure within Lepidium L. (Brassicaceae), Int. J. Plant Sci., 1999, vol. 160, pp. 917–929.

    Article  CAS  PubMed  Google Scholar 

  6. Bukhari, G., Zhang, J., Stevens, P.F., and Zhang, W., Evolution of the process underlying floral zygomorphy development in pentapetalous angiosperms, Am. J. Bot., 2017, vol. 104, pp. 1846–1856.

    Article  PubMed  Google Scholar 

  7. Cardoso, D., De Lima, H.C., Rodrigues, R.S., et al., 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, 2012a, vol. 61, pp. 1057–1073.

    Article  Google Scholar 

  8. Cardoso, D., De Queiroz, L.P., Pennington, R.T., et al., Revisiting the phylogeny of papilionoid legumes: new insights from comprehensively sampled early-branching lineages, Am. J. Bot., 2012b, vol. 99, pp. 1991–2013.

    Article  PubMed  Google Scholar 

  9. Cardoso, D., São-Mateus, M.B., Cruz, D.T., et al., Filling in the gaps of the papilionoid legume phylogeny. The enigmatic Amazonian genus Petaladenium is a new branch of the early-diverging Amburaneae clade, Mol. Phylogenet. Evol., 2015, vol. 84, pp. 112–124.

    Article  PubMed  Google Scholar 

  10. Choob, V.V. and Sinyushin, A.A., Flower and shoot fasciation: from phenomenology to the construction of models of apical meristem transformations, Russ. J. Plant Physiol., 2012, vol. 59, no. 4, pp. 530–545.

    Article  CAS  Google Scholar 

  11. Chub, V.V., Rol’ pozitsionnoi informatsii v regulyatsii razvitiya organov tsvetka i listovykh serii pobegov (The Role of Positional Information in the Regulation of the Development of Flower Organs and Leaf Series of Shoots), Moscow: BINOM. Laboratoriya Znanii, 2010.

  12. Citerne, H.L., Luo, D., Pennington, R.T., et al., A phylogenomic investigation of CYCLOIDEA-like TCP genes in the Leguminosae, Plant Physiol., 2003, vol. 131, pp. 1042–1053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Citerne, H.L., Pennington, R.T., and Cronk, Q.C.B., An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, pp. 12017–12020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Clark, R.P., Mackinder, B.A., and Banks, H., Cheniella gen. nov. (Leguminosae: Cercidoideae) from Southern China, Indochina and Malaysia, Eur. J. Taxon., 2017, vol. 360, pp. 1–37.

    Google Scholar 

  15. Clark, S.E., Running, M.P., and Meyerowitz, E.M., CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1, Development, 1995, vol. 121, pp. 2057–2067.

    Article  CAS  Google Scholar 

  16. De Barros, T.C., Pedersoli, G.D., Paulino, J.V., and Teixeira, S.P., In the interface of caesalpinioids and mimosoids: comparative floral development elucidates shared characters in Dimorphandra mollis and Pentaclethra macroloba (Leguminosae), Am. J. Bot., 2017, vol. 104, pp. 218–232.

    Article  CAS  PubMed  Google Scholar 

  17. Derstine, K.S. and Tucker, S.C., Organ initiation and development of inflorescences and flower of Acacia baileyana, Am. J. Bot., 1991, vol. 78, pp. 816–832.

    Article  Google Scholar 

  18. Endress, P.K., Chaotic floral phyllotaxis and reduced perianth in Achlys (Berberidaceae), Bot. Acta, 1989, vol. 102, pp. 159–163.

    Article  Google Scholar 

  19. Endress, P.K., The immense diversity of floral monosymmetry and asymmetry across angiosperms, Bot. Rev., 2012, vol. 78, pp. 345–397.

    Article  Google Scholar 

  20. Falcão, M.J.A., Paulino, J.V., Kochanovski, F.J., et al., Development of inflorescences and flowers in Fabaceae subfamily Dialioideae: an evolutionary overview and complete ontogenetic series for Apuleia and Martiodendron, Bot. J. Linn. Soc., 2020, vol. 193, pp. 19–46.

    Article  Google Scholar 

  21. Feng, X., Zhao, Z., Tian, Z., et al., Control of petal shape and floral zygomorphy in Lotus japonicus, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, pp. 4970–4975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fougère-Danezan, M., Herendeen, P.S., Maumont, S., and Bruneau, A., Morphological evolution in the variable resin-producing Detarieae (Fabaceae): do morphological characters retain a phylogenetic signal? Ann. Bot., 2010, vol. 105, pp. 311–325.

    Article  PubMed  CAS  Google Scholar 

  23. Gómez-Acevedo, S.L., Magallón, S., and Rico-Arce, L., Floral development in three species of Acacia (Leguminosae, Mimosoideae), Aust. J. Bot., 2007, vol. 55, pp. 30–41.

    Article  Google Scholar 

  24. Hagemann, W. and Gleissberg, S., Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms, Plant Syst. Evol., 1996, vol. 199, pp. 121–152.

    Article  Google Scholar 

  25. Harlan, J.R., Crops and Man, Madison, WI: Am. Soc. Agron., 1992.

    Book  Google Scholar 

  26. He, L., Lei, Y., Li, X., et al., SYMMETRIC PETALS 1 encodes an ALOG domain protein that controls floral organ internal asymmetry in pea (Pisum sativum L.), Int. J. Mol. Sci., 2020, vol. 21, p. 4060.

    Article  CAS  PubMed Central  Google Scholar 

  27. Hsu, H.C., Chen, C.Y., Lee, T.K., et al., Quantitative analysis of floral symmetry and tube dilation in an F2 cross of Sinningia speciosa, Sci. Hortic. (Amsterdam), 2015, vol. 188, pp. 71–77.

    Article  Google Scholar 

  28. Hsu, H.J., He, C.W., Kuo, W.S., et al., Genetic analysis of floral symmetry transitions in African violet suggests the involvement of trans-acting factor for CYCLOIDEA expression shifts, Front. Plant Sci., 2018, vol. 9, p. 1008.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kirkbride, J.H., Dupuya, a new genus of Malagasy legumes, Novon: J. Bot. Nomencl., 2005, vol. 15, pp. 305–314.

    Google Scholar 

  30. Klitgård, B., Forest, F., Booth, T.J., and Saslis-Lagoudakis, C.H., A detailed investigation of the Pterocarpus clade (Leguminosae: Dalbergieae): Etaballia with radially symmetrical flowers is nested within the papilionoid-flowered Pterocarpus, S. Afr. J. Bot., 2013, vol. 89, pp. 128–142.

    Article  Google Scholar 

  31. Krüger, H., Tiedt, L.R., and Wessels, D.C.J., Floral development in the legume tree Colophospermum mopane, Caesalpinioideae: Detarieae, Bot. J. Linn. Soc., 1999, vol. 131, pp. 223–233.

    Article  Google Scholar 

  32. Leite, V.G., Teixeira, S.P., Mansano, V.F., and Prenner, G., Floral development of the early-branching papilionoid legume Amburana cearensis (Leguminosae) reveals rare and novel characters, Int. J. Plant Sci., 2015, vol. 176, pp. 94–106.

    Article  Google Scholar 

  33. Liu, Z., Ma, L., Nan, Z., and Wang, Y., Comparative transcriptional profiling provides insights into the evolution and development of the zygomorphic flower of Vicia sativa (Papilionoideae), PLoS One, 2013, vol. 8, p. e57338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Luo, D., Carpenter, R., Copsey, L., et al., Control of organ asymmetry in flowers of Antirrhinum, Cell, 1999, vol. 99, pp. 367–376.

    Article  CAS  PubMed  Google Scholar 

  35. Luo, Z., Hu, J., Zhao, Z., and Zhang, D., Transcriptomic analysis of heteromorphic stamens in Cassia biscapsularis L., Sci. Rep., 2016, vol. 6, p. 31600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. McMahon, M. and Hufford, L., Developmental morphology and structural homology of corolla-androecium synorganization in the tribe Amorpheae (Fabaceae: Papilionoideae), Am. J. Bot., 2002, vol. 89, pp. 1884–1898.

    Article  PubMed  Google Scholar 

  37. McMahon, M. and Hufford, L., Evolution and development in the amorphoid clade (Amorpheae: Papilionoideae: Leguminosae): petal loss and dedifferentiation, Int. J. Plant Sci., 2005, vol. 166, pp. 383–396.

    Article  Google Scholar 

  38. Marazzi, B., Conti, E., and Endress, P.K., Diversity in anthers and stigmas in the buzz-pollinated genus Senna (Leguminosae, Cassiinae), Int. J. Plant Sci., 2007, vol. 168, pp. 371–391.

    Article  Google Scholar 

  39. Martín-Trillo, M. and Cubas, P., TCP genes: a family snapshot ten year later, Trends Plant Sci., 2010, vol. 15, pp. 31–39.

    Article  PubMed  CAS  Google Scholar 

  40. Movafeghi, A., Naghiloo, S., and Dadpour, M.R., Inflorescence and floral development in Astragalus lagopoides Lam. (Leguminosae: Papilionoideae: Galegeae), Flora, 2011, vol. 206, pp. 219–226.

    Article  Google Scholar 

  41. Naghiloo, S., Dadpour, M.R., and Movafeghi, A., Floral ontogeny in Astragalus compactus (Leguminosae: Papilionoideae: Galegeae): variable occurrence of bracteoles and variable patterns of sepal initiation, Planta, 2012, vol. 235, pp. 793–805.

    Article  CAS  PubMed  Google Scholar 

  42. Ojeda, D.I., Jaén-Molina, R., Santos-Guerra, A., et al., Temporal, but not spatial, changes in expression patterns of petal identity genes are associated with loss of papillate conical cells and the shift to bird pollination in Macaronesian Lotus (Leguminosae), Plant Biol., 2017, vol. 19, pp. 420–427.

    Article  CAS  PubMed  Google Scholar 

  43. Ojeda, D.I., Koenen, E., Cervantes, S., et al., Phylogenomic analyses reveal an exceptionally high number of evolutionary shifts in a florally diverse clade of African legumes, Mol. Phylogenet. Evol., 2019, vol. 137, pp. 156–167.

    Article  PubMed  Google Scholar 

  44. Paulino, J.V., Mansano, V.F., and Teixeira, S.P., Elucidating the unusual floral features of Swartzia dipetala (Fabaceae), Bot. J. Linn. Soc., 2013, vol. 173, pp. 303–320.

    Article  Google Scholar 

  45. Paulino, J.V., Prenner, G., Mansano, V.F., and Teixeira, S.P., Comparative development of rare cases of a polycarpellate gynoecium in an otherwise monocarpellate family, Leguminosae, Am. J. Bot., 2014, vol. 101, pp. 572–586.

    Article  PubMed  Google Scholar 

  46. Paulino, J.V., Mansano, V.F., and Prenner, G., Evidence for division of labor and division of function related to the pollen release in Papilionoideae (Leguminosae) with a heteromorphic androecium, Int. J. Plant Sci., 2016, vol. 177, pp. 590–607.

    Article  Google Scholar 

  47. Paulino, J.V., Mansano, V.F., Prenner, G., and Teixeira, S.P., High developmental lability in the perianth of Inga (Fabales, Fabaceae): a neotropical woody rosid with gamopetalous corolla, Bot. J. Linn. Soc., 2017, vol. 183, pp. 146–161.

    Google Scholar 

  48. Pedersoli, G.D., Paulino, J.V., Leite, V.G., and Teixeira, S.P., Elucidating enigmatic floral tissues in Copaifera langsdorffi Desf. (Leguminosae, Caesalpinioideae), Int. J. Plant Sci., 2010, vol. 171, pp. 834–846.

    Article  Google Scholar 

  49. Pennington, R.T., Klitgaard, B.B., Ireland, H., and Lavin, M., New insights into floral evolution of basal Papilionoideae from molecular phylogenies, in Advances in Legume Systematics, Herendeen, P.S., Brungau, A., and Pollard, P.S., Eds., L., Kew: R. Bot. Gardens, 2000, part 9, pp. 233–248.

  50. Povydysh, M.N., Goncharov, M.Yu., and Yakovlev, G.P., Morphological features of flowers in “basal” Papilionoideae and their taxonomic significance, Bot. Zh., 2014, vol. 99, pp. 377–383.

    Article  Google Scholar 

  51. Prenner, G., Floral ontogeny of Acacia celastrifolia: an enigmatic mimosoid legume with pronounced polyandry and multiple carpels, in Flowers on the Tree of Life, Wanntorp, L. and Ronse Decraene, L.P., Eds., Cambridge: Cambridge Univ. Press, 2011, pp. 256–278.

    Google Scholar 

  52. Prenner, G., Flower development in Abrus precatorius (Leguminosae: Papilionoideae: Abreae) and a review of androecial characters in Papilionoideae, S. Afr. J. Bot., 2013, vol. 89, pp. 210–218.

    Article  Google Scholar 

  53. Prenner, G. and Klitgaard, B.B., Towards unlocking the deep nodes of Leguminosae: floral development and morphology of the enigmatic Duparquetia orchidacea (Leguminosae, Caesalpinioideae), Am. J. Bot., 2008, vol. 95, pp. 1349–1365.

    Article  PubMed  Google Scholar 

  54. Preston, J.C. and Hileman, L.C., Developmental genetics of floral symmetry evolution, Trends Plant Sci., 2009, vol. 14, pp. 147–154.

    Article  CAS  PubMed  Google Scholar 

  55. Remizowa, M.V., One upward, two steps down: order of floral organ initiation, Russ. J. Dev. Biol., 2019, vol. 50, no. 6, pp. 325–340.

    Article  Google Scholar 

  56. Remizowa, M.V., Sokoloff, D.D., Calvo, S., et al., Flowers and inflorescences of the seagrass Posidonia (Posidoniaceae, Alismatales), Am. J. Bot., 2012, vol. 99, pp. 1592–1608.

    Article  PubMed  Google Scholar 

  57. Ronse Decraene, L.P. and Smets, E.F., Dédoublement revisited: towards a renewed interpretation of the androecium of the Magnoliophytina, Bot. J. Linn. Soc., 1993, vol. 113, pp. 103–124.

    Article  Google Scholar 

  58. Schmitz, F., Die Blüthen-Entwicklung der Piperaceen, in Botanische Abhandlungen aus dem Gebiet der Morphologie und Physiologie, Hanstein, J., Ed., Bonn: Adolph Marcus Verlag, 1872, vol. 2, p. 86.

    Google Scholar 

  59. Simon, M.F., Grether, R., De Queiroz, L.P., et al., The evolutionary history of Mimosa (Leguminosae): toward a phylogeny of the sensitive plants, Am. J. Bot., 2011, vol. 98, pp. 1201–1221.

    Article  PubMed  Google Scholar 

  60. Sinjushin, A.A., Origin and variation of polymerous gynoecia in Fabaceae: evidence from floral mutants of pea (Pisum sativum L.), Plant Syst. Evol., 2014, vol. 300, pp. 717–727.

    Article  Google Scholar 

  61. Sinjushin, A.A., Is the leguminous flower closed? Wulfenia, 2015, vol. 22, pp. 281–287.

    Google Scholar 

  62. Sinjushin, A.A., Effects of stem fasciation on inflorescence and flower morphology in legumes, Wulfenia, 2016, vol. 23, pp. 127–134.

    Google Scholar 

  63. Sinjushin, A.A., Floral ontogeny in Cordyla pinnata (A. Rich.) Milne-Redh. (Leguminosae, Papilionoideae): away from stability, Flora, 2018, vol. 241, pp. 8–15.

    Article  Google Scholar 

  64. Sinjushin, A.A., Notes on floral symmetry in the Pterocarpus clade (Leguminosae: Papilionoideae: Dalbergieae), Wulfenia, 2019, vol. 26, pp. 175–188.

    Google Scholar 

  65. Sinjushin, A.A. and Karasyova, T.A., Stability of the floral structure in Leguminosae with flag versus non-flag blossom, Wulfenia, 2017, vol. 24, pp. 1–10.

    Google Scholar 

  66. Sinjushin, A.A., Bagheri, A., Maassoumi, A.A., and Rahiminejad, M.R., Terata of two legume species with radialized corolla: come correlations in floral symmetry, Plant Syst. Evol., 2015, vol. 301, pp. 2387–2397.

    Article  Google Scholar 

  67. Sinjushin, A.A., Tekdal, D., Ciftci, C., and Cetiner, S., Floral development in Thermopsis turcica, an unusual multicarpellate papilionoid legume, Plant Syst. Evol., 2018, vol. 304, pp. 461–471.

    Article  Google Scholar 

  68. Sinjushin, A.A., Bykova, E.A., and Choob, V.V., Interaction between floral merism and symmetry: evidence from fasciated mutant of Lupinus angustifolius L. (Leguminosae), Symmetry, 2019, vol. 11, p. 321.

    Article  CAS  Google Scholar 

  69. Sokoloff, D.D., Degtjareva, G.V., Endress, P.K., et al., Inflorescence and early flower development in Loteae (Leguminosae) in a phylogenetic and taxonomic context, Int. J. Plant Sci., 2007, vol. 168, pp. 801–833.

    Article  Google Scholar 

  70. Sokolov, D.D., The structure of androecium in Anthyllis vulneraria L. (Papilionaceae, Loteae), Vestn. Mosk. Univ., Ser. 16: Biol., 1995, no. 4, pp. 51–54.

  71. Tasaki, K., Nakatsuka, A., Cheon, K.-S., et al., Morphological and expression analyses of MADS genes in Japanese traditional narrow- and/or staminoid-petaled cultivars of Rhododendron kaempferi Planch., Sci. Hort. (Amsterdam), 2012, vol. 134, pp. 191–199.

    Article  CAS  Google Scholar 

  72. Taubert, P., Leguminosae, in Die Natürlichen Pflanzenfamilien, Engler, A., Ed., Leipzig: Verlag von Wilhelm Engelmann, 1894, pp. 147–153.

    Google Scholar 

  73. Tucker, S.C., Unidirectional organ initiation in leguminous flower, Am. J. Bot., 1984, vol. 71, pp. 1139–1148.

    Article  Google Scholar 

  74. Tucker, S.C., Heteromorphic flower development in Neptunia pubescens, a mimosoid legume, Am. J. Bot., 1988, vol. 75, pp. 205–224.

    Article  Google Scholar 

  75. Tucker, S.C., Evolutionary implications of floral ontogeny in legumes, in Advances in Legume Biology, Stirton, C.H. and Zarucchi, J.L., Eds., St. Louis: Missouri Bot. Garden, 1989a, pp. 59–75.

    Google Scholar 

  76. Tucker, S.C., Overlapping organ initiation and common primordia in flowers of Pisum sativum (Leguminosae: Papilionoideae), Am. J. Bot., 1989b, vol. 76, pp. 714–729.

    Article  Google Scholar 

  77. Tucker, S.C., Helical floral organogenesis in Gleditsia, a primitive caesalpinioid legume, Am. J. Bot., 1991, vol. 78, pp. 1130–1149.

    Article  Google Scholar 

  78. Tucker, S.C., The developmental basis for sexual expression in Ceratonia siliqua (Leguminosae: Caesalpinioideae: Cassieae), Am. J. Bot., 1992, vol. 79, pp. 318–327.

    Article  Google Scholar 

  79. Tucker, S.C., Floral development and homeosis in Saraca (Leguminosae: Caesalpinioideae: Detarieae), Int. J. Plant Sci., 2000, vol. 161, pp. 537–549.

    Article  Google Scholar 

  80. Tucker, S.C., The ontogenetic basis for missing petals in Crudia (Leguminosae: Caeslpinioideae: Detarieae), Int. J. Plant Sci., 2001, vol. 162, pp. 83–89.

    Article  Google Scholar 

  81. Tucker, S.C., Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). 1. Radially symmetrical taxa lacking organ suppression, Am. J. Bot., 2002a, vol. 89, pp. 875–887.

    Article  PubMed  Google Scholar 

  82. Tucker, S.C., Floral ontogeny of Cercis (Leguminosae: Caesalpinioideae: Cercideae): does it show convergence with papilionoids, Int. J. Plant Sci., 2002b, vol. 163, pp. 75–87.

    Article  Google Scholar 

  83. Tucker, S.C., Floral ontogeny in Swartzia (Leguminosae: Papilionoideae: Swartzieae): distribution and role of the ring meristem, Am. J. Bot., 2003a, vol. 90, pp. 1271–1292.

    Article  PubMed  Google Scholar 

  84. Tucker, S.C., Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). III. Adaxially initiated whorls in Julbernardia and Sindora, Int. J. Plant Sci., 2003b, vol. 164, pp. 275–286.

    Article  Google Scholar 

  85. Wang, Z., Luo, Y., Li, X., et al., Genetic control of floral zygomorphy in pea (Pisum sativum L.), Proc. Natl. Acad. Sci. U.S.A., 2008, vol. 105, pp. 10414–10419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Woollacott, C. and Cronk, Q.C.B., The hooded mutant of Lathyrus odoratus (Fabaceae) is associated with a cycloidea gene mutation, Botany, 2018, vol. 96, pp. 47–55.

    Article  CAS  Google Scholar 

  87. Yakovlev, G.P., Bobovye zemnogo shara (Fabaceae Plant of the World), Leningrad: Nauka, 1991.

  88. Yun, J.Y., Weigel, D., and Lee, I., Ectopic expression of SUPERMAN suppresses development of petals and stamens, Plant Cell Physiol., 2002, vol. 43, pp. 52–57.

    Article  CAS  PubMed  Google Scholar 

  89. Xu, S., Luo, Y., Cai, Z., et al., Functional diversity of CYCLOIDEA-like TCP genes in the control of zygomorphic flower development in Lotus japonicus, J. Integr. Plant Biol., 2013, vol. 55, pp. 221–231.

    Article  CAS  PubMed  Google Scholar 

  90. Zimmerman, E., Prenner, G., and Bruneau, A., Floral ontogeny in Dialiinae (Caesalpinioideae: Cassieae), a study in organ loss and instability, S. Afr. J. Bot., 2013, vol. 89, pp. 188–209.

    Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

Author expresses his gratitude to Prof. D.D. Sokoloff and Prof. V.V. Choob for helpful discussion of some points of this paper.

ADDITIONAL INFORMATION

The article is translated by the author.

Funding

The work was supported by the Russian Foundation for Basic Research (project no. 19-14-50618).

Author information

Authors and Affiliations

  1. Moscow State University, Moscow, Russia

    A. A. Sinjushin

Authors
  1. A. A. Sinjushin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Sinjushin.

Ethics declarations

Conflict of interests. The author declares that he has no conflict of interests.

Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by the author.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sinjushin, A.A. Evolutionary History of the Leguminous Flower. Biol Bull Rev 11, 400–413 (2021). https://doi.org/10.1134/S2079086421040083

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086421040083

Keywords:

Search

Navigation