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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Flower development in species of Croton (Euphorbiaceae) and its implications for floral morphological diversity in the genus

Karina Bertechine Gagliardi A C , Inês Cordeiro B and Diego Demarco A
+ Author Affiliations
- Author Affiliations

A Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo – SP, Brazil.

B Centro de Pesquisa em Plantas Vasculares, Núcleo de Pesquisa Curadoria do Herbário, Instituto de Botânica, 04301-012, São Paulo – SP, Brazil.

C Corresponding author. Email: kabertechine3@usp.br

Australian Journal of Botany 65(7) 538-549 https://doi.org/10.1071/BT17045
Submitted: 18 March 2017  Accepted: 15 September 2017   Published: 2 October 2017

Abstract

The Euphorbiaceae are notable for floral diversity and evolutionary complexity. Croton is the second largest genus in the family and exhibits particular diversity in its flowers. The aim of this study was to investigate the floral ontogeny and structure of three Croton species with distinct morphologies, with a focus on testing the hypothesis that the filaments of female flowers, which have received different interpretations in the literature and are currently described as reduced petals, are staminodes and part of a vestigial androecium. With the ontogenetic study we can understand the origin of the organs and associate these with flower evolution in the genus. Flowers in several stages of development were analysed using light microscopy and scanning electron microscopy. In the early stage of development, the sepals are the first structures to be formed, although they do not continue to grow in female Croton fuscescens Spreng. flowers. Petals are absent in female flowers, with filamentous, petaloid structures, interpreted here as staminodes, alternating with the sepals in Croton lundianus (Didr.) Müll. Arg. In Croton sphaerogynus Baill., the staminodes are located between the nectary lobes. The stamens exhibit centripetal development in the flower bud stage, and the carpels are post-genitally connate, with differences in style branching. Besides the ontogenetic interpretation for the filamentous structures, the genus shows transitional structures that we consider evolutionary reductions. Our results can explain how developmental alterations have influenced the suppression and modification of floral organs in the genus.

Additional keywords: Crotonoideae, evolution, ontogeny, perianth, petals, staminodes.


References

Baum DA, Donoghue MJ (2002) Transference of function, heterotopy, and the evolution of plant development. In ‘Developmental genetics and plant evolution’. (Eds Q Cronk, R Bateman, J Hawkins) pp. 52–69. (Taylor & Francis: London)

Berry PE, Hipp AL, Wurdack KJ, Van Ee B, Riina R (2005) Molecular phylogenetics of the giant genus Croton and tribe Crotoneae (Euphorbiaceae sensu stricto) using ITS and TRNL-TRNF DNA sequence data. American Journal of Botany 92, 1520–1534.
Molecular phylogenetics of the giant genus Croton and tribe Crotoneae (Euphorbiaceae sensu stricto) using ITS and TRNL-TRNF DNA sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGntrbJ&md5=98301b16d73250624e4bc5c10a3d86d2CAS |

Cacho NI, Berry PE, Olson ME, Steinmann VW, Baum DA (2010) Are spurred cyathia a key innovation? Molecular systematics and trait evolution in the slipper spurges (Pedilanthus clade: Euphorbia, Euphorbiaceae). American Journal of Botany 97, 493–510.
Are spurred cyathia a key innovation? Molecular systematics and trait evolution in the slipper spurges (Pedilanthus clade: Euphorbia, Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlSnsLw%3D&md5=71bde1c3428cae53e5fbd37c1b25ee63CAS |

Caruzo MBR, Cordeiro I (2007) Sinopse da tribo Crotoneae Dumort. (Euphorbiaceae s.s.) no Estado de São Paulo, Brasil. Brittonia 34, 571–585.

Caruzo MBR, Cordeiro I (2013) Taxonomic revision of Croton section Cleodora (Euphorbiaceae). Phytotaxa 121, 1–41.
Taxonomic revision of Croton section Cleodora (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar |

Caruzo MBR, Van Ee BW, Cordeiro I, Berry PE, Riina R (2011) Molecular phylogenetics and character evolution of the ‘sacaca; clade: novel relationships of Croton section Cleodora (Euphorbiaceae). Molecular Phylogenetics and Evolution 60, 193–206.
Molecular phylogenetics and character evolution of the ‘sacaca; clade: novel relationships of Croton section Cleodora (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnt1Kmur8%3D&md5=b3dbb91f9395446183255bb14c85d3c2CAS |

Cordeiro I, Secco R, Carneiro-Torre DS, Lima LR, Caruzo MBR, Berry P, Riina R, Silva OLM, Silva MJ, Sodré RC (2016) Croton. In ‘Lista de espécies da flora do Brasil. Jardim Botânico do Rio de Janeiro’. Available at http://floradobrasil.jbrj.gov.br/jabot/floadobrasil/FB17497 [Verified in 15 January 2016].

De-Paula OC, Sajo MG (2011) Morphology and development of anthers and ovules in Croton and Astraea (Euphorbiaceae). Nordic Journal of Botany 29, 505–511.
Morphology and development of anthers and ovules in Croton and Astraea (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar |

De-Paula OC, Sajo MG, Prenner G, Cordeiro I, Rudall PJ (2011) Morphology, development and homologies of the perianth and floral nectaries in Croton and Astraea (Euphorbiaceae-Malpighiales). Plant Systematics and Evolution 292, 1–14.
Morphology, development and homologies of the perianth and floral nectaries in Croton and Astraea (Euphorbiaceae-Malpighiales).Crossref | GoogleScholarGoogle Scholar |

Endress PK (2011a) Angiosperm ovules: diversity, development, evolution. Annals of Botany 107, 1465–1489.
Angiosperm ovules: diversity, development, evolution.Crossref | GoogleScholarGoogle Scholar |

Fahn A (1979) ‘Secretory tissues in plants.’ (Academic Press: London)

Fahn A (2000) Structure and function of secretory cells. Advances in Botanical Research 31, 37–75.
Structure and function of secretory cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltFKgsLw%3D&md5=dcd5451de38309b17149f32899848d34CAS |

Gagliardi KB (2014) Estudo ontogenético da redução floral em Euphorbiaceae e das estruturas secretoras associadas: anatomia e evolução. Dissertação apresentada ao Instituto de Biociências da Universidade de São Paulo. Departamento de Botânica, São Paulo, Brasil.

Gagliardi KB, Rosado A, Souza LA, Moscheta IS, Albiero ALM (2012) Structure and development of fruits and seeds of weed species of Euphorbiaceae. Acta Botanica Brasílica 26, 38–45.
Structure and development of fruits and seeds of weed species of Euphorbiaceae.Crossref | GoogleScholarGoogle Scholar |

Gagliardi KB, Souza LA, Albiero ALM (2014) Comparative fruit development in some Euphorbiaceae and Phyllanthaceae. Plant Systematics and Evolution 300, 775–782.
Comparative fruit development in some Euphorbiaceae and Phyllanthaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFensLjL&md5=654d162c85c136da0b9f1c96641a7bbfCAS |

Gerlach D (1984) ‘Botanische Mikrotechnik: eine Einführung.’ (Georg Thieme: Stuttgart, Germany)

Haber JM (1925) The anatomy and the morphology of the flower of Euphorbia. Annals of Botany os-39, 657–705.
The anatomy and the morphology of the flower of Euphorbia.Crossref | GoogleScholarGoogle Scholar |

Johansen DA (1940) ‘Plant microtechnique.’ (McGraw-Hill: New York)

Johri BM, Ambegaokar KB, Srivastava PS (1992) ‘Comparative embryology of angiosperms.’ (Springer-Verlag: Berlin)

Lillie RD (1965) ‘Histopathologic technic and practical histochemistry.’ (McGraw-Hill: New York)

Lima LR, Pirani JR (2003) O gênero Croton L. na Cadeia do Espinhaço, Minas Gerais, Brasil. Boletim de Botânica da Universidade de São Paulo 21, 299–344.
O gênero Croton L. na Cadeia do Espinhaço, Minas Gerais, Brasil.Crossref | GoogleScholarGoogle Scholar |

Liu HF, Deng YF, Liao JP (2008) Floral organogenesis of three species of Jatropha (Euphorbiaceae). Journal of Systematics and Evolution 46, 53–61.

Martins FM, Cunha-Neto IL, Pereira TM (2016) Floral morphology and anatomy of Dalechampia alata Klotzsch ex Baill. (Euphorbiaceae), with emphasis on secretory structures. Brazilian Journal of Biology 76, 233–244.
Floral morphology and anatomy of Dalechampia alata Klotzsch ex Baill. (Euphorbiaceae), with emphasis on secretory structures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC28jgtVSltg%3D%3D&md5=f5d3a7dedb5abe9c93169d001b10e5e5CAS |

Narbona E, Ortiz PL, Arista M (2008) Sexual dimorphism in the andromonoecious Euphorbia nicaeensis: effects of gender and inflorescence development. Annals of Botany 101, 717–726.
Sexual dimorphism in the andromonoecious Euphorbia nicaeensis: effects of gender and inflorescence development.Crossref | GoogleScholarGoogle Scholar |

Prenner G, Rudall PJ (2007) Comparative ontogeny of the cyathium in Euphorbia (Euphorbiaceae) and its allies: exploring the organ-flower-inflorescence boundary. American Journal of Botany 94, 1612–1629.
Comparative ontogeny of the cyathium in Euphorbia (Euphorbiaceae) and its allies: exploring the organ-flower-inflorescence boundary.Crossref | GoogleScholarGoogle Scholar |

Prenner G, Cacho NI, Baum D, Rudall PJ (2011) Is LEAFY a useful marker gene for the flower-inflorescence boundary in the Euphorbia cyathium? Journal of Experimental Botany 62, 345–350.
Is LEAFY a useful marker gene for the flower-inflorescence boundary in the Euphorbia cyathium?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurnF&md5=249c0afe6249cbd75abfddeaa554927bCAS |

Rijpkema A, Gerats T, Vandenbussche M (2006) Genetics of floral development in petunia. Advances in Botanical Research 44, 237–278.
Genetics of floral development in petunia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gmuro%3D&md5=2f8db34831d7f49183af5d691e7e37d2CAS |

Ronse De Craene LP (2003) The evolutionary significance of homeosis in flowers: a morphological perspective. International Journal of Plant Sciences 164, S225–S235.
The evolutionary significance of homeosis in flowers: a morphological perspective.Crossref | GoogleScholarGoogle Scholar |

Ronse De Craene LP (2007) Are petals sterile stamens or bracts? The origin and evolution of petals in the core eudicots. Annals of Botany 100, 621–630.
Are petals sterile stamens or bracts? The origin and evolution of petals in the core eudicots.Crossref | GoogleScholarGoogle Scholar |

Ronse De Craene LP, Brockington S (2013) Origin and evolution of petals in angiosperms. Plant Ecology and Evolution 146, 5–25.
Origin and evolution of petals in angiosperms.Crossref | GoogleScholarGoogle Scholar |

Ronse De Craene LP, Smets EF (2001) Staminodes: their morphological and evolutionary significance. Botanical Review 67, 351–402.
Staminodes: their morphological and evolutionary significance.Crossref | GoogleScholarGoogle Scholar |

Rudall PJ (2007) ‘Anatomy of flowering plants: an introduction to structure and development.’ (Cambridge University Press: Cambridge, UK)

Silva JS, Sales MF, Gomes APS, Carneiro-Torres DS (2010) Sinopse das espécies de Croton L. (Euphorbiaceae) no estado de Pernambuco, Brasil. Acta Botanica Brasílica 24, 441–453.
Sinopse das espécies de Croton L. (Euphorbiaceae) no estado de Pernambuco, Brasil.Crossref | GoogleScholarGoogle Scholar |

Souza LA, Silva AC, Moscheta IS (2010) Morphology and anatomy of flowers of Dalechampia stipulacea MÜLL. ARG. (Euphorbiaceae). Acta Botanica Venezuelica 33, 103–117.

Tokuoka T (2007) Molecular phylogenetic analysis of Euphorbiaceae sensu stricto based on plastid and nuclear DNA sequences and ovule and seed character evolution. Journal of Plant Research 120, 511–522.
Molecular phylogenetic analysis of Euphorbiaceae sensu stricto based on plastid and nuclear DNA sequences and ovule and seed character evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntFOgurY%3D&md5=68a8bf6b4f33a4159f84fca881d19da2CAS |

Tokuoka T, Tobe H (1995) Embryology and systematics of Euphorbiaceae sens. lat.: a review and perspective. Journal of Plant Research 108, 97–106.
Embryology and systematics of Euphorbiaceae sens. lat.: a review and perspective.Crossref | GoogleScholarGoogle Scholar |

Tokuoka T, Tobe H (1998) Ovules and seeds in Crotonoideae (Euphorbiaceae): structure and systematic implications. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 120, 165–186.

Tokuoka T, Tobe H (2002) Ovules and seeds in Euphorbioideae (Euphorbiaceae): structure and systematic implications. Journal of Plant Research 115, 361–374.
Ovules and seeds in Euphorbioideae (Euphorbiaceae): structure and systematic implications.Crossref | GoogleScholarGoogle Scholar |

Tokuoka T, Tobe H (2003) Ovules and seeds in Acalyphoideae (Euphorbiaceae): structure and systematic implications. Journal of Plant Research 116, 355–380.
Ovules and seeds in Acalyphoideae (Euphorbiaceae): structure and systematic implications.Crossref | GoogleScholarGoogle Scholar |

Tokuoka T, Tobe H (2006) Phylogenetic analysis of Malpighiales using plastid and nuclear DNA sequences, with particular reference to the embryology of Euphorbiaceae s. str. Journal of Plant Research 119, 599–616.
Phylogenetic analysis of Malpighiales using plastid and nuclear DNA sequences, with particular reference to the embryology of Euphorbiaceae s. str.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1elsLfM&md5=004c0d4f1186aa81ae5cc09929b1c72fCAS |

Van Ee BW, Riina R, Berry PE (2011) A revised infrageneric classification and molecular phylogeny of New World Croton (Euphorbiaceae). Taxon 60, 1–33.

Walker-Larsen J, Harder LD (2000) The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention. American Journal of Botany 87, 1367–1384.
The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngt12muw%3D%3D&md5=dbfc850879c91e8d5c425c9acca4675aCAS |

Weberling F (1989) ‘Morphology of flowers and inflorescences.’ (Cambridge University Press: Cambridge, UK)

Webster GL (1967) The genera of Euphorbiaceae from southeastern United States. Journal of the Arnold Arboretum 48, 303–361.