Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Comparative floral ontogeny of single-flowered and double-flowered phenotypes of Alcea rosea (Malvaceae)

Somayeh Naghiloo A C , Zahra Esmaillou B and Mohammad Reza Dadpour B
+ Author Affiliations
- Author Affiliations

A Department of Plant Biology, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran.

B Department of Horticultural Sciences, Faculty of Agriculture, University of Tabriz, Tabriz, Iran.

C Corresponding author. Email: some_naghiloo@yahoo.com

Australian Journal of Botany 62(3) 217-228 https://doi.org/10.1071/BT14070
Submitted: 11 April 2014  Accepted: 27 May 2014   Published: 2 July 2014

Abstract

A comparative study of floral ontogeny in single- and double-flowered Alcea rosea L. was conducted using epi-illumination light microscopy. In both floral types, floral differentiation starts with the appearance of three epicalyx lobes, which subsequently subdivide to produce a 7–10-parted epicalyx. Five sepals appear then in a unidirectional or possibly spiral sequence. In single flowers, a corolla-androecium common primordium is formed and subsequently differentiated into five androecial sectors (= primary androecial primordia). Petals are developed at the base of the androecial sectors and secondary androecial primordia are initiated centrifugally in two rows on each sector. Later, tertiary androecial primordia are formed by the subdivision of secondary androecial primordia, which then differentiate into androecial units. Three types of double flowers were identified regarding androecial development. The first type of double flowers shows a more or less disorganised nature. However, 10 proliferation zones can be indentified in the proximal and distal tips of the androecial sectors. In the second and third types of double flowers, androecial development follows similar developmental pathways to that of single flowers. However, in second-type double flowers, the secondary androecial primordia differentiate into petals and the stamens then develop from the free space between the two rows of secondary androecial primordia. In third-type double flowers, after complete primordial partitioning, some primordia on the marginal parts of each androecial sector develop into petaloids or intermediate appendages. The gynoecium appears similarly in both floral types as numerous congenitally united carpel primordia. The double-flowered phenotypes of Alcea appear to fit the criteria for homoheterotopy with complete or partial replacement of stamens with petals, as well as for neoheterotopy, with the formation of stamens in a new position. Based on mutant phenotypes, it is suggested that different functions possibly contribute to the proliferation and differentiation of common primordia.

Additional keywords: androecial sectors, homoheterotopy, neoheterotopy.


References

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

Bayer C (1999) The bicolor unit – homology and transformation of an inflorescence structure unique to core Malvales. Plant Systematics and Evolution 214, 187–198.
The bicolor unit – homology and transformation of an inflorescence structure unique to core Malvales.Crossref | GoogleScholarGoogle Scholar |

Bayer C, Kubitzki K (2003) Malvaceae. In ‘Flowering plants, dicotyledons: Malvales, Capparales, and non-betalain Caryophyllales’. (Eds K Kubitzki, C Bayer) pp. 225–311. (Springer-Verlag: Berlin)

Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the PLENA locus of Antirrhinum. Cell 72, 85–95.
Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the PLENA locus of Antirrhinum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlamu7g%3D&md5=2bccf57a1f84e527a4e1350b8cd4d2b9CAS | 8093684PubMed |

Charlton WA, Macdonald AD, Posluszny U, Wilkins CP (1989) Additions to the technique of epi-illumination light microscopy for the study of floral and vegetative apices. Canadian Journal of Botany 67, 1739–1743.
Additions to the technique of epi-illumination light microscopy for the study of floral and vegetative apices.Crossref | GoogleScholarGoogle Scholar |

Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353, 31–37.
The war of the whorls: genetic interactions controlling flower development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MzltFejtg%3D%3D&md5=079dec6bff60a64d09cd6a6ce8a60413CAS | 1715520PubMed |

Corner EJH (1958) Transference of function. Botanical Journal of the Linnean Society 56, 33–40.
Transference of function.Crossref | GoogleScholarGoogle Scholar |

Dadpour MR, Grigorian W, Nazemieh A, Valizadeh M (2008) Application of epi-illumination light microscopy for study of floral ontogeny in fruit trees. International Journal of Botany 4, 49–55.
Application of epi-illumination light microscopy for study of floral ontogeny in fruit trees.Crossref | GoogleScholarGoogle Scholar |

Dadpour MR, Movafeghi A, Grigorian W, Omidi Y (2011a) Determination of floral initiation in Malus domestica: a novel morphogenetic approach. Biologia Plantarum 55, 243–252.
Determination of floral initiation in Malus domestica: a novel morphogenetic approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVKru7k%3D&md5=f70adb1744a160ebbd964344d858b5d7CAS |

Dadpour MR, Naghiloo S, Aliakbari M, Panahirad S, Movafeghi A (2011b) A comparison of early floral ontogeny in wild-type and double-flowered phenotypes of Syringa vulgaris. Scientia Horticulturae 127, 535–541.
A comparison of early floral ontogeny in wild-type and double-flowered phenotypes of Syringa vulgaris.Crossref | GoogleScholarGoogle Scholar |

Endress PK, Matthews ML (2006) Elaborate petals and staminodes in eudicots: diversity, function, and evolution. Organisms, Diversity & Evolution 6, 257–293.
Elaborate petals and staminodes in eudicots: diversity, function, and evolution.Crossref | GoogleScholarGoogle Scholar |

Galimba KD, Tolkin TR, Sullivan AM, Melzer R, Theißen G, Di Stilio VS (2012) Loss of deeply conserved C-class floral homeotic gene function and C- and E-class protein interaction in a double-flowered ranunculid mutant. Proceedings of the National Academy of Sciences of the United States of America 109, E2267–E2275.
Loss of deeply conserved C-class floral homeotic gene function and C- and E-class protein interaction in a double-flowered ranunculid mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVaku7fP&md5=70df8c0c16b4b520bc44503be4cde507CAS | 22853954PubMed |

Gustafson-Brown C, Savidge B, Yanosky MF (1994) Regulation of the Arabidopsis floral homeotic gene APETALA1. Cell 76, 131–143.
Regulation of the Arabidopsis floral homeotic gene APETALA1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht1Kru7s%3D&md5=08e10cb3514c5e96dc3ea432d99ec7abCAS | 7506995PubMed |

Hill JP, Lord EM (1989) Floral development in Arabidopsis thaliana: a comparison of the wild type and the homeotic pistillata mutant. Canadian Journal of Botany 67, 2922–2936.
Floral development in Arabidopsis thaliana: a comparison of the wild type and the homeotic pistillata mutant.Crossref | GoogleScholarGoogle Scholar |

Hufford L (1998) Early development of androecia in polystemonous Hydrangeaceae. American Journal of Botany 85, 1057–1067.
Early development of androecia in polystemonous Hydrangeaceae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MnhslWmsw%3D%3D&md5=13093597b5d91c59758486af6f51d2c3CAS | 21684991PubMed |

Janka H, von Balthazar M, Alverson WS, Baum DA, Semir J, Bayer C (2008) Structure, development and evolution of the androecium in Adansonieae (core Bombacoideae, Malvaceae s.l.). Plant Systematics and Evolution 275, 69–91.
Structure, development and evolution of the androecium in Adansonieae (core Bombacoideae, Malvaceae s.l.).Crossref | GoogleScholarGoogle Scholar |

Jenny M (1989) Organstellung und Androeceumentwicklung ausgewählter Sterculiaceae. Abstract 26. In ‘9th symposium morphology, anatomy and systematic, Wien 26’.

Kirchoff BK (1991) Homeosis in the flowers of the Zingiberales. American Journal of Botany 78, 833–837.
Homeosis in the flowers of the Zingiberales.Crossref | GoogleScholarGoogle Scholar |

Lehmann N, Sattler R (1993) Homeosis in floral development of Sanguinaria canadensis and S. canadensis ‘Multiplex’ (Papaveraceae). American Journal of Botany 80, 1323–1335.
Homeosis in floral development of Sanguinaria canadensis and S. canadensis ‘Multiplex’ (Papaveraceae).Crossref | GoogleScholarGoogle Scholar |

Lehmann N, Sattler R (1994) Floral development and homeosis in Actaea rubra (Ranunculaceae). International Journal of Plant Sciences 155, 658–671.
Floral development and homeosis in Actaea rubra (Ranunculaceae).Crossref | GoogleScholarGoogle Scholar |

Lönnig WE, Saedler H (1994) The homeotic Macho mutant in Antirrhinum majus reverts to wild-type or mutates to the homeotic plena phenotype. Molecular & General Genetics 245, 636–643.
The homeotic Macho mutant in Antirrhinum majus reverts to wild-type or mutates to the homeotic plena phenotype.Crossref | GoogleScholarGoogle Scholar |

Ma H (1994) The unfolding drama of flower development: recent results from genetic and molecular analyses. Genes & Development 8, 745–756.
The unfolding drama of flower development: recent results from genetic and molecular analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFCjtb4%3D&md5=6daad7af5139149d4f194f691b9013eaCAS |

MacIntyre JB, Lacroix C (1996) Comparative development of perianth and androecial primordia of the single flower and the homeotic double-flowered mutant in Hibiscus rosa-sinensis (Malvaceae). Canadian Journal of Botany 74, 1871–1882.
Comparative development of perianth and androecial primordia of the single flower and the homeotic double-flowered mutant in Hibiscus rosa-sinensis (Malvaceae).Crossref | GoogleScholarGoogle Scholar |

Meyerowitz EM, Smyth DR, Bowman JL (1989) Abnormal flowers and pattern formation in floral development. Development 106, 209–217.

Rasmussen N, Green PB (1993) Organogenesis in flowers of the homeotic green pistillate mutant of tomato (Lycopersicon esculentum). American Journal of Botany 80, 805–813.
Organogenesis in flowers of the homeotic green pistillate mutant of tomato (Lycopersicon esculentum).Crossref | GoogleScholarGoogle Scholar |

Reynolds J, Tampion J (1983) ‘Double flowers: a scientific study.’ (Van Nostrand Reinhold: New York)

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 (2008) Homology and evolution of petals in the core eudicots. Systematic Botany 33, 301–325.
Homology and evolution of petals in the core eudicots.Crossref | GoogleScholarGoogle Scholar |

Ronse De Craene LP, Clinckemaillie D, Smets EF (1993) Stamen-petal complexes in Magnoliatae. Bulletin du Jardin Botanique National de Belgique 62, 97–112.
Stamen-petal complexes in Magnoliatae.Crossref | GoogleScholarGoogle Scholar |

Rudall PJ, Bateman RM (2002) Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots. Biological Reviews of the Cambridge Philosophical Society 77, 403–441.
Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots.Crossref | GoogleScholarGoogle Scholar | 12227521PubMed |

Sattler R (1988) Homeosis in plants. American Journal of Botany 75, 1606–1617.
Homeosis in plants.Crossref | GoogleScholarGoogle Scholar |

van Heel WA (1966) Morphology of the androecium in Malvales. Blumea 13, 177–394.

van Heel WA (1978) Morphology of the pistil in Malvaceae – Ureneae. Blumea 24, 123–137.

van Heel WA (1995) Morphology of the gynoecium of Kitaibelia vitifolia Willd. and Malope trifida L. (Malvaceae-Malopeae). Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 117, 485–493.

von Balthazar M, Alverson WS, Schönenberger J, Baum DA (2004) Comparative floral development and androecium structure in Malvoideae (Malvaceae s.l.). International Journal of Plant Sciences 165, 445–473.
Comparative floral development and androecium structure in Malvoideae (Malvaceae s.l.).Crossref | GoogleScholarGoogle Scholar |

von Balthazar M, Schönenberger J, Alverson WS, Janka H, Bayer C, Baum DA (2006) Structure and evolution of the androecium in the Malvatheca clade (Malvaceae s.l.) and implications for Malvaceae and Malvales. Plant Systematics and Evolution 260, 171–197.

Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78, 203–209.
The ABCs of floral homeotic genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFehsbc%3D&md5=9f26387e0d2a3f4a0334f0a1272dc813CAS | 7913881PubMed |

Wuest SE, O’Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proceedings of the National Academy of Sciences, USA 109, 13 452–13 457.
Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVamt7%2FN&md5=e4e34df7fb9396ffe1db643b16e70cc6CAS |