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

Pollen development and orbicule and pollen grain morphology in species of Cephalanthus (Rubiaceae-Naucleeae) from the Americas

María Florencia Romero A D , Roberto Salas A B and Ana Maria Gonzalez A C
+ Author Affiliations
- Author Affiliations

A Instituto de Botánica del Nordeste (IBONE, UNNE-CONICET), Sargento Cabral 2131, C.P. 3400, Corrientes, C.C. 209, Argentina.

B Facultad de Ciencias Exactas y Naturales y Agrimensura (FaCENA-UNNE), Avenida Libertad 5470, C.P. 3400, Corrientes, Argentina.

C Facultad de Ciencias Agrarias (FCA-UNNE), Sargento Cabral 2131, C. P. 3400, Corrientes, Argentina.

D Corresponding author. Email: mariafloromero@gmail.com

Australian Journal of Botany 65(3) 233-247 https://doi.org/10.1071/BT16238
Submitted: 24 November 2016  Accepted: 27 March 2017   Published: 30 May 2017

Abstract

This paper is the first embryological report on the genus Cephalanthus L. and contributes to future studies in other genera of the tribe Naucleeae. The development of the anther wall in Cephalanthus glabratus (Spreng.) K. Schum. corresponds to the dicot type and microsporogenesis is simultaneous. The young wall of the anther has four layers; epidermis, endothecium, one middle layer and the secretory tapetum. The tissue of the septum has idioblasts with crystalline sand. In the wall of the mature anther, only the endothecium and remnants of epidermal cells were preserved. The occurrence and morphology of orbicules were observed in the mature anthers of all three species of Cephalanthus with scanning electron microscopy. The orbicules have taxonomic value at species level, since these structures allow us to distinguish between the species analysed. The presence of a protruding oncus was observed for the first time in Cephalanthus in non-acetolysed pollen grains. According to our observations, this structure is not affected by the state of anther dehiscence in C. glabratus because the oncus is visible and prominent in the mature pollen grains in both indehiscent and dehiscent anthers.

Additional keywords: anther development, Cephalanthus glabratus, microsporogenesis, oncus, orbicules.


References

Arbo MM, López A, Schinini A, Pieszko G (2002) Las Plantas Hidrófilas. In ‘Flora del Iberá’. (Eds MM Arbo, SG Tressens) pp. 9–110. (EUDENNE: Corrientes, Argentina)

Bacigalupo NM (1974) Rubiaceae. 6a. In ‘Flora Ilustrada de Ríos’. (Ed. AE Burkart) pp. 3–50. (Instituto Nacional de Tecnología Agropecuaria: Buenos Aires)

Bhandari NN (1984) The microsporangium. In ‘Embryology of Angiosperms’. (Ed. BM Johri) pp. 53–121. (Springer-Verlag: Berlin)

Bremer B, Eriksson T (2009) Time tree of Rubiaceae: phylogeny and dating the family, subfamilies, and tribes. International Journal of Plant Sciences 170, 766–793.
Time tree of Rubiaceae: phylogeny and dating the family, subfamilies, and tribes.Crossref | GoogleScholarGoogle Scholar |

Bremer B, Jansen RK, Oxelman B, Backlund M, Lantz H, Kim KJ (1999) More characters or more taxa for a robust phylogeny case study from the coffee family (Rubiaceae). Systematic Biology 48, 413–435.
More characters or more taxa for a robust phylogeny case study from the coffee family (Rubiaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zitleksw%3D%3D&md5=8de9c2623a06116a34d0340eb25870e4CAS |

Cabaña Fader AA (2013) Estudios Biosistemáticos en especies americanas de Diodia s.lat. (Rubiaceae). Doctoral Thesis, Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Argentina.

Cabrera AL, Zardini EM (1978) ‘Manual de la flora de los alrededores de Buenos Aires.’ (ACME: Buenos Aires)

Davis GL (1966) ‘Systematic embryology of the Angiosperms.’ (Wiley: New York)

Dessein S, Ochoterena H, De Block P, Lens F, Robbrecht E, Schols P, Smets E, Vinckier S, Huysmans S (2005) Palynological characters and their phylogenetic signal in Rubiaceae. Botanical Review 71, 354–414.
Palynological characters and their phylogenetic signal in Rubiaceae.Crossref | GoogleScholarGoogle Scholar |

Devi H (1980) Embryology of two species of Dentella (Dentella repens and Dentella serpyllifolia). Proceedings of the Indian Academy of Sciences: Plant Sciences 89, 213–218.

Erdtman G (1960) The acetolysis method. Svensk Botanisk Tidskrift 54, 561–564.

Galati BG (1988) Estudios embriológicos en la tribu Spermacoceae (Rubiaceae). PhD thesis, Universidad de Buenos Aires, Argentina.

Galati BG (1991) Estudios embriológicos en la tribu Spermacoceae (Rubiaceae). Parte I: Anatomía floral. Microsporogénesis. Megasporogénesis. Boletín de la Sociedad Argentina de Botánica 27, 7–20.

Galati BG (2003) Ubisch bodies in Angiosperms. In ῾Advances in plant reproductive biology. Vol. II’. (Eds AK Pandey, MR Dhakal) pp. 1–21. (Narendra Publishing House: Delhi)

Galati BG, Goteli MM, Rosenfeldt S, Torretta JP, Zarlavsky G (2010) Orbicules in relation to the pollination modes. In ῾Pollen: structure, types and effects’. (Eds BJ Kaiser) pp. 1–15. (Nova Science Publishers Inc.: New York)

Goldberg RB, Beals TP, Sanders PM (1993) Anther development : basic principles and practical applications. The Plant Cell 5, 1217–1229.
Anther development : basic principles and practical applications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7gvValsg%3D%3D&md5=500e0572ffce59dd7b9be50dc6690c7fCAS |

Gonzalez AM (2016) Floral structure, development of the gynoecium, and embryology in Schinopsis balansae Engler (Anacardiaceae) with particular reference to aporogamy. International Journal of Plant Sciences 177, 326–338.
Floral structure, development of the gynoecium, and embryology in Schinopsis balansae Engler (Anacardiaceae) with particular reference to aporogamy.Crossref | GoogleScholarGoogle Scholar |

Gonzalez AM, Cristóbal CL (1997) Anatomía y ontogenia de semillas de Helicteres lhostzkyana (Sterculiaceae). Bonplandia 9, 287–294.

Hesse M, Waha M (1989) A new look at the acetolysis method. Plant Systematics and Evolution 163, 147–152.
A new look at the acetolysis method.Crossref | GoogleScholarGoogle Scholar |

Horner HT, Wagner BL (1992) Association of four different calcium crystals in the anther connective tissue and hypodermal stomium of Capsicum annuum (Solanaceae) during microsporogenesis. American Journal of Botany 79, 531–541.
Association of four different calcium crystals in the anther connective tissue and hypodermal stomium of Capsicum annuum (Solanaceae) during microsporogenesis.Crossref | GoogleScholarGoogle Scholar |

Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in Angiosperms: morphology, function, distribution, and relation with tapetum types. Botanical Review 64, 240–272.
Orbicules in Angiosperms: morphology, function, distribution, and relation with tapetum types.Crossref | GoogleScholarGoogle Scholar |

Huysmans S, El-Ghazaly G, Nilsson S, Smets E (1997) Systematic value of tapetal orbicules: a preliminary survey of the Cinchonoideae (Rubiaceae). Canadian Journal of Botany 75, 815–826.
Systematic value of tapetal orbicules: a preliminary survey of the Cinchonoideae (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |

Hyde HA (1955) Oncus, a new term in pollen morphology. New Phytologist 54, 255–256.
Oncus, a new term in pollen morphology.Crossref | GoogleScholarGoogle Scholar |

Inamuddin M, Farooq M (1984) The embryology of Richardia brasiliensis Gomes (syn. Richardsonia pilosa H.B. & K.) (Rubiaceae) – a reinvestigation. Pakistan Journal of Botany 16, 139–144.

Johansen DA (1940) ‘Plant microtechnique.’ (Mc Graw-Hill Book Co. Inc.: New York)

Kandus P, Morandeira N, Schivo F (2010) ‘Bienes y Servicios Ecosistémicos de los Humedales del Delta del Paraná.’ (Wetlands International: Fundación Humedales)

Kuang YF, Kirchoff BK, Tang YJ, Liang YH, Liao JP (2008) Palynological characters and their systematic significance in Naucleeae (Cinchonoideae, Rubiaceae). Review of Palaeobotany and Palynology 151, 123–135.
Palynological characters and their systematic significance in Naucleeae (Cinchonoideae, Rubiaceae).Crossref | GoogleScholarGoogle Scholar |

Kuang YF, Kirchoff BK, Liao JP (2012) Presence of the protruding oncus is affected by anther dehiscence and acetolysis technique. Grana 51, 253–262.
Presence of the protruding oncus is affected by anther dehiscence and acetolysis technique.Crossref | GoogleScholarGoogle Scholar |

Luque RH, Souza C, Kraus JE (1996) Métodos de coloracão do Roeser (1972) Modoficado – E Kropp (1972), visado a substituicão do azul de astra por azul de alcião 8GS on 8GX. Acta Botanica Brasílica 10, 199–212.

Manns U, Bremer B (2010) Molecular phylogenetics and evolution towards a better understanding of intertribal relationships and stable tribal delimitations within Cinchonoideae s. s. (Rubiaceae). Molecular Phylogenetics and Evolution 56, 21–39.
Molecular phylogenetics and evolution towards a better understanding of intertribal relationships and stable tribal delimitations within Cinchonoideae s. s. (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |

Marks GE (1954) An aceto-carmine glycerol jelly for use in pollen fertility counts. Stain Technology 29, 277–277.
An aceto-carmine glycerol jelly for use in pollen fertility counts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2M%2FgslCrsg%3D%3D&md5=18c806e57d1fdc699ffde4913f8a7e55CAS |

Martínez Crovetto RN (1981) Las plantas utilizadas en medicina popular en el Noroeste de Corrientes-Argentina. Miscelánea 69, 1–140.

Mauseth JD (1988) ‘Plant anatomy.’ (The Benjamin/Cummings Publishing Company: Menlo Park, CA, USA)

Muntzing A (1941) Differential response to x-ray treatment of diploid and tetraploid barley. Kungl Fysiograf Sallskapets Lund Förhand 11, 1–10.

Nilsson S, Praglowski J (1992) ‘Erdtman’s handbook of palynology.’ (2nd edn) (Munksgaard: Copenhagen)

O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue. Protoplasma 59, 368–373.
Polychromatic staining of plant cell walls by toluidine blue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXmtVOmsw%3D%3D&md5=d183c608703bcccd3624c90579e2c3faCAS |

Periasamy K, Swamy BGL (1966) Morphology of the anther tapetum in angiosperms. Current Science 35, 427–430.

Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143, 1–81.
Glossary of pollen and spore terminology.Crossref | GoogleScholarGoogle Scholar |

Ridsdale CE (1976) A revision of the tribe Cephalantheae (Rubiaceae). Blumea 23, 177–188.

Robbrecht E (1988) Tropical woody Rubiaceae. Opera Botany Belgica 1, 1–176.

Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sexual Plant Reproduction 11, 297–322.
Anther developmental defects in Arabidopsis thaliana male-sterile mutants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVSjt7w%3D&md5=3bfe96f71cbf2237c0645c9562a1e7ccCAS |

Schleiden MJ (1837) Einige Blickeauf die Entwicklungsgeschichte des vegetabilischen Organismusbei den Phanerogamen. Archiv für Naturgeschichte 1, 289–320.

Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. The Plant Cell 16, S46–S60.
Stamen structure and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFWltL8%3D&md5=fc46e1c74d1431592f34c4eeef90f856CAS |

Siegloch AM, Marchiori JNC, dos Santos SR (2011) Anatomia do lenho de Cephalanthus glabratus (Spreng.) K. Schum. (Rubiaceae). Balduinia 31, 20–26.

Verellen J, Dessein S, Razafimandimbison SG, Smets E, Huysmans S (2007) Pollen morphology of the tribes Naucleeae and Hymenodictyeae (Rubiaceae-Cinchonoideae) and its phylogenetic significance. Botanical Journal of the Linnean Society 153, 329–341.
Pollen morphology of the tribes Naucleeae and Hymenodictyeae (Rubiaceae-Cinchonoideae) and its phylogenetic significance.Crossref | GoogleScholarGoogle Scholar |

Verstraete B, Groeninckx I, Smets E, Huysmans S (2011) Phylogenetic signal of orbicules at family level: Rubiaceae as case study. Taxon 60, 742–757.

Vinckier S, Smets E (2002) Systematic importance of orbicule diversity in Gentianales. Grana 41, 158–182.
Systematic importance of orbicule diversity in Gentianales.Crossref | GoogleScholarGoogle Scholar |

Vinckier S, Smets E (2005) A histological study of microsporogenesis in Tarenna gracilipes (Rubiaceae). Grana 44, 30–44.
A histological study of microsporogenesis in Tarenna gracilipes (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |

Vinckier S, Huysmans S, Smets E (2000) Morphology and ultrastructure of orbicules in the subfamily Ixoroideae (Rubiaceae). Review of Palaeobotany and Palynology 108, 151–174.
Morphology and ultrastructure of orbicules in the subfamily Ixoroideae (Rubiaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbhsFGktA%3D%3D&md5=57b15207b17e3c90f475f7b669f32037CAS |