Development and evolution of the gynoecium in Myrteae (Myrtaceae)
Rafael R. Pimentel A D , Natália P. Barreira A , Diego P. Spala A , Nathane B. Cardim A , Marcelo C. Souza B , Bárbara Sá-Haiad A , Silvia R. Machado C , Joecildo F. Rocha B and Lygia D. R. Santiago-Fernandes A
+ Author Affiliations
- Author Affiliations
A Departamento de Botânica, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, 22940-040 Rio de Janeiro, RJ, Brazil.
B Universidade Federal Rural do Rio de Janeiro, Instituto de Biologia, Departamento de Botânica, Caixa Postal 74582, 23851-970 Seropédica, RJ, Brazil.
C Universidade Estadual Paulista, Instituto de Biociências, Departamento de Botânica, Caixa Postal 510, 18618-000 Botucatu, SP, Brazil.
D Corresponding author. Email: rafaelribeiropimentel@gmail.com
Australian Journal of Botany 62(4) 335-346 https://doi.org/10.1071/BT14058
Submitted: 6 March 2014 Accepted: 16 July 2014 Published: 27 August 2014
Abstract
Characters of the gynoecium are considered potentially significant for the systematics of Myrtaceae. However, only two such characters – ovule number and placentation – have been addressed from an evolutionary perspective. Colleter presence in flowers is a synapomorphy of Myrtales; however, no morphological and histochemical descriptions of such structures have been done in Myrtaceae. Here we analysed the ontogeny and anatomy of the gynoecium combined with the ontogeny, anatomy, ultrastructure, and histochemistry of the colleters to study the evolution of these characters and map their states in the Myrteae phylogenetic tree. Our findings may help elucidate the evolutionary history of this tribe of fleshy-fruit producers so important towards maintaining ecological balance in the rainforest. Floral anatomy and ontogeny were analysed using light microscopy. Colleter samples were processed using standard methods for light and transmission electron microscopy. The main metabolites in colleters were detected via histochemistry. To map character states the program Mesquite version 2.71 was used. The morphological characters of the South American Myrteae here analysed provided an overview of the evolution of gynoecium – with cauline or carpellate placenta – and of colleters, as well as synapomorphies for the clades Plinia + Myrcia and Eugenia + Pimenta. The presence of two integuments in the ovules associated with sclereids and colleters in the gynoecium and the young fleshy fruit assures the efficient dispersal of their seeds. Our findings regarding gynoecium structural diversity of the tribe Myrteae give a new insight on their morphologically uniform flowers.
Additional keywords: antomy, colleter, histochemistry, ontogeny, ultrastructure.
References
Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161, 105–121.| An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III.Crossref | GoogleScholarGoogle Scholar |
Burrows GE (2000) An anatomical study of epicormic bud strand structure in Eucalyptus cladocalyx (Myrtaceae). Australian Journal of Botany 48, 233–245.
| An anatomical study of epicormic bud strand structure in Eucalyptus cladocalyx (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Carrucan AE, Drinnan AN (2000) The ontogenetic basis for floral diversity in the Baeckea sub-group (Myrtaceae). Kew Bulletin 55, 593–613.
| The ontogenetic basis for floral diversity in the Baeckea sub-group (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Costa IR (2009) Estudos evolutivos em Myrtaceae: aspectos citotaxonômicos e filogenéticos em Myrteae, enfatizando Psidium e gêneros relacionados. PhD thesis, Universidade Estadual de Campinas, Brazil.
Costello A, Motley TJ (2004) The development of the superior ovary in Tetraplasandra (Araliaceae). American Journal of Botany 91, 644–655.
| The development of the superior ovary in Tetraplasandra (Araliaceae).Crossref | GoogleScholarGoogle Scholar | 21653419PubMed |
Couvreur TLP, Richardson JE, Sosef MSM, Erkens RHJ, Chatrou LW (2008) Evolution of syncarpy and other morphological characters in African Annonaceae: a posterior mapping approach. Molecular Phylogenetics and Evolution 47, 302–318.
| Evolution of syncarpy and other morphological characters in African Annonaceae: a posterior mapping approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktV2jtrY%3D&md5=1d0e8b453f8a351dd7095ec74dfd5a9dCAS |
Craven LA, Biffin E (2010) An infrageneric classification of Syzygium (Myrtaceae). Blumea 55, 94–99.
| An infrageneric classification of Syzygium (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
da Silva CJ, Barbosa LCA, Marques AE, Baracat-Pereira MC, Pinheiro AL, Meira RMSA (2012) Anatomical characterisation of the foliar colleters in Myrtoideae (Myrtaceae). Australian Journal of Botany 60, 707–717.
| Anatomical characterisation of the foliar colleters in Myrtoideae (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Denardi JD, Oliveira DMT, Paiva EAS (2012) Glandular trichomes in Connarus suberosus (Connaraceae): distribution, structural organization and probable functions. Revista de Biologia Tropical 60, 505–513.
Endress PK (1982) Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms. Taxon 31, 48–52.
| Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms.Crossref | GoogleScholarGoogle Scholar |
Endress PK (2011) Evolutionary diversification of the flowers in angiosperms. American Journal of Botany 98, 370–396.
| Evolutionary diversification of the flowers in angiosperms.Crossref | GoogleScholarGoogle Scholar | 21613132PubMed |
Fahn A (1988) Secretory tissues in vascular plants. New Phytologist 108, 229–257.
| Secretory tissues in vascular plants.Crossref | GoogleScholarGoogle Scholar |
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=bd4e1ca6491366e89670d409091d02ebCAS |
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. American Journal of Botany 55, 123–143.
| Plant microtechnique: some principles and new methods.Crossref | GoogleScholarGoogle Scholar |
Foster AS (1949) ‘Practical plant anatomy.’ (Van Nostrand: New York)
Gabe M (1968) ‘Techiniques histologique.’ (Masson & Cie: Paris)
Gahan PB (1984) ‘Plant histochemistry and cytochemistry: an introduction.’ (Academic Press: London)
Horner HTJ, Lersten NR (1968) Development, structure and function of secretory trichomes in Psychotria bacteriophila (Rubiaceae) American Journal of Botany 55, 1089–1099.
| Development, structure and function of secretory trichomes in Psychotria bacteriophila (Rubiaceae)Crossref | GoogleScholarGoogle Scholar |
Jensen WA (1962) ‘Botanical histochemistry: principles and practice.’ (W. H. Freeman & Co: San Francisco, CA)
Johansen DA (1940) ‘Plant microtechnique.’ (MacGraw-Hill Company Book: New York)
Johnson LAS, Briggs BG (1984) Myrtales and Myrtaceae – a phylogenetic analysis. Annals of the Missouri Botanical Garden 71, 700–756.
| Myrtales and Myrtaceae – a phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |
Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2009) ‘Sistemática vegetal: um enfoque filogenético.’ 3rd edn. (Artmed: Porto Alegre, Brazil)
Kaplan DR (1967) Floral morphology, organogenesis and interpretation of the inferior ovary in Dawningia Bacigalupii. American Journal of Botany 54, 1274–1290.
| Floral morphology, organogenesis and interpretation of the inferior ovary in Dawningia Bacigalupii.Crossref | GoogleScholarGoogle Scholar |
Landrum LR (1986) Campomanesia, Pimenta, Blepharocalyx, Legrandia, Acca, Myrrhinium, and Luma (Myrtaceae). Flora Neotropica 45, 1–178.
Lucas EJ, Harris SA, Mazine FF, Belsham SR, Lughadha EMN, Telford A, Gasson PE, Chase MW (2007) Suprageneric philogenetics of Myrteae, the generically richest tribe in Myrtaceae (Myrtales). Taxon 56, 1105–1128.
| Suprageneric philogenetics of Myrteae, the generically richest tribe in Myrtaceae (Myrtales).Crossref | GoogleScholarGoogle Scholar |
Lughadha EN, Proença C (1996) Survey of the reproductive biology of the Myrtoideae (Myrtaceae). Annals of the Missouri Botanical Garden 83, 480–503.
| Survey of the reproductive biology of the Myrtoideae (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Machado SR (2000) Aspectos subcelulares da secreção. In ‘Tópicos atuais em botânica’. (Eds TB Cavalcanti, BMT Walter) pp. 90–94. (Embrapa Recursos Genéticos e Biotecnologia/Sociedade Botânica do Brasil)
Maddison WP, Maddison DR (2009) ‘Mesquite: a modular system for evolutionary analysis. Version 2.71.’ Available at http://mesquiteproject.org [Verified 7 September 2009]
Louro RP, Ortiz B, Santiago LJM (2003) Leaf ultrastructure of Croton compressus Lam (Euphorbiaceae). Acta Microscopica 12(B), 61–62.
Paiva EAS, Machado SR (2006) Ontogenesis, structure and ultrastructure of Hymenaea stigonocarpa (Fabaceae-Caesalpinioideae) colleters. Revista de Biologia Tropical 54, 943–950.
Pearse AGE (1980) ‘Histochemistry theoretical and applied. Vol. 2.’ 4th edn. (Longman Press: London)
Proença CB, Gibbs PE (1994) Reproductive biology of eight sympatric Myrtaceae from central Brazil. New Phytologist 126, 343–354.
| Reproductive biology of eight sympatric Myrtaceae from central Brazil.Crossref | GoogleScholarGoogle Scholar |
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 17, 208–212.
| The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXktVClu70%3D&md5=f282759e43f3f190f524395b5056db1eCAS | 13986422PubMed |
Sass JE (1951) ‘Botanical microtechnique.’ (The Iowa State College Press: Ames, IA)
Scharaschkin T, Doyle JA (2006) Character evolution in Anaxagorea (Annonaceae). American Journal of Botany 93, 36–54.
| Character evolution in Anaxagorea (Annonaceae).Crossref | GoogleScholarGoogle Scholar |
Schmid R (1972) Floral anatomy of Myrtaceae, II. Eugenia. Journal of the Arnold Arboretum. Arnold Arboretum 53, 336–363.
Snow N, Cantley J (2010) New species of Uromyrtus and Rhodomyrtus (Myrtaceae: Myrteae) from Kamiali wildlife management area, Papua New Guinea, with an updated key to Rodomyrtus. Harvard Papers in Botany 15, 63–70.
| New species of Uromyrtus and Rhodomyrtus (Myrtaceae: Myrteae) from Kamiali wildlife management area, Papua New Guinea, with an updated key to Rodomyrtus.Crossref | GoogleScholarGoogle Scholar |
Soltis DE, Hufford L (2002) Ovary position diversity in Saxifragaceae: clarifying the homology of epigyny. International Journal of Plant Sciences 163, 277–293.
| Ovary position diversity in Saxifragaceae: clarifying the homology of epigyny.Crossref | GoogleScholarGoogle Scholar |
Taboga SR, Vilamaior PSL (2001) Citoquímica. In ‘A célula’. (Eds HF Carvalho, SM Recco-Pimentel) pp. 42–50. (Manoli: Barueri, São Paulo, Brazil)
The Plant List (2010) ‘The plant list. Version 1.’ Available at http://www.theplantlist.org/ [Verified 1 September 2012]
Thomas V (1991) Structural, functional and phylogenetic aspects of the colleter. Annals of Botany 68, 287–305.
Wilson PG (2011) Myrtaceae. In ‘The families and genera of vascular plants. Vol. 10. Flowering plants Eudicots’. (Ed. K Kubitzki) pp. 212–271. (Springer-Verlag: Berlin)
Wilson PG, O’Brien MM, Gadek PA, Quinn CJ (2001) Myrtaceae revisited: a reassessment of infrafamilial groups. American Journal of Botany 88, 2013–2025.
| Myrtaceae revisited: a reassessment of infrafamilial groups.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngt1aiuw%3D%3D&md5=a0217cab01d54eb08c84c0ad3506b729CAS | 21669634PubMed |
Wilson PG, O’Brien MM, Helsewood MM, Quinn CJ (2005) Relationships within Myrtaceae sensu lato based on a matK phylogeny. Plant Systematics and Evolution 251, 3–19.
| Relationships within Myrtaceae sensu lato based on a matK phylogeny.Crossref | GoogleScholarGoogle Scholar |
