Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T13:42:23.241Z Has data issue: false hasContentIssue false
  • English
  • Français

A new seed coat water-impermeability mechanism in Chaetostoma armatum (Melastomataceae): evolutionary and biogeographical implications of physiophysical dormancy

Published online by Cambridge University Press:  11 March 2015

Rafaella C. Ribeiro ,
Denise M.T. Oliveira  and
Fernando A.O. Silveira
Rafaella C. Ribeiro
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, CP 486, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Denise M.T. Oliveira*
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, CP 486, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Fernando A.O. Silveira
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, CP 486, 31270-901, Belo Horizonte, Minas Gerais, Brazil
*
*Correspondence E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Determining the phylogenetic and biogeographic distribution of physical dormancy remains a major challenge in germination ecology. Here, our goal was to describe a novel water-impermeable seed coat mechanism causing physical dormancy (PY) in the seeds of Chaetostoma armatum (Melastomataceae). Although seed coat permeability tests indicated a significant increase in seed weight after soaking in distilled water, anatomical and dye-tracking analyses showed that both water and dyes penetrated the seed coat but not the embryo, which remained in a dry state. The water and dye penetrated the lumen of the exotestal cells, which have a thin outer periclinal face and thickened secondary walls with U-shaped phenolic compounds. Because of this structure, water and dye do not penetrate the inner periclinal face of the exotestal cells, indicating PY. Puncturing the seeds increased germination more than tenfold compared to that of the control, but GA3 did not increase germination further. A significant fraction of the seeds did not germinate after puncturing, indicating that embryos are also physiologically dormant (PD). This paper constitutes the first report of the water-impermeable seed coat in the Myrtales and the first report of physiophysical (PD+PY) dormancy in a shrub from a tropical montane area.

Keywords

campo rupestregerminationMicrolicieaeMyrtalesphysical dormancyphysiological dormancyseed anatomy
Type
Research Papers
Information
Seed Science Research , Volume 25 , Special Issue 2: Seed Dormancy , June 2015 , pp. 194 - 202
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

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.Google Scholar
Baskin, C.C. and Baskin, J.M. (2014) Seeds: Ecology, biogeography, and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Baskin, C.C., Baskin, J.M. and Chester-Edward, C. (1999) Seed dormancy and germination in Rhexia mariana var. interior (Melastomataceae) and eco-evolutionary implications. Canadian Journal of Botany 77, 488–493.CrossRefGoogle Scholar
Baskin, J.M. and Baskin, C.C. (2000) Evolutionary considerations of claims for physical dormancy-break by microbial action and abrasion by soil particles. Seed Science Research 10, 409–413.Google Scholar
Baskin, J.M., Baskin, C.C. and Xiaojie, L.I. (2000) Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biology 15, 139–152.Google Scholar
Baumgratz, J.F.A. (1985) Morfologia dos frutos e sementes de Melastomatáceas brasileiras. Arquivos do Jardim Botânico do Rio de Janeiro 27, 113–155.Google Scholar
Beerling, D.J. and Osborne, C.P. (2006) The origin of the savannah biome. Global Change Biology 12, 2023–2031.Google Scholar
Benites, V.C., Schaefer, C.E.G.R., Simas, F.N.B. and Santos, H.G. (2007) Soils associated with rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço. Revista Brasileira de Botânica 30, 569–577.Google Scholar
Bond, W.J. and Keeley, J.E. (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends in Ecology and Evolution 20, 387–394.Google Scholar
Briggs, C.L., Morris, E.C. and Ashford, A.E. (2005) Investigations into seed dormancy in Grevillea linearifolia, G. buxifolia and G. sericea: anatomy and histochemistry of the seed coat. Annals of Botany 96, 965–980.Google Scholar
Clausing, G. and Renner, S.S. (2001) Molecular phylogenetics of Melastomataceae and Memecylaceae: implications for character evolution. American Journal of Botany 88, 486–498.Google Scholar
Corner, E.J.H. (1976) The seeds of dicotyledons. Cambridge, Cambridge University Press.Google Scholar
Delouche, J.C., Sill, T.W., Raspet, M. and Lienhard, M. (1962) The tetrazolium test for seed viability. Missouri Agriculture Experimental Station Technical Bulletin 51, 1–63.Google Scholar
Egerton-Warburton, L. (1998) A smoke-induced alteration of the subtesta cuticle in seeds of the post-fire recruiter, Emmenanthe penduliflora Benth. (Hydrophyllaceae). Journal of Experimental Botany 49, 1317–1327.Google Scholar
Franklin, G.L. (1945) Preparation of thin sections of synthetic resins and wood-resin composites, and a new macerating method for wood. Nature 155, 51.Google Scholar
Fritsch, P.W., Almeda, F., Renner, S.S., Martins, A.B. and Cruz, B.C. (2004) Phylogeny and circumscription of the near-endemic Brazilian tribe Microlicieae (Melastomataceae). American Journal of Botany 91, 1105–1114.CrossRefGoogle ScholarPubMed
Garwood, N.C. (1983) Seed germination in a seasonal tropical forest in Panama: a community study. Ecological Monographs 53, 159–181.Google Scholar
Giulietti, A.M., Pirani, J.R. and Harley, R.M. (1997) Espinhaço range region, eastern Brazil. pp. 397–404 in Davis, S.D.; Heywood, V.H.; Herrera-MacBryde, O.; Villa-Lobos, J.; Hamilton, A.C. (Eds) Centres of plant diversity: a guide and strategy for their conservation, vol. 3. Cambridge, WWF/IUCN.Google Scholar
Groenendijk, J.P., Bouman, F. and Cleef, M. (1996) An exploratory study on seed morphology of Miconia Ruiz & Pavón (Melastomataceae), with taxonomic and ecological implications. Acta Botanica Neerlandica 45, 323–344.Google Scholar
Jensen, W.A. (1962) Botanical histochemistry: principles and practice. San Francisco, W.H. Freeman.Google Scholar
Johansen, D.A. (1940) Plant microtechnique. New York, McGraw-Hill.Google Scholar
Koschnitzke, C. and Martins, A.B. (2006) Revisão taxonômica de Chaetostoma DC. (Melastomataceae, Microlicieae). Arquivos do Museu Nacional do Rio de Janeiro 64, 95–119.Google Scholar
Le Stradic, S. (2012) Composition, phenology and restoration of campo rupestre mountain grasslands – Brazil. PhD thesis, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.Google Scholar
Madeira, J.A. and Fernandes, G.W. (1999) Reproductive phenology of sympatric species of Chamaecrista (Leguminosae) in Serra do Cipó, Brazil. Journal of Tropical Ecology 15, 463–479.CrossRefGoogle Scholar
Mahadevan, N. and Jayasuriya, K.M.G.G (2013) Water-impermeable fruits of the parasitic angiosperm Cassytha filiformis (Lauraceae): confirmation of physical dormancy in Magnoliidae and evolutionary considerations. Australian Journal of Botany 61, 322–329.Google Scholar
Mazia, D., Brewer, P.A. and Alfert, M. (1953) The cytochemical staining and measurement of protein with mercuric bromphenol blue. Biological Bulletin 104, 57–67.Google Scholar
Mendes-Rodrigues, C., Araújo, F.P., Barbosa-Souza, C., Barbosa-Souza, V., Ranal, M., Santana, D.G. and Oliveira, P.E. (2010) Multiple dormancy and maternal effect on Miconia ferruginata (Melastomataceae) seed germination, Serra de Caldas Novas, Goiás, Brazil. Revista Brasileira de Botânica 33, 93–105.Google Scholar
O'Brien, T.P. and McCully, M.E. (1981) The study of plant structure: Principles and selected methods. Melbourne, Termarcarphi Pty. Ltd.Google Scholar
O'Brien, T.P., Feder, N. and McCully, M.E. (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368–373.Google Scholar
Ocampo, G. and Almeda, F. (2013) Seed diversity in the Miconieae (Melastomataceae): morphological characterization and phenetic relationships. Phytotaxa 80, 1–129.CrossRefGoogle Scholar
Paiva, E.A.S, Pinho, S.Z. and Oliveira, D.M.T. (2011) Large plant samples: how to process for GMA embedding? pp. 37–49 in Chiarini-Garcia, H.; Melo, R.C.N. (Eds) Light microscopy: Methods and protocols. New York, Springer/Humana Press.Google Scholar
Ranal, M.A. and Santana, D.G. (2006) How and why to measure the germination process? Revista Brasileira de Botânica 29, 1–11.Google Scholar
Renner, S.S. (2004) Bayesian analysis of combined chloroplast loci, using multiple calibrations, supports the recent arrival of Melastomataceae in Africa and Madagascar. American Journal of Botany 91, 1427–1435.Google Scholar
Ribeiro, L.C. and Borghetti, F. (2014) Comparative effects of desiccation, heat shock and high temperatures on seed germination of savannah and forest tree species. Austral Ecology 39, 267–278.Google Scholar
Ribeiro, R.C. and Oliveira, D.M.T. (2014) Small and hard seeds: a practical and inexpensive method to improve embedding techniques for light microscopy. Acta Botanica Brasilica 28, 624–630.Google Scholar
Sileshi, G.W. (2012) A critique of current trends in the statistical analysis of seed germination and viability data. Seed Science Research 22, 145–159.Google Scholar
Silveira, F.A.O. (2011) Evolutionary ecophysiology of seed dormancy and germination of Melastomataceae from rupestrian fields. PhD thesis, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil.Google Scholar
Silveira, F.A.O., Ribeiro, R.C., Oliveira, D.M.T., Fernandes, G.W. and Lemos-Filho, J.P. (2012) Evolution of physiological dormancy multiple times in Melastomataceae from Neotropical montane vegetation. Seed Science Research 22, 37–44.Google Scholar
Silveira, F.A.O., Fernandes, G.W. and Lemos-Filho, J.P. (2013) Seed and seedling ecophysiology of Neotropical Melastomataceae: implications for conservation and restoration of savannas and rain forests. Annals of the Missouri Botanical Garden 99, 82–99.Google Scholar
Simon, M.F., Grether, R., Queiroz, L.P., Skema, C., Pennington, R.T. and Hughes, C.E. (2009) Recent assembly of the Cerrado, a Neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of Sciences, USA 106, 20359–20364.Google Scholar
Werker, E. (1997) Seed anatomy. Berlin, Gebrüder Borntraeger.Google Scholar
Willis, C.G., Baskin, C.C., Baskin, J.M., Auld, J.R., Venable, D.L., Cavender-Bares, J., Donohue, K., de Casas, R.R. and The NESCent Germination Working Group. (2014) The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants. New Phytologist 203, 300–309.CrossRefGoogle ScholarPubMed
Supplementary material: File

Ribeiro supplementary material

Figure S1

Download Ribeiro supplementary material(File)
File 103.5 KB
Supplementary material: File

Ribeiro supplementary material

Figure S2

Download Ribeiro supplementary material(File)
File 486.8 KB