Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-21T23:55:48.364Z Has data issue: false hasContentIssue false
  • English
  • Français

Exceptional flooding tolerance in the totipotent recalcitrant seeds of Eugenia stipitata

Published online by Cambridge University Press:  09 May 2017

Geângelo P. Calvi ,
Antônio M. G. Anjos ,
Ilse Kranner ,
Hugh W. Pritchard  and
Isolde D. K. Ferraz
Geângelo P. Calvi*
Affiliation:
National Institute for Amazonian Research (INPA), Biodiversity Coordination, CP 2223, Manaus, 69065-970, AM, Brazil
Antônio M. G. Anjos
Affiliation:
National Institute for Amazonian Research (INPA), Biodiversity Coordination, CP 2223, Manaus, 69065-970, AM, Brazil Chico Mendes Institute for Biodiversity Conservation, Flona de Açú. CP 40, Assú, 59650-000, RN, Brazil
Ilse Kranner
Affiliation:
Royal Botanic Gardens, Kew, Wellcome Trust Millennium Building, Wakehurst Place, Ardingly, West Sussex RH17 6TN, UK Department of Botany and Centre of Molecular Biosciences (CMBI), University of Innsbruck, Sternwartestraße 15, A-6020 Innsbruck, Austria
Hugh W. Pritchard
Affiliation:
Royal Botanic Gardens, Kew, Wellcome Trust Millennium Building, Wakehurst Place, Ardingly, West Sussex RH17 6TN, UK
Isolde D. K. Ferraz
Affiliation:
National Institute for Amazonian Research (INPA), Biodiversity Coordination, CP 2223, Manaus, 69065-970, AM, Brazil
*
*Correspondence E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Eugenia stipitata occurs along rivers in Western Amazonia and produces berry-type fruits with economic potential. Its large recalcitrant (i.e. desiccation-intolerant) seeds have been proposed as a model to study seed stress response, as no apparent differentiation between the embryonic axis and the fused cotyledons are visible. Here, the longevity of submerged seeds was analysed with a view to understanding adaptive mechanisms to seasonal flooding. Submerged seeds began germinating after 2 months. After 1 year, 87 and 96% total germination was reached when seeds were submerged under a water column of 6 cm (where seedlings could emerge from under the water) and 26 cm (where seedlings could not reach the water surface), respectively. Seedling morphology was altered underwater, with short internodes and rudimentary leaf blades, and when submersion was terminated, seedlings transplanted to nursery conditions recovered a normal phenotype. Furthermore, when seedlings were detached from the seeds, the ‘resown’ seeds produced a second, normal seedling within 9 months. Concentrations of the antioxidant glutathione, which was measured as a stress marker, increased with submersion time in water. Seeds that had developed roots and shoots underwater had higher concentrations of glutathione disulphide than non-germinated seeds, suggesting that the flooding stress was more intense for seedlings than seeds, although more oxidizing cellular redox environments are also consistent with the conditions required for differentiation. Submergence underwater is recommended for storage of the recalcitrant seeds of E. stipitata for up to 1 year.

Keywords

Amazoniagermination testglutathioneMyrtaceaestoragetetrazolium stainingtotipotent seed
Type
Research Papers
Information
Seed Science Research , Volume 27 , Special Issue 2: Seed Ecology , June 2017 , pp. 121 - 130
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Association of Official Analytical Chemists (AOAC) (1975) Official methods of analysis of the AOAC, 20th edition. Washington, DC.Google Scholar
Anjos, A.M.G. and Ferraz, I.D.K. (1999) Morfologia, germinação e teor de água das sementes de araçá-boi (Eugenia stipitata ssp. sororia). Acta Amazonica 29, 337–348.Google Scholar
Armstrong, W. (1979). Aeration in higher plants. In Woolhouse, H.W.W. (ed), Advances in Botanical Research, vol. 7, pp. 225–332. London: Academic Press.Google Scholar
Asomaning, J.M., Olympio, N.S. and Sacande, M. (2011) Desiccation sensitivity and germination of recalcitrant Garcinia kola Heckel seeds. Research Journal of Seed Science 4, 15–27.CrossRefGoogle Scholar
Bailey-Serres, J. and Voesenek, L.A.C.J. (2008). Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.Google Scholar
Bailly, C. and Kranner, I. (2011) Analyses of reactive oxygen species and antioxidants in relation to seed longevity and germination. In Kermode, A.R. (ed), Seed Dormancy: Methods and Protocols, vol. 773: Methods in Molecular Biology, pp. 343–367. New York: Springer Science and Business Media.Google Scholar
Birtić, S., Colville, L., Pritchard, H.W., Pearce, S.R. and Kranner, I. (2011) Mathematically combined half-cell reduction potentials of low-molecular-weight thiols as markers of seed ageing. Free Radical Research 45, 1093–1102.CrossRefGoogle ScholarPubMed
Brasil. (2009) Regras para análise de sementes. Brasília, Ministério da Agricultura, Pecuária e Abastecimento.Google Scholar
Calvi, G.P., Aud, F.F., Ferraz, I.D.K., Pritchard, H.W. and Kranner, I. (2017) Analyses of several seed viability markers in individual recalcitrant seeds of Eugenia stipitata McVaugh with totipotent germination. Plant Biology 19, 6–13.CrossRefGoogle ScholarPubMed
Crawford, R.M.M. (1992). Oxygen availability as an ecological limit to plant distribution. Advances in Ecological Research 23, 93–185.CrossRefGoogle Scholar
Daws, M.I., Garwood, N.C. and Pritchard, H.W. (2005) Traits of recalcitrant seeds in a semi-deciduous tropical forest in Panama: some ecological implications. Functional Ecology 19, 874–885.CrossRefGoogle Scholar
Delgado, L.F., Mello, J.I.O. and Barbedo, C.J. (2010) Potential for regeneration and propagation from cut seeds of Eugenia (Myrtaceae) tropical tree species. Seed Science and Technology 38, 624–634.CrossRefGoogle Scholar
Ferreira, C.S., Piedade, M.T.F., Tiné, M.A.S., Rossatto, D.R., Parolin, P. and Buckeridge, M.S. (2009) The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded conditions. Annals of Botany 104, 1111–1119.Google Scholar
Flores, E.M. and Rivera, D.I. (1989) Criptocotilia en algunas dicotiledoneas tropicales. Brenesia 32, 19–26.Google Scholar
Gentil, D.F.O. and Ferreira, S.A.N. (1999) Viabilidade e superação da dormência em sementes de araçá-boi (Eugenia stipitata ssp. sororia). Acta Amazonica 29, 21–31.CrossRefGoogle Scholar
Gentil, D.F.O. and Ferreira, S.A.N. (2000) Métodos de extração e limpeza de sementes de araçá-boi (Eugenia stipitata). Acta Amazonica 30, 23–30.Google Scholar
Goldstein, J.L. and Swain, T. (1963) Changes in tannins in ripening fruits. Phytochemistry 2, 371–383.Google Scholar
Gurnell, A., Goodson, J., Thompson, K., Mountford, O. and Clifford, N. (2007). Three seedling emergence methods in soil seed bank studies: implications for interpretation of propagule deposition in riparian zones. Seed Science Research 17, 183–199.Google Scholar
Ha, C.O., Sands, V.E., Soepadmo, E. and Jong, K. (1988) Reproductive patterns of selected understorey trees in the Malaysian rain forest: the apomictic species. Botanical Journal of the Linnean Society 97, 317–331.CrossRefGoogle Scholar
Hook, D.D. (1984) Adaptations to flooding with fresh water. In Kozlowski, T.T. (ed), Flooding and Plant Growth, pp. 265–294. Orlando, Academic Press.CrossRefGoogle Scholar
Instituto Adolfo Lutz (1985) Normas analíticas: métodos químicos e físicos para análise de alimentos. São Paulo, Instituto Adolfo Lutz.Google Scholar
Jackson, M.B. and Ram, P.C. (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Annals of Botany 91, 227–241.CrossRefGoogle ScholarPubMed
Joshi, G., Kumar, A.N.A., Gowda, B. and Srinivasa, Y. B. (2006) Production of supernumerary plants from seed fragments in Garcinia gummi-gutta: evolutionary implications of mammalian frugivory. Current Science 91, 372–376.Google Scholar
Junk, W.J., Bayley, P.B. and Sparks, R.E. (1989). The flood pulse concept in river-floodplain systems. In Dodge, D.P. (ed), Proceedings of the International Large River Symposium, pp. 110–127. Ottawa, Canadian Special Publication of Fisheries and Aquatic Sciences.Google Scholar
Kozlowski, T.T. and Pallardy, S.G. (1997). Growth Control in Woody Plants. San Diego, Academic Press.Google Scholar
Kranner, I. and Grill, D. (1996) Determination of glutathione and glutathione disulphide in lichens: a comparison of frequently used methods. Phytochemical Analysis 7, 24–28.Google Scholar
Kranner, I., Birtić, S., Anderson, K.M. and Pritchard, H.W. (2006) Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radical Biology and Medicine 40, 2155–2165.Google Scholar
Kranner, I., Minibayeva, F.V., Beckett, R.P. and Seal, C.E. (2010) What is stress? Concepts, definitions and applications in seed science. New Phytologist 188, 655–673.Google Scholar
Long, R.L., Gorecki, M.J., Renton, M., Scott, J.K., Colville, L., Goggin, D.E., Commander, L.E., Westcott, D.A., Cherry, H. and Finch-Savage, W.E. (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biological Reviews 90, 31–59.Google Scholar
Malik, S.K., Chaudhury, R. and Kalia, R.K. (2005) Rapid in vitro multiplication and conservation of Garcinia indica: a tropical medicinal tree species. Scientia Horticulturae 106, 539–553.CrossRefGoogle Scholar
Marinho, T.A.S., Lopes, A., Assis, R.L., Ramos, S.L.F., Gomes, L.R.P., Wittmann, F. and Schöngart, J. (2013) Distribuição e crescimento de Garcinia brasiliensis Mart. e Hevea spruceana (Benth.) Müll. Arg. em uma floresta inundável em Manaus, Amazonas. Ciência Florestal 23, 223–232.Google Scholar
Matos, F.J.A. (1988) Introdução à fitoquímica experimental. Fortaleza, Editora da Universidade Federal do Ceará, Brazil.Google Scholar
McClean, J. (2000) Wetter is not always better: flood tolerance of woody species. Technical Note 52 Watershed Protection Techniques 1, 207–209.Google Scholar
McVaugh, R. (1958) Flora of Peru. Botanical Series Field Museum of Natural History 13, 569–818.Google Scholar
Melo, R.B., Franco, A.C., Silva, C.O., Piedade, M.T.F. and Ferreira, C.S. (2015) Seed germination and seedling development in response to submergence in tree species of the Central Amazonian floodplains. AoB PLANTS 7, 1–12.Google Scholar
Melo, Z.L.O., Gonçalvez, J.F.C., Mazzafera, P. and Santos, D.Y.A.C. (2009) Mobilization of seed reserves during germination of four tropical species of the Amazon rainforest. Seed Science and Technology 37, 597–607.Google Scholar
Mendes, A.M.S. (2011) Eugenia stipitata ssp. sororia McVaugh (araçá-boi) – Myrtaceae: abordagem fisiológica e morfoanatômica da semente, germinação e plântula. PhD Universidade Federal do Amazonas, Manaus, Brazil.Google Scholar
Mendes, A.M.S. and Mendonça, M.S. (2012) Tratamentos pré-germinativos em sementes de araçá-boi (Eugenia stipitata). Revista Brasileira de Fruticultura 34, 921–929.Google Scholar
Mollard, F.P., Insausti, P. and Sánchez, R.A. (2007). Flooding induces secondary dormancy in Setaria parviflora seeds. Seed Science Research 17, 55–62.CrossRefGoogle Scholar
Ofori, D.A., Asomaning, J.M., Peprah, T., Agyeman, V.K., Anjarwalla, P., Tchoundjeu, Z., Mowo, J.G. and Jamnadass, R. (2015) Addressing constraints in propagation of Allanblackia spp. through seed sectioning and air layering. Journal of Experimental Biology and Agricultural Sciences 3, 89–96.Google Scholar
Parolin, P. (2001) Seed germination and early establishment of 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains. Aquatic Botany 70, 89–103.Google Scholar
Parolin, P. (2009). Submerged in darkness: adaptations to prolonged submergence by woody species of the Amazonian floodplains. Annals of Botany 103, 359–376.Google Scholar
Piedade, M.T.F., Junk, W.J. and Parolin, P. (2000). The flood pulse and photosynthetic response of trees in a white water floodplain (várzea) of the Central Amazon, Brazil. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen 27, 1734–1739.Google Scholar
Pinedo, M.H.P., Ramírez, F.N. and Blasco, M.L. (1981) Notas preliminares sobre El arazá (Eugenia stipitata), frutal nativo de La Amazonia peruana. Lima, INIA/IICA.Google Scholar
Rai, H. and Hill, G. (1980) Classification of Central Amazon lakes on the basis of their microbiological and physico-chemical characteristics. Hydrobiologia 72, 85–99.CrossRefGoogle Scholar
Santana, D.G. and Ranal, M.A. (2004) Análise da germinação – um enfoque estatístico. Brasília. Editora Unversidade de Brasília.Google Scholar
Scarano, F.R., Cattânio, J.H. and Crawford, R.M.M. (1994) Root carbohydrate storage in young saplings of an Amazonian tidal varzea forest before the onset of the wet season. Acta Botanica Brasilica 8, 129–139.Google Scholar
Shanderl, S.H. (1970) Tannins and related phenolics. In Joslyn, M.A. (ed), Methods in Food Analysis, pp. 701–772. New York: Academic Press.Google Scholar
Silva, C.V., Bilia, D.A.C. and Barbedo, C.J. (2005) Fracionamento e germinação de sementes de Eugenia . Revista Brasileira de Sementes 27, 86–92.CrossRefGoogle Scholar
Silva, C.V., Bilia, D.A.C., Maluf, A.M. and Barbedo, C.J. (2003) Fracionamento e germinação de uvaia (Eugenia pyriformis Cambess. – Myrtaceae). Revista Brasileira de Botânica 26, 213–221.Google Scholar
Southgate, D.A.T. (1976) Determination of Food Carbohydrates. London: Applied Science Publishers Ltd.Google Scholar
Weidner, S., Chrzanowski, S., Karamać, M., Król, A., Badowiec, A., Mostek, A. and Amarowicz, R. (2014) Analysis of phenolic compounds and antioxidant abilities of extracts from germinating Vitis californica seeds submitted to cold stress conditions and recovery after the stress. International Journal of Molecular Sciences 15, 16211–16225.Google Scholar
Wittmann, F. and Parolin, P. (1999) Phenology of six tree species from central Amazonian Várzea. Ecotropica 5, 51–57.Google Scholar
Zagorchev, L., Seal, C.E., Kranner, I. and Odjakova, M. (2012) Redox state of low-molecular-weight thiols and disulphides during somatic embryogenesis of salt-treated suspension cultures of Dactylis glomerata L. Free Radical Research 46, 656–664.Google Scholar