Skip to main content
Log in

Submergence, seed germination, and seedling development of the Amazonian floodplain tree Pseudobombax munguba: evidence for root oxytropism

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Primary root of seeds germinating while submerged grew upwards towards oxygen-rich surface layers. Height of water column influenced germination and root growth. Seedlings removed from water attached to substrate and grow vertically.

Abstract

Oxygen and light are potentially limiting resources in floodplain forests where plants are subjected to long periods of flooding, particularly in early stages of the life cycle. We experimentally evaluated the effect of flooding and availability of oxygen and light on germination and initial growth of Pseudobombax munguba (Malvaceae), a tree characteristic of the lower portions of the flood-level gradient in Central Amazonian floodplains. Neither flooding nor darkness affected germination (≥93%); however, only seeds that germinated in light developed into seedlings. Germinated seeds floating in water showed positive gravitropic curvature of the primary root and presence of starch-dense amyloplasts (statoliths) in the root cap. Seed germination decreased under 5–7 cm of non-aerated water and the primary root curved upward, extending towards the water surface where oxygen concentration would be higher. Statoliths were not present in the cap cells of these upwardly growing roots suggesting an absence of gravity-directed growth and the involvement, instead, of re-orientation along an oxygen gradient. Although about 50% of seeds germinated under 10 cm of non-aerated water, their primary root did not elongate further after emergence. Seedlings removed from water and positioned horizontally on the surface of a moist, well-aerated substrate attached themselves as roots curved downward, penetrated into the substrate and anchored the plant. The stem bent upright and resumed vertical growth. These features contribute to reducing the time required for establishment in this type of environment where successful colonization is constrained by the short terrestrial phase.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–332

    Article  CAS  Google Scholar 

  • Baskin JM, Baskin CC (2014) Seeds: ecology, biogeography and evolution of dormancy and germination, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiol 116:651–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blancaflor EB (2013) Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am J Bot 100:143–152. doi:10.3732/ajb.1200283

    Article  CAS  PubMed  Google Scholar 

  • Borisjuk L, Macherel D, Benamar A, Wobus U, Rolletschek H (2007) Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol 176:813–823. doi:10.1111/j.1469-8137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colmer TD, Armstrong W, Greenway H, Ismail AM, Kirk GJD, Atwell BJ (2014) Tolerance in rice: transient complete submergence and prolonged standing water. Progress Bot 75:255–307

    Article  CAS  Google Scholar 

  • Crawford RMM (2003) Seasonal differences in plant responses to flooding and anoxia. Can J Bot 81:1224–1246. doi:10.1139/b03-127

    Article  CAS  Google Scholar 

  • De Melo RB, Franco AC, Silva CO, Piedade MTF, Ferreira CS (2015) Seed germination and seedling development in response to submergence in tree species of the Central Amazonian floodplains. AoB Plants 7:041. doi:10.1093/aobpla/plv041

    Google Scholar 

  • Ferreira CS, Piedade MTF, Junk WJ, Parolin P (2007) Floodplain and upland populations of Amazonian Himatanthus sucuuba: effects of flooding on germination, seedling growth and mortality. Environ Exp Bot 60:477–483. doi:10.1016/j.envexpbot.2007.01.005

    Article  Google Scholar 

  • Ferreira CS, Piedade MTF, Franco AC, Gonçalves JFC, Junk WJ (2009) Adaptive strategies to tolerate prolonged flooding in seedlings of floodplain, upland populations of Himatanthus sucuuba, a Central Amazon tree. Aquatic Bot 90:246–252

    Article  Google Scholar 

  • Ferreira CS, Piedade MTF, Oliveira Wittmann A, Franco AC (2010) Plant reproduction in the Central Amazonian floodplains: challenges and adaptations. AoB Plants 10:009. doi:10.1093/aobpla/plq009

    Google Scholar 

  • Freitas CT, Shepard GH, Piedade MTF (2015) The floating forest: traditional knowledge and use of Matupá vegetation islands by riverine peoples of the Central Amazon. PLoS One 10:e0122542. doi:10.1371/journal.pone.0122542

    Article  PubMed  PubMed Central  Google Scholar 

  • Irion G, Junk WJ, Mello JASN (1997) The large Central Amazonian river floodplains near Manaus: geological, climatological, hydrological, and geomorphological aspects. In: Junk WJ (ed) The Central Amazon floodplains. v. Springer, Berlin, pp 23–46

    Chapter  Google Scholar 

  • Jackson MB, Ishizawa K, Ito O (2009) Evolution and mechanisms of plant tolerance to flooding stress. Ann Bot 103:137–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen WA (1962) Botanical histochemistry: principles and practice. WH Freeman, San Francisco

    Google Scholar 

  • Junk WJ, Piedade MTF (1993) Biomass and primary production of herbaceous plant communities in the Amazon floodplain. Hydrobiologia 263:155–162

    Article  Google Scholar 

  • Junk WJ, Barley PB, Sparks RE (1989) The flood-pulse concept in river-floodplain systems. Can Spec Publ Fish Aquat Sci 106:110–127

    Google Scholar 

  • Junk WJ, Piedade MTF, Parolin P, Wittmann F, Schöngart J (2010) Ecophysiology, biodiversity and sustainable management of Central Amazonian floodplain forests. A synthesis. In: Junk WJ, Piedade MTF, Wittmann F; Schöngart J, Parolin P (eds) Central Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management. Heidelberg: Springer Ecological Studies, 210, pp 510–540

  • Kolb RM, Joly CA (2010) Germination and anaerobic metabolism of seeds of Tabebuia cassinoides (Lam.) DC subjected to flooding and anoxia. Flora 205:112–117. doi:10.1016/j.flora.2009.01.001

    Article  Google Scholar 

  • Kubitzki K, Ziburski A (1994) Seed dispersal in flood plain forests of Amazonia. Biotropica 26:30–43

    Article  Google Scholar 

  • Lucas CM, Mekdeçe F, Nascimento CMN, Holanda ASS, Braga J, Dias S, Sousa S, Rosa PS, Suemitsu C (2012) Effects of short-term and prolonged saturation on seed germination of Amazonian floodplain forest species. Aquatic Bot 99:49–55. doi:10.1016/j.aquabot.2012.02.004

    Article  Google Scholar 

  • Maia MA (2001) Frutos da amazônia fonte de alimento para peixes, 1st edn. Sebrae/AM, Amazonas, Manaus

    Google Scholar 

  • Miro B, Ismail AM (2013) Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.). Front Plant Sci 269:1–18. doi:10.3389/fpls.2013.00269

    Google Scholar 

  • Molisch H (1884) Ueber die Ablenkung der Wurzeln von ihrer normalen Wachsthumsrichtung durch Gase (Aerotropismus). Ber Dtsch Bot Ges 2:160–169. doi:10.3389/fpls.2015.01176

    Google Scholar 

  • Myers JA, Harms KE (2011) Seed arrival and ecological filters interact to assemble high-diversity plant communities. Ecology 92:676–686. doi:10.1890/10-1001.1

    Article  PubMed  Google Scholar 

  • Oliveira Wittmann A, Piedade MTF, Lopes A, Conserva A, Wittmann F (2010) Germination and seedling establishmentin floodplain forests. In: Junk WJ, Piedade MTF, Wittmann F; Schöngart J, Parolin P (eds) Central Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management. Heidelberg: Springer Ecological Studies, 210, pp 259–289

  • Oliveira Wittmann A, Piedade MTF, Parolin P, Wittmann F (2007) Germination in four low-várzea tree species of Central Amazonia. Aquatic Bot 86:197–203. doi:10.1016/j.aquabot.2006.10.001

    Article  Google Scholar 

  • Parolin P (2009) Submerged in darkness: adaptations to prolonged submergence by woody species of the Amazonian floodplains. Ann Bot 103:359–376. doi:10.1093/aob/mcn216

    Article  PubMed  Google Scholar 

  • Parolin P, Wittmann F, Ferreira LV (2013) Fruit and seed dispersal in Amazonian floodplain trees: a review. Ecotropica 19:15–32

    Google Scholar 

  • Perbal G, Driss-Ecole D, Tewinkel M, Volkmann D (1997) Statocyte polarity and gravisensitivity in seedling roots grown in microgravity. Planta 203:S57–S62

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Ramos IM, Marañón T (2009) Effects of waterlogging on seed germination of three Mediterranean oak species: ecological implications. Acta Oecol 35:422–428

    Article  Google Scholar 

  • Piedade MTF, Worbes M, Junk WJ (2001) Geo-ecological controls on elemental fluxes in communities of higher plants in Amazonian floodplains. In: McClain ME, Victoria RL, Richey JE (ed) The Biogeochemistry of the Amazon Basin. Oxford University Press, pp 209–234

  • Piedade MTF, Ferreira CS, Wittmann AO, Buckeridge MS, Parolin P (2010) Biochemistry of Amazonian Floodplain Trees. In: Junk WJ, Piedade MTF, Wittmann F; Schöngart J, Parolin P (eds) Central Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management. Heidelberg: Springer Ecological Studies, 210, pp 123–134

  • Piedade MTF, Schöngart J, Wittmann F, Pia Parolin, Junk W (2013) Impactos da inundação e seca na vegetação de áreas alagáveis amazônicas. In: Borma LS, Nobre C (eds) Secas na Amazônia: causas e consequências. São Paulo, Oficina de Textos, pp 268–305

    Google Scholar 

  • Porterfield DM (2002) Environmental Sensing and Directional Growth of Plant Roots. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, 3rd edn. Marcel Dekker Inc, New York, pp 705–730

    Google Scholar 

  • Porterfield DM, Musgrave ME (1998) The tropic response of plant roots to oxygen: Oxytropism in Pisum sativum L. Planta 206:1–6

    Article  CAS  PubMed  Google Scholar 

  • Porterfield DM, Matthews SW, Daugherty CJ, Musgrave ME (1997) Spaceflight exposure effects on transcription, activity, and localization of alcohol dehydrogenase in the roots of Arabidopsis thaliana. Plant Physiol 113:685–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team, 2008. R: A language and environment for statistical computing. In: Computing RFfS (ed), Vienna, Austria

  • Schmidt LH (2000) Guide to handling of tropical and subtropical forest seed., Danida Forest Seed Centre

  • Sena Gomes AR, Kozlowski TT (1980) Responses of Melaleuca quinquenervia seedlings to flooding. Physiol Plant 49:373–377

    Article  Google Scholar 

  • Thiel J, Rolletschek H, Friedel S, Lunn JE, Nguyen TH, Feil R, Tschiersch H, Muller M, Borisjuk L (2011) Seed-specific elevation of non-symbiotic hemoglobin AtHb1: beneficial effects and underlying molecular networks in Arabidopsis thaliana. BMC Plant Biol 11:48. doi:10.1186/1471-2229-11-48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandenbrink JP, Kiss JZ, Herranz R, Medina FJ (2014) Light and gravity signals synergize in modulating plant development. Front Plant Sci 5:563. doi:10.3389/fpls.2014.00563

    Article  PubMed  PubMed Central  Google Scholar 

  • Voesenek LA, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206:57–73. doi:10.1111/nph.13209

    Article  CAS  PubMed  Google Scholar 

  • Wiersum LK (1967) Potential subsoil utilization by roots. Plant Soil 27:383–400

    Article  Google Scholar 

  • Wittmann F, Junk WJ, Piedade MTF (2004) The várzea forests in Amazonia: flooding and the highly dynamic geomorphology interact with natural forest succession. For Ecol Manage 196:199–212. doi:10.1016/j.foreco.2004.02.060

    Article  Google Scholar 

  • Wittmann F, Schöngart J, Junk WJ (2010a) Phytogeography, species diversity, community structure and dynamics of Amazonian floodplain forests. In: Junk WJ, Piedade MTF, Wittmann F; Schöngart J, Parolin P (eds) Central Amazonian Floodplain Forests: ecophysiology, biodiversity and sustainable management. Heidelberg: Springer Ecological Studies, 210, pp 61–105

  • Wittmann F, Schongart J, De Brito JM, Wittmann AO, Piedade MTF, Parolin P, Junk WJ, Guillaumet JL (2010b) Manual de árvores de várzeada Amazônia Central.Taxonomia, ecologia e uso. Editora INPA, Manaus

  • Wittmann F, Householder E, Piedade MTF, Assis RL, Schöngart J, Parolin P, Junk WJ (2012) Habitat specifity, endemism and the neotropical distribution of Amazonian white-water floodplain trees. Ecography 36:690–707

    Article  Google Scholar 

  • Worbes M, Klinge H, Revilla JD, Martins C (1992) On the dynamics, floristic subdivision and geographical distribution of várzea forests in Central Amazonia. J Veg Sci 3:553–564

    Article  Google Scholar 

  • Wuebker EF, Mullen RE, Koehler K (2001) Flooding and temperature effects on soybean germination. Crop Sci 41:1857–1861

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by Fundação de Apoio à Pesquisa do Distrito Federal (FAPDF) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil. The authors thank the Research Group MAUA/National Institute for Amazonian for logistical support in the field, Thomas Christopher Rhys Williams and reviewers for the many helpful comments on the manuscript, Marina Scalon for assistance with statistical analysis and Jéssika Paula Vieira for help with anatomical studies.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Augusto Cesar Franco.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by M. Buckeridge.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferreira, C.S., Piedade, M.T.F. & Franco, A.C. Submergence, seed germination, and seedling development of the Amazonian floodplain tree Pseudobombax munguba: evidence for root oxytropism. Trees 31, 705–716 (2017). https://doi.org/10.1007/s00468-016-1501-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-016-1501-7

Keywords

Navigation