Skip to main content

Rhizome, Root/Sediment Interactions, Aerenchyma and Internal Pressure Changes in Seagrasses

  • Chapter
  • First Online:
Seagrasses of Australia

Abstract

Life in seawater presents several challenges for seagrasses owing to low O2 and CO2 solubility and slow gas diffusion rates. Seagrasses have evolved numerous adaptations to these environmental conditions including porous tissue providing low-resistance internal gas channels (aerenchyma ) and carbon concentration mechanisms involving the enzyme carbonic anhydrase. Moreover, seagrasses grow in reduced, anoxic sediments , and aerobic metabolism in roots and rhizomes therefore has to be sustained via rapid O2 transport through the aerenchyma . Tissue aeration is driven by internal concentration gradients between leaves and belowground tissues, where the leaves are the source of O2 and the rhizomes and roots function as O2 sinks. Inadequate internal aeration e.g., due to low O2 availability in the surrounding water during night time, can lead to sulphide intrusion into roots and rhizomes , which has been linked to enhanced seagrass mortality. Under favourable conditions , however, seagrasses leak O2 and dissolved organic carbon into the rhizosphere, where it maintains oxic microzones protecting the plant against reduced phytotoxic compounds and generates dynamic chemical microgradients that modulate the rhizosphere microenvironment. Local radial O2 loss from belowground tissues of seagrasses leads to sulphide oxidation in the rhizosphere, which generates protons and results in local acidification. Such low-pH microniches can lead to dissolution of carbonates and protolytic phosphorus solubilisation in carbonate-rich sediments. The seagrass rhizosphere is also characterised by numerous high-pH microniches indicative of local stimulation of proton consuming microbial processes such as sulphate reduction via root/rhizome exudates and/or release of alkaline substances. High sediment pH shifts the sulphide speciation away from H2S towards non-tissue-penetrating HS ions, which can alleviate the belowground tissue exposure to phytotoxic H2S. High sulphide production can also lead to iron and phosphorus mobilization through sulphide-induced reduction of insoluble Fe(III)oxyhydroxides to dissolved Fe(II) with concomitant phosphorus release to the porewater. Adequate internal tissue aeration is thus of vital importance for seagrasses as it ensures aerobic metabolism in distal parts of the roots and provides protection against intrusion of phytotoxins from the surrounding sediment.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 299.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 379.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 379.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Armstrong W (1979) Aeration in higher plants. In: Advances in botanical research, vol 7. Academic Press, London, pp 225–332

    Google Scholar 

  • Armstrong J, Armstrong W (2001) Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. Am J Bot 88:1359–1370

    Article  CAS  PubMed  Google Scholar 

  • Armstrong J, Armstrong W (2005) Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96(4):625–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45:369–392

    Article  CAS  Google Scholar 

  • Barnabas AD (1996) Casparian band-like structures in the root hypodermis of some aquatic angiosperms. Aquat Bot 55:217–225

    Article  Google Scholar 

  • Beer S, Björk M, Hellblom F, Axelson L (2002) Inorganic carbon utilization in marine angiosperms (seagrasses). Funct Plant Biol 29:349–454

    Article  CAS  Google Scholar 

  • Binzer T, Borum J, Pedersen O (2005) Flow velocity affects internal oxygen conditions in the seagrass Cymodocea nodosa. Aquat Bot 83:239–247

    Article  Google Scholar 

  • Blaabjerg V, Mouritsen KN, Finster K (1998) Diel cycles of sulphate reduction rates in sediments of a Zostera marina bed (Denmark). Aquat Microb Ecol 15(1):97–102

    Article  Google Scholar 

  • Bodensteiner LE (2006) The impact of light availability on benthic oxygen release by the seagrasses Thalassia testudinum (Banks ex König) and Zostera marina. MS thesis, San Jose State University

    Google Scholar 

  • Borum J, Pedersen O, Greve TM, Frankovich TA, Zieman JC, Fourqurean JW, Madden CJ (2005) The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. J Ecol 93:148–158

    Article  CAS  Google Scholar 

  • Borum J, Sand-Jensen K, Binzer T, Pedersen O, Greve T (2006) Oxygen movement in seagrasses. In: Larkum AWD, Orth JR, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Berlin, Dordrecht, The Netherlands, pp 255–270

    Google Scholar 

  • Borum J, Pedersen O, Kotula L, Fraser MW, Statton J, Colmer TD, Kendrick GA (2015) Photosynthetic response to globally increasing CO2 of co-occurring temperate seagrass species. Plant Cell Environ. https://doi.org/10.1111/pce.12658

  • Brodersen KE, Nielsen DA, Ralph PJ, Kühl M (2014) A split flow chamber with artificial sediment to examine the below-ground microenvironment of aquatic macrophytes. Mar Biol 161(12):2921–2930. https://doi.org/10.1007/s00227-014-2542-3

    Article  Google Scholar 

  • Brodersen KE, Lichtenberg M, Paz LC, Kühl M (2015a) Epiphyte-cover on seagrass (Zostera marina L.) leaves impedes plant performance and radial O2 loss from the below-ground tissue. Front Mar Sci 2:58. https://doi.org/10.3389/fmars.2015.00058

    Article  Google Scholar 

  • Brodersen KE, Nielsen DA, Ralph PJ, Kühl M (2015b) Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide. New Phytol 205(3):1264–1276. https://doi.org/10.1111/nph.13124

    Article  PubMed  CAS  Google Scholar 

  • Brodersen KE, Koren K, Lichtenberg M, Kühl M (2016) Nanoparticle-based measurements of pH and O2 dynamics in the rhizosphere of Zostera marina L.: effects of temperature elevation and light/dark transitions. Plant Cell Environ 39:1619–1630

    Google Scholar 

  • Brodersen KE, Koren K, Moßhammer M, Ralph PJ, Kühl M, Santner J (2017a). Seagrass-mediated phosphorus and iron solubilization in tropical sediments. Environ Sci Technol 51:14155–14163

    Google Scholar 

  • Brodersen KE, Hammer KJ, Schrameyer V, Floytrup A, Rasheed MA, Ralph PJ, Kühl M, Pedersen O (2017b) Sediment resuspension and deposition on seagrass leaves impedes internal plant aeration and promotes phytotoxic H2S intrusion. Front Plant Sci 8:657

    Google Scholar 

  • Carlson PR Jr, Yarbro LA, Barber TR (1994) Relationship of sediment sulfide to mortality of Thalassia testudinum in Florida Bay. Bull Mar Sci 54:733–746

    Google Scholar 

  • Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36

    Article  CAS  Google Scholar 

  • Connell EL, Colmer TD, Walker DI (1999) Radial oxygen loss from intact roots of Halophila ovalis as a function of distance behind the root tip and shoot illumination. Aquat Bot 63:219–228

    Article  Google Scholar 

  • Dennison WC (1987) Effects of light on seagrass photosynthesis, growth and depth distribution. Aquat Bot 27(1):15–26

    Article  Google Scholar 

  • Drake LA, Dobbs FC, Zimmerman RC (2003) Effects of epiphyte load on optical properties and photosynthetic potential of the seagrasses Thalassia testudinum Banks ex König and Zostera marina L. Limnol Oceanogr 48(1, part 2):456–463

    Google Scholar 

  • Enstone DE, Peterson CA, Ma F (2003) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351

    Article  CAS  Google Scholar 

  • Erftemeijer PLA, Lewis RRR (2006) Environmental impacts of dredging on seagrasses: a review. Mar Pollut Bull 52(12):1553–1572

    Article  CAS  PubMed  Google Scholar 

  • Fourqurean JW, Zieman JC (2002) Nutrient content of the seagrass Thalassia testudinum reveals regional patterns of relative availability of nitrogen and phosphorus in the Florida Keys USA. Biogeochemistry 61(3):229–245

    Article  CAS  Google Scholar 

  • Frederiksen MS, Glud RN (2006) Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study. Limnol Oceanogr 51(2):1072–1083

    Article  Google Scholar 

  • Glud RN, Berg P, Fossing H, Jørgensen BB (2007) Effects of the diffusive boundary layer (DBL) on benthic mineralization and O2 distribution: a theoretical model analysis. Limnol Oceanogr 52:547–557

    Google Scholar 

  • Golicz AA, Schliep M, Lee HT, Larkum AWD, Dolferus R et al (2015) Genome-wide survey of the seagrass Zostera muelleri suggests modification of the ethylene signalling network. J Exp Bot 66:1489–1498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greve TM, Borum J, Pedersen O (2003) Meristematic oxygen variability in eelgrass (Zostera marina). Limnol Oceanogr 48(1):210–216

    Article  Google Scholar 

  • Hansen JW, Udy JW, Perry CJ, Dennison WC, Lomstein BA (2000) Effect of the seagrass Zostera capricorni on sediment microbial processes. Mar Ecol Prog Ser 199:83–96

    Article  Google Scholar 

  • Hasler-Sheetal H, Holmer M (2015) Sulfide intrusion and detoxification in the seagrass Zostera marina. PLoS ONE 10(6):e0129136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmer M, Hasler-Sheetal H (2014) Sulfide intrusion in seagrasses assessed by stable sulfur isotopes—a synthesis of current results. Front Mar Sci 1:64

    Article  Google Scholar 

  • Holmer M, Pedersen O, Ikejima K (2006) Sulfur cycling and sulfide intrusion in mixed Southeast Asian tropical seagrass meadows. Bot Mar 49:91–102

    Article  CAS  Google Scholar 

  • Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36(3):453–472

    Article  CAS  PubMed  Google Scholar 

  • Isaksen MF, Finster K (1996) Sulphate reduction in the root zone of the seagrass Zostera noltii on the intertidal flats of a coastal lagoon (Arcachon, France). Mar Ecol Prog Ser 137(1):187–194

    Article  CAS  Google Scholar 

  • Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    Article  CAS  Google Scholar 

  • Jensen SI, Kühl M, Glud RN, Jorgensen LB, Prieme A (2005) Oxic microzones and radial oxygen loss from roots of Zostera marina. Mar Ecol Prog Ser 293:49–58

    Article  CAS  Google Scholar 

  • Jovanovic Z, Pedersen MØ, Larsen M, Kristensen E, Glud RN (2015) Rhizosphere O2 dynamics in young Zostera marina and Ruppia maritima. Mar Ecol Prog Ser 518:95–105

    Google Scholar 

  • Jørgensen BB (1982) Mineralization of organic matter in the sea bed—the role of sulfate reduction. Nature 296:643–645

    Article  Google Scholar 

  • Jørgensen BB, Revsbech NP (1985) Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol Oceanogr 30(1):111–122

    Article  Google Scholar 

  • Jørgensen BB, Des Marais DJ (1990) The diffusive boundary layer of sediments: oxygen microgradients over a microbial mat. Limnol Oceanogr 35(6):1343–1355

    Article  PubMed  Google Scholar 

  • Kim YK, Kim SH, Lee K-S (2015) Seasonal growth responses of the seagrass Zostera marina under severely diminished light conditions. Estuaries Coasts 38:558–568

    Article  CAS  Google Scholar 

  • Koren K, Brodersen KE, Jakobsen SL, Kühl M (2015) Optical sensor nanoparticles in artificial sediments—a new tool to visualize O2 dynamics around the rhizome and roots of seagrasses. Environ Sci Technol 49(4):2286–2292. https://doi.org/10.1021/es505734b

    Article  PubMed  CAS  Google Scholar 

  • Kühl M, Revsbech NP (2001) Biogeochemical microsensors for boundary layer studies. In: Boudreau BP, Jørgensen BB (eds) The benthic boundary layer. Oxford University Press, New York, pp 180–210

    Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115

    Article  CAS  Google Scholar 

  • Lamers LP, Govers LL, Janssen IC, Geurts JJ, Van der Welle ME, Van Katwijk MM, Van der Heide T, Roelofs JG, Smolders AJ (2013) Sulfide as a soil phytotoxin—a review. Front Plant Sci 4:268. https://doi.org/10.3389/fpls.2013.00268

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larkum AWD, James PL (1996) Towards a model for inorganic carbon uptake in seagrasses involving carbonic anhydrase. In: Kuo J, Phillips RC, Walker DI, Kirkman H (eds) Seagrass biology: proceedings of an International Workshop. Nedlands, The University of Western Australia, pp 191–196

    Google Scholar 

  • Larkum AWD, McComb AJ, Shepherd SA (1989) Biology of seagrass. Elsevier, Amsterdam, Amsterdam

    Google Scholar 

  • Larkum AWD, Koch E-MW, Kühl M (2003) Diffusive boundary layers and photosynthesis of the epilithic algal community of coral reefs. Marine Biol 142:1073–1082

    Google Scholar 

  • Larkum AWD, Orth RJ, Duarte CM (2006a) Seagrasses: biology, ecology and conservation. Springer, Berlin, Printed in Dordrecht, The Netherlands

    Google Scholar 

  • Larkum AWD, Drew EA, Ralph PJ (2006b) Photosynthesis and metabolism at the cellular level. In: Larkum AWD, Orth JJ, Duarte CA (eds) Seagrasses: biology, ecology and their conservation. Springer, Berlin

    Google Scholar 

  • Maberly SC (2014) The fitness of the environments of air and water for photosynthesis, growth, reproduction and dispersal of photoautotrophs: an evolutionary and biogeochemical perspective. Aquat Bot 118:4–13

    Article  Google Scholar 

  • Madsen JD, Chambers PA, James WF, Koch EW, Westlake DF (2001) The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444(1–3):71–84

    Article  Google Scholar 

  • Moriarty DJW, Iverson RL, Pollard PC (1986) Exudation of organic carbon by the seagrass Halodule wrightii Aschers. and its effect on bacterial growth in the sediment. J Exp Mar Biol Ecol 96(2):115–126

    Article  CAS  Google Scholar 

  • Nielsen LB, Finster K, Welsh DT, Donelly A, Herbert RA, De Wit R, Lomstein BA (2001) Sulphate reduction and nitrogen fixation rates associated with roots, rhizomes and sediments from Zostera noltii and Spartina maritima meadows. Environ Microbiol 3(1):63–71

    Article  CAS  PubMed  Google Scholar 

  • Nobel PS (1990) Physicochemical and environmental plant physiology. Academic Press, San Diego, USA

    Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL Jr, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S et al (2006) A global crisis for seagrass ecosystems. Bioscience 56(12):987–996

    Article  Google Scholar 

  • Pagès A, Teasdale PR, Robertson D, Bennett WW, Schäfer J, Welsh DT (2011) Representative measurement of two-dimensional reactive phosphate distributions and co-distributed iron(II) and sulfide in seagrass sediment porewaters. Chemosphere 85(8):1256–1261

    Article  CAS  PubMed  Google Scholar 

  • Pagès A, Welsh DT, Robertson D, Panther JG, Schäfer J, Tomlinson RB, Teasdale PR (2012) Diurnal shifts in co-distributions of sulfide and iron(II) and profiles of phosphate and ammonium in the rhizosphere of Zostera capricorni. Estuar Coast Shelf Sci 115:282–290

    Article  CAS  Google Scholar 

  • Pedersen O, Borum J, Duarte CM, Fortes MD (1998) Oxygen dynamics in the rhizosphere of Cymodocea rotundata. Mar Ecol Prog Ser 169:283–288

    Article  CAS  Google Scholar 

  • Pedersen O, Borum J, Duarte CM, Fortes MD (1999) ERRATUM: oxygen dynamics in the rhizosphere of Cymodocea rotundata. Mar Ecol Prog Ser 178:310

    CAS  Google Scholar 

  • Pedersen O, Binzer T, Borum J (2004) Sulphide intrusion in eelgrass (Zostera marina L.). Plant, Cell Environ 27:595–602

    Article  CAS  Google Scholar 

  • Pollard PC, Moriarty DJW (1991) Organic carbon decomposition, primary and bacterial productivity, and sulphate reduction, in tropical seagrass beds of the Gulf of Carpentaria, Australia. Mar Ecol Prog Ser 69(1):149–159

    Article  CAS  Google Scholar 

  • Raven JA (1977) The evolution of vascular land plants in relation to supracellular transport processes. Adv Bot Res 5:153–219

    Article  CAS  Google Scholar 

  • Sand-Jensen K, Pedersen O, Binzer T, Borum J (2005) Contrasting oxygen dynamics in the freshwater isoetid Lobelia dortmanna and the marine seagrass Zostera marina. Ann Bot 96:613–623

    Article  PubMed  PubMed Central  Google Scholar 

  • Short FT, Burdick DM (1995) Mesocosm experiments quantify the effects of eutrophication on eelgrass, Zostera marina. Limnol Oceanogr 40:740–749

    Article  Google Scholar 

  • Short FT, Duarte CM (2001) Methods for the measurement of seagrass growth and production. In Short FT, Coles RG (eds) Global seagrass research methods. Elsevier, Amsterdam, pp 155–182

    Google Scholar 

  • Staehr P, Borum J (2011) Seasonal acclimation in metabolism reduces light requirements of eelgrass (Zostera marina). J Exp Mar Biol Ecol 407(2):139–146

    Article  Google Scholar 

  • Van den Honert TH (1948) Water transport in plants as a catenary process. Discuss Faraday Soc 3:146–153

    Article  Google Scholar 

  • Ward LG, Kemp WM, Boynton WR (1984) The influence of waves and seagrass communities on suspended particulates in an estuarine embayment. Mar Geol 59(1):85–103

    Article  Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL Jr, Hughes AR et al (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. PNAS 106:12377–12381

    Article  PubMed  Google Scholar 

  • Wetzel RG, Penhale PA (1979) Transport of carbon and excretion of dissolved organic carbon by leaves and roots/rhizomes in seagrasses and their epiphytes. Aquat Bot 6:149–158

    Article  CAS  Google Scholar 

  • York PH, Carter AB, Chartrand K, Sankey T, Wells L, Rasheed MA (2015) Dynamics of a deep-water seagrass population on the great barrier reef: annual occurrence and response to a major dredging program. Sci Rep 5:13167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmerman RC, Alberte RS (1996) Effect of light/dark transition on carbon translocation in eelgrass Zostera marina seedlings. Mar Ecol Prog Ser 136:305–309

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kasper Elgetti Brodersen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Brodersen, K.E., Kühl, M., Nielsen, D.A., Pedersen, O., Larkum, A.W.D. (2018). Rhizome, Root/Sediment Interactions, Aerenchyma and Internal Pressure Changes in Seagrasses. In: Larkum, A., Kendrick, G., Ralph, P. (eds) Seagrasses of Australia. Springer, Cham. https://doi.org/10.1007/978-3-319-71354-0_13

Download citation

Publish with us

Policies and ethics