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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Submergence tolerance in Hordeum marinum: dissolved CO2 determines underwater photosynthesis and growth

Ole Pedersen A C E , Al I. Malik A B D and Timothy D. Colmer A B
+ Author Affiliations
- Author Affiliations

A School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B Future Farm Industries CRC, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

C Freshwater Biological Laboratory, Institute of Biology, University of Copenhagen, Helsingørsgade 51, DK-3400 Hillerød, Denmark.

D Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan.

E Corresponding author. Email: opedersen@bio.ku.dk

Functional Plant Biology 37(6) 524-531 https://doi.org/10.1071/FP09298
Submitted: 15 December 2009  Accepted: 28 February 2010   Published: 20 May 2010

Abstract

Floodwaters differ markedly in dissolved CO2, yet the effects of CO2 on submergence responses of terrestrial plants have rarely been examined. The influence of dissolved CO2 on underwater photosynthesis and growth was evaluated for three accessions of the wetland plant Hordeum marinum Huds. All three accessions tolerated complete submergence, but only when in CO2 enriched floodwater. Plants submerged for 7 days in water at air equilibrium (18 µM CO2) suffered loss of biomass, whereas those with 200 µM CO2 continued to grow. Higher underwater net photosynthesis at 200 µM CO2 increased by 2.7- to 3.2-fold sugar concentrations in roots of submerged plants, compared with at air equilibrium CO2. Leaf gas films enhancing gas exchange with floodwater, lack of a shoot elongation response conserving tissue sugars and high tissue porosity (24–31% in roots) facilitating internal O2 movement, would all contribute to submergence tolerance in H. marinum. The present study demonstrates that dissolved CO2 levels can determine submergence tolerance of terrestrial plants. So, submergence experiments should be conducted with defined CO2 concentrations and enrichment might be needed to simulate natural environments and, thus, provide relevant plant responses.

Additional keywords: aerenchyma, elevated CO2, flooding tolerance, sea barleygrass, tissue porosity, tissue sugars, Triticeae, waterlogging tolerance, wetland plant, wild Hordeum.


Acknowledgements

We thank the Faculty of Natural and Agricultural Sciences for a distinguished visitor travel award for OP, CLEAR for financial support to OP, AIM was supported by a JSPS fellowship. Research on wild Hordeum species in the laboratory of TDC is supported by GRDC and the Future Farm Industries CRC. Sarah M Rich is thanked for comments on the manuscript. We thank Roland von Bothmer for providing H. marinum accessions from the Nordic Gene Bank.


References


Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 225–332.
Crossref | GoogleScholarGoogle Scholar | open url image1

Armstrong W, Wright EJ (1975) Radial oxygen loss from roots: the theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique. Physiologia Plantarum 35, 21–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.
Crossref | GoogleScholarGoogle Scholar | open url image1

Binzer T, Borum J, Pedersen O (2005) Flow velocity affects internal oxygen conditions in the seagrass Cymodocea nodosa. Aquatic Botany 83, 239–247.
Crossref | GoogleScholarGoogle Scholar | open url image1

Borum J, Pedersen O, Greve TM, Frankovich T, Zieman JC, Fourqurean JW, Madden C (2005) The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. Journal of Ecology 93, 148–158.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell & Environment 26, 17–36.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colmer TD, Pedersen O (2008a) Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange. New Phytologist 177, 918–926.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colmer TD, Pedersen O (2008b) Oxygen dynamics in submerged rice (Oryza sativa). New Phytologist 178, 326–334.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665–681.
Crossref | GoogleScholarGoogle Scholar | open url image1

Garthwaite AJ, von Bothmer R, Colmer TD (2003) Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum. Functional Plant Biology 30, 875–889.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gaynard TJ , Armstrong W (1987) Some aspects of internal plant aeration in amphibious habitats. In ‘Plant life in aquatic and amphibious habitats’. (Ed. RMM Crawford) pp. 303–320. (Blackwell Scientific Publications: Oxford)

Hunt R (1978) ‘Plant growth analysis.’ (Edward Arnold Ltd: London)

Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography 21, 540–547. open url image1

Keeley JE (1998) CAM photosynthesis in submerged aquatic plants. Botanical Review 64, 121–175.
Crossref | GoogleScholarGoogle Scholar | open url image1

Maberly SC, Spence DHN (1983) Photosynthetic inorganic carbon use by freshwater plants. Journal of Ecology 71, 705–724.
Crossref | GoogleScholarGoogle Scholar | open url image1

Malik AI, English JP, Colmer TD (2009) Tolerance of Hordeum marinum accessions to O2 deficiency, salinity and these stresses combined. Annals of Botany 103, 237–248.
Crossref | GoogleScholarGoogle Scholar | open url image1

McDonald MP, Calwey NW, Colmer TD (2001) Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant, Cell & Environment 24, 585–596.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mommer L, Visser EJW (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Annals of Botany 96, 581–589.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mommer L, Pedersen O, Visser EJW (2004) Acclimation of a terrestrial plant to submergence facilitates gas exchange under water. Plant, Cell & Environment 27, 1281–1287.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mommer L, Wolters-Arts M, Andersen C, Visser EJW, Pedersen O (2007) Submergence-induced leaf acclimation in terrestrial species varying in flooding tolerance. New Phytologist 176, 337–345.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pedersen O, Colmer TD, Vos H (2006) Oxygen dynamics during submergence in the halophytic stem succulent Halosarcia pergranulata. Plant, Cell & Environment 29, 1388–1399.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pedersen O, Rich SM, Colmer TD (2009) Surviving floods: leaf gas films improve O2 and CO2 exchange, root aeration, and growth of completely submerged rice. The Plant Journal 58, 147–156.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ram PC, Singh AK, Singh BB, Singh VK, Singh HP, Setter TL, Singh VP, Singh RK (1999) Environmental characterization of floodwater in Eastern India: relevance to submergence tolerance of lowland rice. Experimental Agriculture 35, 141–152.
Crossref | GoogleScholarGoogle Scholar | open url image1

Raskin I (1983) A method for measuring leaf volume, density, thickness, and internal gas volume. HortScience 18, 698–699. open url image1

Revsbech NP (1989) An oxygen microsensor with a guard cathode. Limnology and Oceanography 34, 474–478. open url image1

Sand-Jensen K, Pedersen MF, Nielsen SL (1992) Photosynthetic use of inorganic carbon among primary and secondary water plants in streams. Freshwater Biology 27, 283–293.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sand-Jensen K, Pedersen O, Binzer T, Borum J (2005) Contrasting oxygen dynamics in two aquatic plants Lobelia dortmanna and Zostera marina. Annals of Botany 96, 613–623.
Crossref | GoogleScholarGoogle Scholar | open url image1

Setter TL, Laureles EV (1996) The beneficial effect of reduced eleongation growth on submergence tolerance of rice. Journal of Experimental Botany 47, 1551–1559.
Crossref | GoogleScholarGoogle Scholar | open url image1

Setter TL, Kupkanchanakul T, Kupkanchankul K, Bhekasut P, Wiengweera A, Greenway H (1987) Concentrations of CO2 and O2 in floodwater and in internodal lacunae of floating rice growing at 1–2 metre water depths. Plant, Cell & Environment 10, 767–776. open url image1

Setter TL, Waters I, Wallace I, Bhekasut P, Greenway H (1989a) Submergence of rice I. Growth and photosynthetic response to CO2 enrichment of floodwater. Australian Journal of Plant Physiology 16, 251–263.
Crossref | GoogleScholarGoogle Scholar | open url image1

Setter TL, Greenway H, Kupkanchankul T (1989b) Submergence of rice II. Adverse effects of low CO2 concentrations. Australian Journal of Plant Physiology 16, 265–278.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stumm W , Morgan JJ (1996) ‘Aquatic chemistry.’ 3rd edn. (John Wiley & Sons: New York)

Thomson CJ, Armstrong W, Waters I, Greenway H (1990) Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat. Plant, Cell & Environment 13, 395–403.
Crossref | GoogleScholarGoogle Scholar | open url image1

Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytologist 170, 213–226.
Crossref | GoogleScholarGoogle Scholar | open url image1

von Bothmer R , Jacobsen N , Baden C , Jørgensen RB , Linde-Laursen I (1995) ‘An ecogeographical study of the genus Hordeum. Systematic and ecogeographic studies on crop genepools 7.’ 2nd edn. (International Plant Genetic Resources Institute: Rome)

Waters I, Armstrong W, Thomson CJ, Setter TL, Adkins S, Gibbs J, Greenway H (1989) Diurnal changes in radial oxygen loss and ethanol metabolism in roots of submerged and non-submerged rice seedlings. New Phytologist 113, 439–451.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wiengweera A, Greenway H, Thomson CJ (1997) The use of agar nutrient solution to simulate lack of convection in waterlogged soils. Annals of Botany 80, 115–123.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57, 508–514. open url image1