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

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 http://dx.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.


References

Armstrong W 1979 Aeration in higher plants. Advances in Botanical Research 7 225 332 doi:10.1016/S0065-2296(08)60089-0

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 doi:10.1111/j.1399-3054.1975.tb03861.x

Bailey-Serres J Voesenek LACJ 2008 Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59 313 339 doi:10.1146/annurev.arplant.59.032607.092752

Binzer T Borum J Pedersen O 2005 Flow velocity affects internal oxygen conditions in the seagrass Cymodocea nodosa. Aquatic Botany 83 239 247 doi:10.1016/j.aquabot.2005.07.001

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 doi:10.1111/j.1365-2745.2004.00943.x

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 doi:10.1046/j.1365-3040.2003.00846.x

Colmer TD Pedersen O 2008 a Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange. New Phytologist 177 918 926 doi:10.1111/j.1469-8137.2007.02318.x

Colmer TD Pedersen O 2008 b Oxygen dynamics in submerged rice (Oryza sativa). New Phytologist 178 326 334 doi:10.1111/j.1469-8137.2007.02364.x

Colmer TD Voesenek LACJ 2009 Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36 665 681 doi:10.1071/FP09144

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 doi:10.1071/FP03058

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

Keeley JE 1998 CAM photosynthesis in submerged aquatic plants. Botanical Review 64 121 175
doi:10.1007/BF02856581

Maberly SC Spence DHN 1983 Photosynthetic inorganic carbon use by freshwater plants. Journal of Ecology 71 705 724 doi:10.2307/2259587

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 doi:10.1093/aob/mcn142

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 doi:10.1046/j.0016-8025.2001.00707.x

Mommer L Visser EJW 2005 Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Annals of Botany 96 581 589 doi:10.1093/aob/mci212

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 doi:10.1111/j.1365-3040.2004.01235.x

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 doi:10.1111/j.1469-8137.2007.02166.x

Pedersen O Colmer TD Vos H 2006 Oxygen dynamics during submergence in the halophytic stem succulent Halosarcia pergranulata. Plant, Cell & Environment 29 1388 1399 doi:10.1111/j.1365-3040.2006.01522.x

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 doi:10.1111/j.1365-313X.2008.03769.x

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 doi:10.1017/S0014479799002057

Raskin I 1983 A method for measuring leaf volume, density, thickness, and internal gas volume. HortScience 18 698 699

Revsbech NP 1989 An oxygen microsensor with a guard cathode. Limnology and Oceanography 34 474 478


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
doi:10.1111/j.1365-2427.1992.tb00540.x

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 doi:10.1093/aob/mci214

Setter TL Laureles EV 1996 The beneficial effect of reduced eleongation growth on submergence tolerance of rice. Journal of Experimental Botany 47 1551 1559 doi:10.1093/jxb/47.10.1551

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

Setter TL Waters I Wallace I Bhekasut P Greenway H 1989 a Submergence of rice I. Growth and photosynthetic response to CO2 enrichment of floodwater. Australian Journal of Plant Physiology 16 251 263
doi:10.1071/PP9890251

Setter TL Greenway H Kupkanchankul T 1989 b Submergence of rice II. Adverse effects of low CO2 concentrations. Australian Journal of Plant Physiology 16 265 278 doi:10.1071/PP9890265

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 doi:10.1111/j.1365-3040.1990.tb02144.x

Voesenek LACJ Colmer TD Pierik R Millenaar FF Peeters AJM 2006 How plants cope with complete submergence. New Phytologist 170 213 226 doi:10.1111/j.1469-8137.2006.01692.x

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 doi:10.1111/j.1469-8137.1989.tb00355.x

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 doi:10.1006/anbo.1996.0405

Yemm EW Willis AJ 1954 The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57 508 514



Supplementary MaterialSupplementary Material 61.8 KB Export Citation