Contrasting oxygen dynamics in Limonium narbonense and Sarcocornia fruticosa during partial and complete submergence
Elisa Pellegrini A B C , Dennis Konnerup B , Anders Winkel B , Valentino Casolo A and Ole Pedersen B
+ Author Affiliations
- Author Affiliations
A Plant Biology Unit, Department of Agricultural, Food, Environmental and Animal Science, University of Udine, via delle Scienze 206, 33100 Udine, Italy.
B Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, Universitetsparken 4, 2100 Copenhagen, Denmark.
C Corresponding author. Email: elisa.pellegrini87@gmail.com
Functional Plant Biology 44(9) 867-876 https://doi.org/10.1071/FP16369
Submitted: 25 October 2016 Accepted: 5 May 2017 Published: 5 June 2017
Abstract
Terrestrial saltmarsh plants inhabiting flood-prone habitats undergo recurrent and prolonged flooding driven by tidal regimes. In this study, the role of internal plant aeration in contrasting hypoxic/anoxic conditions during submergence was investigated in the two halophytes Limonium narbonense Mill. and Sarcocornia fruticosa (L.) A.J. Scott. Monitoring of tissue O2 dynamics was performed in shoots and roots using microelectrodes under drained conditions, waterlogging, partial and complete submergence, in light or darkness. For both species, submergence in darkness resulted in significant declines in tissue O2 status and when in light, in rapid O2 increases first in shoot tissues and subsequently in roots. During partial submergence, S. fruticosa benefitted from snorkelling and efficiently transported O2 to roots, whereas the O2 concentration in roots of L. narbonense declined by more than 90%. Significantly thinner leaves and articles were recorded under high degree of flooding stress and both species showed considerably high tissue porosity. The presence of aerenchyma seemed to support internal aeration in S. fruticosa whereas O2 diffusion in L. narbonense seemed impeded, despite the higher porosity (up to 50%). Thus, the results obtained for L. narbonense, being well adapted to flooding, suggests that processes other than internal aeration could be involved in better flooding tolerance e.g. fermentative processes, and that traits resulting in flooding tolerance in plants are not yet fully understood.
Additional keywords: aerenchyma, dark respiration, flooding, oxygen diffusion, photosynthesis.
References
Adam P (1990) ‘Salt marsh ecology.’ (Cambridge University Press: Cambridge, UK)Adams JB, Bate GC (1994) The effect of salinity and inundation on the estuarine macrophyte Sarcocornia perennis (Mill.) AJ Scott. Aquatic Botany 47, 341–348.
| The effect of salinity and inundation on the estuarine macrophyte Sarcocornia perennis (Mill.) AJ Scott.Crossref | GoogleScholarGoogle Scholar |
Armstrong W (1971) Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiologia Plantarum 25, 192–197.
| Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging.Crossref | GoogleScholarGoogle Scholar |
Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 225–332.
| Aeration in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsVeiu7c%3D&md5=bd7ac671ff6c7a11056c42b86a2c3f67CAS |
Armstrong J, Armstrong W (1988) Phragmites australis – a preliminary study of soil-oxidizing sites and internal gas transport pathways. New Phytologist 108, 373–382.
| Phragmites australis – a preliminary study of soil-oxidizing sites and internal gas transport pathways.Crossref | GoogleScholarGoogle Scholar |
Aschan G, Pfanz H (2003) Non-foliar photosynthesis – a strategy of additional carbon acquisition. Flora – Morphology, Distribution, Functional Ecology of Plants 198, 81–97.
| Non-foliar photosynthesis – a strategy of additional carbon acquisition.Crossref | GoogleScholarGoogle Scholar |
Borum J, Raun AL, Hasler-Sheetal H, Pedersen MØ, Pedersen O, Holmer M (2014) Eelgrass fairy rings: sulfide as inhibiting agent. Marine Biology 161, 351–358.
| Eelgrass fairy rings: sulfide as inhibiting agent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Sgt7fJ&md5=5cbfbab31ff1c053c8246aa88870df79CAS |
Burdick DM, Mendelssohn IA (1990) Relationship between anatomical and metabolic responses to soil waterlogging in the coastal grass Spartina patens. Journal of Experimental Botany 41, 223–228.
| Relationship between anatomical and metabolic responses to soil waterlogging in the coastal grass Spartina patens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslOntL0%3D&md5=5ef0e3eb3029ee045035164b8936cb10CAS |
Castillo JM, Fernández-Baco L, Castellanos EM, Luque CJ, Figueroa ME, Davy AJ (2000) Lower limits of Spartina densiflora and S. maritima in a Mediterranean salt marsh determined by different ecophysiological tolerances. Journal of Ecology 88, 801–812.
| Lower limits of Spartina densiflora and S. maritima in a Mediterranean salt marsh determined by different ecophysiological tolerances.Crossref | GoogleScholarGoogle Scholar |
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.
| Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlKrtLs%3D&md5=7cd6e1d97585c4a75886b1021b03461fCAS |
Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytologist 179, 964–974.
| Flooding tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqurzM&md5=d8cb4704fef9d0c23ee159168da5f6a7CAS |
Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytologist 178, 326–334.
| Oxygen dynamics in submerged rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Gqt70%3D&md5=e4c71617cd60327e5a30a81f88f4dde0CAS |
Colmer TD, Pedersen O, Wetson AM, Flowers TJ (2013) Oxygen dynamics in a salt-marsh soil and in Suaeda maritima during tidal submergence. Environmental and Experimental Botany 92, 73–82.
| Oxygen dynamics in a salt-marsh soil and in Suaeda maritima during tidal submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXovVChtL8%3D&md5=fdd890123b3d60028465ad509d9deb52CAS |
Duarte B, Santos D, Caçador I (2013) Halophyte anti-oxidant feedback seasonality in two salt marshes with different degrees of metal contamination: search for an efficient biomarker. Functional Plant Biology 40, 922–930.
| Halophyte anti-oxidant feedback seasonality in two salt marshes with different degrees of metal contamination: search for an efficient biomarker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1arsrrE&md5=8a825a04f132335b30903ea9514c8645CAS |
Eley Y, Dawson L, Pedentchouk N (2016) Investigating the carbon isotope composition and leaf wax n-alkane concentration of C3 and C4 plants in Stiffkey saltmarsh, Norfolk, UK. Organic Geochemistry 96, 28–42.
| Investigating the carbon isotope composition and leaf wax n-alkane concentration of C3 and C4 plants in Stiffkey saltmarsh, Norfolk, UK.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XksVSht7s%3D&md5=f1d00e1cd8d14ea0358911c788680ffaCAS |
Herzog M, Pedersen O (2014) Partial versus complete submergence – snorkeling aids root aeration in Rumex palustris but not in R. acetosa. Plant, Cell & Environment 37, 2381–2390.
Huber H, Chen X, Hendriks M, Keijsers D, Voesenek LACJ, Pierik R, Poorter H, de Kroon H, Visser EJW (2012) Plasticity as a plastic response: how submergence-induced leaf elongation in Rumex palustris depends on light and nutrient availability in its early life stage. New Phytologist 194, 572–582.
| Plasticity as a plastic response: how submergence-induced leaf elongation in Rumex palustris depends on light and nutrient availability in its early life stage.Crossref | GoogleScholarGoogle Scholar |
Jensen CR, Luxmoore RJ, van Gundy SD, Stolzy LH (1969) Root air measurements by a pycnometer method. Agronomy Journal 61, 474–475.
| Root air measurements by a pycnometer method.Crossref | GoogleScholarGoogle Scholar |
Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytologist 106, 465–495.
| The anatomical characteristics of roots and plant response to soil flooding.Crossref | GoogleScholarGoogle Scholar |
Kester D, Duedall IW, Connors DN, Pytkowicz RM (1967) Preparation of artificial seawater. Limnology and Oceanography 12, 176–179.
| Preparation of artificial seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXhtFylur0%3D&md5=f85de663f8fd3e919f2bded70cbf9b66CAS |
Konnerup D, Moir-Barnetson L, Pedersen O, Veneklaas EJ, Colmer TD (2015) Contrasting submergence tolerance in two species of stem-succulent halophytes is not determined by differences in stem internal oxygen dynamics. Annals of Botany 115, 409–418.
| Contrasting submergence tolerance in two species of stem-succulent halophytes is not determined by differences in stem internal oxygen dynamics.Crossref | GoogleScholarGoogle Scholar |
Lang F, von der Lippe M, Schimpel S, Scozzafava-Jaeger T, Straub W (2010) Topsoil morphology indicates bio-effective redox conditions in Venice salt marshes. Estuarine, Coastal and Shelf Science 87, 11–20.
| Topsoil morphology indicates bio-effective redox conditions in Venice salt marshes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVart7g%3D&md5=9b5f8145bb233269e250e18b03aac217CAS |
Loreti E, van Veen H, Perata P (2016) Plant responses to flooding stress. Current Opinion in Plant Biology 33, 64–71.
| Plant responses to flooding stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XpvFaqtbw%3D&md5=4e6412b3e06290e292c31626929cc2e1CAS |
McKee KL, Patrick WH (1988) The relationship of smooth cordgrass (Spartina alterniflora) to tidal datums: a review. Estuaries 11, 143–151.
| The relationship of smooth cordgrass (Spartina alterniflora) to tidal datums: a review.Crossref | GoogleScholarGoogle Scholar |
Millero FJ (2010) Carbonate constants for estuarine waters. Marine and Freshwater Research 61, 139–142.
| Carbonate constants for estuarine waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFyns7o%3D&md5=a2daa9c2e58e5e8f391523cd56f0482fCAS |
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.
| Submergence-induced leaf acclimation in terrestrial species varying in flooding tolerance.Crossref | GoogleScholarGoogle Scholar |
Pandža M, Franjić J, Škvorc Ž (2007) The salt marsh vegetation on the East Adriatic coast. Biologia 62, 24–31.
| The salt marsh vegetation on the East Adriatic coast.Crossref | GoogleScholarGoogle Scholar |
Pedersen O, Vos H, Colmer TD (2006) Oxygen dynamics during submergence in the halophytic stem succulent Halosarcia pergranulata. Plant, Cell & Environment 29, 1388–1399.
| Oxygen dynamics during submergence in the halophytic stem succulent Halosarcia pergranulata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVGjs74%3D&md5=4f7c1849dac234e8b524e219687b12c4CAS |
Pedersen O, Colmer TD, Sand-Jensen K (2013) Underwater photosynthesis of submerged plants - recent advances and methods. Frontiers in Plant Science 4, 1–19.
Perata P, Armstrong W, Voesenek LACJ (2011) Plants and flooding stress. New Phytologist 190, 269–273.
| Plants and flooding stress.Crossref | GoogleScholarGoogle Scholar |
Ponnamperuma F (1984) Effects of flooding on soils. In ‘Flooding and plant growth’. (Ed. Kozlowski T) pp. 9–45 (Academic Press: New York)
R Core Team (2013) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna) Available at http://www.R-project.org/ [Verified 6 May 2017].
Raskin I (1983) A method for measuring leaf volume, density, thickness and internal gas volume. HortScience 18, 698–699.
Redondo-Gómez S, Mateos-Naranjo E, Davy AJ, Fernández-Muñoz F, Castellanos EM, Luque T, Figueroa ME (2007) Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. Annals of Botany 100, 555–563.
| Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides.Crossref | GoogleScholarGoogle Scholar |
Rich SM, Pedersen O, Ludwig M, Colmer TD (2013) Shoot atmospheric contact is of little importance to aeration of deeper portions of the wetland plant Meionectes brownii; submerged organs mainly acquire O2 from the water column or produce it endogenously in underwater photosynthesis. Plant, Cell & Environment 36, 213–223.
| Shoot atmospheric contact is of little importance to aeration of deeper portions of the wetland plant Meionectes brownii; submerged organs mainly acquire O2 from the water column or produce it endogenously in underwater photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhsl2lsrrO&md5=926fe065b77250ef7a458d054fb1ed6cCAS |
Rivoal J, Hanson AD (1993) Evidence for a large and sustained glycolytic flux to lactate in anoxic roots of some members of the halophytic genus Limonium. Plant Physiology 101, 553–560.
| Evidence for a large and sustained glycolytic flux to lactate in anoxic roots of some members of the halophytic genus Limonium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhsVemtLY%3D&md5=4ec4c90f2e924016a088fa95f6e67c0dCAS |
Sarretta A, Pillon S, Molinaroli E, Guerzoni S, Fontolan G (2010) Sediment budget in the Lagoon of Venice, Italy. Continental Shelf Research 30, 934–949.
| Sediment budget in the Lagoon of Venice, Italy.Crossref | GoogleScholarGoogle Scholar |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKntb7P&md5=d0e047c13797abd8a794b8b1e00e9cedCAS |
Silvestri S, Defina A, Marani M (2005) Tidal regime, salinity and salt marsh plant zonation. Estuarine, Coastal and Shelf Science 62, 119–130.
| Tidal regime, salinity and salt marsh plant zonation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKmtLfL&md5=e104b5bb3f42a5c179bd4cd3e84c9951CAS |
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.
| Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat.Crossref | GoogleScholarGoogle Scholar |
Visser EJW, Voesenek LACJ, Vartapetian BB, Jackson MB (2003) Flooding and plant growth. Annals of Botany 91, 107–109.
| Flooding and plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVCks7k%3D&md5=4a94ef9e1bb5de97b4268c457304d140CAS |
Vittori Antisari L, De Nobili M, Ferronato C, Natale M, Pellegrini E, Vianello G (2016) Hydromorphic to subaqueous soils transitions in the central Grado lagoon (Northern Adriatic Sea, Italy). Estuarine, Coastal and Shelf Science 173, 39–48.
| Hydromorphic to subaqueous soils transitions in the central Grado lagoon (Northern Adriatic Sea, Italy).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktFGks7g%3D&md5=2816e224b12a49b5a3648a854fb43077CAS |
White AC, Colmer TD, Cawthray GR, Hanley ME (2014) Variable response of three Trifolium repens ecotypes to soil flooding by seawater. Annals of Botany 114, 347–355.
| Variable response of three Trifolium repens ecotypes to soil flooding by seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ygtL%2FP&md5=83eb54f2ce51a76fdbc28c770beb536fCAS |
Winkel A, Borum J (2009) Use of sediment CO2 by submersed rooted plants. Annals of Botany 103, 1015–1023.
| Use of sediment CO2 by submersed rooted plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsFWgtbc%3D&md5=90ede3b918c61f5708fe7dcc73fcd70bCAS |
