Leaf gas film retention during submergence of 14 cultivars of wheat (Triticum aestivum)
Dennis Konnerup A B , Anders Winkel A , Max Herzog A and Ole Pedersen AA Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, Universitetsparken 4, 3rd floor, 2100 Copenhagen, Denmark.
B Corresponding author. Email: dennis.konnerup@bio.ku.dk
Functional Plant Biology 44(9) 877-887 https://doi.org/10.1071/FP16401
Submitted: 10 November 2016 Accepted: 31 January 2017 Published: 23 March 2017
Abstract
Flooding of fields after sudden rainfall events can result in crops being completely submerged. Some terrestrial plants, including wheat (Triticum aestivum L.), possess superhydrophobic leaf surfaces that retain a thin gas film when submerged, and the gas films enhance gas exchange with the floodwater. However, the leaves lose their hydrophobicity during submergence, and the gas films subsequently disappear. We tested gas film retention time of 14 different wheat cultivars and found that wheat could retain the gas films for a minimum of 2 days, whereas the wild wetland grass Glyceria fluitans (L.) R.Br. had thicker gas films and could retain its gas films for a minimum of 4 days. Scanning electron microscopy showed that the wheat cultivars and G. fluitans possessed high densities of epicuticular wax platelets, which could explain their superhydrophobicity. However, G. fluitans also had papillae that contributed to higher hydrophobicity during the initial submergence and could explain why G. fluitans retained gas films for a longer period of time. The loss of gas films was associated with the leaves being covered by an unidentified substance. We suggest that leaf gas film is a relevant trait to use as a selection criterion to improve the flood tolerance of crops that become temporarily submerged.
Additional keywords: air film, flooding, underwater photosynthesis, wettability.
References
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 |
Bailey-Serres J, Lee SC, Brinton E (2012) Waterproofing crops: effective flooding survival strategies. Plant Physiology 160, 1698–1709.
| Waterproofing crops: effective flooding survival strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKmt73E&md5=837dcf1844c946482fb56732ab57bcb5CAS |
Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society 126, 237–260.
| Classification and terminology of plant epicuticular waxes.Crossref | GoogleScholarGoogle Scholar |
Barthlott W, Schimmel T, Wiersch S, Koch K, Brede M, Barczewski M, Walheim S, Weis A, Kaltenmaier A, Leder A (2010) The Salvinia paradox: superhydrophobic surfaces with hydrophilic pins for air retention under water. Advanced Materials 22, 2325–2328.
| The Salvinia paradox: superhydrophobic surfaces with hydrophilic pins for air retention under water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntVyjtLY%3D&md5=33fd98d8b8c637a345ee57b176b1a4abCAS |
Bhushan B, Jung YC (2008) Wetting, adhesion and friction of superhydrophobic and hydrophilic leaves and fabricated micro/nanopatterned surfaces. Journal of Physics Condensed Matter 20, 225010
| Wetting, adhesion and friction of superhydrophobic and hydrophilic leaves and fabricated micro/nanopatterned surfaces.Crossref | GoogleScholarGoogle Scholar |
Brewer CA, Smith WK (1997) Patterns of leaf surface wetness for montane and subalpine plants. Plant, Cell & Environment 20, 1–11.
| Patterns of leaf surface wetness for montane and subalpine plants.Crossref | GoogleScholarGoogle Scholar |
Cerman Z, Striffler BF, Barthlott W (2009) Dry in the water: the superhydrophobic water fern Salvinia – a model for biomimetic surfaces. In ‘Functional surfaces in biology’. (Ed. SN Gorb) pp. 97–111. (Springer: Berlin)
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, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62, 39–57.
| Ion transport in seminal and adventitious roots of cereals during O2 deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurnE&md5=99126213578359bcfb5543995a40fdd2CAS |
Colmer TD, Pedersen O (2008) Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange. New Phytologist 177, 918–926.
| Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVSnsLo%3D&md5=78dfa1f650f746deff73ab47902b25abCAS |
Colmer TD, Winkel A, Pedersen O (2011) A perspective on underwater photosynthesis in submerged terrestrial wetland plants. AoB Plants 2011, plr030
| A perspective on underwater photosynthesis in submerged terrestrial wetland plants.Crossref | GoogleScholarGoogle Scholar |
Ensikat HJ, Ditsche-Kuru P, Neinhuis C, Barthlott W (2011) Superhydrophobicity in perfection: the outstanding properties of the lotus leaf. Beilstein Journal of Nanotechnology 2, 152–161.
| Superhydrophobicity in perfection: the outstanding properties of the lotus leaf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFaqtr0%3D&md5=805bbc821ce93f6a38d6ca812b12e711CAS |
Herzog M, Konnerup D, Pedersen O, Winkel A, Colmer TD (2016a) Leaf gas films contribute to rice (Oryza sativa) submergence tolerance during saline floods. Plant, Cell & Environment
| Leaf gas films contribute to rice (Oryza sativa) submergence tolerance during saline floods.Crossref | GoogleScholarGoogle Scholar |
Herzog M, Striker GG, Colmer TD, Pedersen O (2016b) Mechanisms of waterlogging tolerance in wheat – a review of root and shoot physiology. Plant, Cell & Environment 39, 1068–1086.
| Mechanisms of waterlogging tolerance in wheat – a review of root and shoot physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlvVaitLg%3D&md5=508e5fcf5d45eb9688a05ead789d2847CAS |
Huang B, Johnson JW (1995) Root respiration and carbohydrate status of two wheat genotypes in response to hypoxia. Annals of Botany 75, 427–432.
| Root respiration and carbohydrate status of two wheat genotypes in response to hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsVKjtb0%3D&md5=7540b9b5320cf71d380cb6f63f6bc48eCAS |
Huang B, Johnson JW, Box JE, NeSmith DS (1997) Root characteristics and hormone activity of wheat in response to hypoxia and ethylene. Crop Science 37, 812–818.
| Root characteristics and hormone activity of wheat in response to hypoxia and ethylene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkt1Olu7Y%3D&md5=bfdfc7aa6f2b82a5f6edc87988de67e6CAS |
Koch K, Barthlott W (2009) Superhydrophobic and superhydrophilic plant surfaces: an inspiration for biomimetic materials. Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences 367, 1487–1509.
| Superhydrophobic and superhydrophilic plant surfaces: an inspiration for biomimetic materials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvVWhtLo%3D&md5=a5d681ef9eb604b18cf39b9b8193592cCAS |
Koch K, Ensikat H-J (2008) The hydrophobic coatings of plant surfaces: epicuticular wax crystals and their morphologies, crystallinity and molecular self-assembly. Micron (Oxford, England) 39, 759–772.
| The hydrophobic coatings of plant surfaces: epicuticular wax crystals and their morphologies, crystallinity and molecular self-assembly.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Wgtrc%3D&md5=711c4abf041f3a51932bbb94d9e4be18CAS |
Koch K, Hartmann KD, Schreiber L, Barthlott W, Neinhuis C (2006) Influences of air humidity during the cultivation of plants on wax chemical composition, morphology and leaf surface wettability. Environmental and Experimental Botany 56, 1–9.
| Influences of air humidity during the cultivation of plants on wax chemical composition, morphology and leaf surface wettability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhtlaktro%3D&md5=257bd4a7676a168f6cb95f00c00a816cCAS |
Koch K, Bhushan B, Barthlott W (2008) Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4, 1943–1963.
| Diversity of structure, morphology and wetting of plant surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFemurfK&md5=06e1fa0c61b1f8fbfa2d55feb1270a8cCAS |
Konnerup D, Malik AI, Islam AKMR, Colmer TD (2017) Evaluation of root porosity and radial oxygen loss of disomic addition lines of Hordeum marinum in wheat. Functional Plant Biology 44, 400–409.
| Evaluation of root porosity and radial oxygen loss of disomic addition lines of Hordeum marinum in wheat.Crossref | GoogleScholarGoogle Scholar |
Mackereth FJH, Heron J, Talling JF (1978) Water analysis: some revised methods for limnologists. Freshwater Biological Association Publication No. 36. (Springer-Verlag: Berlin)
Mackinney G (1941) Absorption of light by chlorophyll solutions. The Journal of Biological Chemistry 140, 315–322.
Malik AI, Islam AKMR, Colmer TD (2011) Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum–wheat amphiploids. New Phytologist 190, 499–508.
| Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum–wheat amphiploids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MzjvFaruw%3D%3D&md5=fe4779c83550ce29003208c03015b52aCAS |
Mommer L, Visser EJW (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Annals of Botany 96, 581–589.
| Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitLnE&md5=dbfa0f2525706626807ea3ae67ecb8dbCAS |
Mommer L, Pons TL, Wolters-Arts M, Venema JH, Visser EJW (2005) Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance. Plant Physiology 139, 497–508.
| Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgurrL&md5=870040d339c792e9b0d41dedd56f573eCAS |
Mony C, Mercier E, Bonis A, Bouzille J-B (2010) Reproductive strategies may explain plant tolerance to inundation: a mesocosm experiment using six marsh species. Aquatic Botany 92, 99–104.
| Reproductive strategies may explain plant tolerance to inundation: a mesocosm experiment using six marsh species.Crossref | GoogleScholarGoogle Scholar |
Neinhuis C, Barthlott W (1997) Characterization and distribution of water-repellent, self-cleaning plant surfaces. Annals of Botany 79, 667–677.
| Characterization and distribution of water-repellent, self-cleaning plant surfaces.Crossref | GoogleScholarGoogle Scholar |
Neinhuis C, Koch K, Barthlott W (2001) Movement and regeneration of epicuticular waxes through plant cuticles. Planta 213, 427–434.
| Movement and regeneration of epicuticular waxes through plant cuticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvFGitL0%3D&md5=eb45eaab23ab87fa98563177c951d448CAS |
Parry ML (2007) ‘Climate change 2007-impacts, adaptation and vulnerability: Working Group II contribution to the fourth assessment report of the IPCC.’ (Cambridge University Press: Cambridge, UK)
Pedersen O, Colmer TD (2012) Physical gills prevent drowning of many wetland insects, spiders and plants. Journal of Experimental Biology 215, 705–709.
| Physical gills prevent drowning of many wetland insects, spiders and plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvFagsbg%3D&md5=aeb2ca11f52734000679f02d2d558524CAS |
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.
| Surviving floods: leaf gas films improve O2 and CO2 exchange, root aeration, and growth of completely submerged rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Cns70%3D&md5=3de0ee7e38b4bae2e2c6244c583ee3a9CAS |
Pedersen O, Colmer TD, Sand-Jensen K (2013) Underwater photosynthesis of submerged plants - recent advances and methods. Frontiers in Plant Science 4, 140
| Underwater photosynthesis of submerged plants - recent advances and methods.Crossref | GoogleScholarGoogle Scholar |
Ponnamperuma FN (1984) Effects of flooding on soils. In ‘Flooding and plant growth’. (Ed. T Kozlowski) pp. 9–45. (Academic Press: New York)
Raskin I (1983) A method for measuring leaf volume, density, thickness, and internal gas volume. HortScience 18, 698–699.
Raskin I, Kende H (1983) How does deep water rice solve its aeration problem. Plant Physiology 72, 447–454.
| How does deep water rice solve its aeration problem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXks1OksL8%3D&md5=fa2825475573ad32c63d4a010b2985e8CAS |
Sayre KD, Van Ginkel M, Rajaram S, Ortiz-Monasterio I (1994) Tolerance to waterlogging losses in spring bread wheat: effect of time of onset on expression. Annual Wheat Newsletter 40, 165–171.
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 |
Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant and Soil 253, 1–34.
| Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsb4%3D&md5=7473c39317add5fab1cf03665dbbbd5aCAS |
Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytologist 190, 289–298.
| Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1GktLg%3D&md5=1870a3095896d70bf8ac085e350612ecCAS |
Smart RM, Barko JW (1985) Laboratory culture of submersed freshwater macrophytes on natural sediments. Aquatic Botany 21, 251–263.
| Laboratory culture of submersed freshwater macrophytes on natural sediments.Crossref | GoogleScholarGoogle Scholar |
Stosch AK, Solga A, Steiner U, Oerke E-C, Barthlott W, Cermann Z (2007) Efficiency of self-cleaning properties in wheat (Triticum aestivum L.). Journal of Applied Botany and Food Quality 81, 49–55.
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 |
Trnka M, Rötter RP, Ruiz-Ramos M, Kersebaum KC, Olesen JE, Žalud Z, Semenov MA (2014) Adverse weather conditions for European wheat production will become more frequent with climate change. Nature Climate Change 4, 637–643.
| Adverse weather conditions for European wheat production will become more frequent with climate change.Crossref | GoogleScholarGoogle Scholar |
Verboven P, Pedersen O, Ho QT, Nicolai BM, Colmer TD (2014) The mechanism of improved aeration due to gas films on leaves of submerged rice. Plant, Cell & Environment 37, 2433–2452.
Winkel A, Colmer TD, Ismail AM, Pedersen O (2013) Internal aeration of paddy field rice (Oryza sativa) during complete submergence importance of light and floodwater O2. New Phytologist 197, 1193–1203.
| Internal aeration of paddy field rice (Oryza sativa) during complete submergence importance of light and floodwater O2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVOjurc%3D&md5=7c634649af48abfc283b2b6c01e9477eCAS |
Winkel A, Pedersen O, Ella E, Ismail AM, Colmer TD (2014) Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes. Journal of Experimental Botany 65, 3225–3233.
| Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1Wqu73P&md5=e206445114c1fbb62640e164bbd59414CAS |
Winkel A, Herzog M, Konnerup D, Fløytrup AH, Pedersen O (2017) Flood tolerance of wheat – the importance of leaf gas films during complete submergence. Functional Plant Biology 44, 888–898.
| Flood tolerance of wheat – the importance of leaf gas films during complete submergence.Crossref | GoogleScholarGoogle Scholar |