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

Flood tolerance of wheat – the importance of leaf gas films during complete submergence

Anders Winkel A B , Max Herzog A , Dennis Konnerup A , Anja Heidi Floytrup A and Ole Pedersen A
+ Author Affiliations
- Author Affiliations

A The Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, Universitetsparken 4, 3rd floor, 2100 Copenhagen, Denmark.

B Corresponding author. Email: awinkel@bio.ku.dk

Functional Plant Biology 44(9) 888-898 https://doi.org/10.1071/FP16395
Submitted: 7 November 2016  Accepted: 23 March 2017   Published: 26 April 2017

Abstract

Submergence invokes a range of stressors to plants with impeded gas exchange between tissues and floodwater being the greatest challenge. Many terrestrial plants including wheat (Triticum aestivum L.), possess superhydrophobic leaf cuticles that retain a thin gas film when submerged, and the gas films enhance gas exchange with the floodwater. However, leaf hydrophobicity is lost during submergence and the gas films disappear accordingly. Here, we completely submerged wheat (with or without gas films) for up to 14 days and found that plants with gas films survived significantly longer (13 days) than plants without (10 days). Plants with gas films also had less dead tissue following a period of recovery. However, this study also revealed that reflections by gas films resulted in a higher light compensation point for underwater net photosynthesis for leaves with gas films compared with leaves without (IC = 52 vs 35 µmol photons m–2 s–1 with or without gas films, respectively). Still, already at ~5% of full sunlight the beneficial effect of gas films overcame the negative under ecologically relevant CO2 concentrations. Our study showed that dryland crops also benefit from leaf gas films during submergence and that this trait should be incorporated to improve flood tolerance of wheat.

Additional keywords: air film, flooding tolerance, hydrophobicity, underwater photosynthesis, underwater respiration, water repellent.


References

Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 225–332.
Aeration in higher plants.CrossRef | 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 | 1:CAS:528:DC%2BC38XhvVKmt73E&md5=837dcf1844c946482fb56732ab57bcb5CAS |

Barthlott W, Neinhuis C (1997) Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202, 1–8.
Purity of the sacred lotus, or escape from contamination in biological surfaces.CrossRef | 1:CAS:528:DyaK2sXjtFyis78%3D&md5=16392d235af6324185f363cf82cae877CAS |

Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Annals of Botany 91, 301–309.
Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.).CrossRef | 1:CAS:528:DC%2BD3sXitVCkt78%3D&md5=63f66fa158784ed44448aeebd00f0af9CAS |

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 | 1:CAS:528:DC%2BD1cXktVSnsLo%3D&md5=78dfa1f650f746deff73ab47902b25abCAS |

Colmer TD, Vos H, Pedersen O (2009) Tolerance of combined submergence and salinity in the halophytic stem-succulent Tecticornia pergranulata. Annals of Botany 103, 303–312.
Tolerance of combined submergence and salinity in the halophytic stem-succulent Tecticornia pergranulata.CrossRef | 1:CAS:528:DC%2BD1MXjsFCkuro%3D&md5=66b3b986efa9a8cffc35b52b7cf56e9bCAS |

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 |

Frost-Christensen H, Sand-Jensen K (1992) The quantum efficiency of photosynthesis in macroalgae and sumberged angiosperms. Oecologia 91, 377–384.
The quantum efficiency of photosynthesis in macroalgae and sumberged angiosperms.CrossRef | 1:STN:280:DC%2BC1czot1Smtw%3D%3D&md5=ca902712747cdec4e6a99edc148b7b79CAS |

Herzog M, Konnerup D, Pedersen O, Winkel A, Colmer TD (2016a) Role of leaf gas films in improving rice (Oryza sativa) submergence tolerance during saline floods. Plant, Cell & Environment
Role of leaf gas films in improving rice (Oryza sativa) submergence tolerance during saline floods.CrossRef |

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 | 1:CAS:528:DC%2BC28XlvVaitLg%3D&md5=508e5fcf5d45eb9688a05ead789d2847CAS |

Hunt R (1982) ‘Plant growth curves. The functional approach to 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.
Mathematical formulation of the relationship between photosynthesis and light for phytoplankton.CrossRef | 1:CAS:528:DyaE28XlvVaisbc%3D&md5=92dadcb93d2ddba68ca838d8da80acb9CAS |

Justin S, 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 |

Konnerup DW, Winkel A, Herzog M, Pedersen O (2017) Leaf gas film retention during submergence of 14 cultivars of wheat (Triticum aestivum). Functional Plant Biology
Leaf gas film retention during submergence of 14 cultivars of wheat (Triticum aestivum).CrossRef |

Maberly SC, Madsen TV (2002) Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. Functional Plant Biology 29, 393–405.
Freshwater angiosperm carbon concentrating mechanisms: processes and patterns.CrossRef | 1:CAS:528:DC%2BD38XjsVCltLo%3D&md5=5ec4a5c3a5f204d270c5896ba49d2f04CAS |

Madsen TV, Sand-Jensen K (1991) Photosynthetic carbon assimilation in aquatic macrophytes. Aquatic Botany 41, 5–40.
Photosynthetic carbon assimilation in aquatic macrophytes.CrossRef | 1:CAS:528:DyaK3MXmsFajtr8%3D&md5=e57d8cc86218ae14e192aaeaedbdad29CAS |

Madsen TV, Sand-Jensen K, Beer S (1993) Comparison of photosynthetic performance and carboxylation capacity in a range of aquatic macrophytes of different growth forms. Aquatic Botany 44, 373–384.
Comparison of photosynthetic performance and carboxylation capacity in a range of aquatic macrophytes of different growth forms.CrossRef | 1:CAS:528:DyaK3sXksVGgu78%3D&md5=4d8f23a8a58a1aceb6e89542e6e00ba7CAS |

Malik AI, Colmer TD, Lambers H, Schortemeyer M (2003) Aerenchyma formation and radial O2 loss along adventitious roots of wheat with only the apical root portion exposed to O2 deficiency. Plant, Cell and Environment 26, 1713–1722.
Aerenchyma formation and radial O2 loss along adventitious roots of wheat with only the apical root portion exposed to O2 deficiency.CrossRef |

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 |

Parry ML, Canziani OF, Palutikof JP, Van Der Linden PJ, Hanson CE (2006) ‘Climate change 2007: impacts, adaptation and vulnerability.’ (Cambridge University Press: Cambridge, UK)

Pedersen O, Colmer TD (2012) Physical gills prevent drowning of many wetland insects, spiders and plants. The Journal of Experimental Biology 215, 705–709.
Physical gills prevent drowning of many wetland insects, spiders and plants.CrossRef | 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 | 1:CAS:528:DC%2BD1MXks1Cns70%3D&md5=3de0ee7e38b4bae2e2c6244c583ee3a9CAS |

Pedersen O, Malik AI, Colmer TD (2010) Submergence tolerance in Hordeum marinum: dissolved CO2 determines underwater photosynthesis and growth. Functional Plant Biology 37, 524–531.
Submergence tolerance in Hordeum marinum: dissolved CO2 determines underwater photosynthesis and growth.CrossRef | 1:CAS:528:DC%2BC3cXmt12ksr8%3D&md5=6c49afb6b4a4f4823158101374e25727CAS |

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 | 1:CAS:528:DyaL3sXks1OksL8%3D&md5=fa2825475573ad32c63d4a010b2985e8CAS |

Setter TL, Waters I, Wallace I, Bekhasut P, Greenway H (1989) Submergence of rice. I. Growth and photosynthetic response to CO2 enrichment of floodwater. Australian Journal of Plant Physiology 16, 251–263.
Submergence of rice. I. Growth and photosynthetic response to CO2 enrichment of floodwater.CrossRef |

Singh S, Mackill DJ, Ismail AM (2009) Responses of SUB1 rice introgression lines to submergence in the field: yield and grain quality. Field Crops Research 113, 12–23.
Responses of SUB1 rice introgression lines to submergence in the field: yield and grain quality.CrossRef |

Striker G (2012) Time is on our side: the importance of considering a recovery period when assessing flooding tolerance in plants. Ecological Research 27, 983–987.
Time is on our side: the importance of considering a recovery period when assessing flooding tolerance in plants.CrossRef |

Stumm W, Morgan JJ (1996) ‘Chemical equilibria and rates in natural waters.’ (John Wiley & Sons Inc.: New York)

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.

Vervuren PJA, Blom CWPM, de Kroon H (2003) Extreme flooding events on the Rhine and the survival and distribution of riparian plant species. Journal of Ecology 91, 135–146.
Extreme flooding events on the Rhine and the survival and distribution of riparian plant species.CrossRef |

Waters I, Armstrong W, Thompson 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.
Diurnal changes in radial oxygen loss and ethanol-metabolism in roots of submerged and non-submerged rice seedlings.CrossRef | 1:CAS:528:DyaK3cXhsFGgsLk%3D&md5=9db970b8ba9eda1ab3759ecf9e0cd426CAS |

Winkel A, Colmer TD, Pedersen O (2011) Leaf gas films of Spartina anglica enhance rhizome and root oxygen during tidal submergence. Plant, Cell & Environment 34, 2083–2092.
Leaf gas films of Spartina anglica enhance rhizome and root oxygen during tidal submergence.CrossRef | 1:CAS:528:DC%2BC3MXhs1Glt7nJ&md5=20a9c218c7162f2b690d8e2052b3ed8bCAS |

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 | 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 |

Winkel A, Visser EJ, Colmer TD, Brodersen KP, Voesenek LA, Sand-Jensen K, Pedersen O (2016) Leaf gas films, underwater photosynthesis and plant species distributions in a flood gradient. Plant, Cell & Environment 39, 1537–1548.
Leaf gas films, underwater photosynthesis and plant species distributions in a flood gradient.CrossRef | 1:CAS:528:DC%2BC28XpsFejs7w%3D&md5=60774696f543dd1cfe600f1fcc66aa2aCAS |

Wintermans JFGM, De Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochimica et Biophysica Acta 109, 448–453.
Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol.CrossRef | 1:CAS:528:DyaF28XksFersw%3D%3D&md5=33563db6dfaf91066275b71f908620a4CAS |

Zhang Z, Cheng Z-J, Gan L, Zhang H, Wu F-Q, Lin Q-B, Wang J-L, Wang J, Guo X-P, Zhang X, Zhao Z-C, Lei C-L, Zhu S-S, Wang C-M, Wan J-M (2016) OsHSD1, a hydroxysteroid dehydrogenase, is involved in cuticle formation and lipid homeostasis in rice. Plant Science 249, 35–45.
OsHSD1, a hydroxysteroid dehydrogenase, is involved in cuticle formation and lipid homeostasis in rice.CrossRef | 1:CAS:528:DC%2BC28Xps12ntb4%3D&md5=994fddb2dbb2c0e687f2101150a41e27CAS |



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