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

No escape? Costs and benefits of leaf de-submergence in the pasture grass Chloris gayana under different flooding regimes

Gustavo G. Striker A B E F , Cecilia Casas C , Xiaolin Kuang A B and Agustín A. Grimoldi A D
+ Author Affiliations
- Author Affiliations

A IFEVA, Universidad de Buenos Aires, CONICET, Facultad de Agronomía, Avenuenida San Martín 4453, CPA 1417, DSE Buenos Aires, Argentina.

B Cátedra de Fisiología Vegetal, Facultad de Agronomía, Universidad de Buenos Aires. Av. San Martín 4453 (CPA 1417 DSE) Buenos Aires, Argentina.

C Cátedra de Edafología, Facultad de Agronomía, Universidad de Buenos Aires. Av. San Martín 4453 (CPA 1417 DSE) Buenos Aires, Argentina.

D Cátedra de Forrajicultura, Facultad de Agronomía, Universidad de Buenos Aires. Av. San Martín 4453 (CPA 1417 DSE) Buenos Aires, Argentina.

E School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

F Corresponding author. Email: striker@agro.uba.ar

Functional Plant Biology 44(9) 899-906 https://doi.org/10.1071/FP17128
Submitted: 2 May 2017  Accepted: 20 June 2017   Published: 21 July 2017

Abstract

Elongation-induced leaf emergence is one way for plants to deal with complete submergence by ‘escaping’ from water. This growth strategy is hypothesised to be more beneficial under single long-term submergence than under repeated short-term submergence events (i.e. fluctuating environment), as costs of repeated plant ‘adjustment’ would exceed the initial benefits of shoot elongation. To test this idea, 2-week-old plants of Chloris gayana Kunth. cv. Fine Cut (a submergence-tolerant cultivar first selected by a screening experiment) were grown for 4 weeks under (i) control conditions, (ii) two 1-week submergence cycles, or (iii) one 2-week submergence cycle. Additionally, a set of plants were placed below nettings to assess the cost of remaining forcedly submerged. Impeding leaves emergence through nettings did not compromise survival when submergence was 1-week long, but determined the death of all plants when extended to 2 weeks. Growth as affected by flooding regime revealed that under one 2-week submergence event, plants accumulated a 2.9-fold higher dry mass than when they experienced the same submergence duration in separate events along 1week. The ‘escape’ strategy in the grass C. gayana, by which leaf contact with air is re-established, is essential for its survival, and it is more beneficial for plant growth under long-term submergence than under repeated short-term submergence cycles.

Additional keywords: Chloris gayana cultivars, flooding timing, leaf desiccation, leaf greenness, plant recovery, Rhodes grass, shoot elongation.


References

Akman M, Bhikharie AV, McLean EH, Boonman A, Visser EJW, Schranz ME, van Tienderen PH (2012) Wait or escape? Contrasting submergence tolerance strategies of Rorippa amphibian, Rorippa sylvestris and their hybrid. Annals of Botany 109, 1263–1276.
Wait or escape? Contrasting submergence tolerance strategies of Rorippa amphibian, Rorippa sylvestris and their hybrid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvVOlsbc%3D&md5=07b7454eb9c778ba269772799a04b6e3CAS |

Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.
Flooding stress: acclimations and genetic diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsLc%3D&md5=d90a6c2ec0e60f70cf1ac88123e7f803CAS |

Boschma SP, Lodge GM, Harden S (2008) Herbage mass and persistence of pasture legumes and grasses at two potentially different saline and waterlogging sites in northern New South Wales. Australian Journal of Experimental Agriculture 48, 553–567.
Herbage mass and persistence of pasture legumes and grasses at two potentially different saline and waterlogging sites in northern New South Wales.Crossref | GoogleScholarGoogle Scholar |

Čatský J (1960) Determination of water deficits in discs cut out from leaf blades. Biologia Plantarum 2, 76–78.
Determination of water deficits in discs cut out from leaf blades.Crossref | GoogleScholarGoogle Scholar |

Chen X, Visser EJW, de Kroon H, Pierik R, Voesenek LACJ, Huber H (2011) Fitness consequences of natural variation in flooding-induced shoot elongation in Rumex palustris. New Phytologist 190, 409–420.
Fitness consequences of natural variation in flooding-induced shoot elongation in Rumex palustris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtlajsr8%3D&md5=f700e86d2d8f48a66c7997df8538bc07CAS |

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

Dear BS, Reed KFM, Craig AD (2008) Outcomes of the search for new perennial and salt tolerant pasture plants for southern Australia. Australian Journal of Experimental Agriculture 48, 578–588.
Outcomes of the search for new perennial and salt tolerant pasture plants for southern Australia.Crossref | GoogleScholarGoogle Scholar |

Di Bella CE, Striker GG, Loreti J, Cosentino DJ, Grimoldi AA (2016) Soil water regime of grassland communities along subtle topographic gradient in the flooding pampa (Argentina). Soil and Water Research 11, 90–96.
Soil water regime of grassland communities along subtle topographic gradient in the flooding pampa (Argentina).Crossref | GoogleScholarGoogle Scholar |

Fillery IRP, Vlek PLG (1982) The significance of denitrification of applied nitrogen in fallow and cropped rice soils under different flooding regimes. Plant and Soil 65, 153–169.
The significance of denitrification of applied nitrogen in fallow and cropped rice soils under different flooding regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XksFCksrg%3D&md5=80a1f6dafe7b2003c33bc330e2b3d8d8CAS |

Gautam P, Lal B, Tripathi R, Baig MJ, Shahid M, Maharana S, Bihari P, Nayak AK (2017) Impact of seedling age and nitrogen application on submergence tolerance of Sub1 and non-Sub1 cultivars of rice (Oryza sativa L.). Journal of Plant Growth Regulation
Impact of seedling age and nitrogen application on submergence tolerance of Sub1 and non-Sub1 cultivars of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |

Hirabayashi Y, Mahendran R, Koirala S, Konoshima L, Yamazaki D, Watanabe S, Kim H, Kanae S (2013) Global flood risk under climate change. Nature Climate Change 3, 816–821.
Global flood risk under climate change.Crossref | GoogleScholarGoogle Scholar |

Imaz JA, Gimenez DO, Grimoldi AA, Striker GG (2012) The effects of submergence on anatomical, morphological and biomass allocation responses of tropical grasses Chloris gayana and Panicum coloratum at seedling stage. Crop and Pasture Science 63, 1145–1155.
The effects of submergence on anatomical, morphological and biomass allocation responses of tropical grasses Chloris gayana and Panicum coloratum at seedling stage.Crossref | GoogleScholarGoogle Scholar |

Imaz JA, Gimenez DO, Grimoldi AA, Striker GG (2015) High recovery ability overrides the negative effects of flooding on growth of tropical grasses Chloris gayana and Panicum coloratum. Crop and Pasture Science 66, 100–106.

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 |

Malik AI, Colmer TD, Lambers H, Setter TL, Schortemeyer M (2002) Short-term waterlogging has long-term effects on the growth and physiology of wheat. New Phytologist 153, 225–236.
Short-term waterlogging has long-term effects on the growth and physiology of wheat.Crossref | GoogleScholarGoogle Scholar |

Malkin B, Waisel Y (1986) Mass selection for salt resistance in Rhodes grass (Chloris gayana). Physiologia Plantarum 66, 443–446.
Mass selection for salt resistance in Rhodes grass (Chloris gayana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhvVentrs%3D&md5=2ff30ced437a8fa8e7a074f478c5273cCAS |

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 |

Pierik R, van Aken JM, Voesenek LACJ (2009) Is elongation-induced leaf emergence beneficial for submerged Rumex species? Annals of Botany 103, 353–357.
Is elongation-induced leaf emergence beneficial for submerged Rumex species?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FmtFansw%3D%3D&md5=eafe5f9968ab7c9268a92ce9355a6ad2CAS |

Ponsens J, Hanson J, Schellberg J, Moeseler BM (2010) Characterization of phenotypic diversity, yield and response to drought stress in a collection of Rhodes grass (Chloris gayana Kunth) accessions. Field Crops Research 118, 57–72.
Characterization of phenotypic diversity, yield and response to drought stress in a collection of Rhodes grass (Chloris gayana Kunth) accessions.Crossref | GoogleScholarGoogle Scholar |

Ribotta A, Griffa S, Díaz D, Carloni E, López Colomba E, Tommasino E, Quiroga M, Luna C, Grunberg K (2013) Selecting salt-tolerant clones and evaluating genetic variability to obtain parents of new diploid and tetraploid germplasm in rhodesgrass (Chloris gayana K.). South African Journal of Botany 84, 88–93.
Selecting salt-tolerant clones and evaluating genetic variability to obtain parents of new diploid and tetraploid germplasm in rhodesgrass (Chloris gayana K.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnslOqtQ%3D%3D&md5=f5d6bd6682c98992a92dae1bd2821b7bCAS |

Rivera-Contreras IK, Zamora-Hernández T, Huerta-Heredia AA, Capataz-Tafur J, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM (2016) Transcriptomic analysis of submergence-tolerant and sensitive Brachypodium distachyon ecotypes reveals oxidative stress as a major tolerance factor. Scientific Reports 6, 27686
Transcriptomic analysis of submergence-tolerant and sensitive Brachypodium distachyon ecotypes reveals oxidative stress as a major tolerance factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XpvF2qurY%3D&md5=8c3b5b404347884788b897339d7de514CAS |

Sasidharan R, Voesenek LACJ (2015) Ethylene-mediated acclimations to flooding stress. Plant Physiology 169, 3–12.
Ethylene-mediated acclimations to flooding stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XkslOrsQ%3D%3D&md5=3f8c19fcb74f9afe8cac16ca534c4a8dCAS |

Setter TL, Laureles EV (1996) The beneficial effect of reduced elongation growth on submergence tolerance of rice. Journal of Experimental Botany 47, 1551–1559.
The beneficial effect of reduced elongation growth on submergence tolerance of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XntValtL0%3D&md5=2b2154c1aab4992b71dfedd4841d34fcCAS |

Setter TL, Bhekasut P, Greenway H (2010) Desiccation of leaves after de-submergence is one cause for intolerance to complete submergence of the rice cultivar IR 42. Functional Plant Biology 37, 1096–1104.
Desiccation of leaves after de-submergence is one cause for intolerance to complete submergence of the rice cultivar IR 42.Crossref | GoogleScholarGoogle Scholar |

Striker GG (2012a) Flooding stress on plants: anatomical, morphological and physiological responses. In ‘Botany Part I: adaptations and responses to environmental extremes’. pp. 3–28. (InTech Publisher: Rijeka, Croatia)

Striker GG (2012b) 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 | GoogleScholarGoogle Scholar |

Striker GG, Colmer TD (2017) Flooding tolerance of forage legumes. Journal of Experimental Botany 68, 1851–1872.

Striker GG, Manzur ME, Grimoldi AA (2011) Increasing defoliation frequency constrains regrowth of Lotus tenuis under flooding. The role of crown reserves. Plant and Soil 343, 261–272.
Increasing defoliation frequency constrains regrowth of Lotus tenuis under flooding. The role of crown reserves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFSksL8%3D&md5=38e73402e93b76e569b2adede9b4be36CAS |

Striker GG, Izaguirre RF, Manzur ME, Grimoldi AA (2012) Different strategies of Lotus japonicus, L. corniculatus and L. tenuis to deal with complete submergence at seedling stage. Plant Biology 14, 50–55.

Taleisnik E, Peyrano G, Córdoba A, Arias C (1999) Water retention capacity in root segments differing in the degree of exodermis development. Annals of Botany 83, 19–27.
Water retention capacity in root segments differing in the degree of exodermis development.Crossref | GoogleScholarGoogle Scholar |

van der Sman AJM, Joosten NN, Blom CWPM (1993) Flooding regimes and life-history characteristics of short-lived species in river forelands. Journal of Ecology 81, 121–130.
Flooding regimes and life-history characteristics of short-lived species in river forelands.Crossref | GoogleScholarGoogle Scholar |

Voesenek LACJ, Bailey-Serres J (2015) Air conditional. Nature Plants
Air conditional.Crossref | GoogleScholarGoogle Scholar |

Voesenek LACJ, Rijnders JHGM, Peeters AJM, van de Steeg HM, de Kroon H (2004) Plant hormones regulate fast shoot elongation under water: from genes to communities. Ecology 85, 16–27.
Plant hormones regulate fast shoot elongation under water: from genes to communities.Crossref | GoogleScholarGoogle Scholar |

Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytologist 170, 213–226.
How plants cope with complete submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltFamtLw%3D&md5=d00fab0c7667de204b8722ff9e4242a4CAS |