Shaking off the blow: plant adjustments during submergence and post-stress growth in Lotus forage species

Florencia B. Buraschi; Federico P. O. Mollard; Carla E. Di Bella; Agustín A. Grimoldi; Gustavo G. Striker

doi:10.1071/FP23172

RESEARCH ARTICLE (Open Access)

Previous Next Contents Vol 51(1)

Shaking off the blow: plant adjustments during submergence and post-stress growth in Lotus forage species

Florencia B. Buraschi

^A ^B ^* , Federico P. O. Mollard

^A ^B , Carla E. Di Bella

^A ^C , Agustín A. Grimoldi

^A ^C and Gustavo G. Striker

^A ^B ^D ^*

+ Author Affiliations

- Author Affiliations

^A IFEVA, Universidad de Buenos Aires, CONICET, Facultad de Agronomía, Avenida San Martín 4453, Buenos Aires C1417DSE, Argentina.

^B Cátedra de Fisiología Vegetal, Departamento Biología Aplicada y Alimentos, Facultad de Agronomía, Universidad de Buenos Aires, Buenos Aires, Argentina.

^C Cátedra de Forrajicultura, Departamento de Producción Animal, Facultad de Agronomía, Universidad de Buenos Aires, Buenos Aires, Argentina.

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

^* Correspondence to: fburaschi@agro.uba.ar, gustavo.striker@uwa.edu.au

Handling Editor: Ole Pedersen

Functional Plant Biology 51, FP23172 https://doi.org/10.1071/FP23172

Submitted: 3 August 2023 Accepted: 20 September 2023 Published: 10 October 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Flooding significantly hampers global forage production. In flood-prone regions, Lotus tenuis and Lotus corniculatus are common forage legumes, yet little is known about their responses to partial or complete submergence. To address this, we evaluated 10 Lotus accessions subjected to 11 days of either partial or complete submergence, analysing growth traits related to tolerance and recovery after de-submergence. Principal component analyses revealed that submergence associated growth parameters were linked to L. corniculatus accessions, whereas recovery was associated with L. tenuis accessions. Notably, in L. tenuis, recovery from complete submergence positively correlated with leaf mass fraction but negatively with root mass fraction, showing an opposite pattern than in L. corniculatus. Encouragingly, no trade-off was found between inherent growth capacity and submergence tolerance (both partial and complete) or recovery ability, suggesting genetic selection for increased tolerance would not compromise growth potential. L. tenuis exhibited accessions with both partial and complete submergence tolerance, making them versatile for flood-prone environments, whereas L. corniculatus accessions were better suited for partial submergence. These findings offer valuable insights to enhance forage production in flood-prone areas and guide the selection of appropriate Lotus accessions for specific flood conditions.

Keywords: complete submergence, correlations, Lotus corniculatus, Lotus tenuis, partial submergence, PCA, recovery, submergence tolerance.

References

Antonelli CJ, Calzadilla PI, Vilas JM, Campestre MP, Escaray FJ, Ruiz OA (2019) Physiological and anatomical traits associated with tolerance to long-term partial submergence stress in the Lotus genus: responses of forage species, a model and an interspecific hybrid. Journal of Agronomy and Crop Science 205, 65-76.
| Crossref | Google Scholar |

Artola A, de los Santos GG, Castañeda GC (2003) A seed vigour test for birdsfoot trefoil (Lotus corniculatus L.). Seed Science and Technology 31, 753-757.
| Crossref | Google Scholar |

Assmann SM (2013) Natural variation in abiotic stress and climate change responses in Arabidopsis: implications for twenty-first-century agriculture. International Journal of Plant Sciences 174, 3-26.
| Crossref | Google Scholar |

Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313-339.
| Crossref | Google Scholar | PubMed |

Buraschi FB, Mollard FPO, Grimoldi AA, Striker GG (2020) Eco-physiological traits related to recovery from complete submergence in the model legume Lotus japonicus. Plants 9, 538.
| Crossref | Google Scholar | PubMed |

Chapin FS, III, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. The American Naturalist 142, S78-S92.
| Crossref | Google Scholar |

Chapman SC, Chakraborty S, Dreccer MF, Howden SM (2012) Plant adaptation to climate change – opportunities and priorities in breeding. Crop & Pasture Science 63, 251-268.
| Crossref | Google Scholar |

Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665-681.
| Crossref | Google Scholar | PubMed |

Dear BS, Moore GA, Hughes SJ (2003) Adaptation and potential contribution of temperate perennial legumes to the southern Australian wheatbelt: a review. Australian Journal of Experimental Agriculture 43, 1-18.
| Crossref | Google Scholar |

Di Bella CE, Kotula L, Striker GG, Colmer TD (2020) Submergence tolerance and recovery in Lotus: variation among fifteen accessions in response to partial and complete submergence. Journal of Plant Physiology 249, 153180.
| Crossref | Google Scholar | PubMed |

Escaray FJ, Menendez AB, Gárriz A, Pieckenstain FL, Estrella MJ, Castagno LN, Carrasco P, Sanjuán J, Ruiz OA (2012) Ecological and agronomic importance of the plant genus Lotus. Its application in grassland sustainability and the amelioration of constrained and contaminated soils. Plant Science 182, 121-133.
| Crossref | Google Scholar | PubMed |

Escaray FJ, Antonelli CJ, Carrasco P, Ruiz OA (2019) Interspecific hybridization improves the performance of Lotus spp. under saline stress. Plant Science 283, 202-210.
| Crossref | Google Scholar | PubMed |

Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiology 131, 872-877.
| Crossref | Google Scholar | PubMed |

Hunt R (1982) ‘Plant growth curves: the functional approach to plant growth analysis.’ (Edward Arnold: London, UK)

James EK, Crawford RMM (1998) Effect of oxygen availability on nitrogen fixation by two Lotus species under flooded conditions. Journal of Experimental Botany 49, 599-609.
| Crossref | Google Scholar |

Kundzewicz ZW, Su B, Wang Y, Wang G, Wang G, Huang J, Jiang T (2019) Flood risk in a range of spatial perspectives–from global to local scales. Natural Hazards and Earth System Sciences 19, 1319-1328.
| Crossref | Google Scholar |

Luo F-L, Nagel KA, Zeng B, Schurr U, Matsubara S (2009) Photosynthetic acclimation is important for post-submergence recovery of photosynthesis and growth in two riparian species. Annals of Botany 104, 1435-1444.
| Crossref | Google Scholar | PubMed |

Manzur ME, Grimoldi AA, Insausti P, Striker GG (2009) Escape from water or remain quiescent? Lotus tenuis changes its strategy depending on depth of submergence. Annals of Botany 104, 1163-1169.
| Crossref | Google Scholar | PubMed |

Marinoni L, Zabala JM, Patiño J, Pensiero JF (2017) Efecto de la temperatura y salinidad en la germinación y crecimiento inicial de un material naturalizado de Lotus tenuis Waldst. & Kit. Fave Sección Ciencias Agrarias 16, 47-60 [In Spanish].
| Google Scholar |

Menon-Martínez FE, Grimoldi AA, Striker GG, Di Bella CE (2021) Variability among Festuca arundinacea cultivars for tolerance to and recovery from waterlogging, salinity and their combination. Crop & Pasture Science 72, 75-84.
| Crossref | Google Scholar |

Nasrullah , Ali S, Umar M, Sun L, Naeem M, Yasmin H, Khan N (2022) Flooding tolerance in plants: from physiological and molecular perspectives. Brazilian Journal of Botany 45, 1161-1176.
| Crossref | Google Scholar |

Nichols P, Craig A, Bonython A, Rogers M-J, Ballard R, Charman N, Hughes S, Colmer T, McClements D, Barrett-Lennard E (2010) Development of Melilotus siculus – a new salt and waterlogging-tolerant annual fodder legume species for Mediterranean-type climates. In ‘Sustainable use of genetic diversity in forage and turf breeding’. (Ed. C Huyghe) pp. 131–135. (Springer: Dordrecht, Netherlands)

Nichols PGH, Revell CK, Humphries AW, Howie JH, Hall EJ, Sandral GA, Ghamkhar K, Harris CA (2012) Temperate pasture legumes in Australia – their history, current use, and future prospects. Crop & Pasture Science 63, 691-725.
| Crossref | Google Scholar |

Pajuelo E, Stougaard J (2005) Lotus japonicus’s a model system. In ‘Lotus japonicus Handbook’. (Ed. AJ Márquez) pp. 3–24. (Springer: Dordrecht, Netherlands)

Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO₂, nutrients and water: a quantitative review. Functional Plant Biology 27, 1191.
| Crossref | Google Scholar |

Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193, 30-50.
| Crossref | Google Scholar | PubMed |

Rebuffo M (1998) Lotus corniculatus INIA Draco; características agronómicas. In ‘Jornada de Lechería y Pasturas’. pp. 103–106. (Instituto Nacional de Investigación Agropecuaria, INIA: Montevideo, Uruguay)

Sasidharan R, Bailey-Serres J, Ashikari M, Atwell BJ, Colmer TD, Fagerstedt K, Fukao T, Geigenberger P, Hebelstrup KH, Hill RD, Holdsworth MJ, Ismail AM, Licausi F, Mustroph A, Nakazono M, Pedersen O, Perata P, Sauter M, Shih M-C, Sorrell BK, Striker GG, van Dongen JT, Whelan J, Xiao S, Visser EJW, Voesenek LACJ (2017) Community recommendations on terminology and procedures used in flooding and low oxygen stress research. New Phytologist 214, 1403-1407.
| Crossref | Google Scholar | PubMed |

Sasidharan R, Hartman S, Liu Z, Martopawiro S, Sajeev N, van Veen H, Yeung E, Voesenek LACJ (2018) Signal dynamics and interactions during flooding stress. Plant Physiology 176, 1106-1117.
| Crossref | Google Scholar | PubMed |

Signorelli S, Corpas FJ, Borsani O, Barroso JB, Monza J (2013) Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus. Plant Science 201-202, 137-146.
| Crossref | Google Scholar | PubMed |

Sivakumaran S, Rumball W, Lane GA, Fraser K, Foo LY, Yu M, Meagher LP (2006) Variation of proanthocyanidins in Lotus species. Journal of Chemical Ecology 32, 1797-1816.
| Crossref | Google Scholar | PubMed |

Steffens B, Steffen-Heins A, Sauter M (2013) Reactive oxygen species mediate growth and death in submerged plants. Frontiers in Plant Science 4, 179.
| Crossref | Google Scholar | PubMed |

Striker GG (2012) Time is on our side: the importance of considering a recovery period when assessing flooding tolerance in plants. Ecological Research 27, 983-987.
| Crossref | Google Scholar |

Striker GG, Colmer TD (2017) Flooding tolerance of forage legumes. Journal of Experimental Botany 68, 1851-1872.
| Crossref | Google Scholar | PubMed |

Striker GG, Ploschuk RA (2018) Recovery from short-term complete submergence in temperate pasture grasses. Crop & Pasture Science 69, 745-753.
| Crossref | Google Scholar |

Striker GG, Insausti P, Grimoldi AA, Ploschuk EL, Vasellati V (2005) Physiological and anatomical basis of differential tolerance to soil flooding of Lotus corniculatus L. and Lotus glaber Mill. Plant and Soil 276, 301-311.
| Crossref | Google Scholar |

Striker GG, Insausti P, Grimoldi AA (2008) Flooding effects on plants recovering from defoliation in Paspalum dilatatum and Lotus tenuis. Annals of Botany 102, 247-254.
| Crossref | Google Scholar | PubMed |

Striker GG, Manzur ME, Grimoldi AA (2011) Increasing defoliation frequency constrains regrowth of the forage legume Lotus tenuis under flooding. The role of crown reserves. Plant and Soil 343, 261-272.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar | PubMed |

Striker GG, Casas C, Manzur ME, Ploschuk RA, Casal JJ (2014) Phenomic networks reveal largely independent root and shoot adjustment in waterlogged plants of Lotus japonicus. Plant, Cell & Environment 37, 2278-2293.
| Crossref | Google Scholar | PubMed |

Striker GG, Casas C, Kuang X, Grimoldi AA (2017) No escape? Costs and benefits of leaf de-submergence in the pasture grass Chloris gayana under different flooding regimes. Functional Plant Biology 44, 899-906.
| Crossref | Google Scholar | PubMed |

Striker GG, Kotula L, Colmer TD (2019) Tolerance to partial and complete submergence in the forage legume Melilotus siculus: an evaluation of 15 accessions for petiole hyponastic response and gas-filled spaces, leaf hydrophobicity and gas films, and root phellem. Annals of Botany 123, 169-180.
| Crossref | Google Scholar | PubMed |

Teakle NL, Real D, Colmer TD (2006) Growth and ion relations in response to combined salinity and waterlogging in the perennial forage legumes Lotus corniculatus and Lotus tenuis. Plant and Soil 289, 369-383.
| Crossref | Google Scholar |

Voesenek LACJ, Bailey-Serres J (2013) Flooding tolerance: O₂ sensing and survival strategies. Current Opinion in Plant Biology 16, 647-653.
| Crossref | Google Scholar | PubMed |

Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytologist 170, 213-226.
| Crossref | Google Scholar | PubMed |

Weih M (2001) Evidence for increased sensitivity to nutrient and water stress in a fast-growing hybrid willow compared with a natural willow clone. Tree Physiology 21, 1141-1148.
| Crossref | Google Scholar | PubMed |

Wilson JB (1988) Shoot competition and root competition. Journal of Applied Ecology 25, 279-296.
| Crossref | Google Scholar |