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RESEARCH ARTICLE
Contents Vol 51(12)

Submergence of forage legumes: Lotus species show better tolerance than Trifolium and Melilotus species due to their superior recovery after stress

Florencia B. Buraschi https://orcid.org/0009-0006-1170-5710 A B * , Federico P. O. Mollard https://orcid.org/0000-0002-1648-1983 A B , Gabriela Cordon A C , Agustín A. Grimoldi A D and Gustavo G. Striker A B E
+ Author Affiliations
- Author Affiliations

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

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

C Área de Educación Agropecuaria y Ambiental, Facultad de Agronomía, Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina.

D Cátedra de Forrajicultura, Departamento de Producción Animal, Facultad de Agronomía, Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina.

E 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

Handling Editor: Fanrong Zeng

Functional Plant Biology 51, FP24206 https://doi.org/10.1071/FP24206
Submitted: 14 August 2024  Accepted: 5 December 2024  Published: 23 December 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Climate change is leading to increased heavy rainfall, making plant submergence in flood-prone pastures more common. Forage legumes play a vital role in boosting herbage production and quality, especially when grown with grasses in low nitrogen input areas. However, their tolerance to complete submergence and subsequent recovery remains poorly understood. This study evaluated eight forage legumes after 5 or 10 days of complete submergence: (1)Lotus tenuis; (2) Lotus corniculatus; (3) Lotus japonicus; (4) Trifolium repens; (5) Trifolium fragiferum; (6) Trifolium pratense; (7) Trifolium michelianum; and (8) Melilotus albus. We assessed physiological and growth traits related to tolerance and recovery. All species survived except M. albus and T. michelianum. For the six surviving species, growth parameters linked to recovery were more prominent in Lotus species than in Trifolium species. Lotus species maintained higher biomass, improved stomatal conductance, and increased chlorophyll concentration in young leaves, along with a quicker recovery of PSII efficiency. In contrast, T. pratense showed the least tolerance and recovery, indicating its unsuitability for waterlogged areas. L. tenuis emerged as the most promising species for submergence tolerance, with L. corniculatus also showing potential, particularly in areas prone to short-term flooding.

Keywords: chlorophyll fluorescence, complete submergence, leaf greenness, Lotus species, plant growth, recovery, stomatal conductance, Trifolium species.

References

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

Barhoumi Z (2024) Effects of nitrogen deficiency on photosynthesis and chlorophyll a fluorescence attributes at two contrasting legume forages. Russian Journal of Plant Physiology 71, 1.
| Crossref | Google Scholar |

Bullard MJ, Crawford TJ (1995) Productivity of Lotus corniculatus L. (bird’s-foot trefoil) in the UK when grown under low-input conditions as spaced plants, monoculture swards or mixed swards. Grass and Forage Science 50(4), 439-446.
| Crossref | Google Scholar |

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(4), 538.
| Crossref | Google Scholar | PubMed |

Buraschi FB, Mollard FPO, Di Bella CE, Grimoldi AA, Striker GG (2024) Shaking off the blow: plant adjustments during submergence and post-stress growth in Lotus forage species. Functional Plant Biology 51, FP23172.
| Google Scholar |

Burdon JJ (1983) Trifolium repens L. Journal of Ecology 71(1), 307-330.
| Crossref | Google Scholar |

Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36(8), 665-681.
| Crossref | Google Scholar | PubMed |

Colmer TD, Winkel A, Pedersen O (2011) A perspective on underwater photosynthesis in submerged terrestrial wetland plants. AoB PLANTS 2011, plr030.
| Crossref | Google Scholar |

Craig AD (1998) Register of Australian herbage plant cultivars. B. Legumes. 1. Clover Trifolium michelianum Savi (balansa clover) cv. Bolta. Australian Journal of Experimental Agriculture 38(5), 531-532.
| Google Scholar |

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), 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 |

Díaz P, Borsani O, Monza J (2005) Lotus-related species and their agronomic importance. In ‘Lotus japonicus handbook’. (Ed. AJ Márquez) pp. 25–37. (Springer: Dordrecht)

Enkhbat G, Ryan MH, Foster KJ, Nichols PGH, Kotula L, Hamblin A, Inukai Y, Erskine W (2021) Large variation in waterlogging tolerance and recovery among the three subspecies of Trifolium subterranean L. is related to root and shoot responses. Plant and Soil 464, 467-487.
| Crossref | Google Scholar |

Gibberd MR, Cocks PS (1997) Effect of waterlogging and soil pH on the micro-distribution of naturalised annual legumes. Australian Journal of Agricultural Research 48(2), 223-230.
| Crossref | Google Scholar |

Gibberd MR, Colmer TD, Cocks PS (1999) Root porosity and oxygen movement in waterlogging-tolerant Trifolium tomentosum and -intolerant Trifolium glomeratum. Plant, Cell & Environment 22(9), 1161-1168.
| Crossref | Google Scholar |

Gibberd MR, Gray JD, Cocks PS, Colmer TD (2001) Waterlogging tolerance among a diverse range of Trifolium accessions is related to root porosity, lateral root formation and ‘aerotropic rooting’. Annals of Botany 88(4), 579-589.
| Crossref | Google Scholar |

Harrison SP, Bartlein PJ, Brewer S, Prentice IC, Boyd M, Hessler I, Holmgren K, Izumi K, Willis K (2014) Climate model benchmarking with glacial and mid-Holocene climates. Climate Dynamics 43, 671-688.
| Crossref | Google Scholar |

Harrison PA, Dunford RW, Holman IP, Rounsevell MDA (2016) Climate change impact modelling needs to include cross-sectoral interactions. Nature Climate Change 6, 885-890.
| Crossref | Google 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.
| Crossref | Google Scholar |

Huber H, Jacobs E, Visser EJW (2009) Variation in flooding-induced morphological traits in natural populations of white clover (Trifolium repens) and their effects on plant performance during soil flooding. Annals of Botany 103(2), 377-386.
| Crossref | Google Scholar | PubMed |

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

James EK, Crawford RMM (1998) Effect of oxygen availability on nitrogen fixation by two Lotus species under flooded conditions. Journal of Experimental Botany 49(320), 599-609.
| Crossref | Google Scholar |

Jones RM, Kersten SM (1992) Trifolium repens L. In ‘Plant Resources of South-East Asia No 4: Forages’. (Eds LT Mannetje, RM Jones) (PROSEA (Plant Resources of South-East Asia) Foundation): Bogor, Indonesia)

Jones DA, Turkington R (1986) Biological flora of the British Isles no. 163. Lotus corniculatus L. Journal of Ecology 74, 1185-1212.
| Google Scholar |

Kidd DR, Di Bella CE, Kotula L, Colmer TD, Ryan MH, Striker GG (2020) Defining the waterlogging tolerance of Ornithopus spp. for the temperate pasture zone of southern Australia. Crop and Pasture Science 71(5), 506-516.
| 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(7), 1435-1444.
| Crossref | Google Scholar | PubMed |

Luo F-L, Nagel KA, Scharr H, Zeng B, Schurr U, Matsubara S (2011) Recovery dynamics of growth, photosynthesis and carbohydrate accumulation after de-submergence: a comparison between two wetland plants showing escape and quiescence strategies. Annals of Botany 107(1), 49-63.
| 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(6), 1163-1169.
| Crossref | Google Scholar | PubMed |

Manzur ME, Grimoldi AA, Striker GG (2020) The forage grass Paspalum dilatatum tolerates partial but not complete submergence caused by either deep water or repeated defoliation. Crop and Pasture Science 71(2), 190-198.
| Crossref | Google Scholar |

Marten GC (1989) Breeding forage grasses to maximize animal performance. In ‘Contributions From breeding forage and turf grasses. Vol. 15’. (Eds DA Sleper, KH Asay, JF Pedersen) pp. 71–104. (CSSA Special Publications)

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. Journal of Experimental Botany 51(345), 659-668.
| Crossref | Google Scholar | PubMed |

Nichols PGH, Craig A, Bonython A, Rogers MJ, Ballard R, Charman N, Hughes S, Colmer TD, 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 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 and Pasture Science 63(9), 691-725.
| Crossref | Google Scholar |

Pajuelo E, Stougaard J (2005) Lotus japonicu’s as model system. In ‘Lotus japonicus handbook’. (Ed. AJ Márquez) pp. 3–24. (Springer)

Phelan P, Moloney AP, McGeough EJ, Humphreys J, Bertilsson J, O’Riordan EG, O’Kiely P (2015) Forage legumes for grazing and conserving in ruminant production systems. Critical Reviews in Plant Sciences 34(1–3), 281-326.
| Crossref | Google Scholar |

Rochon JJ, Doyle CJ, Greef JM, Hopkins A, Molle G, Sitzia M, Scholefield D, Smith CJ (2004) Grazing legumes in Europe: a review of their status, management, benefits, research needs and future prospects. Grass and Forage Science 59(3), 197-214.
| Crossref | Google Scholar |

Rogers ME, Noble CL (1991) The effect of NaCl on the establishment and growth of balansa clover (Trifolium michelianum Savi var. balansae Boiss.). Australian Journal of Agricultural Research 42(5), 847-857.
| Crossref | Google Scholar |

Rogers ME, West DW (1993) The effects of rootzone salinity and hypoxia on shoot and root growth in Trifolium species. Annals of Botany 72(5), 503-509.
| Crossref | Google Scholar |

Rogers ME, Colmer TD, Frost K, Henry D, Cornwall D, Hulm E, Deretic J, Hughes SR, Craig AD (2008) Diversity in the genus Melilotus for tolerance to salinity and waterlogging. Plant and Soil 304, 89-101.
| Crossref | Google Scholar |

Satell R, Dick R, Hemphill D, McGrath D (1998) Red clover (Trifolium pratense). In ‘Using cover crops in Oregon’. EM 8704 (Ed. O Corvallis) (Oregon State University Extension Services)

Simova-Stoilova L, Demirevska K, Kingston-Smith A, Feller U (2012) Involvement of the leaf antioxidant system in the response to soil flooding in two Trifolium genotypes differing in their tolerance to waterlogging. Plant Science 183, 43-49.
| Crossref | Google Scholar | PubMed |

Smetham ML (1973) Grazing management. In ‘Pastures and pasture plants’. (Ed. RHM Langer) pp. 179–228. (A.H. and A.W. Reed: London)

Smith RW, Penrose B, Langworthy AD, Humphries AW, Harris CA, Rogers ME, Nichols PGH, Hayes RC (2023) Strawberry clover (Trifolium fragiferum): current status and future role in Australian agriculture. Crop & Pasture Science 74, 680-699.
| Crossref | Google Scholar |

Sparrow EB, Sparrow SD, Cochran VL (1993) Phosphorus and nitrogen dynamics during field incubations in forest and fallow subarctic soils. Biology and Fertility of Soils 16, 243-248.
| Crossref | Google Scholar |

Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindjee) pp. 321–362. (Dordrecht: Springer Netherlands)

Striker GG (2012) Time is on our side: the importance of considering a recovery period when assessing flooding tolerance in plants. Ecological Research 27(5), 983-987.
| Crossref | Google Scholar |

Striker GG (2023) An overview of oxygen transport in plants: diffusion and convection. Plant Biology 25(6), 842-847.
| Crossref | Google Scholar | PubMed |

Striker GG, Colmer TD (2017) Flooding tolerance of forage legumes. Journal of Experimental Botany 68(8), 1851-1872.
| Crossref | Google Scholar | PubMed |

Striker GG, Ploschuk RA (2018) Recovery from short-term complete submergence in temperate pasture grasses. Crop and Pasture Science 69(7), 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, 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(1), 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(10), 2278-2293.
| Crossref | Google Scholar | PubMed |

Striker GG, Teakle NL, Colmer TD, Barrett-Lennard EG (2015) Growth responses of Melilotus siculus accessions to combined salinity and root-zone hypoxia are correlated with differences in tissue ion concentrations and not differences in root aeration. Environmental and Experimental Botany 109, 89-98.
| Crossref | Google Scholar |

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(1), 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, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytologist 170(2), 213-226.
| Crossref | Google Scholar | PubMed |

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(4), 1193-1203.
| Crossref | Google Scholar | PubMed |

Yeung E, Bailey-Serres J, Sasidharan R (2019) After the deluge: plant revival post-flooding. Trends in Plant Science 24(5), 443-454.
| Crossref | Google Scholar | PubMed |

Young ND, Cannon SB, Sato S, Kim D, Cook DR, Town CD, Roe BA, Tabata S (2005) Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiology 137(4), 1174-1181.
| Crossref | Google Scholar | PubMed |

Zhang Q, Huber H, Beljaars SJM, Birnbaum D, de Best S, de Kroon H, Visser EJW (2017) Benefits of flooding-induced aquatic adventitious roots depend on the duration of submergence: linking plant performance to root functioning. Annals of Botany 120(1), 171-180.
| Crossref | Google Scholar | PubMed |