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

Waterlogging priming alleviates the oxidative damage, carbohydrate consumption, and yield loss in soybean (Glycine max) plants exposed to waterlogging

Darwin Alexis Pomagualli Agualongo https://orcid.org/0000-0001-9339-7665 A B # , Cristiane Jovelina Da-Silva https://orcid.org/0000-0003-3239-5927 A # * , Natália Garcia https://orcid.org/0000-0002-9154-7284 A , Fabiane Kletke de Oliveira https://orcid.org/0000-0002-6487-5397 A , Eduardo Pereira Shimoia https://orcid.org/0000-0002-2889-4259 A , Douglas Antônio Posso https://orcid.org/0000-0003-1560-2023 A , Ana Cláudia Barneche de Oliveira https://orcid.org/0000-0002-8856-2344 C , Denise dos Santos Colares de Oliveira A and Luciano do Amarante https://orcid.org/0000-0002-4219-9404 A
+ Author Affiliations
- Author Affiliations

A Departamento de Botânica, Universidade Federal de Pelotas, Capão do Leão 96160-000, Brazil.

B State University of Bolívar, Guaranda 020150, Ecuador.

C Empresa Brasileira de Pesquisa Agropecuária, Embrapa Clima Temperado, Pelotas 96010-971, Brazil.

* Correspondence to: cristianejovs@yahoo.com.br
# These authors contributed equally to this paper

Handling Editor: Fanrong Zeng

Functional Plant Biology 49(12) 1029-1042 https://doi.org/10.1071/FP22030
Submitted: 8 February 2022  Accepted: 15 July 2022   Published: 1 August 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

In this study, we tested whether waterlogging priming at the vegetative stage would mitigate a subsequent waterlogging event at the reproductive stage in soybean [Glycine max (L.) Merr.]. Plants (V3 stage) were subjected to priming for 7 days and then exposed to waterlogging stress for 5 days (R2 stage) with non-primed plants. Roots and leaves were sampled on the fifth day of waterlogging and the second and fifth days of reoxygenation. Overall, priming decreased the H2O2 concentration and lipid peroxidation in roots and leaves during waterlogging and reoxygenation. Priming also decreased the activity of antioxidative enzymes in roots and leaves and increased the foliar concentration of phenols and photosynthetic pigments. Additionally, priming decreased fermentation and alanine aminotransferase activity during waterlogging and reoxygenation. Finally, priming increased the concentration of amino acids, sucrose, and total soluble sugars in roots and leaves during waterlogging and reoxygenation. Thus, primed plants were higher and more productive than non-primed plants. Our study shows that priming alleviates oxidative stress, fermentation, and carbohydrate consumption in parallel to increase the yield of soybean plants exposed to waterlogging and reoxygenation.

Keywords: carbohydrate mobilisation, fermentation, flooding, hypoxia, oxidative stress, plant memory, plant productivity, pre-treatment.


References

Agarwal S, Grover A (2006) Molecular biology, biotechnology and genomics of flooding-associated low O2 stress response in plants. Critical Reviews in Plant Sciences 25, 1–21.
Molecular biology, biotechnology and genomics of flooding-associated low O2 stress response in plants.Crossref | GoogleScholarGoogle Scholar |

Alam I, Lee D-G, Kim K-H, Park C-H, Sharmin SA, Lee H, Oh K-W, Yun B-W, Lee B-H (2010) Proteome analysis of soybean roots under waterlogging stress at an early vegetative stage. Journal of Biosciences 35, 49–62.
Proteome analysis of soybean roots under waterlogging stress at an early vegetative stage.Crossref | GoogleScholarGoogle Scholar |

Amarante L, Sodek L (2006) Waterlogging effect on xylem sap glutamine of nodulated soybean. Biologia Plantarum 50, 405–410.
Waterlogging effect on xylem sap glutamine of nodulated soybean.Crossref | GoogleScholarGoogle Scholar |

Andrade CA, Souza KRDd, Santos MdO, Silva DMd, Alves JD (2018) Hydrogen peroxide promotes the tolerance of soybeans to waterlogging. Scientia Horticulturae 232, 40–45.
Hydrogen peroxide promotes the tolerance of soybeans to waterlogging.Crossref | GoogleScholarGoogle Scholar |

Andrzejczak OA, Havelund JF, Wang WQ, Kovalchuk S, Hagensen CE, Hasler-Sheetal H, Hebelstrup KH (2020) The hypoxic proteome and metabolome of barley (Hordeum vulgare L.) with and without phytoglobin priming. International Journal of Molecular Sciences 21, 1546
The hypoxic proteome and metabolome of barley (Hordeum vulgare L.) with and without phytoglobin priming.Crossref | GoogleScholarGoogle Scholar |

Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiologia Plantarum 104, 280–292.
Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley.Crossref | GoogleScholarGoogle Scholar |

Bakker DM, Hamilton GJ, Houlbrooke DJ, Spann C, Burgel AV (2007) Productivity of crops grown on raised beds on duplex soils prone to waterlogging in Western Australia. Australian Journal of Experimental Agriculture 47, 1368–1376.
Productivity of crops grown on raised beds on duplex soils prone to waterlogging in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Barickman TC, Simpson CR, Sams CE (2019) Waterlogging causes early modification in the physiological performance, carotenoids, chlorophylls, proline, and soluble sugars of cucumber plants. Plants 8, 160
Waterlogging causes early modification in the physiological performance, carotenoids, chlorophylls, proline, and soluble sugars of cucumber plants.Crossref | GoogleScholarGoogle Scholar |

Bertrand A, Castonguay Y, Nadeau P, Laberge S, Michaud R, Bélanger G, Rochette P (2003) Oxygen deficiency affects carbohydrate reserves in overwintering forage crops. Journal of Experimental Botany 54, 1721–1730.
Oxygen deficiency affects carbohydrate reserves in overwintering forage crops.Crossref | GoogleScholarGoogle Scholar |

Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Analytical Biochemistry 17, 278–293.
Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography.Crossref | GoogleScholarGoogle Scholar |

Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiology 116, 651–658.
Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings.Crossref | GoogleScholarGoogle Scholar |

Borella J, Amarante Ld, Oliveira DdSCd, Oliveira ACBd, Braga EJB (2014) Waterlogging-induced changes in fermentative metabolism in roots and nodules of soybean genotypes. Scientia Agricola 71, 499–508.
Waterlogging-induced changes in fermentative metabolism in roots and nodules of soybean genotypes.Crossref | GoogleScholarGoogle Scholar |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar |

Bramley H, Tyerman S (2010) Root water transport under waterlogged conditions and the roles of aquaporins. In ‘Waterlogging signalling and tolerance in plants’. (Eds S Mancuso, S Shabala) pp. 151–180. (Springer: Berlin, Heidelberg)

Bui LT, Novi G, Lombardi L, Iannuzzi C, Rossi J, Santaniello A, Mensuali A, Corbineau F, Giuntoli B, Perata P, Zaffagnini M, Licausi F (2019) Conservation of ethanol fermentation and its regulation in land plants. Journal of Experimental Botany 70, 1815–1827.
Conservation of ethanol fermentation and its regulation in land plants.Crossref | GoogleScholarGoogle Scholar |

Castonguay Y, Nadeau P, Simard RR (1993) Effects of flooding on carbohydrate and ABA levels in roots and shoots of alfalfa. Plant, Cell & Environment 16, 695–702.
Effects of flooding on carbohydrate and ABA levels in roots and shoots of alfalfa.Crossref | GoogleScholarGoogle Scholar |

Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis 6, 71–80.
Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid.Crossref | GoogleScholarGoogle Scholar |

Cho H-Y, Loreti E, Shih M-C, Perata P (2021) Energy and sugar signaling during hypoxia. New Phytologist 229, 57–63.
Energy and sugar signaling during hypoxia.Crossref | GoogleScholarGoogle Scholar |

Da-Silva CJ, do Amarante L (2020a) Time-course biochemical analyses of soybean plants during waterlogging and reoxygenation. Environmental and Experimental Botany 180, 104242
Time-course biochemical analyses of soybean plants during waterlogging and reoxygenation.Crossref | GoogleScholarGoogle Scholar |

da-Silva CJ, do Amarante L (2020b) Short-term nitrate supply decreases fermentation and oxidative stress caused by waterlogging in soybean plants. Environmental and Experimental Botany 176, 104078
Short-term nitrate supply decreases fermentation and oxidative stress caused by waterlogging in soybean plants.Crossref | GoogleScholarGoogle Scholar |

Da-Silva CJ, do Amarante L (2022) Nitric oxide signaling in plants during flooding stress. In ‘Nitric oxide in plant biology: an ancient molecule with emerging roles’. (Eds VP Singh, S Singh, D Tripathi, M Romero-Puertas, L Sandalio) pp. 241–260. (Academic Press)

Da-Silva CJ, Shimoia EP, Posso DA, Cardoso AA, Batz TA, Oliveira ACB, do Amarante L (2021) Nitrate nutrition increases foliar levels of nitric oxide and waterlogging tolerance in soybean. Acta Physiologiae Plantarum 43, 116
Nitrate nutrition increases foliar levels of nitric oxide and waterlogging tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |

Dat JF, Capelli N, Folzer H, Bourgeade P, Badot P-M (2004) Sensing and signalling during plant flooding. Plant Physiology and Biochemistry 42, 273–282.
Sensing and signalling during plant flooding.Crossref | GoogleScholarGoogle Scholar |

de Oliveira FK, Da-Silva CJ, Garcia N, Agualongo DAP, de Oliveira ACB, Kanamori N, Takasaki H, Urano K, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K, Nepomuceno AL, Henning LMM, do Amarante L (2022) The overexpression of NCED results in waterlogging sensitivity in soybean. Plant Stress 3, 100047
The overexpression of NCED results in waterlogging sensitivity in soybean.Crossref | GoogleScholarGoogle Scholar |

de San Celedonio RP, Abeledo LG, Miralles DJ (2018) Physiological traits associated with reductions in grain number in wheat and barley under waterlogging. Plant and Soil 429, 469–481.
Physiological traits associated with reductions in grain number in wheat and barley under waterlogging.Crossref | GoogleScholarGoogle Scholar |

Delias DS, Da-Silva CJ, Martins AC, de Oliveira DS, do Amarante L (2021) Iron toxicity increases oxidative stress and impairs mineral accumulation and leaf gas exchange in soybean plants during hypoxia. Environmental Science and Pollution Research 29, 22427–22438.
Iron toxicity increases oxidative stress and impairs mineral accumulation and leaf gas exchange in soybean plants during hypoxia.Crossref | GoogleScholarGoogle Scholar |

do Amarante L, Lima JD, Sodek L (2006) Growth and stress conditions cause similar changes in xylem amino acids for different legume species. Environmental and Experimental Botany 58, 123–129.
Growth and stress conditions cause similar changes in xylem amino acids for different legume species.Crossref | GoogleScholarGoogle Scholar |

Dolferus R, Wolansky M, Carroll R, Miyashita Y, Ismond K, Good A (2008) Functional analysis of lactate dehydrogenase during hypoxic stress in Arabidopsis. Functional Plant Biology 35, 131–140.
Functional analysis of lactate dehydrogenase during hypoxic stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine Max (L.) Merrill. Crop Science 11, 929–931.
Stage of development descriptions for soybeans, Glycine Max (L.) Merrill.Crossref | GoogleScholarGoogle Scholar |

Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia – is survival a balancing act? Trends in Plant Science 9, 449–456.
Plant responses to hypoxia – is survival a balancing act?Crossref | GoogleScholarGoogle Scholar |

Fukao T, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM (2019) Submergence and waterlogging stress in plants: a review highlighting research opportunities and understudied aspects. Frontiers in Plant Science 10, 340
Submergence and waterlogging stress in plants: a review highlighting research opportunities and understudied aspects.Crossref | GoogleScholarGoogle Scholar |

Garcia N, da-Silva CJ, Cocco KLT, Pomagualli D, de Oliveira FK, da Silva JVL, de Oliveira ACB, do Amarante L (2020) Waterlogging tolerance of five soybean genotypes through different physiological and biochemical mechanisms. Environmental and Experimental Botany 172, 103975
Waterlogging tolerance of five soybean genotypes through different physiological and biochemical mechanisms.Crossref | GoogleScholarGoogle Scholar |

Garnczarska M (2002) Hypoxic induction of alcohol and lactate dehydrogenases in lupine seedlings. Acta Physiologiae Plantarum 24, 265–272.
Hypoxic induction of alcohol and lactate dehydrogenases in lupine seedlings.Crossref | GoogleScholarGoogle Scholar |

Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314.
Superoxide dismutases: I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar |

Good AG, Muench DG (1992) Purification and characterization of an anaerobically induced alanine aminotransferase from barley roots. Plant Physiology 99, 1520–1525.
Purification and characterization of an anaerobically induced alanine aminotransferase from barley roots.Crossref | GoogleScholarGoogle Scholar |

Gupta KJ, Zabalza A, Van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiologia Plantarum 137, 383–391.
Regulation of respiration when the oxygen availability changes.Crossref | GoogleScholarGoogle Scholar |

Hanson AD, Jacobsen JV (1984) Control of lactate dehydrogenase, lactate glycolysis, and α-amylase by O2 deficit in barley aleurone layers. Plant Physiology 75, 566–572.
Control of lactate dehydrogenase, lactate glycolysis, and α-amylase by O2 deficit in barley aleurone layers.Crossref | GoogleScholarGoogle Scholar |

Hanson AD, Jacobsen JV, Zwar JA (1984) Regulated expression of three alcohol dehydrogenase genes in barley aleurone layers. Plant Physiology 75, 573–581.
Regulated expression of three alcohol dehydrogenase genes in barley aleurone layers.Crossref | GoogleScholarGoogle Scholar |

Hartman S, Liu Z, van Veen H, Vicente J, Reinen E, Martopawiro S, Zhang H, van Dongen N, Bosman F, Bassel GW, Visser EJW, Bailey-Serres J, Theodoulou FL, Hebelstrup KH, Gibbs DJ, Holdsworth MJ, Sasidharan R, Voesenek LACJ (2019) Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nature Communications 10, 4020
Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress.Crossref | GoogleScholarGoogle Scholar |

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 |

Hussain S, Yin H, Peng S, Khan FA, Khan F, Sameeullah M, Hussain HA, Huang J, Cui K, Nie L (2016) Comparative transcriptional profiling of primed and non-primed rice seedlings under submergence stress. Frontiers in Plant Science 7, 1125
Comparative transcriptional profiling of primed and non-primed rice seedlings under submergence stress.Crossref | GoogleScholarGoogle Scholar |

Jennings AC (1981) The determination of dihydroxy phenolic compounds in extracts of plant tissues. Analytical Biochemistry 118, 396–398.
The determination of dihydroxy phenolic compounds in extracts of plant tissues.Crossref | GoogleScholarGoogle Scholar |

Kennedy RA, Rumpho ME, Fox TC (1992) Anaerobic metabolism in plants. Plant Physiology 100, 1–6.
Anaerobic metabolism in plants.Crossref | GoogleScholarGoogle Scholar |

Kęska K, Szcześniak MW, Makałowska I, Czernicka M (2021a) Long-term waterlogging as factor contributing to hypoxia stress tolerance enhancement in cucumber: comparative transcriptome analysis of waterlogging sensitive and tolerant accessions. Genes 12, 189
Long-term waterlogging as factor contributing to hypoxia stress tolerance enhancement in cucumber: comparative transcriptome analysis of waterlogging sensitive and tolerant accessions.Crossref | GoogleScholarGoogle Scholar |

Kęska K, Szcześniak MW, Adamus A, Czernicka M (2021b) Waterlogging-stress-responsive LncRNAs, their regulatory relationships with miRNAs and target genes in cucumber (Cucumis sativus L.). International Journal of Molecular Sciences 22, 8197
Waterlogging-stress-responsive LncRNAs, their regulatory relationships with miRNAs and target genes in cucumber (Cucumis sativus L.).Crossref | GoogleScholarGoogle Scholar |

León J, Castillo MC, Gayubas B (2021) The hypoxia–reoxygenation stress in plants. Journal of Experimental Botany 72, 5841–5856.
The hypoxia–reoxygenation stress in plants.Crossref | GoogleScholarGoogle Scholar |

Li C, Jiang D, Wollenweber B, Li Y, Dai T, Cao W (2011) Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anthesis in wheat. Plant Science 180, 672–678.
Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anthesis in wheat.Crossref | GoogleScholarGoogle Scholar |

Li X, Topbjerg HB, Jiang D, Liu F (2015) Drought priming at vegetative stage improves the antioxidant capacity and photosynthesis performance of wheat exposed to a short-term low temperature stress at jointing stage. Plant and Soil 393, 307–318.
Drought priming at vegetative stage improves the antioxidant capacity and photosynthesis performance of wheat exposed to a short-term low temperature stress at jointing stage.Crossref | GoogleScholarGoogle Scholar |

Li X, Tan D-X, Jiang D, Liu F (2016) Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. Journal of Pineal Research 61, 328–339.
Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley.Crossref | GoogleScholarGoogle Scholar |

Linkemer G, Board JE, Musgrave ME (1998) Waterlogging effects on growth and yield components in late-planted soybean. Crop Science 38, 1576–1584.
Waterlogging effects on growth and yield components in late-planted soybean.Crossref | GoogleScholarGoogle Scholar |

Liu S, Li X, Larsen DH, Zhu X, Song F, Liu F (2017) Drought priming at vegetative growth stage enhances nitrogen-use efficiency under post-anthesis drought and heat stress in wheat. Journal of Agronomy and Crop Science 203, 29–40.
Drought priming at vegetative growth stage enhances nitrogen-use efficiency under post-anthesis drought and heat stress in wheat.Crossref | GoogleScholarGoogle Scholar |

Loreti E, Perata P (2020) The many facets of hypoxia in plants. Plants 9, 745
The many facets of hypoxia in plants.Crossref | GoogleScholarGoogle Scholar |

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 |

Lothier J, Diab H, Cukier C, Limami AM, Tcherkez G (2020) Metabolic responses to waterlogging differ between roots and shoots and reflect phloem transport alteration in Medicago truncatula. Plants 9, 1373
Metabolic responses to waterlogging differ between roots and shoots and reflect phloem transport alteration in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |

Lukić N, Kukavica B, Davidović-Plavšić B, Hasanagić D, Walter J (2020) Plant stress memory is linked to high levels of anti-oxidative enzymes over several weeks. Environmental and Experimental Botany 178, 104166
Plant stress memory is linked to high levels of anti-oxidative enzymes over several weeks.Crossref | GoogleScholarGoogle Scholar |

Miyashita Y, Dolferus R, Ismond KP, Good AG (2007) Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana. The Plant Journal 49, 1108–1121.
Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Mustroph A, Albrecht G (2003) Tolerance of crop plants to oxygen deficiency stress: fermentative activity and photosynthetic capacity of entire seedlings under hypoxia and anoxia. Physiologia Plantarum 117, 508–520.
Tolerance of crop plants to oxygen deficiency stress: fermentative activity and photosynthetic capacity of entire seedlings under hypoxia and anoxia.Crossref | GoogleScholarGoogle Scholar |

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867–880.
Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar |

Oh M, Komatsu S (2015) Characterization of proteins in soybean roots under flooding and drought stresses. Journal of Proteomics 114, 161–181.
Characterization of proteins in soybean roots under flooding and drought stresses.Crossref | GoogleScholarGoogle Scholar |

Oliveira HC, Sodek L (2013) Effect of oxygen deficiency on nitrogen assimilation and amino acid metabolism of soybean root segments. Amino Acids 44, 743–755.
Effect of oxygen deficiency on nitrogen assimilation and amino acid metabolism of soybean root segments.Crossref | GoogleScholarGoogle Scholar |

Oliveira HC, Freschi L, Sodek L (2013) Nitrogen metabolism and translocation in soybean plants subjected to root oxygen deficiency. Plant Physiology and Biochemistry 66, 141–149.
Nitrogen metabolism and translocation in soybean plants subjected to root oxygen deficiency.Crossref | GoogleScholarGoogle Scholar |

Paul MV, Iyer S, Amerhauser C, Lehmann M, van Dongen JT, Geigenberger P (2016) Oxygen sensing via the ethylene response transcription factor RAP2.12 affects plant metabolism and performance under both normoxia and hypoxia. Plant Physiology 172, 141–153.
Oxygen sensing via the ethylene response transcription factor RAP2.12 affects plant metabolism and performance under both normoxia and hypoxia.Crossref | GoogleScholarGoogle Scholar |

Phukan UJ, Mishra S, Shukla RK (2016) Waterlogging and submergence stress: affects and acclimation. Critical Reviews in Biotechnology 36, 956–966.
Waterlogging and submergence stress: affects and acclimation.Crossref | GoogleScholarGoogle Scholar |

Posso DA, Borella J, Reissig GN, Guidorizi KA, Bacarin MA (2020) Short-term root flooding and recovery conditions—affected photosynthetic process of common bean plants. Theoretical and Experimental Plant Physiology 32, 287–300.
Short-term root flooding and recovery conditions—affected photosynthetic process of common bean plants.Crossref | GoogleScholarGoogle Scholar |

Pucciariello C, Perata P (2017) New insights into reactive oxygen species and nitric oxide signalling under low oxygen in plants. Plant, Cell & Environment 40, 473–482.
New insights into reactive oxygen species and nitric oxide signalling under low oxygen in plants.Crossref | GoogleScholarGoogle Scholar |

Pucciariello C, Banti V, Perata P (2012) ROS signaling as common element in low oxygen and heat stresses. Plant Physiology and Biochemistry 59, 3–10.
ROS signaling as common element in low oxygen and heat stresses.Crossref | GoogleScholarGoogle Scholar |

Rhine MD, Stevens G, Shannon G, Wrather A, Sleper D (2010) Yield and nutritional responses to waterlogging of soybean cultivars. Irrigation Science 28, 135–142.
Yield and nutritional responses to waterlogging of soybean cultivars.Crossref | GoogleScholarGoogle Scholar |

Roberts JK, Callis J, Jardetzky O, Walbot V, Freeling M (1984) Cytoplasmic acidosis as a determinant of flooding intolerance in plants. Proceedings of the National Academy of Sciences of the United States of America 81, 6029–6033.
Cytoplasmic acidosis as a determinant of flooding intolerance in plants.Crossref | GoogleScholarGoogle Scholar |

Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiology 152, 1501–1513.
Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus.Crossref | GoogleScholarGoogle Scholar |

Sairam RK, Dharmar K, Chinnusamy V, Meena RC (2009) Waterlogging-induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata). Journal of Plant Physiology 166, 602–616.
Waterlogging-induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata).Crossref | GoogleScholarGoogle Scholar |

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.
Signal dynamics and interactions during flooding stress.Crossref | GoogleScholarGoogle Scholar |

Sasidharan R, Schippers JHM, Schmidt RR (2021) Redox and low-oxygen stress: signal integration and interplay. Plant Physiology 186, 66–78.
Redox and low-oxygen stress: signal integration and interplay.Crossref | GoogleScholarGoogle Scholar |

Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming of plants against multiple abiotic stresses: mission possible? Trends in Plant Science 21, 329–340.
Chemical priming of plants against multiple abiotic stresses: mission possible?Crossref | GoogleScholarGoogle Scholar |

Shikov AE, Chirkova TV, Yemelyanov VV (2020) Post-anoxia in plants: reasons, consequences, and possible mechanisms. Russian Journal of Plant Physiology 67, 45–59.
Post-anoxia in plants: reasons, consequences, and possible mechanisms.Crossref | GoogleScholarGoogle Scholar |

Shingaki-Wells R, Millar AH, Whelan J, Narsai R (2014) What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation. Plant, Cell & Environment 37, 2260–2277.
What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation.Crossref | GoogleScholarGoogle Scholar |

Solaiman Z, Colmer TD, Loss SP, Thomson BD, Siddique KHM (2007) Growth responses of cool-season grain legumes to transient waterlogging. Australian Journal of Agricultural Research 58, 406–412.
Growth responses of cool-season grain legumes to transient waterlogging.Crossref | GoogleScholarGoogle Scholar |

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.
Time is on our side: the importance of considering a recovery period when assessing flooding tolerance in plants.Crossref | GoogleScholarGoogle Scholar |

Tadege M, Dupuis I, Kuhlemeier C (1999) Ethanolic fermentation: new functions for an old pathway. Trends in Plant Science 4, 320–325.
Ethanolic fermentation: new functions for an old pathway.Crossref | GoogleScholarGoogle Scholar |

Tamang BG, Magliozzi JO, Maroof MAS, Fukao T (2014) Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings. Plant, Cell & Environment 37, 2350–2365.
Physiological and transcriptomic characterization of submergence and reoxygenation responses in soybean seedlings.Crossref | GoogleScholarGoogle Scholar |

Tan X, Xu H, Khan S, Equiza MA, Lee SH, Vaziriyeganeh M, Zwiazek JJ (2018) Plant water transport and aquaporins in oxygen-deprived environments. Journal of Plant Physiology 227, 20–30.
Plant water transport and aquaporins in oxygen-deprived environments.Crossref | GoogleScholarGoogle Scholar |

Toral-Juárez MA, Avila RT, Cardoso AA, Brito FAL, Machado KLG, Almeida WL, Souza RPB, Martins SCV, DaMatta FM (2021) Drought-tolerant coffee plants display increased tolerance to waterlogging and post-waterlogging reoxygenation. Environmental and Experimental Botany 182, 104311
Drought-tolerant coffee plants display increased tolerance to waterlogging and post-waterlogging reoxygenation.Crossref | GoogleScholarGoogle Scholar |

van Handel E (1968) Direct microdetermination of sucrose. Analytical Biochemistry 22, 280–283.
Direct microdetermination of sucrose.Crossref | GoogleScholarGoogle Scholar |

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151, 59–66.
Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |

Vwioko E, Adinkwu O, El-Esawi MA (2017) Comparative physiological, biochemical, and genetic responses to prolonged waterlogging stress in okra and maize given exogenous ethylene priming. Frontiers in Physiology 8, 632
Comparative physiological, biochemical, and genetic responses to prolonged waterlogging stress in okra and maize given exogenous ethylene priming.Crossref | GoogleScholarGoogle Scholar |

Vwioko ED, El-Esawi MA, Imoni ME, Al-Ghamdi AA, Ali HM, El-Sheekh MM, Abdeldaym EA, Al-Dosary MA (2019) Sodium azide priming enhances waterlogging stress tolerance in okra (Abelmoschus esculentus L.). Agronomy 9, 679
Sodium azide priming enhances waterlogging stress tolerance in okra (Abelmoschus esculentus L.).Crossref | GoogleScholarGoogle Scholar |

Wang X, Huang M, Zhou Q, Cai J, Dai T, Cao W, Jiang D (2016) Physiological and proteomic mechanisms of waterlogging priming improves tolerance to waterlogging stress in wheat (Triticum aestivum L.). Environmental and Experimental Botany 132, 175–182.
Physiological and proteomic mechanisms of waterlogging priming improves tolerance to waterlogging stress in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |

Wang X, Liu F-l, Jiang D (2017) Priming: a promising strategy for crop production in response to future climate. Journal of Integrative Agriculture 16, 2709–2716.
Priming: a promising strategy for crop production in response to future climate.Crossref | GoogleScholarGoogle Scholar |

Wany A, Gupta AK, Kumari A, Mishra S, Singh N, Pandey S, Vanvari R, Igamberdiev AU, Fernie AR, Gupta KJ (2019) Nitrate nutrition influences multiple factors in order to increase energy efficiency under hypoxia in Arabidopsis. Annals of Botany 123, 691–705.
Nitrate nutrition influences multiple factors in order to increase energy efficiency under hypoxia in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.Crossref | GoogleScholarGoogle Scholar |

Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. Analyst 80, 209–214.
The determination of amino-acids with ninhydrin.Crossref | GoogleScholarGoogle Scholar |

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

Youssef MS, Mira MM, Renault S, Hill RD, Stasolla C (2016) Phytoglobin expression influences soil flooding response of corn plants. Annals of Botany 118, 919–931.
Phytoglobin expression influences soil flooding response of corn plants.Crossref | GoogleScholarGoogle Scholar |

Zabalza A, van Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, Schmälzlin E, Igal M, Orcaray L, Royuela M, Geigenberger P (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiology 149, 1087–1098.
Regulation of respiration and fermentation to control the plant internal oxygen concentration.Crossref | GoogleScholarGoogle Scholar |

Zhang X, Shabala S, Koutoulis A, Shabala L, Johnson P, Hayes D, Nichols DS, Zhou M (2015) Waterlogging tolerance in barley is associated with faster aerenchyma formation in adventitious roots. Plant and Soil 394, 355–372.
Waterlogging tolerance in barley is associated with faster aerenchyma formation in adventitious roots.Crossref | GoogleScholarGoogle Scholar |

Zhou M (2010) Improvement of plant waterlogging tolerance. In ‘Waterlogging signalling and tolerance in plants’. (Eds S Mancuso, S Shabala) pp. 267–285. (Springer: Berlin, Heidelberg)