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

Nitrate supply decreases fermentation and alleviates oxidative and ionic stress in nitrogen-fixing soybean exposed to saline waterlogging

Tamires da Silva Martins https://orcid.org/0000-0002-4987-314X A * , Cristiane Jovelina Da-Silva https://orcid.org/0000-0003-3239-5927 A * , Eduardo Pereira Shimoia https://orcid.org/0000-0002-2889-4259 A , Douglas Antônio Posso A , Ivan Ricardo Carvalho B , Ana Claudia Barneche de Oliveira C and Luciano do Amarante A
+ Author Affiliations
- Author Affiliations

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

B Departamento de Estudos Agrários, Universidade Regional do Noroeste do Estado do Rio Grande do Sul, Ijuí 98700-000, Brazil.

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


Handling Editor: Ulrike Mathesius

Functional Plant Biology 50(5) 416-433 https://doi.org/10.1071/FP22145
Submitted: 30 June 2022  Accepted: 18 March 2023   Published: 11 April 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Nitrate (NO3) nutrition is known to mitigate the damages caused by individual stresses of waterlogging and salinity. Here, we investigated the role of NO3 in soybean plants exposed to these stresses in combination. Nodulated soybean cultivated under greenhouse conditions and daily fertilised with a nutrient solution without nitrogen were subjected to the following treatments: Water, NO3, NaCl, and NaCl + NO3. Then, plants were exposed to waterlogging (6 days) and drainage (2 days). Compared to plants exposed to isolated stress, the saline waterlogging resulted in higher concentrations of H2O2, O2˙, and lipid peroxidation at the whole-plant level, mainly during drainage. Furthermore, saline waterlogging increased fermentation and the concentrations of Na+ and K+ in roots and leaves both during waterlogging and drainage. NO3 supplementation led to augments in NO3 and NO levels, and stimulated nitrate reductase activity in both organs. In addition, NO3 nutrition alleviated oxidative stress and fermentation besides increasing the K+/Na+ ratio in plants exposed to saline waterlogging. In conclusion, NO3 supplementation is a useful strategy to help soybean plants overcome saline waterlogging stress. These findings are of high relevance for agriculture as soybean is an important commodity and has been cultivated in areas prone to saline waterlogging.

Keywords: antioxidants metabolism, drainage, hypoxia, Na+/K+, nitric oxide, reactive oxygen species, reoxygenation, salinity.


References

Abd El-Hay SS, Colyer CL (2017) Development of high-throughput method for measurement of vascular nitric oxide generation in microplate reader. Molecules 22, 127
Development of high-throughput method for measurement of vascular nitric oxide generation in microplate reader.Crossref | GoogleScholarGoogle Scholar |

Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7, 18
Plant responses to salt stress: adaptive mechanisms.Crossref | GoogleScholarGoogle Scholar |

Adhikari B, Dhungana SK, Kim I-D, Shin D-H (2020) Effect of foliar application of potassium fertilizers on soybean plants under salinity stress. Journal of the Saudi Society of Agricultural Sciences 19, 261–269.
Effect of foliar application of potassium fertilizers on soybean plants under salinity stress.Crossref | GoogleScholarGoogle Scholar |

Ahanger MA, Qin C, Begum N, Maodong Q, Dong XX, El-Esawi M, El-Sheikh MA, Alatar AA, Zhang L (2019) Nitrogen availability prevents oxidative effects of salinity on wheat growth and photosynthesis by up-regulating the antioxidants and osmolytes metabolism, and secondary metabolite accumulation. BMC Plant Biology 19, 479
Nitrogen availability prevents oxidative effects of salinity on wheat growth and photosynthesis by up-regulating the antioxidants and osmolytes metabolism, and secondary metabolite accumulation.Crossref | GoogleScholarGoogle Scholar |

Akram S, Siddiqui MN, Hussain BMN, Al Bari MA, Mostofa MG, Hossain MA, Tran L-SP (2017) Exogenous glutathione modulates salinity tolerance of soybean [Glycine max (L.) Merrill] at reproductive stage. Journal of Plant Growth Regulation 36, 877–888.
Exogenous glutathione modulates salinity tolerance of soybean [Glycine max (L.) Merrill] at reproductive stage.Crossref | GoogleScholarGoogle Scholar |

Akram NA, Hafeez N, Farid-ul-Haq M, Ahmad A, Sadiq M, Ashraf M (2020) Foliage application and seed priming with nitric oxide causes mitigation of salinity-induced metabolic adversaries in broccoli (Brassica oleracea L.) plants. Acta Physiologiae Plantarum 42, 155
Foliage application and seed priming with nitric oxide causes mitigation of salinity-induced metabolic adversaries in broccoli (Brassica oleracea L.) plants.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 |

Anee TI, Nahar K, Rahman A, Al Mahmud J, Bhuiyan TF, Ul Alam M, Fujita M, Hasanuzzaman M (2019) Oxidative damage and antioxidant defense in Sesamum indicum after different waterlogging durations. Plants 8, 196
Oxidative damage and antioxidant defense in Sesamum indicum after different waterlogging durations.Crossref | GoogleScholarGoogle Scholar |

Antonelli CJ, Calzadilla PI, Campestre MP, Escaray FJ, Ruiz OA (2021) Contrasting response of two Lotus corniculatus L. accessions to combined waterlogging–saline stress. Plant Biology 23, 363–374.
Contrasting response of two Lotus corniculatus L. accessions to combined waterlogging–saline stress.Crossref | GoogleScholarGoogle Scholar |

Aridhi F, Sghaier H, Gaitanaros A, Khadri A, Aschi-Smiti S, Brouquisse R (2020) Nitric oxide production is involved in maintaining energy state in Alfalfa (Medicago sativa L.) nodulated roots under both salinity and flooding. Planta 252, 22
Nitric oxide production is involved in maintaining energy state in Alfalfa (Medicago sativa L.) nodulated roots under both salinity and flooding.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 |

Bacanamwo M, Purcell LC (1999) Soybean dry matter and N accumulation responses to flooding stress, N sources and hypoxia. Journal of Experimental Botany 50, 689–696.
Soybean dry matter and N accumulation responses to flooding stress, N sources and hypoxia.Crossref | GoogleScholarGoogle Scholar |

Banu MNA, Hoque MA, Watanabe-Sugimoto M, Matsuoka K, Nakamura Y, Shimoishi Y, Murata Y (2009) Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress. Journal of Plant Physiology 166, 146–156.
Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress.Crossref | GoogleScholarGoogle Scholar |

Behr JH, Bouchereau A, Berardocco S, Seal CE, Flowers TJ, Zörb C (2017) Metabolic and physiological adjustment of Suaeda maritima to combined salinity and hypoxia. Annals of Botany 119, 965–976.
Metabolic and physiological adjustment of Suaeda maritima to combined salinity and hypoxia.Crossref | GoogleScholarGoogle Scholar |

Bhardwaj S, Kapoor D, Singh S, Gautam V, Dhanjal DS, Jan S, Ramamurthy PC, Prasad R, Singh J (2021) Nitric oxide: a ubiquitous signal molecule for enhancing plant tolerance to salinity stress and their molecular mechanisms. Journal of Plant Growth Regulation 40, 2329–2341.
Nitric oxide: a ubiquitous signal molecule for enhancing plant tolerance to salinity stress and their molecular mechanisms.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 |

Board JE (2008) Waterlogging effects on plant nutrient concentrations in soybean. Journal of Plant Nutrition 31, 828–838.
Waterlogging effects on plant nutrient concentrations in soybean.Crossref | GoogleScholarGoogle Scholar |

Boluwade A, Madramootoo C, Yari A (2016) Application of unsupervised clustering techniques for management zone delineation: case study of variable rate irrigation in Southern Alberta, Canada. Journal of Irrigation and Drainage Engineering 142, 05015007
Application of unsupervised clustering techniques for management zone delineation: case study of variable rate irrigation in Southern Alberta, Canada.Crossref | GoogleScholarGoogle Scholar |

Borella J, Durigon MA, Amarante Ld, Emygdio BM (2013) Atividade de enzimas fermentativas em raízes e nódulos de soja sob condições de hipóxia e pós-hipóxia. Ciência Rural 43, 970–977.
Atividade de enzimas fermentativas em raízes e nódulos de soja sob condições de hipóxia e pós-hipóxia.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 |

Borella J, Oliveira HC, de Oliveira DdSC, Braga EJB, de Oliveira ACB, Sodek L, do Amarante L (2017) Hypoxia-driven changes in glycolytic and tricarboxylic acid cycle metabolites of two nodulated soybean genotypes. Environmental and Experimental Botany 133, 118–127.
Hypoxia-driven changes in glycolytic and tricarboxylic acid cycle metabolites of two nodulated soybean genotypes.Crossref | GoogleScholarGoogle Scholar |

Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83, 463–468.
Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max).Crossref | GoogleScholarGoogle Scholar |

Cao X, Wu L, Wu M, Zhu C, Jin Q, Zhang J (2020) Abscisic acid mediated proline biosynthesis and antioxidant ability in roots of two different rice genotypes under hypoxic stress. BMC Plant Biology 20, 198
Abscisic acid mediated proline biosynthesis and antioxidant ability in roots of two different rice genotypes under hypoxic stress.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 |

Chakraborty K, Ray S, Vijayan J, Molla KA, Nagar R, Jena P, Mondal S, Panda BB, Shaw BP, Swain P, Chattopadhyay K, Sarkar RK (2021) Preformed aerenchyma determines the differential tolerance response under partial submergence imposed by fresh and saline water flooding in rice. Physiologia Plantarum 173, 1597–1615.
Preformed aerenchyma determines the differential tolerance response under partial submergence imposed by fresh and saline water flooding in rice.Crossref | GoogleScholarGoogle Scholar |

Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Science 45, 437–448.
Understanding and improving salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar |

Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62, 39–57.
Ion transport in seminal and adventitious roots of cereals during O2 deficiency.Crossref | GoogleScholarGoogle Scholar |

Corpas FJ, del Río LA, Palma JM (2019) Impact of nitric oxide (NO) on the ROS metabolism of peroxisomes. Plants 8, 37
Impact of nitric oxide (NO) on the ROS metabolism of peroxisomes.Crossref | GoogleScholarGoogle Scholar |

Da-Silva CJ, do Amarante L (2020a) 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 (2020b) 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 (2022) Nitric oxide signaling in plants during flooding stress. In ‘Nitric oxide in plant biology’. (Eds V Pratap Singh, S Singh, DK Tripathi, MC Romero-Puertas, LM Sandalio) pp. 241–260. (Academic Press: London, UK) https://doi.org/10.1016/b978-0-12-818797-5.00009-1

Da-Silva CJ, Modolo LV (2018) Hydrogen sulfide: a new endogenous player in an old mechanism of plant tolerance to high salinity. Acta Botanica Brasilica 32, 150–160.
Hydrogen sulfide: a new endogenous player in an old mechanism of plant tolerance to high salinity.Crossref | GoogleScholarGoogle Scholar |

Da-Silva CJ, Batista Fontes EP, Modolo LV (2017) Salinity-induced accumulation of endogenous H2S and NO is associated with modulation of the antioxidant and redox defense systems in Nicotiana tabacum L. cv. Havana. Plant Science 256, 148–159.
Salinity-induced accumulation of endogenous H2S and NO is associated with modulation of the antioxidant and redox defense systems in Nicotiana tabacum L. cv. Havana.Crossref | GoogleScholarGoogle Scholar |

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 |

de Sousa CAF, Sodek L (2003) Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and subsequent return to normoxia. Environmental and Experimental Botany 50, 1–8.
Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and subsequent return to normoxia.Crossref | GoogleScholarGoogle Scholar |

Dodds F, Bartram J (2016) ‘The water, food, energy and climate nexus: challenges and an agenda for action’. (Eds F Dodds, J Bartram). (Routledge: London, UK)

Emna B, Mounira Z, Mohamed H (2016) Development of a flow and transport model for drainage network conception in Northern Tunisia. Journal of Irrigation and Drainage Engineering 142, 05015006
Development of a flow and transport model for drainage network conception in Northern Tunisia.Crossref | GoogleScholarGoogle Scholar |

Falakboland Z, Zhou M, Zeng F, Kiani-Pouya A, Shabala L, Shabala S (2017) Plant ionic relation and whole-plant physiological responses to waterlogging, salinity and their combination in barley. Functional Plant Biology 44, 941–953.
Plant ionic relation and whole-plant physiological responses to waterlogging, salinity and their combination in barley.Crossref | GoogleScholarGoogle Scholar |

Fan HF, Du CX, Ding L, Xu YL (2014) Exogenous nitric oxide promotes waterlogging tolerance as related to the activities of antioxidant enzymes in cucumber seedlings. Russian Journal of Plant Physiology 61, 366–373.
Exogenous nitric oxide promotes waterlogging tolerance as related to the activities of antioxidant enzymes in cucumber seedlings.Crossref | GoogleScholarGoogle Scholar |

Fancy NN, Bahlmann A-K, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant, Cell & Environment 40, 462–472.
Nitric oxide function in plant abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Farnese FS, Menezes-Silva PE, Gusman GS, Oliveira JA (2016) When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Frontiers in Plant Science 7, 471
When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radical Biology and Medicine 56, 172–183.
The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants.Crossref | GoogleScholarGoogle Scholar |

Garcia N, da-Silva CJ, Cocco KLT, Pomagualli D, de Oliveira FK, da Silva JVL, de Oliveira ACB, Amarante Ld (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 |

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 |

Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Frontiers in Plant Science 4, 419
Nitric oxide, antioxidants and prooxidants in plant defence responses.Crossref | GoogleScholarGoogle Scholar |

Guan L, Haider MS, Khan N, Nasim M, Jiu S, Fiaz M, Zhu X, Zhang K, Fang J (2018) Transcriptome sequence analysis elaborates a complex defensive mechanism of grapevine (Vitis vinifera l.) in response to salt stress. International Journal of Molecular Sciences 19, 4019
Transcriptome sequence analysis elaborates a complex defensive mechanism of grapevine (Vitis vinifera l.) in response to salt stress.Crossref | GoogleScholarGoogle Scholar |

Gupta P, Seth CS (2020) Interactive role of exogenous 24 Epibrassinolide and endogenous NO in Brassica juncea L. under salinity stress: evidence for NR-dependent NO biosynthesis. Nitric Oxide - Biology and Chemistry 97, 33–47.
Interactive role of exogenous 24 Epibrassinolide and endogenous NO in Brassica juncea L. under salinity stress: evidence for NR-dependent NO biosynthesis.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 |

Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station 347, 32

Igamberdiev AU, Baron K, Manac’h-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Annals of Botany 96, 557–564.
The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling.Crossref | GoogleScholarGoogle Scholar |

Jensen ES (1986) The influence of rate and time of nitrate supply on nitrogen fixation and yield in pea (Pisum sativum L.). Fertilizer Research 10, 193–202.
The influence of rate and time of nitrate supply on nitrogen fixation and yield in pea (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar |

Jia L, Qin X, Lyu D, Qin S, Zhang P (2019) ROS production and scavenging in three cherry rootstocks under short-term waterlogging conditions. Scientia Horticulturae 257, 108647
ROS production and scavenging in three cherry rootstocks under short-term waterlogging conditions.Crossref | GoogleScholarGoogle Scholar |

Justino GC, Sodek L (2013) Recovery of nitrogen fixation after short-term flooding of the nodulated root system of soybean. Journal of Plant Physiology 170, 235–241.
Recovery of nitrogen fixation after short-term flooding of the nodulated root system of soybean.Crossref | GoogleScholarGoogle Scholar |

Khan MA, Khan AL, Imran QM, Asaf S, Lee S-U, Yun B-W, Hamayun M, Kim T-H, Lee I-J (2019) Exogenous application of nitric oxide donors regulates short-term flooding stress in soybean. PeerJ 7, e7741
Exogenous application of nitric oxide donors regulates short-term flooding stress in soybean.Crossref | GoogleScholarGoogle Scholar |

Khator K, Shekhawat GS (2020) Nitric oxide mitigates salt-induced oxidative stress in Brassica juncea seedlings by regulating ROS metabolism and antioxidant defense system. 3 Biotech 10, 499
Nitric oxide mitigates salt-induced oxidative stress in Brassica juncea seedlings by regulating ROS metabolism and antioxidant defense system.Crossref | GoogleScholarGoogle Scholar |

Kotula L, Kwa HY, Nichols PGH, Colmer TD (2019) Tolerance and recovery of the annual pasture legumes Melilotus siculus, Trifolium michelianum and Medicago polymorpha to soil salinity, soil waterlogging and the combination of these stresses. Plant and Soil 444, 267–280.
Tolerance and recovery of the annual pasture legumes Melilotus siculus, Trifolium michelianum and Medicago polymorpha to soil salinity, soil waterlogging and the combination of these stresses.Crossref | GoogleScholarGoogle Scholar |

Li C, Bai T, Ma F, Han M (2010) Hypoxia tolerance and adaptation of anaerobic respiration to hypoxia stress in two Malus species. Scientia Horticulturae 124, 274–279.
Hypoxia tolerance and adaptation of anaerobic respiration to hypoxia stress in two Malus species.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 X, Chen C, Liu Y, Liu Y, Zhao Y, Chen M (2020) The presence of moderate salt can increase tolerance of Elaeagnus angustifolia seedlings to waterlogging stress. Plant Signaling & Behavior 15, 1743518
The presence of moderate salt can increase tolerance of Elaeagnus angustifolia seedlings to waterlogging stress.Crossref | GoogleScholarGoogle Scholar |

Mahmood U, Hussain S, Hussain S, Ali B, Ashraf U, Zamir S, Al-Robai SA, Alzahrani FO, Hano C, El-Esawi MA (2021) Morpho-physio-biochemical and molecular responses of maize hybrids to salinity and waterlogging during stress and recovery phase. Plants 10, 1345
Morpho-physio-biochemical and molecular responses of maize hybrids to salinity and waterlogging during stress and recovery phase.Crossref | GoogleScholarGoogle Scholar |

Maiber L, Koprivova A, Bender D, Kopriva S, Fischer-Schrader K (2022) Characterization of the amidoxime reducing components ARC1 and ARC2 from Arabidopsis thaliana. The FEBS Journal 289, 5656–5669.
Characterization of the amidoxime reducing components ARC1 and ARC2 from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Medina-Andrés R, Solano-Peralta A, Saucedo-Vázquez JP, Napsucialy-Mendivil S, Pimentel-Cabrera JA, Sosa-Torres ME, Dubrovsky JG, Lira-Ruan V (2015) The nitric oxide production in the moss Physcomitrella patens is mediated by nitrate reductase. PLoS ONE 10, e0119400
The nitric oxide production in the moss Physcomitrella patens is mediated by nitrate reductase.Crossref | GoogleScholarGoogle 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 and Pasture Science 72, 75–84.
Variability among Festuca arundinacea cultivars for tolerance to and recovery from waterlogging, salinity and their combination.Crossref | GoogleScholarGoogle Scholar |

Modolo LV, Augusto O, Almeida IM, Magalhaes JR, Salgado I (2005) Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Letters 579, 3814–3820.
Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae.Crossref | GoogleScholarGoogle Scholar |

Molajou A, Afschar A, Khosravi M, Soleimanian E, Vahabzadeh M, Akbari V, Variani HA (2021) A new paradigm of water, food, and energy nexus. Environmental Science and Pollution Research 54, 1–11.
A new paradigm of water, food, and energy nexus.Crossref | GoogleScholarGoogle Scholar |

Mur LAJ, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJM, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5, pls052
Nitric oxide in plants: an assessment of the current state of knowledge.Crossref | GoogleScholarGoogle Scholar |

Muthiah S, Longer DE, Harris WM (1994) Staging soybean seedling growth from germination to emergence. Crop Science 34, 289–291.
Staging soybean seedling growth from germination to emergence.Crossref | GoogleScholarGoogle Scholar |

Nabi RBS, Tayade R, Hussain A, Kulkarni KP, Imran QM, Mun B-G, Yun B-W (2019) Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environmental and Experimental Botany 161, 120–133.
Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress.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 |

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, Salgado I, Sodek L (2013) Involvement of nitrite in the nitrate-mediated modulation of fermentative metabolism and nitric oxide production of soybean roots during hypoxia. Planta 237, 255–264.
Involvement of nitrite in the nitrate-mediated modulation of fermentative metabolism and nitric oxide production of soybean roots during hypoxia.Crossref | GoogleScholarGoogle Scholar |

Oliveira FKd, 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 |

Peng R, Bian Z, Zhou L, Cheng W, Hai N, Yang C, Yang T, Wang X, Wang C (2016) Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L.). Plant Cell Reports 35, 2325–2340.
Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |

Phang T-H, Shao G, Lam H-M (2008) Salt tolerance in soybean. Journal of Integrative Plant Biology 50, 1196–1212.
Salt tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |

Pissolato MD, Silveira NM, Prataviera PJC, Machado EC, Seabra AB, Pelegrino MT, Sodek L, Ribeiro RV (2020) Enhanced nitric oxide synthesis through nitrate supply improves drought tolerance of sugarcane plants. Frontiers in Plant Science 11, 970
Enhanced nitric oxide synthesis through nitrate supply improves drought tolerance of sugarcane plants.Crossref | GoogleScholarGoogle Scholar |

Ploschuk RA, Miralles DJ, Striker GG (2022) A quantitative review of soybean responses to waterlogging: agronomical, morpho-physiological and anatomical traits of tolerance. Plant and Soil 475, 237–252.
A quantitative review of soybean responses to waterlogging: agronomical, morpho-physiological and anatomical traits of tolerance.Crossref | GoogleScholarGoogle Scholar |

Posso DA, Borella J, Reissig GN, Bacarin MA (2018) Root flooding-induced changes in the dynamic dissipation of the photosynthetic energy of common bean plants. Acta Physiologiae Plantarum 40, 212
Root flooding-induced changes in the dynamic dissipation of the photosynthetic energy of common bean plants.Crossref | GoogleScholarGoogle Scholar |

Posso DA, Borella J, Reissig GN, do Amarante L, Bacarin MA (2020) Nitrate-mediated maintenance of photosynthetic process by modulating hypoxic metabolism of common bean plants. Acta Physiologiae Plantarum 42, 117
Nitrate-mediated maintenance of photosynthetic process by modulating hypoxic metabolism of common bean plants.Crossref | GoogleScholarGoogle Scholar |

Ramadan AA, Abd Elhamid EM, Sadak MS (2019) Comparative study for the effect of arginine and sodium nitroprusside on sunflower plants grown under salinity stress conditions. Bulletin of the National Research Centre 43, 118
Comparative study for the effect of arginine and sodium nitroprusside on sunflower plants grown under salinity stress conditions.Crossref | GoogleScholarGoogle Scholar |

Rena AB, Masciotti GZ (1976) The effect of dehydration on nitrogen metabolism and growth of 4 bean cultivars (Phaseolus vulgaris L.). Revista Ceres 23, 288–301.

Richter GL, Zanon Júnior A, Streck NA, Guedes JVC, Kräulich B, Rocha TSMd, Winck JEM, Cera JC (2014) Estimating leaf area of modern soybean cultivars by a non-destructive method. Bragantia 73, 416–425.
Estimating leaf area of modern soybean cultivars by a non-destructive method.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 |

Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. Journal of Experimental Botany 53, 103–110.
Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |

Saturno DF, Cerezini P, Moreira da Silva P, Oliveira ABd, Oliveira MCNd, Hungria M, Nogueira MA (2017) Mineral nitrogen impairs the biological nitrogen fixation in soybean of determinate and indeterminate growth types. Journal of Plant Nutrition 40, 1690–1701.
Mineral nitrogen impairs the biological nitrogen fixation in soybean of determinate and indeterminate growth types.Crossref | GoogleScholarGoogle Scholar |

Saxena I, Shekhawat GS (2013) Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration. Nitric Oxide 32, 13–20.
Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration.Crossref | GoogleScholarGoogle Scholar |

Sevilla F, Camejo D, Ortiz-Espín A, Calderón A, Lázaro JJ, Jiménez A (2015) The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. Journal of Experimental Botany 66, 2945–2955.
The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species.Crossref | GoogleScholarGoogle Scholar |

Shams M, Ekinci M, Ors S, Turan M, Agar G, Kul R, Yildirim E (2019) Nitric oxide mitigates salt stress effects of pepper seedlings by altering nutrient uptake, enzyme activity and osmolyte accumulation. Physiology and Molecular Biology of Plants 25, 1149–1161.
Nitric oxide mitigates salt stress effects of pepper seedlings by altering nutrient uptake, enzyme activity and osmolyte accumulation.Crossref | GoogleScholarGoogle Scholar |

Sharma PC, Kumar A, Vineeth TV (2017) Current trends in salinity and waterlogging tolerance. In ‘Abiotic stress management for resilient agriculture’. (Eds P Minhas, J Rane, R Pasala) pp. 177–220. (Springer: Singapore) https://doi.org/10.1007/978-981-10-5744-1

Sikder RK, Wang X, Zhang H, Gui H, Dong Q, Jin D, Song M (2020) Nitrogen enhances salt tolerance by modulating the antioxidant defense system and osmoregulation substance content in Gossypium hirsutum. Plants 9, 450
Nitrogen enhances salt tolerance by modulating the antioxidant defense system and osmoregulation substance content in Gossypium hirsutum.Crossref | GoogleScholarGoogle Scholar |

Singh M, Singh VP, Prasad SM (2019) Nitrogen alleviates salinity toxicity in Solanum lycopersicum seedlings by regulating ROS homeostasis. Plant Physiology and Biochemistry 141, 466–476.
Nitrogen alleviates salinity toxicity in Solanum lycopersicum seedlings by regulating ROS homeostasis.Crossref | GoogleScholarGoogle Scholar |

Sparacino-Watkins CE, Tejero J, Sun B, Gauthier MC, Thomas J, Ragireddy V, Merchant BA, Wang J, Azarov I, Basu P, Gladwin MT (2014) Nitrite reductase and nitric-oxide synthase activity of the mitochondrial molybdopterin enzymes mARC1 and mARC2. Journal of Biological Chemistry 289, 10345–10358.
Nitrite reductase and nitric-oxide synthase activity of the mitochondrial molybdopterin enzymes mARC1 and mARC2.Crossref | GoogleScholarGoogle Scholar |

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.
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.Crossref | GoogleScholarGoogle Scholar |

Su J, Zhang Y, Nie Y, Cheng D, Wang R, Hu H, Chen J, Zhang J, Du Y, Shen W (2018) Hydrogen-induced osmotic tolerance is associated with nitric oxide-mediated proline accumulation and reestablishment of redox balance in alfalfa seedlings. Environmental and Experimental Botany 147, 249–260.
Hydrogen-induced osmotic tolerance is associated with nitric oxide-mediated proline accumulation and reestablishment of redox balance in alfalfa seedlings.Crossref | GoogleScholarGoogle Scholar |

Sun H, Li J, Song W, Tao J, Huang S, Chen S, Hou M, Xu G, Zhang Y (2015) Nitric oxide generated by nitrate reductase increases nitrogen uptake capacity by inducing lateral root formation and inorganic nitrogen uptake under partial nitrate nutrition in rice. Journal of Experimental Botany 66, 2449–2459.
Nitric oxide generated by nitrate reductase increases nitrogen uptake capacity by inducing lateral root formation and inorganic nitrogen uptake under partial nitrate nutrition in rice.Crossref | GoogleScholarGoogle Scholar |

Thomas AL, Guerreiro SMC, Sodek L (2005) Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Annals of Botany 96, 1191–1198.
Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean.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 |

Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu D-T, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425, 393–397.
Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins.Crossref | GoogleScholarGoogle Scholar |

Turkan I, Demiral T, Sekmen AH (2013) The regulation of antioxidant enzymes in two Plantago species differing in salinity tolerance under combination of waterlogging and salinity. Functional Plant Biology 40, 484–493.
The regulation of antioxidant enzymes in two Plantago species differing in salinity tolerance under combination of waterlogging and salinity.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 |

Voesenek LACJ, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytologist 206, 57–73.
Flood adaptive traits and processes: an overview.Crossref | GoogleScholarGoogle Scholar |

Wang F, Chen Z-H, Liu X, Shabala L, Yu M, Zhou M, Salih A, Shabala S (2019) The loss of RBOHD function modulates root adaptive responses to combined hypoxia and salinity stress in Arabidopsis. Environmental and Experimental Botany 158, 125–135.
The loss of RBOHD function modulates root adaptive responses to combined hypoxia and salinity stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Wany A, Gupta AK, Kumari A, Mishra S (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 |

Yin X, Zhang C, Song X, Jiang Y (2017) Interactive short-term effects of waterlogging and salinity stress on growth and carbohydrate, lipid peroxidation, and nutrients in two perennial ryegrass cultivars. Journal of the American Society for Horticultural Science 142, 110–118.
Interactive short-term effects of waterlogging and salinity stress on growth and carbohydrate, lipid peroxidation, and nutrients in two perennial ryegrass cultivars.Crossref | GoogleScholarGoogle Scholar |

Zandalinas SI, Sengupta S, Fritschi FB, Azad RK, Nechushtai R, Mittler R (2021) The impact of multifactorial stress combination on plant growth and survival. New Phytologist 230, 1034–1048.
The impact of multifactorial stress combination on plant growth and survival.Crossref | GoogleScholarGoogle Scholar |

Zeng F, Shabala L, Zhou M, Zhang G, Shabala S (2013) Barley responses to combined waterlogging and salinity stress: separating effects of oxygen deprivation and elemental toxicity. Frontiers in Plant Science 4, 313
Barley responses to combined waterlogging and salinity stress: separating effects of oxygen deprivation and elemental toxicity.Crossref | GoogleScholarGoogle Scholar |

Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224, 545–555.
Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast.Crossref | GoogleScholarGoogle Scholar |

Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiology 134, 849–857.
Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed.Crossref | GoogleScholarGoogle Scholar |