Potential role of nitrogen supplementation in alleviating flooding stress

Authors

  • Yeşim DAL-CANBAR Siirt University, Faculty of Agriculture, Horticulture Department, Kezer Campus Veysel Karani Mah. University Cad. No:1, 56100 Merkez/SİİRT (TR) https://orcid.org/0000-0002-3806-6465

DOI:

https://doi.org/10.15835/nbha53314601

Keywords:

antioxidant enzyme, flooding stress, nitrogen, macronutrients, PCA, prolin

Abstract

Flooding is one of the most damaging abiotic stresses, affecting seventeen million square kilometers of land surface per year, and it is expected to increase in severity in many parts of the world with climate change. Therefore, understanding the mechanisms by which plants cope with flooding stress is important for the development of new flood-tolerant cultivars. The aim of this study was to investigate the effects of different nitrogen doses [no-nitrogen(N0), 100 kg ha-1 (N10), and 200 kg ha-1 (N20)], on the physiological responses of plants under flooding stress. In this context, spinach plants were subjected to flooding stress, and several physiological, biochemical, and nutritional parameters were investigated. The results showed that flooding stress caused a decrease in aboveground fresh and dry weight of spinach, while chlorophyll a (Cl a), b (Cl b), and total chlorophyll (TCl), as well as carotenoid, protein, and proline contents, increased. In addition, the uptake of the macronutrients N, P, K, and Mg increased during flooding stress. N application under flooding stress alleviated its negative effects and suppressed the induction of H2O2 through increased proline biosynthesis. Similarly, Cl a, Cl b, and TCl levels minimized the negative effects of flooding stress. In conclusion, different N doses improved spinach plant parameters and alleviated the effects of flooding stress, with N10 application in particular N10 improved biomass by 22% under flooding producing significant results in suppressing the detrimental effects of stress.

References

Agarwal S, Pandey V (2004). Antioxidant enzyme responses to NaCl stress in Cassia angustifolia. Biologia Plantarum 48(4):555-560. http://dx.doi.org/10.1023/b:biop.0000047152.07878.e7

Aggarwal P, Choudhary KK, Singh AK, Chakraborty D (2006). Variation in soil strength and rooting characteristics of wheat in relation to soil management. Geoderma 136(1-2):353-363. http://dx.doi.org/10.1016/j.geoderma.2006.04.004

Álvarez-Robles T, Orozco Osuna YA, Álvarez Rodríguez FJ (2021). UX evaluation for websites targeting digital libraries with blind users. Investigación Bibliotecológica 35(89):169-194. http://dx.doi.org/10.22201/iibi.24488321xe.2021.89.58451

Angelini R, Federico R (1989). Histochemical evidence of polyamine oxidation and generation of hydrogen peroxide in the cell wall. Journal of Plant Physiology 135(2):212-217. http://dx.doi.org/10.1016/s0176-1617(89)80179-8

Apel K, Hirt H (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55(1):373-399. http://dx.doi.org/10.1146/annurev.arplant.55.031903.141701

Ashraf M A (2012). Waterlogging stress in plants: A review. African Journal of Agricultural Research 7(13): 1976-1981. http://dx.doi.org/10.5897/ajarx11.084

Aslam A, Mahmood A, Ur-Rehman H, Li C, Liang X, Shao J, …, Hassan MU (2023). Plant adaptation to flooding stress under changing climate conditions: Ongoing breakthroughs and future challenges. Plants (Basel).12(22):3824. https://doi.org/10.3390/plants12223824

Aydinoglu F, Akgul B (2019). Investigation of microRNA-mediated redox regulation in leaf growth zones during chilling stress tolerance of maize (Zea mays L.). Anadolu Tarım Bilimleri Dergisi 34(2):172-183. http://dx.doi.org/10.7161/omuanajas.482710

Bailey-Serres J, Voesenek L (2008). Flooding stress: Acclimation and genetic diversity. Annual Review of Plant Biology 59(1): 313-339. http://dx.doi.org/10.1146/annurev.arplant.59.032607.092752

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(6):160. http://dx.doi.org/10.3390/plants8060160

Basit F, Khalid M, El-Keblawy A, Sheteiwy MS, Sulieman S, Josko I, Zulfiqar F (2024). Hypoxia stress: Plant’s sensing, responses, and tolerance mechanisms. Environmental Science and Pollution Research 31:63458-63472. http://dx.doi.org/10.1007/s11356-024-35439-4

Bates LS, Waldren R, Teare I (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39:205-207. http://dx.doi.org/10.1007/bf00018060

Beutler AN, Giacomeli R, Alberto CM, Silva VN, da Silva Neto GF, Machado GA, Santos ATL (2014) Soil hydric excess and soybean yield and development in Brazil. Australian Journal of Crop Science 8(10):1461-1466.

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(1-2):248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3

Canali S, Diacono M, Ciaccia C, Masetti O, Tittarelli F, Montemurro F (2014). Alternative strategies for nitrogen fertilization of overwinter processing spinach (Spinacia oleracea L.) in Southern Italy. European Journal of Agronomy 54:47-53. http://dx.doi.org/10.1016/j.eja.2013.11.013

Caparrotta S, Masi E, Atzori G, Diamanti I, Azzarello E, Mancuso S, Pandolfi C (2019). Growing spinach (Spinacia oleracea L.) with different seawater concentrations: Effects on fresh, boiled and steamed leaves. Scientia Horticulturae 256:108540. http://dx.doi.org/10.1016/j.scienta.2019.05.067

Caruso G, De Pascale S, Cozzolino E, Cuciniello A, Cenvinzo V, Bonini P, … G, Rouphael Y (2019). Yield and nutritional quality of Vesuvian Piennolo tomato PDO as affected by farming system and biostimulant application. Agronomy 9(9):505. http://dx.doi.org/10.3390/agronomy9090505

Chance B, Maehly A (1955). Assay of catalases and peroxidases. Methods in Enzymology 2:764-755. http://dx.doi.org/10.1016/s0076-6879(55)02300-8

Chitwood J, Shi A, Evans M, Rom C ,.. Hensley D (2016). Effect of temperature on seed germination in spinach (Spinacia oleracea). HortScience, 51(12):1475-1478. http://dx.doi.org/10.21273/hortsci11414-16

Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017). Reactive oxygen species, abiotic stress and stress combination. The Plant Journal 90(5):856-867. http://dx.doi.org/10.1111/tpj.13299

Colmer T, Voesenek L (2009). Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36(8):665-681. http://dx.doi.org/10.1071/fp09144

Coussement JR, Villers SL, Nelissen H, Inzé D, Steppe K (2021). Turgor‐time controls grass leaf elongation rate and duration under drought stress. Plant, Cell & Environment 44(5):1361-1378. http://dx.doi.org/10.1111/pce.13989

Da Cruz LL, Cardoso LD, Pala D, De Paula H, Lamounier JA, Silva CAM, Volp ACP, De Freitas RN (2013). Metabolic syndrome components can predict C reactive protein concentration in adolescents. Nutricion hospitalaria 28(5):1580-1586. https://dx.doi.org/10.3305/nh.2013.28.5.6625

Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inzé D, Van Breusegem F (2000). Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57(5):779-795. http://dx.doi.org/10.1007/s000180050041

Demiral T, Türkan İ (2005). Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Envionmental and Experimental Botany 53(3):247-257. https://doi.org/10.1016/j.envexpbot.2004.03.017

Di Mola I, Cozzolino E, Ottaiano L, Giordano M, Rouphael Y, Colla G, Mori M (2019). Effect of vegetal-and seaweed extract-based biostimulants on agronomical and leaf quality traits of plastic tunnel-grown baby lettuce under four regimes of nitrogen fertilization. Agronomy 9(10):571. http://dx.doi.org/10.3390/agronomy9100571

Drew M, Sisworo E (1977). Early effects of flooding on nitrogen deficiency and leaf chlorosis in barley. New Phytologist 79(3):567-571. http://dx.doi.org/10.1111/j.1469-8137.1977.tb02241.x

Drew MC (1997). Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual review of plant biology 48(1):223-250. http://dx.doi.org/10.1146/annurev.arplant.48.1.223

Evans JR, Terashima I (1988). Photosynthetic characteristics of spinach leaves grown with different nitrogen treatments. Plant and Cell Physiology 29(1):157-165. http://dx.doi.org/10.1093/oxfordjournals.pcp.a077462

Fan H, Du C, Ding L, Xu Y (2014). Exogenous nitric oxide promotes waterlogging tolerance as related to the activities of antioxidant enzymes in cucumber seedlings. Russian Journal of Plant Physiology 61(3):366-373. http://dx.doi.org/10.1134/s1021443714030042

Foyer CH (2018). Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environmental and experimental botany 154:134-142. http://dx.doi.org/10.1016/j.envexpbot.2018.05.003

Gibbs J, Greenway H (2003). Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Functional Plant Biology 30(1):1-47. http://dx.doi.org/10.1071/pp98095

Gill SS, Tuteja N (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant physiology and biochemistry 48(12):909-930. https://doi.org/10.1016/j.plaphy.2010.08.016

Glazebrook HS, Robertson AI (1999). The effect of flooding and flood timing on leaf litter breakdown rates and nutrient dynamics in a river red gum (Eucalyptus camaldulensis) forest. Australian Journal of Ecology 24(6):625-635. http://dx.doi.org/10.1046/j.1442-9993.1999.00992.x

Guan C, Cui X, Liu H-y, Li X, Li M-q, Zhang Y-W (2020). Proline biosynthesis enzyme genes confer salt tolerance to switchgrass (Panicum virgatum L.) in cooperation with polyamines metabolism. Frontiers in plant science 11:46. http://dx.doi.org/10.3389/fpls.2020.00046

Guo S, Kaldenhoff R, Uehlein N, Sattelmacher B, Brueck H (2007). Relationship between water and nitrogen uptake in nitrate‐and ammonium‐supplied Phaseolus vulgaris L. plants. Journal of Plant Nutrition and Soil Science 170(1):73-80. http://dx.doi.org/10.1002/jpln.200625073

Gupta KJ, Igamberdiev AU (2016.) Reactive nitrogen species in mitochondria and their implications in plant energy status and hypoxic stress tolerance. Frontiers in Plant Science 7:369. http://dx.doi.org/10.3389/fpls.2016.00369

Halliwell B (2006). Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant physiology 141(2):312-322. http://dx.doi.org/10.1104/pp.106.077073

Hasanuzzaman M, Bhuyan MB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fotopoulos V (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants 9(8):681. https://doi.org/10.3390/antiox9080681

Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012). Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateswarlu B, Shanker A, Shanker C, Maheswari M (Eds). Crop Stress and its Management: Perspectives and Strategies. Springer, Dordrecht pp 261-315. http://dx.doi.org/10.1007/978-94-007-2220-0_8

Havir EA, McHale NA (1987). Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant physiology 84(2):450-455. https://doi.org/10.1104/pp.84.2.450

Irfan M, Hayat S, Hayat Q, Afroz S, Ahmad A (2010). Physiological and biochemical changes in plants under waterlogging. Protoplasma 241:3-17. http://dx.doi.org/10.1007/s00709-009-0098-8

Jackson M, Colmer T (2005). Response and adaptation by plants to flooding stress. Annals of botany 96(4):501-505. http://dx.doi.org/10.1093/aob/mci205

Kal Ü, Dal Y, Kayak N, Yavuz D, Türkmen Ö, Seymen M (2023). Application of nitrogen for mitigating the adverse effects of flooding stress in lettuce. Journal of Plant Nutrition 46(20):4664-4678. http://dx.doi.org/10.1080/01904167.2023.2240831

Kapoor D, Singh S, Kumar V, Romero R, Prasad R, Singh J (2019). Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene 19:100182. http://dx.doi.org/10.1016/j.plgene.2019.100182

Kasım MU, Kasım R (2016). Effects of the different wavelength ultraviolet radiation on postharvest quality of fresh-cut spinach. Yuzuncu Yıl University Journal of Agricultural Sciences 26(3):348-359.

Kaur G, Asthir BJBP (2015). Proline: a key player in plant abiotic stress tolerance. Biologia plantarum 59(4):609-619. https://doi.org/10.1007/s10535-015-0549-3

Kaur G, Singh G, Motavalli PP, Nelson KA, Orlowski JM, Golden BR (2020). Impacts and management strategies for crop production in waterlogged or flooded soils: A review. Agronomy Journal 112(3):1475-1501. http://dx.doi.org/10.1002/agj2.20093

Kerim MC, Başak H, Turan M (2020). The effect of different doses of salt and mycorrhiza applications on the content of hormones, antioxidants, phenolic compounds, and organic acids in peppers. Mustafa Kemal University Journal of Agricultural Sciences. 25(3):488-498. http://dx.doi.org/10.37908/mkutbd.793222

Khan A, Tan DKY, Afridi MZ, Luo H, Tung SA, Ajab M, Fahad S (2017). Nitrogen fertility and abiotic stresses management in cotton crop: a review. Environmental Science and Pollution Research 24(17):14551-14566. http://dx.doi.org/10.1007/s11356-017-8920-x

Kim KH, Cho MJ, Kim J-M, Lee T, Heo JH, Jeong JY, Lee J, Moon J-K, Kang S (2019). Growth response and developing simple test method for waterlogging stress tolerance in soybean. Journal of Crop Science and Biotechnology 22(4):371-378. http://dx.doi.org/10.1007/s12892-019-0271-0

Kıymacı G, Arı BÇ, Türkmen Ö, Paksoy M, Kal Ü, Metin D, Özen RN (2024). Morph-physiological and biochemical properties effects of exogenous nitric oxide applications on spinach under flooding stress conditions. https://doi.org/10.21203/rs.3.rs-4199375/v1

Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter (2010). Biogeochemistry of paddy soils. Geoderma 157(1-2):1-14. http://dx.doi.org/10.1016/j.geoderma.2010.03.009

Kozlowski TT (1984). Extent, causes, and impact of flooding. Flooding and plant growth. New York: Academic Elsevier pp 1-7. https://doi.org/10.1016/B978-0-12-424120-6.50006-7

Lal M, Kumari A, Pooja, Sheokand S (2019) Reactive oxygen species, reactive nitrogen species and oxidative metabolism under waterlogging stress. In reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mechanisms Wiley Hoboken 777-812. https://doi.org/10.1002/9781119468677.ch34

Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003). Nitric oxide: the versatility of an extensive signal molecule. Annual review of plant biology,54(1):109-136. http://dx.doi.org/10.1146/annurev.arplant.54.031902.134752

Lawlor DW (2002). Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. Journal of experimental Botany 53(370):773-787. http://dx.doi.org/10.1093/jexbot/53.370.773

Lee IJ (2022). Nitric oxide modulates Glycine max l. growth and physio-molecular responses during flooding stress. Annals of Agricultural & Crop 7(3): 1-18. http://dx.doi.org/10.26420/annagriccropsci.2022.1116

Lichtenthaler HK, Buschman C (2001). Chlorophylls and carotenoids: Measurement and characterization by UV‐VIS spectroscopy. Current protocols in food analytical chemistry 1(1):F4.3.1-F4.3.8. http://dx.doi.org/10.1002/0471142913.faf0403s01

Liu D, Paul AL, Morgan KT (2022). Effects of oxygen fertilization on damage reduction in flooded snap bean (Phaseolus vulgaris L.). Scientific Reports 12:4282. https://doi.org/10.1038/s41598-022-08165-5

Loreti E, van Veen H, Perata P (2016). Plant responses to flooding stress. Current opinion in plant biology 33:64-71. http://dx.doi.org/10.1016/j.pbi.2016.06.005

Lutts S, Kinet J, Bouharmont J (1996). NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of botany 78(3): 389-398. http://dx.doi.org/10.1006/anbo.1996.0134

Madhava Rao KV, Sresty TVS (2000). Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Science 157(1):113-128. https://doi.org/10.1016/s0168-9452(00)00273-9.

Martínez-Alcántara B, Jover S, Quinones A, Forner-Giner M Á, Rodríguez-Gamir J, Legaz F, … Iglesias DJ (2012). Flooding affects uptake and distribution of carbon and nitrogen in citrus seedlings. Journal of Plant Physiology 169(12):1150-1157. http://dx.doi.org/10.1016/j.jplph.2012.03.016

Meena M, Divyanshu K, Kumar S, Swapnil P, Zehra A, Shukla V, … Upadhyay R (2019). Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon 5(12): e02952 http://dx.doi.org/10.1016/j.heliyon.2019.e02952

Men S, Chen H, Chen S, Zheng S, Shen X, Wang C, Yang Z, Liu D (2020). Effects of supplemental nitrogen application on physiological characteristics, dry matter and nitrogen accumulation of winter rapeseed (Brassica napus L.) under waterlogging stress. Scientific Reports, 10(1):10201. http://dx.doi.org/10.1038/s41598-020-67260-7

Muchate N, Rajurkar N, Suprasanna P, Nikam T (2018). Evaluation of Spinacia oleracea (L.) for phytodesalination and augmented production of bioactive metabolite, 20-hydroxyecdysone. International journal of phytoremediation 20(10):981-994. http://dx.doi.org/10.1080/15226514.2018.1452184

Mugnai S, Azzarello E, Baluška F, Mancuso S (2012). Local root apex hypoxia induces NO-mediated hypoxic acclimation of the entire root. Plant and Cell Physiology 53(5):912-920. http://dx.doi.org/10.1093/pcp/pcs034

Muhammad I, Yang L, Ahmad S, Farooq S, Al-Ghamdi, AA, Khan A, Zhou XB (2022). Nitrogen fertilizer modulates plant growth, chlorophyll pigments and enzymatic activities under different irrigation regimes. Agronomy 12(4):845. https://doi.org/10.3390/agronomy12040845

Navarrete JRC (2016). Development of a breeding strategy for nitrogen use efficiency in spinach (Spinacia oleracea L.) PhD thesis. Wageningen University, Wageningen. https://doi.org/10.18174/379403

Nishihara E, Inoue M, Kondo K, Takahashi K, Nakata N (2001). Spinach yield and nutritional quality affected by controlled soil water matric head. Agricultural Water Management, 51(3):217-229. http://dx.doi.org/10.1016/s0378-3774(01)00123-8

Orcutt DM, Nilsen ET (2000). Physiology of plants under stress: Soil and biotic factors (Vol. 2). John Wiley & Sons p 704.

Overeem R (2015) Physiology and genetic variation of nitrogen use efficiency in spinach (Spinacia oleracea L.). PhD thesis,Wageningen University, Wageningen.

Pan J, Sharif R, Xu X, Chen X (2021). Mechanisms of waterlogging tolerance in plants: Research progress and prospects. Frontiers in Plant Science 11:627331. https://doi.org/10.3389/fpls.2020.627331

Panda D, Sharma SG, Sarkar RK (2008). Chlorophyll fluorescence parameters, CO2 photosynthetic rate and regeneration capacity as a result of complete submergence and subsequent re-emergence in rice (Oryza sativa L.). Aquatic Botany 88(2):127-133. https://doi.org/10.1016/j.aquabot.2007.08.012.

Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017). Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Frontiers in plant science 8:215288. https://doi.org/10.3389/fpls.2027.00581

Patel PK, Singh AK, Tripathi N, Yadav D, Hemantaranjan A (2014). Flooding: abiotic constraint limiting vegetable productivity. Advances in Plants Agriculture Research 1(3):00016.

Phukan UJ, Sonal Mishra S, Shukla RK (2015). Waterlogging and submergence stress: affects and acclimation. Critical Reviews in Biotechnology 36(5):956-966. https://doi.org/10.3109/07388551.2015.1064856

Ponnamperuma FN (1984). Effects of flooding on soils. In: Kozlowski TT. Flooding and plant growth. Academic Press pp 9-45. https://doi.org/10.1016/b978-0-12-424120-6.50007-9

Qi J, Song CP, Wang B, Zhou J, Kangasjärvi J, Zhu JK, Gong Z (2018). Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. Journal of integrative plant biology 60(9):805-826. https://doi.org/10.1111/jipb.12654

Qi X, Li Q, Ma X, Qian C, Wang H, Ren N, … Chen X (2019). Waterlogging-induced adventitious root formation in cucumber is regulated by ethylene and auxin through reactive oxygen species signalling. Plant Cell Environ 42:1458-1470. https://doi.org/10.1111/pce.13504

Radmann EB, Klumb EK, Deuner S, Bianchi VJ (2018). Antioxidant capacity in leaf and root tissues of prunus spp under flooding. Journal of Experimental Agriculture International 26(3):1-10. https://doi.org/10.9734/jeai/2018/43650

Rao R, Li Y (2003). Management of flooding effects on growth of vegetable and selected field crops. HortTechnology 13(4):610-616. https://doi.org/10.21273/horttech.13.4.0610

Rehman AU, Bashir F, Ayaydin F, Kóta Z, Páli T, Vass I (2021). Proline is a quencher of singlet oxygen and superoxide both in in vitro systems and isolated thylakoids. Physiologia Plantarum 172(1):7-18. https://doi.org/10.1111/ppl.13265

Ren B, Dong S, Zhao B, Liu P, Zhang J (2017) Responses of Nitrogen Metabolism, Uptake and Translocation of Maize to Waterlogging at Different Growth Stages. Frontiers in Plant Science 8:1216. http://dx.doi.org/10.3389/fpls.2017.01216

Ren B, Zhang J, Li X, Fan X, Dong S, Liu P, Zhao B (2014). Effects of waterlogging on the yield and growth of summer maize under field conditions. Canadian Journal of Plant Science 94(1):23-31. https://doi.org/10.4141/cjps2013-175

Rouphael Y, Giordano M, Cardarelli M, Cozzolino E, Mori M, Kyriacou MC, …. Colla G (2018). Plant- and seaweed-based extracts increase yield but differentially modulate nutritional quality of greenhouse spinach through biostimulant action. Agronomy 8(7):126. http://dx.doi.org/10.3390/agronomy8070126

Sanchez FJ, Andres EF, Tenorio JL, Ayerbe L (2004). Growth of epicotyls, turgor maintenance and osmotic adjustment in pea plants (Pisum sativum L.) subjected to water stress, Field Crops Research 86(1):81-90. https://doi.org/10.1016/S0378-4290(03)00121-7

Sasidharan R, Hartman S, Liu Z, Martopawiro S, Sajeev N, van Veen H, … Voesenek LA (2018). Signal dynamics and interactions during flooding stress. Plant physiology 176(2):1106-1117. https://doi.org/10.1104/pp.17.01232

Şavkan AN, Başak H, Türkmen Ö (2024). Morphological characterization of some capia pepper (Capsicum annuum L.) genotypes. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi 27(6):1332-1342. https://doi.org/10.18016/ksutarimdoga.vi.1440798

Şavkan AN, Dal Canbar Y, Türkmen Ö (2025). Identification and Selection of Genetic Diversity of Some Selected Summer Squash (Cucurbita pepo L.). Yuzuncu Yıl University Journal of Agricultural Sciences 35(1):121-134. https://doi.org/10.29133/yyutbd.1567738

Schaffer B, Davies FS, Crane JH (2006). Responses of subtropical and tropical fruit trees to flooding in calcareous soil. HortScience 41(3):549-555. http://dx.doi.org/10.21273/hortsci.41.3.549

Seymen M (2021). How does the flooding stress occurring in different harvest times affect the morpho-physiological and biochemical characteristics of spinach? Scientia Horticulturae 275:109713. https://doi.org/10.1016/j.scienta.2020.109713.

Seymen M, Alkhateb R, Mutlu A, Yavuz D (2024). Do exogenous melatonin and nitric oxide mitigate the adverse effects of flooding stress in spinach?. Scientia Horticulturae 330:113081. https://doi.org/10.1016/j.scienta.2024.113081

Singh A, Kumar A, Yadav S, Singh IK (2019). Reactive oxygen species-mediated signaling during abiotic stress. Plant Gene 18:100173. https://doi.org/10.1016/j.plgene.2019.100173

Skujins S (1998). Handbook for ICP-AES (Varian-Vista). A Short Guide to Vista Series ICP-AES Operation (Version 1.0). Varian International AG, Zug, Switzerland.

Taiz L, Zeiger E (2002). Photosynthesis: physiological and ecological considerations. Plant Physiol 9:172-174. https://doi.org/10.1093/hesc/9780197614204.003.0014

Tang J, Xie Y, Wu Y, Liu G (2023). Influence of precipitation change and topography characteristics on the development of farmland gully in the black soil region of northeast China. Catena 224:106999. https://doi.org/10.1016/j.catena.2023.106999

Taş T (2021). The effect of different nitrogen fertilizer levels applied to the dent hybrid corn variety (Zea mays L.) under GAP region conditions on grain yield, quality, and chlorophyll content. Turkish Journal of Agricultural and Natural Sciences 8(3):655-665. https://doi.org/10.30910/turkjans.909545

Thiruvengadam R, Venkidasamy B, Easwaran M, Chi HY, Thiruvengadam M, Kim SH (2024). Dynamic interplay of reactive oxygen and nitrogen species (ROS and RNS) in plant resilience: Unveiling the signaling pathways and metabolic responses to biotic and abiotic stresses. Plant Cell Reports 43(8):198. https://doi.org/10.1007/s00299-024-03281-0

Thomas RM, Verma AK, Prakash C, Krishna H, Prakash S, Kumar A (2019). Utilization of Inland saline underground water for bio-integration of Nile tilapia (Oreochromis niloticus) and spinach (Spinacia oleracea). Agricultural Water Management 222:154-160. https://doi.org/10.1016/j.agwat.2019.06.001

Unger IM, Kennedy AC, Muzika RM (2009). Flooding effects on soil microbial communities. Applied Soil Ecology 42(1):1-8. https://doi.org/10.1016/j.apsoil.2009.01.007

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(1):59-66. https://doi.org/10.1016/S0168-9452(99)00197-1

Walter S, Heuberger H, Schitzler WH (2004). Sensibility of different vegetables to oxygen deficiency and aeration with H2O2 in the rhizosphere. In VII International Symposium on Protected Cultivation in Mild Winter Climates: Production, Pest Management and Global Competition 659:499-508.

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. https://doi.org/10.1111/nph.12048

Withman FH, Blaydes DF, Devlin RM (1971) Experiments in plant physiology. Van Nostrand, New York p 245.

Yadav DK, Hemantaranjan A (2017). Mitigating effects of paclobutrazol on flooding stress damage by shifting biochemical and antioxidant defense mechanisms in mungbean (Vigna radiata L.) at pre-flowering stage. Legume Research-An International Journal 40(3):453-461.

Yamauchi T, Yoshioka M, Fukazawa A, Mori H, Nishizawa NK, Tsutsumi N, … Nakazono M (2017). An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. The Plant Cell 9:775-790. https://doi.org/10.1105/tpc.16.00976

Yavuz D, Kılıç E, Seymen M, Dal Y, Kayak N, Kal Ü, Yavuz N (2022). The effect of irrigation water salinity on the morph-physiological and biochemical properties of spinach under deficit irrigation conditions. Scientia Horticulturae 304:111272.https://doi.org/10.1016/j.scienta.2022.111272

Yavuz D, Seymen M, Süheri S, Yavuz N, Türkmen Ö, Kurtar ES (2020). How do rootstocks of citron watermelon (Citrullus lanatus var. citroides) affect the yield and quality of watermelon under deficit irrigation? Agricultural Water Management 241:106351. https://doi.org/10.1016/j.agwat.2020.106351

Yavuz D, Seymen M, Yavuz N, Çoklar H, Ercan M (2021). Effects of water stress applied at various phenological stages on yield, quality, and water use efficiency of melon. Agricultural Water Management 246:106673. https://doi.org/10.1016/j.agwat.2020.106673

Yordanova R, Popova L (2001). Photosynthetic response of barley plants to soil flooding. Photosynthetica 39(4):515-520. https://doi.org/10.1023/A:1015643710177

Zahra N, Hafeez MB, Shaukat K, Wahid A, Hussain S, Naseer R, … Farooq M (2021) Hypoxia and anoxia stress: Plant responses and tolerance mechanisms. Journal of Agronomy and Crop Science 207(2):249-284. https://doi.org/10.1111/jac.12471

Zhang Q, Qin W, Cao W, Jiao J, Yin Z, Xu H (2023). Response of erosion reduction effect of typical soil and water conservation measures in cropland to rainfall and slope gradient changes and their applicable range in the Chinese Mollisols Region, Northeast China. International Soil and Water Conservation Research 11(2):251-262. https://doi.org/10.1016/j.iswcr.2022.10.005

Zhang Y, Li, G, Dong H, Li C (2021). Waterlogging stress in cotton: Damage, adaptability, alleviation strategies, and mechanisms. The Crop Journal 9(2):257-270. https://doi.org/10.1016/j.cj.2020.08.005

Zheng Y, Xiang S, Zhang H, Ye K, Zhang Y, Ge Y, Feng X, Bao X, Chen J, Zhu X (2021). Vitamin B12 enriched in spinach and its effects on gut microbiota. Journal of Agricultural and Food Chemistry 69(7):2204-2212. https://doi.org/10.1021/acs.jafc.0c07597

Zhou W (2007). Drainage and flooding in karst terranes. Environmental Geology 51(6):963-973. http://dx.doi.org/10.1007/s00254-006-0365-3

Zhou W, Chen F, Meng Y, Chandrasekaran U, Luo X, Yang W (2020). Plant waterlogging/flooding stress responses: from seed germination to maturation. Plant Physiology and Biochemistry 148:228-236. http://dx.doi.org/10.1016/j.plaphy.2020.01.020

Downloads

Published

2025-09-21

How to Cite

DAL-CANBAR, Y. (2025). Potential role of nitrogen supplementation in alleviating flooding stress. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 53(3), 14601. https://doi.org/10.15835/nbha53314601

Issue

Section

Research Articles
CITATION
DOI: 10.15835/nbha53314601