Abstract
Beet growth and sugar production are strongly impacted by drought. Nitric oxide (NO) donors, such as sodium nitroprusside (SNP), have shown promising results in the alleviation of drought stress; however, these effects were not evaluated in beet. The aim of this study was to evaluate the effects of SNP on the morphophysiology and sugar content of beets for human consumption under moderate and severe drought stresses, as well as the role of SNP in the recovery of plants upon re-watering. For this, two experimental sets were performed. In the first, beet plantlets were irrigated with 80% of water holding capacity (WHC—well-watered), 15% WHC (moderate stress), or water restricted (severe stress) up to 36 days after sowing (DAS). In the second, beets were irrigated with 80% WHC, 15% WHC, re-watered after water restriction, or late water restriction (from 44 to 66 DAS). In both sets, beets were leaf sprayed with 100-µM SNP or water. The gas exchanges, photosynthetic pigments, chlorophyll fluorescence, electrolyte leakage, water content, and growth were determined in both developmental stages, and sugar content was determined in 66-d-old plants. 15% WHC and water restriction reduced growth and photosynthetic capacity of plants in both developmental stages, with 36-d-old plantlets being more sensitive than 66-d-old beet plants. SNP reversed the negative effects of 15% WHC but not those of water restriction. Re-watering fully recovered growth and photosynthetic capacity of drought-stressed beets independently of SNP. In summary, SNP alleviated moderate drought stress in beet by modulating its photosynthetic capacity.
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Agathokleous E, Feng ZZ, Peñuelas J (2020) Chlorophyll hormesis: are chlorophylls major components of stress biology in higher plants? Sci Total Environ 726:138637. https://doi.org/10.1016/j.scitotenv.2020.138637
Bajji M, Kinet JM, Lutts S (2001) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul 36:61–70. https://doi.org/10.1023/A:1014732714549
Bloch D, Hoffmann CM, Märländer B (2006) Impact of water supply on photosynthesis, water use and carbon isotope discrimination of sugar beet genotypes. Eur J Agron 24:218–225. https://doi.org/10.1016/j.eja.2005.08.004
Chavoushi M, Najafi F, Salimi A, Angaji SA (2020) Effect of salicylic acid and sodium nitroprusside on growth parameters, photosynthetic pigments and secondary metabolites of safflower under drought stress. Sci Hortic 259:108823. https://doi.org/10.1016/j.scienta.2019.108823
Chhikara N, Kushwaha K, Sharma P, Gat Y, Panghal A (2019) Bioactive compounds of beetroot and utilization in food processing industry: A critical review. Food Chem 272:192–200. https://doi.org/10.1016/j.foodchem.2018.08.022
Choluj D, Karwowska R, Jasińska M, Haber G (2004) Growth and dry matter partitioning in sugar beet plants (Beta vulgaris L.) under moderate drought. Plant Soil Environ 50:265–272
Coussement JR, Villers SLY, Nelissen H, Inzé D, Steppe K (2021) Turgor-time controls grass leaf elongation rate and duration under drought stress. Plant Cell Environ 44:1361–1378. https://doi.org/10.1111/pce.13989
Cruz CD (2016) Genes Software—extended and integrated with the R, Matlab and Selegen. Acta Sci Agron 38:547–552. https://doi.org/10.4025/actasciagron.v38i4.32629
Dhami N, Cazzonelli CI (2020) Environmental impacts on carotenoid metabolism in leaves. Plant Growth Regul 92:455–477. https://doi.org/10.1007/s10725-020-00661-w
Ekinci M, Ors S, Yildirim E, Turan METIN, Sahin U, Dursun A, Kul R (2020) Determination of physiological indices and some antioxidant enzymes of chard exposed to nitric oxide under drought stress. Russ J Plant Physiol 67:740–749. https://doi.org/10.1134/S1021443720040056
Farooq M, Basra SMA, Wahid A, Rehman H (2009) Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agron Crop Sci 195:254–261. https://doi.org/10.1111/j.1439-037X.2009.00367.x
Fugate KK, Lafta AM, Eide JD et al (2018) Methyl jasmonate alleviates drought stress in young sugar beet (Beta vulgaris L.) plants. J Agron Crop Sci 204:566–576. https://doi.org/10.1111/jac.12286
Gohari G, Alavi Z, Esfandiari E et al (2020) Interaction between hydrogen peroxide and sodium nitroprusside following chemical priming of Ocimum basilicum L. against salt stress. Physiol Plant 168:361–373. https://doi.org/10.1111/ppl.13020
Goltsev VN, Kalaji HM, Paunov M et al (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63:869–893. https://doi.org/10.1134/S1021443716050058
Habib N, Ali Q, Ali S et al (2020) Use of nitric oxide and hydrogen peroxide for better yield of wheat (Triticum aestivum L.) under water deficit conditions: growth, osmoregulation, and antioxidative defense mechanism. Plants 9:285. https://doi.org/10.3390/plants9020285
Haile GG, Tang Q, Li W, Liu X, Zhang X (2020) Drought: progress in broadening its understanding. Wiley Interdiscip Rev Water 7:e1407. https://doi.org/10.1002/WAT2.1407
Hajihashemi S, Skalicky M, Brestic M, Pavla V (2021) Effect of sodium nitroprusside on physiological and anatomical features of salt-stressed Raphanus sativus. Plant Physiol Biochem 169:160–170. https://doi.org/10.1016/j.plaphy.2021.11.013
Hao GP, Xing Y, Zhang JH (2008) Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signaling of maize seedling. J Integr Plant Biol 50:435–442. https://doi.org/10.1111/j.1744-7909.2008.00637.x
Hasibeder R, Fuchslueger L, Richter A, Bahn M (2015) Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol 205:1117–1127. https://doi.org/10.1111/nph.13146
He M, Mei S, Zhai Y, Geng G, Yu L, Wang Y (2022) Effects of melatonin on the growth of sugar beet (Beta vulgaris L.) seedlings under drought stress. J Plant Growth Regul. https://doi.org/10.1007/s00344-022-10860-6
Henschel JM, Dantas EFO, Soares VA et al (2022) Salicylic acid mitigates the effects of mild drought stress on radish (Raphanus sativus) growth. Funct Plant Biol 49:822–831. https://doi.org/10.1071/FP22040
Hoffmann CM, Kenter C (2018) Yield potential of sugar beet—have we hit the ceiling? Front Plant Sci 9:289. https://doi.org/10.3389/fpls.2018.00289
Islam MJ, Kim JW, Begum MK, Sohel MAT, Lim YS (2020) Physiological and biochemical changes in sugar beet seedlings to confer stress adaptability under drought condition. Plants 9:1–27. https://doi.org/10.3390/plants9111511
Jangid KK, Dwivedi P (2017) Physiological and biochemical changes by nitric oxide and brassinosteroid in tomato (Lycopersicon esculentum Mill.) under drought stress. Acta Physiol Plant 39:1–10. https://doi.org/10.1007/s11738-017-2373-1
Kalaji HM, Jajoo A, Oukarroum A et al (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:1–11. https://doi.org/10.1007/s11738-016-2113-y
Khodadadi S, Chegini MA, Soltani A, Ajam-Norouzi H, Sadeghzadeh-Hemayati S (2020) Influence of foliar-applied humic acid and some key growth regulators on sugar beet (Beta vulgaris L.) under drought stress: antioxidant defense system, photosynthetic characteristics and sugar yield. Sugar Tech 22:765–772. https://doi.org/10.1007/s12355-020-00839-6
Kumar D, Ohri P (2023) Say “NO” to plant stresses: Unravelling the role of nitric oxide under abiotic and biotic stress. Nitric Oxide. https://doi.org/10.1016/j.niox.2022.11.004
Lau SE, Hamdan MF, Pua TL, Saidi NB, Tan BC (2021) Plant nitric oxide signaling under drought stress. Plants 10:360. https://doi.org/10.3390/plants10020360
Laxa M, Liebthal M, Telman W, Chibani K, Dietz KJ (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants 8:94. https://doi.org/10.3390/antiox8040094
León J, Costa-Broseta Á (2020) Present knowledge and controversies, deficiencies, and misconceptions on nitric oxide synthesis, sensing, and signaling in plants. Plant Cell Environ 43:1–15. https://doi.org/10.1111/pce.13617
Li HD, Wang WB, Li PM et al (2013) Effects of addition of external nitric oxide on the allocation of photosynthetic electron flux in Rumex K-1 leaves under osmotic shock. Photosynthetica 51:509–516. https://doi.org/10.1007/s11099-013-0049-7
Li Y, Liu N, Fan H et al (2019) Effects of deficit irrigation on photosynthesis, photosynthate allocation, and water use efficiency of sugar beet. Agric Water Manag 223:105701. https://doi.org/10.3390/plants9111511
Liao WB, Huang GB, Yu JH, Zhang ML (2012) Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiol Biochem 58:6–15. https://doi.org/10.1016/j.plaphy.2012.06.012
Monti A, Brugnoli E, Scartazza A, Amaducci MT (2006) The effect of transient and continuous drought on yield, photosynthesis and carbon isotope discrimination in sugar beet (Beta vulgaris L.). J Exp Bot 57:1253–1262. https://doi.org/10.1093/jxb/erj091
Monti A, Barbanti L, Venturi G (2007) Photosynthesis on individual leaves of sugar beet (Beta vulgaris) during the ontogeny at variable water regimes. Ann Appl Biol 151:155–165. https://doi.org/10.1111/j.1744-7348.2007.00162.x
Mukarram M, Choudhary S, Kurjak D, Petek A, Khan MMA (2021) Drought: sensing, signalling, effects and tolerance in higher plants. Physiol Plant 172:1291–1300. https://doi.org/10.1111/ppl.13423
Munawar A, Akram NA, Ahmad A, Ashraf M (2019) Nitric oxide regulates oxidative defense system, key metabolites and growth of broccoli (Brassica oleracea L.) plants under water limited conditions. Sci Hortic 254:7–13. https://doi.org/10.1016/j.scienta.2019.04.072
Nabi RBS, Tayade R, Hussain A et al (2019) Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ Exp Bot 161:120–133. https://doi.org/10.1016/j.envexpbot.2019.02.003
Panella L (2010) Sugar beet as an energy crop. Sugar Tech 12:288–293. https://doi.org/10.1007/s12355-010-0041-5
Pradhan N, Singh P, Dwivedi P, Pandey DK (2020) Evaluation of sodium nitroprusside and putrescine on polyethylene glycol induced drought stress in Stevia rebaudiana Bertoni under in vitro condition. Ind Crops Prod 154:112754. https://doi.org/10.1016/j.indcrop.2020.112754
Praveen A (2022) Nitric oxide mediated alleviation of abiotic challenges in plants. Nitric Oxide. https://doi.org/10.1016/j.niox.2022.08.005
Ren T, Weraduwage SM, Sharkey TD (2019) Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cell morphology. J Exp Bot 70:1153–1165. https://doi.org/10.1093/jxb/ery448
Rezayian M, Ebrahimzadeh H, Niknam V (2020) Nitric oxide stimulates antioxidant system and osmotic adjustment in soybean under drought stress. J Soil Sci Plant Nutr 20:1122–1132. https://doi.org/10.1007/s42729-020-00198-x/Published
Romano A, Sorgonà A, Lupini A et al (2013) Morpho-physiological responses of sugar beet (Beta vulgaris L.) genotypes to drought stress. Acta Physiol Plant 35:853–865. https://doi.org/10.1007/s11738-012-1129-1
Sahay S, Khan E, Gupta M (2019) Nitric oxide and abscisic acid protects against PEG-induced drought stress differentially in Brassica genotypes by combining the role of stress modulators, markers and antioxidants. Nitric Oxide 89:81–92. https://doi.org/10.1016/j.niox.2019.05.005
Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought: Do we have all the answers? Plant Sci 239:44–55. https://doi.org/10.1016/j.plantsci.2015.07.012
Santos SK, Gomes DS, Santos LWO et al (2022) Exogenous carnitine mitigates the deleterious effects of mild-water stress on arugula by modulating morphophysiological responses. J Plant Growth Regul. https://doi.org/10.1007/s00344-022-10868-y
Seleiman MF, Al-Suhaibani N, Ali N et al (2021) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants. https://doi.org/10.3390/plants
Shaw B, Thomas TH, Cooke DT (2002) Responses of sugar beet (Beta vulgaris L.) to drought and nutrient deficiency stress. Plant Growth Regul 37:77–83. https://doi.org/10.1023/A:1020381513976
Silveira NM, Hancock JT, Frungillo L et al (2017) Evidence towards the involvement of nitric oxide in drought tolerance of sugarcane. Plant Physiol Biochem 115:354–359. https://doi.org/10.1016/j.plaphy.2017.04.011
Sousa LF, Menezes-Silva PE, Lourenço LL et al (2020) Improving water use efficiency by changing hydraulic and stomatal characteristics in soybean exposed to drought: the involvement of nitric oxide. Physiol Plant 168:576–589. https://doi.org/10.1111/ppl.12983
Stevanato P, Chiodi C, Broccanello C et al (2019) Sustainability of the sugar beet crop. Sugar Tech 21:703–716. https://doi.org/10.1007/s12355-019-00734-9
Sun H, Feng F, Liu J, Zhao Q (2018) Nitric oxide affects rice root growth by regulating auxin transport under nitrate supply. Front Plant Sci 9:1–15. https://doi.org/10.3389/fpls.2018.00659
Sundararajan S, Shanmugam R, Rajendran V, Sivakumar HP, Ramalingam S (2022) Sodium nitroprusside and putrescine mitigate PEG-induced drought stress in seedlings of Solanum lycopersicum. J Soil Sci Plant Nutr 22:1019–1032. https://doi.org/10.1007/s42729-021-00710-x
Takahashi S, Yamasaki H (2002) Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett 512:145–148. https://doi.org/10.1016/S0014-5793(02)02244-5
Waadt R, Seller CA, Hsu P-K et al (2022) Plant hormone regulation of abiotic stress responses. Nat Rev Mol Cell Biol 23:680–694. https://doi.org/10.1038/s41580-022-00479-6
Wang M, Li Q, Fu S, Xiao D, Dong B (2005) Effects of exogenous nitric oxide on drought-resistance of poplar. J Appl Ecol 16:805–810
Wang P, Du Y, Hou YJ et al (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci USA 112:613–618. https://doi.org/10.1073/pnas.1423481112
Wani KI, Naeem M, Castroverde CDM, Kalaji HM, Albaqami M, Aftab T (2021) Molecular mechanisms of nitric oxide (NO) signaling and reactive oxygen species (ROS) homeostasis during abiotic stresses in plants. Int J Mol Sci 22:9656. https://doi.org/10.3390/ijms22179656
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Wodala B, Ördög A, Horváth F (2010) The cost and risk of using sodium nitroprusside as a NO donor in chlorophyll fluorescence experiments. J Plant Physiol 167:1109–1111. https://doi.org/10.1016/j.jplph.2010.03.013
Xu L, Chen N, Zhang X (2019) Global drought trends under 1.5 and 2°C warming. Int J Climatol 39:2375–2385. https://doi.org/10.1002/joc.5958
Yang H, Mu J, Chen L et al (2015) S-Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615. https://doi.org/10.1104/pp.114.255216
Yang X, Lu M, Wang Y et al (2021) Response mechanism of plants to drought stress. Horticulturae 7:50. https://doi.org/10.3390/horticulturae7030050
Yemn EW, Willis AJ (1954) The estimation off carbohydrate in plant extracts by antrone. Bioch J 57:504–514
Yolcu S, Alavilli H, Ganesh P, Panigrahy M, Song K (2021) Salt and drought stress responses in cultivated beets (Beta vulgaris L.) and wild beet (Beta maritima L.). Plants 10:1843. https://doi.org/10.3390/plants10091843
Zhang A, Zhang J, Zhang J et al (2011) Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol 52:181–192. https://doi.org/10.1093/pcp/pcq187
Zhao C, Cai S, Wang Y, Chen ZH (2016) Loss of nitrate reductases NIA1 and NIA2 impairs stomatal closure by altering genes of core ABA signaling components in Arabidopsis. Plant Signal Behav 11:1456–1469. https://doi.org/10.1080/15592324.2016.1183088
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We thank the National Council for Scientific and Technological Development (CNPq—Brazil), Coordination for the Improvement of Higher Education Personnel (CAPES), and Federal University of Paraíba (FAPESQ/UFPB) for the scholarships granted to the students.
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This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brasília, DF, Brazil: Grants no. 301858/2023-3 to JMH and PQ 304214/2022–1 to DSB), Research Support Foundation of the State of Paraíba /Federal University of Paraíba (FAPESQ/UFPB), and Coordination for the Improvement of Higher Education Personnel (CAPES, Brasília, DF, Brazil).
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LMF, JMH, and DSB designed the study; LMF, JMH, JJVAM, DSG, SKS, ASL, and DJA performed the experiments and the analyses; LMF, JMH, and DSB analyzed the data; LMF, JMH, and DSB wrote the article with input from all other authors. All authors read and approved the manuscript.
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Ferreira, L.M., Henschel, J.M., de Almeida Mendes, J.J.V. et al. Sodium Nitroprusside Alleviates Moderate Drought Stress in Beet (Beta vulgaris L. subsp. vulgaris) by Modulating Its Photosynthetic Capacity. J Plant Growth Regul 43, 755–769 (2024). https://doi.org/10.1007/s00344-023-11135-4
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DOI: https://doi.org/10.1007/s00344-023-11135-4