Mitigation strategy of saline stress in Fragaria vesca using natural and synthetic brassinosteroids as biostimulants
Ramiro N. Furio
A * , Ana C. Fernández A , Patricia L. Albornoz B C , Melisa Evangelina Yonny D , María Luisa Toscano Adamo D , Ana I. Ruiz B , Mónica Azucena Nazareno D , Yamilet Coll E , Juan C. Díaz-Ricci F and Sergio M. Salazar A G
A
B
C
D
E
F
G
Abstract
Bassinosteroids (BRs) can induce plant defence responses and promote plant growth. In this work, we evaluated the effect of a natural (EP24) and a synthetic (BB16) brassinosteroid on strawberry (Fragaria vesca) plants exposed to saline stress. Treated plants showed higher shoot dry weight and root growth compared to untreated control plants. In BR-treated plants, crown diameters increased 66% and 40%, leaf area 148% and 112%, relative water content in leaves 84% and 61%, and SPAD values 24% and 26%, in response to BB16 and EP24, respectively. A marked stomatal closure, increased leaflet lignification, and a decrease in cortex thickness, root diameter and stele radius were also observed in treated plants. Treatments also reduces stress-induced damage, as plants showed a 34% decrease in malondialdehyde content and a lower proline content compared to control plants. A 22% and 15% increase in ascorbate peroxidase and total phenolic compound activities was observed in response to BB16, and a 24% increase in total flavonoid compound in response to both BRs, under stress conditions. These results allow us to propose the use of BRs as an environmentally safe crop management strategy to overcome salinity situations that severely affect crop yield.
Keywords: anatomical studies, biochemical markers, biostimulants, brassinosteroids, oxidative stress, salinity stress, tolerance, wild strawberry.
References
Abdelaal KA, Rashed SH, Hossain A, Sabagh AE (2020) Yield and quality of two sugar beet (Beta vulgaris L. ssp. vulgaris var. altissima Döll) cultivars are influenced by foliar application of salicylic acid, irrigation timing, and planting density. Acta Agriculturae Slovenica 115(2), 273-282.
| Crossref | Google Scholar |
Ali B, Hayat S, Ahmad A (2007) 28-Homobrassinolide ameliorates the saline stress in chickpea (Cicer arietinum L.). Environmental and Experimental Botany 59, 217-223.
| Crossref | Google Scholar |
Alyemeni MN, Al-Quwaiz SM (2016) Effect of 28-homobrassinolide on the performance of sensitive and resistant varieties of Vigna radiata. Saudi Journal of Biological Sciences 23, 698-705.
| Crossref | Google Scholar | PubMed |
An YQ, Sun L, Wang XJ, Sun R, Cheng ZY, Zhu ZK, Yan GG, Li YX, Bai JG (2019) Vanillic acid mitigates dehydration stress responses in blueberry plants. Russian Journal of Plant Physiology 66, 806-817.
| Crossref | Google Scholar |
Ansari WA, Atri N, Singh B, Kumar P, Pandey S (2018) Morpho-physiological and biochemical responses of muskmelon genotypes to different degree of water deficit. Photosynthetica 56(4), 1019-1030.
| Crossref | Google Scholar |
Anuradha S, Ram Rao SS (2003) Application of brassinosteroids to rice seeds (Oryza sativa L.) reduced the impact of salt stress on growth, prevented photosynthetic pigment loss and increased nitrate reductase activity. Plant Growth Regulation 40, 29-32.
| Crossref | Google Scholar |
Arkin GF, Taylor HM (1985) Modifying the root environment to reduce crop stress. Soil Science 139(4), 381.
| Crossref | Google Scholar |
Askary M, Talebi SM, Amini F, Bangan ADB (2017) Effects of iron nanoparticles on Mentha piperita L. under salinity stress. Biologija 63(1), 65-75.
| Crossref | Google Scholar |
Awang YB, Atherton JG (1994) Salinity and shading effects on leaf water relations and ionic composition of strawberry plants grown on rockwool. Journal of Horticultural Science 69(2), 377-383.
| Crossref | Google Scholar |
Awang YB, Atherton JG, Taylor AJ (1993) Salinity effects on strawberry plants grown in rockwool. I. Growth and leaf water relations. Journal of Horticultural Science 68(5), 783-790.
| Crossref | Google Scholar |
Bajguz A (2000) Effect of brassinosteroids on nucleic acids and protein content in cultured cells of Chlorella vulgaris. Plant Physiology and Biochemistry 38, 209-215.
| Crossref | Google Scholar |
Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiology and Biochemistry 47, 1-8.
| Crossref | Google Scholar | PubMed |
Barroso MCM, Alvarez CE (1997) Toxicity symptoms and tolerance of strawberry to salinity in the irrigation water. Scientia Horticulturae 71, 177-188.
| Crossref | Google Scholar |
Bartoli CG, Casalongué CA, Simontacchi M, Marquez-Garcia B, Foyer CH (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environmental and Experimental Botany 94, 73-88.
| Crossref | Google Scholar |
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. Journal of Experimental Botany 65(5), 1229-1240.
| Crossref | Google Scholar | PubMed |
Bharath P, Gahir S, Raghavendra AS (2021) Abscisic acid-induced stomatal closure: an important component of plant defense against abiotic and biotic stress. Frontiers in Plant Science 12, 615114.
| Crossref | Google Scholar | PubMed |
Bulgari R, Franzoni G, Ferrante A (2019) Biostimulants application in horticultural crops under abiotic stress conditions. Agronomy 9(6), 306.
| Crossref | Google Scholar |
Cabello JV, Chan RL (2019) Arabidopsis and sunflower plants with increased xylem area show enhanced seed yield. The Plant Journal 99(4), 717-732.
| Crossref | Google Scholar | PubMed |
Carillo P, Gibon Y (2011) Protocol: extraction and determination of proline. PrometheusWiki 1-5.
| Google Scholar |
Carley HE, Watson RD (1966) A new gravimetric method for estimating root-surface areas. Soil Science 102, 289-291.
| Crossref | Google Scholar |
Carrillo Y, Dijkstra FA, LeCain D, Morgan JA, Blumenthal D, Waldron S, Pendall E (2014) Disentangling root responses to climate change in a semiarid grassland. Oecologia 175, 699-711.
| Crossref | Google Scholar | PubMed |
Chaillou LL, Nazareno MA (2006) New method to determine antioxidant activity of polyphenols. Journal of Agricultural and Food Chemistry 54(22), 8397-8402.
| Crossref | Google Scholar | PubMed |
Chaves MM, Zarrouk O, Francisco R, Costa JM, Santos T, Regalado AP, Rodrigues ML, Lopes CM (2010) Grapevine under deficit irrigation: hints from physiological and molecular data. Annals of Botany 105, 661-676.
| Crossref | Google Scholar | PubMed |
Cheng L, Han M, Yang L-M, Li Y, Sun Z, Zhang T (2018) Changes in the physiological characteristics and baicalin biosynthesis metabolism of Scutellaria baicalensis Georgi under drought stress. Industrial Crops and Products 122, 473-482.
| Crossref | Google Scholar |
Chhaya , Yadav B, Jogawat A, Gnanasekaran P, Kumari P, Lakra N, Lal SK, Pawar J, Narayan OP (2021) An overview of recent advancement in phytohormones-mediated stress management and drought tolerance in crop plants. Plant Gene 25, 100264.
| Crossref | Google Scholar |
Chugh V, Kaur N, Gupta AK (2011) Evaluation of oxidative stress tolerance in maize (Zea mays L.) seedlings in response to drought. Indian Journal of Biochemistry and Biophysics 48(1), 47-53.
| Google Scholar | PubMed |
Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutrition, Metabolism and Cardiovascular Diseases 15(4), 316-328.
| Crossref | Google Scholar | PubMed |
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2020) InfoStat versión 2020. Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available at http://www.infostat.com.ar
Dinc S, Kara M, Karipcin MZ, Sari N, Can Z, Cicekci H, Akkus M (2018) The rootstock effects on agronomic and biochemical quality properties of melon under water stress. FEB-Fresenius Environmental Bulletin 27(7), 5008-5021.
| Google Scholar |
Divi UK, Rahman T, Krishna P (2016) Gene expression and functional analyses in brassinosteroid-mediated stress tolerance. Plant Biotechnology Journal 14, 419-432.
| Crossref | Google Scholar | PubMed |
El-Mashad AAA, Mohamed HI (2012) Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants (Vigna sinensis). Protoplasma 249, 625-635.
| Crossref | Google Scholar | PubMed |
Eleiwa ME, Bafeel SO, Ibrahim SA (2011) Influence of brassinosteroids on wheat plant (Triticum aestivum L.) production under salinity stress conditions. I-Growth parameters and photosynthetic pigments. Australian Journal of Basic and Applied Sciences 5, 58-65.
| Google Scholar |
Enstone DE, Peterson CA, Ma F (2002) Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation 21(4), 335-351.
| Crossref | Google Scholar |
Fariduddin Q, Yusuf M, Ahmad I, Ahmad A (2014) Brassinosteroids and their role in response of plants to abiotic stresses. Biologia Plantarum 58, 9-17.
| Crossref | Google Scholar |
Fernández-Linares LC, Rojas-Avelizapa NG, Roldán-Carrillo TG, Ramírez-Islas MH, Zegarra-Martínez HG, Uribe-Hernández R, Reyes-Ávila RJ, Flores-Hernández D, Arce-Ortega JM (2006) Manual de técnicas de análisis de suelos aplicadas a la remediación de sitios contaminados. Instituto Mexicano del Petróleo. SEMARNAT. Instituto Nacional de Ecología, 4.3, pp. 22–23.
Flexas J, Bota J, Escalona JM, Sampol B, Medrano H (2002) Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Functional Plant Biology 29(4), 461-471.
| Crossref | Google Scholar | PubMed |
Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology 6(3), 269-279.
| Crossref | Google Scholar | PubMed |
Furio RN, Albornoz PL, Coll Y, Martínez Zamora GM, Salazar SM, Martos GG, Díaz Ricci JC (2019) Effect of natural and synthetic Brassinosteroids on strawberry immune response against Colletotrichum acutatum. European Journal of Plant Pathology 153, 167-181.
| Crossref | Google Scholar |
Furio RN, Martínez-Zamora GM, Salazar SM, Coll Y, Perato SM, Martos GG, Díaz Ricci JC (2020) Role of calcium in the defense response induced by brassinosteroids in strawberry plants. Scientia Horticulturae 261, 109010.
| Crossref | Google Scholar |
Gadallah MAA, Ramadan T (1997) Effects of zinc and salinity on growth and anatomical structure of Carthamus tinctorius L. Biologia Plantarum 39(3), 411-418.
| Crossref | Google Scholar |
Ghorbel M, Brini F (2021) Hormone mediated cell signaling in plants under changing environmental stress. Plant Gene 28, 100335.
| Crossref | Google Scholar |
Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. The Plant Cell 5, 1439-1451.
| Crossref | Google Scholar | PubMed |
Güler S, Macit I, Koc A, Ibrikci H (2006) Estimating leaf nitrogen status of strawberry by using chlorophyll meter reading. Journal of Biological Sciences 6(6), 1011-1016.
| Crossref | Google Scholar |
Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiology 103, 1067-1073.
| Crossref | Google Scholar | PubMed |
Hayat S, Ali B, Aiman Hasan S, Ahmad A (2007) Brassinosteroid enhanced the level of antioxidants under cadmium stress in Brassica juncea. Environmental and Experimental Botany 60, 33-41.
| Crossref | Google Scholar |
Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A (2010) Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environmental and Experimental Botany 69(2), 105-112.
| Crossref | Google Scholar |
Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Australian Journal of Crop Science 5, 726-734.
| Google Scholar |
Julkowska MM, Koevoets IT, Mol S, Hoefsloot H, Feron R, Tester MA, Keurentjes JJB, Korte A, Haring MA, de Boer G-J, Testerink C (2017) Genetic components of root architecture remodeling in response to salt stress. The Plant Cell 29(12), 3198-3213.
| Crossref | Google Scholar | PubMed |
Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225(2), 353-364.
| Crossref | Google Scholar | PubMed |
Kaya C, Higgs D, Ince F, Amador BM, Cakir A, Sakar E (2003) Ameliorative effects of potassium phosphate on salt-stressed pepper and cucumber. Journal of Plant Nutrition 26(4), 807-820.
| Crossref | Google Scholar |
Kaya C, Akram NA, Ashraf M (2019) Influence of exogenously applied nitric oxide on strawberry (Fragaria × ananassa) plants grown under iron deficiency and/or saline stress. Physiologia Plantarum 165(2), 247-263.
| Crossref | Google Scholar | PubMed |
Khan MA, Gemenet DC, Villordon A (2016) Root system architecture and abiotic stress tolerance: current knowledge in root and tuber crops. Frontiers in Plant Science 7, 1584.
| Crossref | Google Scholar | PubMed |
Kim H-J, Fonseca JM, Choi J-H, Kubota C, Kwon DY (2008) Salt in irrigation water affects the nutritional and visual properties of romaine lettuce (Lactuca sativa L.). Journal of Agricultural and Food Chemistry 56, 3772-3776.
| Crossref | Google Scholar | PubMed |
Korkmaz D (2001) Precipitation titration: “determination of chloride by the Mohr method”. Methods 2(4), 1-6.
| Google Scholar |
Krishna P (2003) Brassinosteroid-mediated stress response. Journal of Plant Growth Regulation 22, 289-297.
| Crossref | Google Scholar | PubMed |
Kumari S, Nazir F, Maheshwari C, Kaur H, Gupta R, Siddique KHM, Khan MIR (2024) Plant hormones and secondary metabolites under environmental stresses: enlightening defense molecules. Plant Physiology and Biochemistry 206, 108238.
| Crossref | Google Scholar |
Lamz Piedra A, González Cepero MC (2013) La salinidad como problema en la agricultura: la mejora vegetal una solución inmediata. Cultivos Tropicales 34, 31-42.
| Google Scholar |
Li N, Wang X, Ma B, Du C, Zheng L, Wang Y (2017) Expression of a Na+/H+ antiporter RtNHX1 from a recretohalophyte Reaumuria trigyna improved salt tolerance of transgenic Arabidopsis thaliana. Journal of Plant Physiology 218, 109-120.
| Crossref | Google Scholar | PubMed |
Li S, Zheng H, Lin L, Wang F, Sui N (2021) Roles of brassinosteroids in plant growth and abiotic stress response. Plant Growth Regulation 93, 29-38.
| Crossref | Google Scholar |
Lovisolo C, Perrone I, Carra A, Ferrandino A, Flexas J, Medrano H, Schubert A (2010) Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update. Functional Plant Biology 37(2), 98-116.
| Crossref | Google Scholar |
Lu KX, Cao BH, Feng XP, He Y, Jiang DA (2009) Photosynthetic response of salt-tolerant and sensitive soybean varieties. Photosynthetica 47, 381-387.
| Crossref | Google Scholar |
Maas EV, Hoffman GJ (1977) Crop salt tolerance–current assessment. Journal of the Irrigation and Drainage Division 103(2), 115-134.
| Crossref | Google Scholar |
Mäkelä P, Kontturi M, Pehu E, Somersalo S (1999) Photosynthetic response of drought- and salt-stressed tomato and turnip rape plants to foliar-applied glycinebetaine. Physiologia Plantarum 105, 45-50.
| Crossref | Google Scholar |
Meggio F, Prinsi B, Negri AS, Simone Di Lorenzo G, Lucchini G, Pitacco A, Failla O, Scienza A, Cocucci M, Espen L (2014) Biochemical and physiological responses of two grapevine rootstock genotypes to drought and salt treatments. Australian Journal of Grape and Wine Research 20(2), 310-323.
| Crossref | Google Scholar |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7(9), 405-410.
| Crossref | Google Scholar | PubMed |
Moreno-Castillo E, Ramírez-Echemendía DP, Hernández-Campoalegre G, Mesa-Tejeda D, Coll-Manchado F, Coll-García Y (2018) In silico identification of new potentially active brassinosteroid analogues. Steroids 138, 35-42.
| Crossref | Google Scholar | PubMed |
Moreshet S, Fuchs M, Cohen Y, Cohen Y, Langensiepen M (1996) Water transport characteristics of cotton as affected by drip irrigation layout. Agronomy Journal 88(5), 717-722.
| Crossref | Google Scholar |
Mulet JM, Campos F, Yenush L (2020) Editorial: Ion homeostasis in plant stress and development. Frontiers in Plant Science 11, 618273.
| Crossref | Google Scholar |
Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & environment 25, 239-250.
| Crossref | Google Scholar | PubMed |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651-681.
| Crossref | Google Scholar | PubMed |
Naveen N, Kumari N, Avtar R, Jattan M, Ahlawat S, Rani B, Malik K, Sharma A, Singh M (2021) Evaluation of effect of brassinolide in Brassica juncea leaves under drought stress in field conditions. Horticulturae 7(11), 514.
| Crossref | Google Scholar |
Nie M, Lu M, Bell J, Raut S, Pendall E (2013) Altered root traits due to elevated CO2: a meta-analysis. Global Ecology and Biogeography 22, 1095-1105.
| Crossref | Google Scholar |
Núñez M, Mazzafera P, Mazorra LM, Siqueira WJ, Zullo MAT (2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biologia Plantarum 47, 67-70.
| Crossref | Google Scholar |
Otie V, Udo I, Shao Y, Itam MO, Okamoto H, An P, Eneji EA (2021) Salinity effects on morpho-physiological and yield traits of soybean (Glycine max L.) as mediated by foliar spray with brassinolide. Plants 10(3), 541.
| Crossref | Google Scholar | PubMed |
Özdemir F, Bor M, Demiral T, Türkan I (2004) Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L.) under salinity stress. Plant Growth Regulation 42, 203-211.
| Crossref | Google Scholar |
Pirlak L, Eşitken A (2004) Salinity effects on growth, proline and ion accumulation in strawberry plants. Acta Agriculturae Scandinavica, Section B – Soil & Plant Science 54, 189-192.
| Crossref | Google Scholar |
Rady MM (2011) Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Scientia Horticulturae 129, 232-237.
| Crossref | Google Scholar |
Reddy MP, Vora AB (1986) Changes in pigment composition, Hill reaction activity and saccharides metabolism in bajra (Pennisetum typhoides S&H) leaves under NaCl salinity. Photosynthetica 20, 50-55.
| Google Scholar |
Ring L, Yeh S-Y, Hücherig S, Hoffmann T, Blanco-Portales R, Fouche M, Villatoro C, Denoyes B, Monfort A, Caballero JL, Muñoz-Blanco J, Gershenson J, Schwab W (2013) Metabolic interaction between anthocyanin and lignin biosynthesis is associated with peroxidase FaPRX27 in strawberry fruit. Plant Physiology 163(1), 43-60.
| Crossref | Google Scholar | PubMed |
Roth CH, Malicki MA, Plagge R (1992) Empirical evaluation of the relationship between soil dielectric constant and volumetric water content as the basis for calibrating soil moisture measurements by TDR. Journal of Soil Science 43(1), 1-13.
| Crossref | Google Scholar |
Ruiz D, Martinez V, Cerdá A (1999) Demarcating specific ion (NaCI, CI−, Na+) and osmotic effects in the response of two citrus rootstocks to salinity. Scientia Horticulturae 80, 289-224.
| Crossref | Google Scholar |
Saied AS, Keutgen AJ, Noga G (2005) The influence of NaCl salinity on growth, yield and fruit quality of strawberry cvs. ‘Elsanta’ and ‘Korona’. Scientia Horticulturae 103(3), 289-303.
| Crossref | Google Scholar |
Santacruz-García AC, Senilliani MG, Gómez AT, Ewens M, Yonny ME, Villalba GF, Nazareno MA (2022) Biostimulants as forest protection agents: do these products have an effect against abiotic stress on a forest native species? Aspects to elucidate their action mechanisms. Forest Ecology and Management 522, 120446.
| Crossref | Google Scholar |
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9(7), 671-675.
| Crossref | Google Scholar | PubMed |
Schultz HR (2003) Differences in hydraulic architecture account for near-isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars during drought. Plant, Cell & Environment 26(8), 1393-1405.
| Crossref | Google Scholar |
Serna M, Coll Y, Zapata PJ, Botella MÁ, Pretel MT, Amorós A (2015) A brassinosteroid analogue prevented the effect of salt stress on ethylene synthesis and polyamines in lettuce plants. Scientia Horticulturae 185, 105-112.
| Crossref | Google Scholar |
Shahid MA, Balal RM, Pervez MA, Garcia-Sanchez F, Gimeno V, Abbas T, Mattson NS, Riaz A (2014) Treatment with 24-epibrassinolide mitigates NaCl-induced toxicity by enhancing carbohydrate metabolism, osmolyte accumulation, and antioxidant activity in Pisum sativum. Turkish Journal of Botany 38(3), 511-525.
| Crossref | Google Scholar |
Shu S, Yuan L-Y, Guo S-R, Sun J, Yuan Y-H (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiology and Biochemistry 63, 209-216.
| Crossref | Google Scholar | PubMed |
Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods in Enzymology 299, 152-178.
| Crossref | Google Scholar |
Soltabayeva A, Ongaltay A, Omondi JO, Srivastava S (2021) Morphological, physiological and molecular markers for salt-stressed plants. Plants 10(2), 243.
| Crossref | Google Scholar | PubMed |
Stępień P, Kłbus G (2006) Water relations and photosynthesis in Cucumis sativus L. leaves under salt stress. Biologia Plantarum 50, 610-616.
| Crossref | Google Scholar |
Sun Y, Niu G, Wallace R, Masabni J, Gu M (2015a) Relative salt tolerance of seven strawberry cultivars. Horticulturae 1(1), 27-43.
| Crossref | Google Scholar |
Sun C, Li X, Hu Y, Zhao P, Xu T, Sun J, Gao X (2015b) Proline, sugars, and antioxidant enzymes respond to drought stress in the leaves of strawberry plants. Horticultural Science and Technology 33(5), 625-632.
| Crossref | Google Scholar |
Surgun-Acar Y, Zemheri-Navruz F (2022) Exogenous application of 24-epibrassinolide improves manganese tolerance in Arabidopsis thaliana L. via the modulation of antioxidant system. Journal of Plant Growth Regulation 41(2), 546-557.
| Crossref | Google Scholar |
Suseela V, Tharayil N, Pendall E, Rao AM (2017) Warming and elevated CO2 alter the suberin chemistry in roots of photosynthetically divergent grass species. AoB Plants 9(5), plx041.
| Crossref | Google Scholar |
Talon M, Zeevaart JAD, Gage DA (1991) Identification of gibberellins in spinach and effects of light and darkness on their levels. Plant Physiology 97(4), 1521-1526.
| Crossref | Google Scholar | PubMed |
Terletskaya N, Duisenbayeva U, Rysbekova A, Kurmanbayeva M, Blavachinskaya I (2019) Architectural traits in response to salinity of wheat primary roots. Acta Physiologiae Plantarum 41(9), 157.
| Crossref | Google Scholar |
Türkan I, Demiral T (2009) Recent developments in understanding salinity tolerance. Environmental and Experimental Botany 67(1), 2-9.
| Crossref | Google Scholar |
van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annual Review of Plant Biology 71, 403-433.
| Crossref | Google Scholar | PubMed |
Vidya Vardhini B, Seeta Ram Rao S (2003) Amelioration of osmotic stress by brassinosteroids on seed germination and seedling growth of three varieties of sorghum. Plant Growth Regulation 41, 25-31.
| Crossref | Google Scholar |
Wilson C, Liu X, Lesch SM, Suarez DL (2006) Growth response of major USA cowpea cultivars: II. Effect of salinity on leaf gas exchange. Plant Science 170(6), 1095-1101.
| Crossref | Google Scholar |
Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation: evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiology 83(2), 278-282.
| Crossref | Google Scholar | PubMed |
Yildirim E, Karlidag H, Turan M (2009) Mitigation of salt stress in strawberry by foliar K, Ca and Mg nutrient supply. Plant, Soil and Environment 55(5), 213-221.
| Crossref | Google Scholar |
Yonny ME, Rodríguez Torressi A, Nazareno MA, Cerutti S (2017) Development of a novel, sensitive, selective, and fast methodology to determine malondialdehyde in leaves of melon plants by ultra-high-performance liquid chromatography-tandem mass spectrometry. Journal of Analytical Methods in Chemistry 2017(1), 4327954.
| Crossref | Google Scholar |
Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogués S (2004) A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. Journal of Experimental Botany 55(399), 1135-1143.
| Crossref | Google Scholar | PubMed |
Yue J, You Y, Zhang L, Fu Z, Wang J, Zhang J, Guy RD (2019) Exogenous 24-epibrassinolide alleviates effects of salt stress on chloroplasts and photosynthesis in Robinia pseudoacacia L. seedlings. Journal of Plant Growth Regulation 38, 669-682.
| Crossref | Google Scholar |
Zapata PJ, Serrano M, Pretel MT, Botella MA (2008) Changes in free polyamine concentration induced by salt stress in seedlings of different species. Plant Growth Regulation 56, 167-177.
| Crossref | Google Scholar |
Zeevaart JAD, Gage DA (1993) ent-Kaurene biosynthesis is enhanced by long photoperiods in the long-day plants Spinacia oleracea L. and Agrostemma githago L. Plant Physiology 101(1), 25-29.
| Crossref | Google Scholar | PubMed |
Zeng H, Tang Q, Hua X (2010) Arabidopsis brassinosteroid mutants det2-1 and bin2-1 display altered salt tolerance. Journal of Plant Growth Regulation 29, 44-52.
| Crossref | Google Scholar |
Zhang M, Zhai Z, Tian X, Duan L, Li Z (2008) Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). Plant Growth Regulation 56, 257-264.
| Crossref | Google Scholar |
Zhang A, Zhang J, Zhang J, Ye N, Zhang H, Tan M, Jiang M (2011) Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant and Cell Physiology 52(1), 181-192.
| Crossref | Google Scholar | PubMed |
Zhang H, Zhao D, Tang Z, Zhang Y, Zhang K, Dong J, Wang F (2022) Exogenous brassinosteroids promotes root growth, enhances stress tolerance, and increases yield in maize. Plant Signaling & Behavior 17(1), 2095139.
| Crossref | Google Scholar | PubMed |
