Abstract
Dehydrins (DHNs) are stress proteins involved in the development of protective reactions in plants against dehydration. The relationship between DHNs and morphological responses such as leaf rolling in plants exposed to water deficit is not well known. In this study, we detected how variations in DHN levels affect the leaf rolling response in maize exposed to osmotic stress in relation to the antioxidant system and ABA level. In this context, we altered the DHN levels in maize seedlings by treatment with bio-regulators (salicylic acid and abscisic acid) under PEG6000-free and PEG6000-induced osmotic stress. When the DHN levels were increased by the bio-regulators (25 µM SA and 100 µM ABA), the relative expression level of the Zea mays dehydrin COR410 gene increased in the seedlings, while reactive oxygen species (ROS) and leaf rolling grade decreased. Moreover, induction of DHNs caused increases in the antioxidant enzyme activity and content of antioxidant substances, and very high amounts of endogenous abscisic acid. When DHN level was suppressed by a bio-regulator (200 µM SA) in the maize seedlings, dehydrin COR410 expression level decreased, while ROS and the leaf rolling grade increased. Moreover, the antioxidant enzyme activity and content of antioxidant substances decreased in the seedlings, while the amount of abscisic acid increased. Taken all together, an increase in DHN level by bio-regulator treatment can stimulate the antioxidant system, enable abscisic acid regulation, and thus reduce leaf rolling through decreased ROS levels. The results also indicated that DHNs may be involved in the signal pathways inducing expression of some genes related to leaf rolling response, possibly by modulating ROS levels, in maize seedlings exposed to osmotic stress.
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References
Aebi HE (1983) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie, Weinhern, pp 273–286
Afridi MS, Sumairab A, Mahmoodc T, Salama A, Mukhtara T, Mehmooda S, Alia J, Khatoona Z, Bibia M, Javedd MT, Sultane T, Chaudharya HJ (2019) Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: involvement of ACC deaminase and antioxidant enzymes. Plant Physiol Biochem 139:569–577. https://doi.org/10.1016/j.plaphy.2019.03.041
Ahmad I, Zaib S, Alves PCMS, Luthe DS, Bano A, Shakeel SN (2019) Molecular and physiological analysis of drought stress responses in Zea mays treated with plant growth promoting rhizobacteria. Biol Plant 63:536–547. https://doi.org/10.32615/bp.2019.092
Baret F, Madec S, Irfan K, Lopez J, Comar A, Hemmerlé M, Dutartre D, Praud S, Tixier MH (2018) Leaf-rolling in maize crops: from leaf scoring to canopy-level measurements for phenotyping. J Exp Bot 69(10):2705–2716. https://doi.org/10.1093/jxb/ery071
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Brini F, Yamamoto A, Jlaiel L, Takeda S, Hobo T, Dinh HQ, Hattori T, Masmoudi K, Hanin M (2011) Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis. Plant Cell Physiol 52(4):676–688. https://doi.org/10.1093/pcp/pcr030
Castillo FJ (1996) Antioxidative protection in the inducible CAM plant Sedum album L. following the imposition of severe water stress and recovery. Oecologia 107:469–477. https://doi.org/10.1007/BF00333937
Eriksson SK, Kutzer M, Procek J, Gröbner G, Harryson P (2011) Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. Plant Cell 23(6):2391–2404. https://doi.org/10.1105/tpc.111.085183
Foyer CH, Halliwell B (1976) Presence of glutathione and glutathione reductase in chloroplast: a proposed role in ascorbic acid metabolism. Planta 133:21–25. https://doi.org/10.1007/BF00386001
Frahry G, Schopfer P (2001) NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212:175–183. https://doi.org/10.1007/s004250000376
Halder T, Upadhyaya G, Basak C, Das A, Chakraborty C, Ray S (2018) Dehydrins impart protection against oxidative stress in transgenic tobacco plants. Front Plant Sci 9:136. https://doi.org/10.3389/fpls.2018.00136
Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298. https://doi.org/10.1007/s00425-003-0986-7
Hassan NM, El-Bastawisy ZM, El-Sayed AK, Ebeed HT, Alla MMN (2015) Roles of dehydrin genes in wheat tolerance to drought stress. J Adv Res 6(2):179–188. https://doi.org/10.1016/j.jare.2013.11.004
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stochiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300. https://doi.org/10.1007/s00344-007-9017-4
Jing H, Li C, Ma F, Ma JH, Khan A, Wang X, Zhao LY, Gong ZH, Chen RG (2016) Genome-wide identification, expression diversication of dehydrin gene family and characterization of CaDHN3 in pepper (Capsicum annuum L.). PLoS ONE 11(8):e0161073. https://doi.org/10.1371/journal.pone.0161073
Juarez MT, Twigg RW, Timmermans CP (2004a) Specification of adaxial cell fate during maize leaf development. Development 131:4533–4544. https://doi.org/10.1242/dev.01328
Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP (2004b) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84. https://doi.org/10.1038/nature02363
Kadioglu A, Saruhan N, Saglam A, Terzi R, Acet T (2011) Exogenous salicylic acid alleviates effects of long term drought stress and delays leaf rolling by ınducing antioxidant system. Plant Growth Regul 64:27–37. https://doi.org/10.1007/s10725-010-9532-3
Kadioglu A, Terzi R, Saruhan N, Saglam A (2012) Current advances in the investigation of leaf rolling caused by biotic and abiotic stress factors. Plant Sci 182:42–48. https://doi.org/10.1016/j.plantsci.2011.01.013
Kadioglu A, Saglam A, Terzi R. (2014) Effect of leaf rolling on gene expression in plants under drought stress. In: 3rd International Molecular Biology and Biotechnology Congress, Sarajevo, Bosnia and Herzegovina. pp. 203.
Kang G, Li G, Xu W, Peng X, Han Q, Zhu Y (2012) Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J Proteome Res 11:6066–6079. https://doi.org/10.1021/pr300728y
Khazaei H, Street K, Bari A, Mackay M, Stoddard FL (2013) The FIGS (focused identification of germplasm strategy) approach identifies traits related to drought adaptation in Vicia faba genetic resources. PLoS ONE 8(5):e63107. https://doi.org/10.1371/journal.pone.0063107
Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147(1):381–390. https://doi.org/10.1104/pp.108.118208
Liso R, Calabrese G, Bitonti MB, Arrigoni O (1984) Relationship between ascorbic acid and cell division. Exp Cell Res 150:314–320. https://doi.org/10.1016/0014-4827(84)90574-3
Liu Y, Jiang H, Zhao Z, An L (2011) Abscisic acid is involved in brassinosteroids-induced chilling tolerance in the suspension cultured cells from Chorispora bungeana. J Plant Physiol 168:853–862. https://doi.org/10.1016/j.jplph.2010.09.020
Liu Y, Song Q, Li D, Yang X, Li D (2017) Multifunctional roles of plant dehydrins in response to environmental stresses. Front Plant Sci 8:1018. https://doi.org/10.3389/fpls.2017.01018
Liu Y, Hu G, Wu G, Liu G, Huan H, Ding X, Yan L, Li X, Zhao B, Zhang X (2019) Differential responses of antioxidants and dehydrin expression in two switchgrass (Panicum virgatum) cultivars contrasting in drought tolerance. BioRxiv. https://doi.org/10.22271/tpr.2020.v7.i1.031
Lv A, Fan N, Xie J, Yuan S, An Y, Zhou P (2017) Expression of CdDHN4, a novel YSK2-type dehydrin gene from Bermuda grass, responses to drought stress through the ABA-dependent signal pathway. Front Plant Sci 8:748. https://doi.org/10.3389/fpls.2017.00748
Maryan KE, Lahiji HS, Farrokhi N, Komeleh HH (2019) Analysis of Brassica napus dehydrins and their co-expression regulatory networks in relation to cold stress. Gene Expr Patterns 31:7–17. https://doi.org/10.1016/j.gep.2018.10.002
Mehrabad Pour-Benab S, Fabriki-Ourang S, Mehrabi AA (2019) Expression of dehydrin and antioxidant genes and enzymatic antioxidant defense under drought stress in wild relatives of wheat. Biotechnol Biotechnol Equip 33(1):1063–1073. https://doi.org/10.1080/13102818.2019.1638300
Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:1–12. https://doi.org/10.3389/fpls.2014.00004
Nakano Y, Asada Y (1987) Purification of ascorbate peroxidase from spinach chloroplasts: its inactivation in ascorbate depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol 28:131–135. https://doi.org/10.1093/oxfordjournals.pcp.a077268
Premachandra GS, Saneoka H, Fujita K, Ogata S (1993) Water stress and potassium fertilization in field grown maize (Zea mays L.): effects of leaf water relations and leaf rolling. J Agron Crop Sci 170:195–201. https://doi.org/10.1111/j.1439-037X.1993.tb01075.x
Saruhan N, Terzi R, Sağlam A, Kadioglu A (2010) Scavenging of reactive oxygen species in apoplastic and symplastic areas of rolled leaves in Ctenanthe setosa under drought stress. Acta Biol Hung 61(3):282–298. https://doi.org/10.1556/ABiol.61.2010.3.5
Saruhan N, Saglam A, Kadioglu A (2012) Salicylic acid pretreatment ınduces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiol Plant 34:97–106. https://doi.org/10.1007/s11738-011-0808-7
Saruhan-Güler N, Terzi R (2020) Dehydrins: an overview of current approaches and advancement. Turk J Bot 44:481–492. https://doi.org/10.3906/bot-2005-78
Sezgin A, Altuntaş C, Saglam A, Terzi R, Demiralay M, Kadioglu A (2018) Abscisic acid cross-talking with hydrogen peroxide and osmolyte compounds may regulate the leaf rolling mechanism under drought. Acta Physiol Plant 40:141. https://doi.org/10.1007/s11738-018-2716-6
Shekhawat UKS, Srinivas L, Ganapathi TR (2011) MusaDHN-1, a novel multiple stress-inducible SK3-type dehydrin gene, contributes affirmatively to drought-and salt-stress tolerance in banana. Planta 234(5):915. https://doi.org/10.1007/s00425-011-1455-3
Sun X, Xi DH, Feng H, Du JB, Lei T, Liang HG, Lin HH (2009) The dual effects salicylic acid on dehydrin accumulation in water-stressed barley seedlings. Russ J Plant Physiol 56(3):348–354. https://doi.org/10.1134/S1021443709030078
Terzi R, Kadioglu A, Kalaycioglu E, Saglam A (2014) Hydrogen peroxide pretreatment induces osmotic stress tolerance by influencing osmolyte and abscisic acid levels in maize leaves. J Plant Interact 9(1):559–565. https://doi.org/10.1080/17429145.2013.871077
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 Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Verma G, Dhar YV, Srivastava D, Kidwai M, Chauhan PS (2017) Genome-wide analysis of rice dehydrin gene family: Its evolutionary conservedness and expression pattern in response to PEG induced dehydration stress. PLoS ONE 12(5):e0176399. https://doi.org/10.1371/journal.pone.0176399
Zhang Y, Li J, Yu F, Cong L, Wang L, Burkard G, Chai T (2006) Cloning and expression analysis of SKn-type dehydrin gene from bean in response to heavy metals. Mol Biotechnol 32(3):205–217. https://doi.org/10.1385/MB:32:3:205
Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735. https://doi.org/10.1105/tpc.108.061457
Zhang H, Zheng J, Su H, Xia K, Jian S, Zhang M (2018) Molecular cloning and functional characterization of the dehydrin (IpDHN) gene from Ipomoea pes-caprae. Front Plant Sci 9:1454. https://doi.org/10.3389/fpls.2018.01454
Zhang D, Lv A, Yang T, Cheng X, Zhao E, Zhou P (2020) Protective functions of alternative splicing transcripts (CdDHN4-L and CdDHN4 S) of CdDHN4 from Bermuda grass under multiple abiotic stresses. Gene X 5:100033. https://doi.org/10.1016/j.gene.2020.100033
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This research was funded by Turkish National Science Foundation (Project No: 114Z253).
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Neslihan Saruhan Guler: the design of the study, analyzed all data and wrote the manuscript. Rabiye Terzi: the design of the study, analyzed all data and wrote the manuscript. Asim Kadioglu: review and editing of manuscript. Mehmet Demiralay and Kamil Ozturk performed the experiments.
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Saruhan Güler, N., Terzi, R., Demiralay, M. et al. Increased dehydrin level decreases leaf rolling grade by altering the reactive oxygen species homeostasis and abscisic acid content in maize subjected to osmotic stress. 3 Biotech 12, 201 (2022). https://doi.org/10.1007/s13205-022-03275-3
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DOI: https://doi.org/10.1007/s13205-022-03275-3