Abstract
The present study investigated the effect of seed pretreatment with sodium nitroprusside (SNP) as nitric oxide (NO) donor on glyoxalase and antioxidant systems in germinating maize (Zea mays L.) seeds under methylglyoxal (MG) toxicity. The seeds were soaked in SNP solutions (0.0, 0.5, and 0.75 mM) for 8 h at 25 °C and then germinated in 0.0 (control) and 3 mM MG medium for 5 days under dark conditions (25 ± 1 °C and 75% humidity). The MG alone caused a strong inhibition on seed germination and seedling growth (root and shoot length) while the SNP pretreatments improved the same parameters in the MG-stressed seedlings. The MG alone increased endogenous MG accumulation, and glyoxalase I (Gly-I) and Gly-II activities eliminating MG toxicity in both organs. In contrast, the SNP pretreatments reduced MG content and further stimulated both enzyme activities in MG-stressed seedlings. MG alone increased reactive oxygen species (ROS) such as O2.− and H2O2, and lipid peroxidation (as malondialdehyde, MDA) levels. But the SNP pretreatments decreased ROS level, except for MDA content in seedlings exposed to MG. Moreover, MG alone stimulated superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR) activities while it inhibited guaiacol peroxidase (GPX) activity. SNP pretreatments in seedlings stressed by MG further elevated SOD, GPX, and GR activities while it inhibited CAT and APX activities. The results showed that seed pretreatment with NO (particularly as 0.75 mM SNP) in maize seedlings exposed to MG ameliorated seed germination, seedling growth, MG accumulation, and oxidative stress by restoring the glyoxalase and antioxidant enzyme activities.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All relevant data have been incorporated in the publication.
References
Ahmad P, Alam P, Balawi TH, Altalayan FH, Ahanger MA, Ashraf M (2020) Sodium nitroprusside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalase cycle. Chemosphere 244:125480. https://doi.org/10.1016/j.chemosphere.2019.125480
Álvarez Viveros MF, Inostroza-Blancheteau C, Timmermann T, González M, Arce-Johnson P (2013) Overexpression of GlyI and GlyII genes in transgenic tomato (Solanum lycopersicum Mill.) plants confers salt tolerance by decreasing oxidative stress. Mol Biol Rep 40:3281–3290. https://doi.org/10.1007/s11033-012-2403-4
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221. https://doi.org/10.1007/PL00008128
Bradford M (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/10.1016/0003-2697(76)90527-3
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053
Dumanović J, Nepovimova E, Natić M, Kuča K, Jaćević V (2021) The significance of reactive oxygen species and antioxidant defense system in plants: a concise overview. Front Plant Sci 11:552969. https://doi.org/10.3389/fpls.2020.552969
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620. https://doi.org/10.1016/0003-2697(76)90488-7
Esim N, Atıcı Ö (2016) Relationships between some endogenous signal compounds and the antioxidant system in response to chilling stress in maize (Zea mays L.) seedlings. Turk J Bot 40(1):37–44. https://doi.org/10.3906/bot-1408-59
Esim N, Atıcı Ö, Mutlu S (2014) Effects of exogenous nitric oxide in wheat seedlings under chilling stress. Toxicol Ind Health 30:268–274
Genç E, Atıcı Ö (2019) Chicken feather protein hydrolysate as a biostimulant improves the growth of wheat seedlings by affecting biochemical and physiological parameters. Turk J Bot 43(1): 67–79. https://doi.org/10.3906/bot-1804-53
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596. https://doi.org/10.1007/s10646-013-1050-4
Hasanuzzaman M, Nahar K, Alam MM, Bhuyan MB, Oku H, Fujita M (2018a) Exogenous nitric oxide pretreatment protects Brassica napus L. seedlings from paraquat toxicity through the modulation of antioxidant defense and glyoxalase systems. Plant Physiol Biochem 126:173–186. https://doi.org/10.1016/j.plaphy.2018.02.021
Hasanuzzaman M, Nahar K, Rahman A, Inafuku M, Oku H, Fujita M (2018b) Exogenous nitric oxide donor and arginine provide protection against short-term drought stress in wheat seedlings. Physiol Mol Biol Plants 24:993–1004. https://doi.org/10.1007/s12298-018-0531-6
Hoque TS, Uraji M, Tuy A, Nakamura Y, Murata Y (2012) Methylglyoxal inhibits seed germination and root elongation and up-regulates transcription of stress-responsive genes in ABA-dependent pathway in Arabidopsis. Plant Biol 14:854–858. https://doi.org/10.1111/j.1438-8677.2012.00607.x
Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran LSP (2016) Methylglyoxal: an emerging signaling molecule in plant abiotic stress responses and tolerance. Front Plant Sci 7:1341. https://doi.org/10.3389/fpls.2016.01341
Hoque TS, Uraji M, Hoque MA, Nakamura Y, Murata Y (2017) Methylglyoxal induces inhibition of growth, accumulation of anthocyanin, and activation of glyoxalase I and II in Arabidopsis thaliana. J Biochem Mol Toxicol 31:e21901. https://doi.org/10.1002/jbt.21901
Kalapos MP (1999) Methylglyoxal in living organisms: chemistry, biochemistry, toxicology and biological implications. Toxicol Lett 110:145–175. https://doi.org/10.1016/S0378-4274(99)00160-5
Kaur C, Singla-Pareek SL, Sopory SK (2014) Glyoxalase and methylglyoxal as biomarkers for plant stress tolerance. Crit Rev Plant Sci 33(6):429–456. https://doi.org/10.1080/07352689.2014.904147
Kharbech O, Sakouhi L, Massoud MB, Mur LAJ, Corpas FJ, Djebali W, Chaoui A (2020) Nitric oxide and hydrogen sulfide protect plasma membrane integrity and mitigate chromium-induced methylglyoxal toxicity in maize seedlings. Plant Physiol Biochem 157:244–255. https://doi.org/10.1016/j.plaphy.2020.10.017
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. https://doi.org/10.1007/s13205-020-02493-x
Li ZG (2016) Methylglyoxal and glyoxalase system in plants: old players, new concepts. Bot Rev 82:183–203. https://doi.org/10.1007/s12229-016-9167-9
Li ZG, Duan XQ, Min X, Zhou ZH (2017) Methylglyoxal as a novel signal molecule induces the salt tolerance of wheat by regulating the glyoxalase system, the antioxidant system, and osmolytes. Protoplasma 254:1995–2006. https://doi.org/10.1007/s00709-017-1094-z
Li ZG, Shi YH, Ai L (2019) Signaling molecule methylglyoxal remits the toxicity of plumbum by modifying antioxidant enzyme and osmoregulation systems in wheat (Triticum aestivum L.) Seedlings. Russ J Plant Physiol 66:564–571. https://doi.org/10.1134/S102144371904006X
Mostofa MG, Ghosh A, Li ZG, Siddiqui MN, Fujita M, Tran LSP (2018) Methylglyoxal-a signaling molecule in plant abiotic stress responses. Free Radical Bio Med 122:96–109. https://doi.org/10.1016/j.freeradbiomed.2018.03.009
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358. https://doi.org/10.1016/0003-2697(79)90738-3
Patel P, Kadur Narayanaswam G, Kataria S, Baghel L (2017) Involvement of nitric oxide in enhanced germination and seedling growth of magnetoprimed maize seeds. Plant Signal Behav 12:e1293217. https://doi.org/10.1080/15592324.2017.1293217
Saito R, Yamamoto H, Makino A, Sugimoto T, Miyake C (2011) Methylglyoxal functions as Hill oxidant and stimulates the photoreduction of O2 at photosystem I: a symptom of plant diabetes. Plant Cell Environ 34:1454–1464. https://doi.org/10.1111/j.1365-3040.2011.02344.x
Saxena M, Bisht R, Roy SD, Sopory SK, Bhalla-Sarin N (2005) Cloning and characterization of a mitochondrial glyoxalase II from Brassica juncea that is upregulated by NaCl, Zn, and ABA. Biochem Biophys Res Commun 336:813–819. https://doi.org/10.1016/j.bbrc.2005.08.178
Shi Q, Din F, Wang X, Wei M (2007) Exogenous nitric oxide protects cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550. https://doi.org/10.1016/j.plaphy.2007.05.005
Wang HH, Huang JJ, Bi YR (2010) Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Sci 179:281–288. https://doi.org/10.1016/j.plantsci.2010.05.014
Wang Y, Ye XY, Qiu XM, Li ZG (2019) Methylglyoxal triggers the heat tolerance in maize seedlings by driving AsA-GSH cycle and reactive oxygen species-/methylglyoxal-scavenging system. Plant Physiol Biochem 138:91–99. https://doi.org/10.1016/j.plaphy.2019.02.027
Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 33. https://doi.org/10.1016/j.bbrc.2005.08.263
Acknowledgements
This work was supported by Atatürk University, Erzurum, Turkey (Grant no: BAP-2015/111).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Á. Gallé.
Rights and permissions
About this article
Cite this article
Yiğit, İ., Atici, Ö. Seed priming with nitric oxide mitigates exogenous methylglyoxal toxicity by restoring glyoxalase and antioxidant systems in germinating maize (Zea mays L.) seeds. CEREAL RESEARCH COMMUNICATIONS 50, 811–820 (2022). https://doi.org/10.1007/s42976-021-00208-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42976-021-00208-3