Melatonin-Induced Chromium Tolerance Requires Hydrogen Sulfide Signaling in Maize
Abstract
:1. Introduction
2. Results
2.1. Response of Endogenous H2S and Melatonin to Cr Stress
2.2. Effects of Exogenous NaHS and Melatonin on Plant Growth
2.3. Effects of Exogenous NaHS and Melatonin on Cr Accumulation
2.4. Effects of Exogenous NaHS and Melatonin on Cell Wall Polysaccharides’ Metabolism under Cr Stress
2.5. Effects of NaHS and Melatonin on Oxidative Damage
2.6. Effects of NaHS and Melatonin on the Antioxidant System
3. Discussion
4. Materials and Methods
4.1. Plant Growth and Experimental Design
4.2. Measurement of Endogenous H2S Content
4.3. Measurement of Endogenous Melatonin Content
4.4. Measurement of Plant Dry Weight and Cr Content
4.5. Determination of Uronic Acid Content and Pectin Methylase Activity
4.6. Assays of Reactive Oxygen Species
4.7. Determination of Superoxide Dismutase, Catalase, and Peroxidase Activities
4.8. Determination of Non-Enzymatic Antioxidant Content
4.9. RNA Extraction and qRT-PCR
4.10. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Singh, S.; Prasad, S.M. Management of chromium(VI) toxicity by calcium and sulfur in tomato and brinjal: Implication of nitric oxide. J. Hazard. Mater. 2019, 373, 212–223. [Google Scholar] [CrossRef] [PubMed]
- Alwutayd, K.M.; Alghanem, S.M.S.; Alwutayd, R.; Alghamdi, S.A.; Alabdallah, N.M.; Al-Qthanin, R.N.; Sarfraz, W.; Khalid, N.; Naeem, N.; Ali, B.; et al. Mitigating chromium toxicity in rice (Oryza sativa L.) via ABA and 6-BAP: Unveiling synergistic benefits on morphophysiological traits and ASA-GSH cycle. Sci. Total Environ. 2024, 908, 168208. [Google Scholar] [CrossRef] [PubMed]
- Wakeel, A.; Xu, M.; Gan, Y.B. Chromium-induced reactive oxygen species accumulation by altering the enzymatic antioxidant system and associated cytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants. Int. J. Mol. Sci. 2020, 21, 728. [Google Scholar] [CrossRef] [PubMed]
- Fan, W.J.; Feng, Y.X.; Li, Y.H.; Lin, Y.J.; Yu, X.Z. Unraveling genes promoting ROS metabolism in subcellular organelles of Oryza sativa in response to trivalent and hexavalent chromium. Sci. Total Environ. 2020, 744, 140951. [Google Scholar] [CrossRef]
- Shi, J.D.; Zhao, D.; Ren, F.T.; Huang, L. Spatiotemporal variation of soil heavy metals in China: The pollution status and risk assessment. Sci. Total Environ. 2023, 871, 161768. [Google Scholar] [CrossRef]
- Li, Y.Y.; Tian, X.Y.; Liang, J.L.; Chen, X.L.; Ye, J.Y.; Liu, Y.S.; Liu, Y.Y.; Wei, Y.M. Remediation of hexavalent chromium in contaminated soil using amorphous iron pyrite: Effect on leachability, bioaccessibility, phytotoxicity and long-term stability. Environ. Pollut. 2020, 264, 114804. [Google Scholar] [CrossRef] [PubMed]
- Wu, X.W.; Song, H.X.; Guan, C.Y.; Zhang, Z.H. Boron alleviates cadmium toxicity in Brassica napus by promoting the chelation of cadmium onto the root cell wall components. Sci. Total Environ. 2020, 728, 138833. [Google Scholar] [CrossRef]
- Sun, C.L.; Lv, T.; Huang, L.; Liu, X.X.; Jin, C.W.; Lin, X.Y. Melatonin ameliorates aluminum toxicity through enhancing aluminum exclusion and reestablishing redox homeostasis in roots of wheat. J. Pineal Res. 2020, 68, e12642. [Google Scholar] [CrossRef]
- Yuan, Y.; Imtiaz, M.; Rizwan, M.; Dai, Z.H.; Hossain, M.M.; Zhang, Y.H.; Huang, H.L.; Tu, S.X. The role and its transcriptome mechanisms of cell wall polysaccharides in vanadium detoxication of rice. J. Hazard. Mater. 2022, 425, 127966. [Google Scholar] [CrossRef]
- Alsahli, A.A.; Bhat, J.A.; Alyemeni, M.N.; Ashraf, M.; Ahmad, P. Hydrogen sulfide (H2S) mitigates arsenic (As)-induced toxicity in pea (Pisum sativum L.) plants by regulating osmoregulation, antioxidant defense system, ascorbate glutathione cycle and glyoxalase system. J. Plant Growth Regul. 2021, 40, 2515–2531. [Google Scholar] [CrossRef]
- Bhatta, D.; Adhikari, A.; Kang, S.M.; Kwon, E.H.; Jan, R.; Kim, K.M.; Lee, I.J. Hormones and the antioxidant transduction pathway and gene expression, mediated by Serratia marcescens DB1, lessen the lethality of heavy metals (As, Ni, and Cr) in Oryza sativa L. Ecotoxicol. Environ. Saf. 2023, 263, 115377. [Google Scholar] [CrossRef] [PubMed]
- Ren, J.H.; Yang, X.X.; Zhang, N.; Feng, L.; Ma, C.Y.; Wang, Y.L.; Yang, Z.P.; Zhao, J. Melatonin alleviates aluminum-induced growth inhibition by modulating carbon and nitrogen metabolism, and reestablishing redox homeostasis in Zea mays L. J. Hazard. Mater. 2022, 423, 127159. [Google Scholar] [CrossRef] [PubMed]
- Muhammad, I.; Ahmad, S.; Shen, W.J. Melatonin-mediated molecular responses in plants: Enhancing stress tolerance and mitigating environmental challenges in cereal crop production. Int. J. Mol. Sci. 2024, 25, 4551. [Google Scholar] [CrossRef]
- Gao, T.; Wang, Z.X.; Dong, Y.L.; Cao, J.; Lin, R.T.; Wang, X.T.; Yu, Z.Q.; Chen, Y.X. Role of melatonin in sleep deprivation-induced intestinal barrier dysfunction in mice. J. Pineal Res. 2019, 67, e12574. [Google Scholar] [CrossRef] [PubMed]
- Colombage, R.; Singh, M.B.; Bhalla, P.L. Melatonin and abiotic stress tolerance in crop plants. Int. J. Mol. Sci. 2023, 24, 7447. [Google Scholar] [CrossRef] [PubMed]
- Gao, Y.Y.; Chen, H.M.; Chen, D.Y.; Hao, G.F. Genetic and evolutionary dissection of melatonin response signaling facilitates the regulation of plant growth and stress responses. J. Pineal Res. 2023, 74, e12850. [Google Scholar] [CrossRef] [PubMed]
- Ahammed, G.J.; Li, Z.; Chen, J.Y.; Dong, Y.F.; Qu, K.H.; Guo, T.M.; Wang, F.H.; Liu, A.R.; Chen, S.C.; Li, X. Reactive oxygen species signaling in melatonin-mediated plant stress response. Plant Physiol. Biochem. 2024, 207, 108398. [Google Scholar] [CrossRef] [PubMed]
- Chen, Q.; Arnao, M.B. Phytomelatonin: An emerging new hormone in plants. J. Exp. Bot. 2022, 73, 5773–5778. [Google Scholar] [CrossRef]
- Jan, R.; Asif, S.; Asaf, S.; Lubna; Du, X.X.; Park, J.R.; Nari, K.; Bhatta, D.; Lee, I.J.; Kim, K.M. Melatonin alleviates arsenic (As) toxicity in rice plants via modulating antioxidant defense system and secondary metabolites and reducing oxidative stress. Environ. Pollut. 2022, 318, 120868. [Google Scholar] [CrossRef]
- Yin, Y.Q.; Hu, J.J.; Tian, X.; Yang, Z.F.; Fang, W.M. Nitric oxide mediates melatonin-induced isoflavone accumulation and growth improvement in germinating soybeans under NaCl stress. J. Plant Physiol. 2022, 279, 153855. [Google Scholar] [CrossRef]
- Altaf, M.A.; Hao, Y.Y.; Shu, H.Y.; Mumtaz, M.A.; Cheng, S.H.; Alyemeni, M.N.; Ahmad, P.; Wang, Z. Melatonin enhanced the heavy metal-stress tolerance of pepper by mitigating the oxidative damage and reducing the heavy metal accumulation. J. Hazard. Mater. 2023, 454, 131468. [Google Scholar] [CrossRef] [PubMed]
- Sun, S.S.; Liu, A.R.; Li, Z.; Guo, T.M.; Chen, S.C.; Ahammed, G.J. Anthocyanin synthesis is critical for melatonin-induced chromium stress tolerance in tomato. J. Hazard. Mater. 2023, 453, 131456. [Google Scholar] [CrossRef] [PubMed]
- Arnao, M.B.; Hernández–Ruiz, J. Melatonin: A new plant hormone and / or a plant master regulator? Trends Plant Sci. 2019, 24, 38–48. [Google Scholar] [CrossRef] [PubMed]
- Hilal, B.; Khan, T.A.; Fariduddin, Q. Recent advances and mechanistic interactions of hydrogen sulfide with plant growth regulators in relation to abiotic stress tolerance in plants. Plant Physiol. Biochem. 2023, 196, 1065–1083. [Google Scholar] [CrossRef] [PubMed]
- Thakur, M.; Anand, A. Hydrogen sulfide: An emerging signaling molecule regulating drought stress response in plants. Physiol. Plant. 2021, 172, 1227–1243. [Google Scholar] [CrossRef] [PubMed]
- Saini, N.; Modolo, L.V.; Deswal, R.; Sehrawat, A.; Yadav, N.; Sangwan, N.S. Expanding Roles of Cross-talk between Hydrogen Sulfide and Nitric Oxide under Abiotic Stress in Plants. Plant Physiol. Biochem. 2024; in press. [Google Scholar]
- Ma, Y.L.; Zhang, W.; Niu, J.; Ren, Y.; Zhang, F. Hydrogen sulfide may function downstream of hydrogen peroxide in salt stress-induced stomatal closure in Vicia faba. Funct. Plant Biol. 2018, 46, 136–145. [Google Scholar] [CrossRef] [PubMed]
- Li, Z.; Zhu, Y.Q.; He, X.S.; Yong, B.; Peng, Y.; Zhang, X.Q.; Ma, X.; Yan, Y.H.; Huang, L.K.; Nie, G. The hydrogen sulfide, a downstream signaling molecule of hydrogen peroxide and nitric oxide, involves spermidine-regulated transcription factors and antioxidant defense in white clover in response to dehydration. Environ. Exp. Bot. 2019, 161, 255–264. [Google Scholar] [CrossRef]
- Du, X.Z.; Jin, Z.P.; Liu, D.M.; Yang, G.D.; Pei, Y.X. Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana. Plant Physiol. Biochem. 2017, 120, 112–119. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.; Feng, K.; Wang, G.; Zhang, S.; Zhao, J.; Yuan, X.; Ren, J. Titanium dioxide nanoparticles alleviates polystyrene nanoplastics induced growth inhibition by modulating carbon and nitrogen metabolism via melatonin signaling in maize. J. Nanobiotechnol. 2024, 22, 262. [Google Scholar] [CrossRef]
- Kharbech, O.; Sakouhi, L.; Mahjoubi, Y.; Massoud, M.B.; Debez, A.; Zribi, O.T.; Djebali, W.; Chaoui, A.; Mur, L.A.J. Nitric oxide donor, sodium nitroprusside modulates hydrogen sulfide metabolism and cysteine homeostasis to aid the alleviation of chromium toxicity in maize seedlings (Zea mays l.). J. Hazard. Mater. 2022, 424, 127302. [Google Scholar] [CrossRef]
- Sun, Y.P.; Ma, C.; Kang, X.; Zhang, L.; Wang, J.; Zheng, S.; Zhang, T.G. Hydrogen sulfide and nitric oxide are involved in melatonin-induced salt tolerance in cucumber. Plant Physiol. Biochem. 2021, 167, 101–112. [Google Scholar] [CrossRef] [PubMed]
- Hancock, J.T. Hydrogen sulfide and environmental stresses. Environ. Exp. Bot. 2019, 161, 50–56. [Google Scholar] [CrossRef]
- Luo, S.L.; Calderón-Urrea, A.; Jihua, Y.U.; Liao, W.B.; Xie, J.M.; Lv, J.; Feng, Z.; Tang, Z.Q. The role of hydrogen sulfide in plant alleviates heavy metal stress. Plant Soil 2020, 449, 1–10. [Google Scholar] [CrossRef]
- Zhou, M.J.; Zhou, H.; Shen, J.; Zhang, Z.R.; Gotor, C.; Romero, L.C.; Yuan, X.X.; Xie, Y.J. H2S action in plant life cycle. Plant Growth Regul. 2021, 94, 1–9. [Google Scholar] [CrossRef]
- Moustafa-Farag, M.; Elkelish, A.; Dafea, M.; Khan, M.; Arnao, M.B.; Abdelhamid, M.T.; El-Ezz, A.A.; Almoneafy, A.; Mahmoud, A.; Awad, M.; et al. Role of melatonin in plant tolerance to soil stressors: Salinity, pH and heavy metals. Molecules 2020, 25, 5359. [Google Scholar] [CrossRef] [PubMed]
- Bose, S.K.; Howlader, P. Melatonin plays multifunctional role in horticultural crops against environmental stresses: A review. Environ. Exp. Bot. 2020, 176, 104063. [Google Scholar] [CrossRef]
- Guo, H.M.; Xiao, T.Y.; Zhou, H.; Xie, Y.J.; Shen, W.B. Hydrogen sulfide: Aversatile regulator of environmental stress in plants. Acta Physiol. Plant. 2016, 38, 16. [Google Scholar] [CrossRef]
- Zhan, J.; Huang, H.G.; Yu, H.Y.; Zhang, X.Z.; Zheng, Z.C.; Wang, Y.D.; Liu, T.; Li, T.X. The combined effects of Cd and Pb enhanced metal binding by root cell walls of the phytostabilizer Athyrium wardii (Hook.). Environ. Pollut. 2020, 258, 113663. [Google Scholar] [CrossRef] [PubMed]
- Jia, H.L.; Wang, X.; Shi, C.; Guo, J.K.; Ma, P.Y.; Ren, X.H.; Wei, T.; Liu, H.X.; Li, J.S. Hydrogen sulfide decreases Cd translocation from root to shoot through increasing Cd accumulation in cell wall and decreasing Cd2+ influx in Isatis indigotica. Plant Physiol. Biochem. 2020, 155, 605–612. [Google Scholar] [CrossRef]
- Wu, X.W.; Tian, H.; Li, L.; Wang, X.Q. Polyaspartic acid alleviates cadmium toxicity in rapeseed leaves by affecting cadmium translocation and cell wall fixation of cadmium. Ecotoxicol. Environ. Saf. 2021, 224, 112685. [Google Scholar] [CrossRef]
- Wang, L.; Li, R.; Yan, X.X.; Liang, X.F.; Sun, Y.B.; Xu, Y.M. Pivotal role for root cell wall polysaccharides in cultivar-dependent cadmium accumulation in Brassica chinensis L. Ecotoxicol. Environ. Saf. 2020, 194, 110369. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.; Yi, K.; Chang, M.M.; Ling, G.Z.; Zhao, Z.K.; Li, X.F. Sequestration of Mn into the cell wall contributes to Mn tolerance in sugarcane (Saccharum officinarum L.). Plant Soil 2019, 436, 475–487. [Google Scholar] [CrossRef]
- Li, T.Q.; Tao, Q.; Shohag, M.J.I.; Yang, X.E.; Sparks, D.L.; Liang, Y.C. Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii. Plant Soil 2015, 389, 387–399. [Google Scholar] [CrossRef]
- Cao, Y.Y.; Qi, C.D.; Li, S.T.; Wang, Z.R.; Wang, X.Y.; Wang, J.F.; Ren, S.X.; Li, X.S.; Zhang, N.; Guo, Y.D. Melatonin alleviates copper toxicity via improving copper sequestration and ROS scavenging in cucumber. Plant Cell Physiol. 2019, 60, 562–574. [Google Scholar] [CrossRef] [PubMed]
- Kaya, C.; Ashraf, M.; Alyemeni, M.N.; Ahmad, P. The role of endogenous nitric oxide in salicylic acid-induced up-regulation of ascorbate-glutathione cycle involved in salinity tolerance of pepper (Capsicum annuum L.) plants. Plant Physiol. Biochem. 2019, 147, 10–20. [Google Scholar] [CrossRef] [PubMed]
- Xu, L.; Zhang, F.; Tang, M.J.; Wang, Y.; Dong, J.H.; Ying, J.L.; Chen, Y.L.; Hu, B.; Li, C.; Liu, L.W. Melatonin confers cadmium tolerance by modulating critical heavy metal chelators and transporters in radish plants. J. Pineal Res. 2020, 69, e12659. [Google Scholar] [CrossRef] [PubMed]
- Hasanuzzaman, M.; Bhuyan, M.H.M.; Anee, T.I.; Parvin, K.; Nahar, K.; Al Mahmud, J.; Fujita, M. Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 2019, 8, 384. [Google Scholar] [CrossRef] [PubMed]
- Kaya, C. Nitrate reductase is required for salicylic acid-induced water stress tolerance of pepper by upraising the AsA-GSH pathway and glyoxalase system. Physiol. Plant. 2021, 172, 351–370. [Google Scholar] [CrossRef] [PubMed]
- Kapoor, D.; Sharma, R.; Handa, N.; Kaur, H.; Rattan, A.; Yadav, P.; Gautam, V.; Kaur, R.; Bhardwaj, R. Redox homeostasis in plants under abiotic stress: Role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front. Environ. Sci. 2015, 3, 13. [Google Scholar] [CrossRef]
- Kaya, C.; Ashraf, M.; Alyemeni, M.N.; Ahmad, P. Responses of nitric oxide and hydrogen sulfide in regulating oxidative defence system in wheat plants grown under cadmium stress. Physiol. Plant. 2020, 168, 345–360. [Google Scholar] [CrossRef]
- Wang, Y.; Ye, X.Y.; Qiu, X.M.; Li, Z.G. Methylglyoxal triggers the heat tolerance in maize seedlings by driving AsA-GSH cycle and reactive oxygen species-/methylglyoxal-scavenging system. Plant Physiol. Biochem. 2019, 138, 91–99. [Google Scholar] [CrossRef] [PubMed]
- Nahar, K.; Hasanuzzaman, M.; Suzuki, T.; Fujita, M. Polyamines-induced aluminum tolerance in mung bean: A study on antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology 2017, 26, 58–73. [Google Scholar] [CrossRef] [PubMed]
- Hoagland, D.R.; Arnon, D.I. The water-culture method for growing plants without soil. Calif. Agric. Ext. Serv. Circ. 1950, 347, 1–32. [Google Scholar]
- Yang, X.X.; Ren, J.H.; Lin, X.Y.; Yang, Z.P.; Deng, X.P.; Ke, Q.B. Melatonin alleviates chromium toxicity in maize by modulation of cell wall polysaccharides biosynthesis, glutathione metabolism, and antioxidant capacity. Int. J. Mol. Sci. 2023, 24, 3816. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.X.; Ren, J.H.; Yang, W.P.; Xue, J.F.; Gao, Z.Q.; Yang, Z.P. Hydrogen sulfide alleviates chromium toxicity by promoting chromium sequestration and re-establishing redox homeostasis in Zea mays L. Environ. Pollut. 2023, 332, 121958. [Google Scholar] [CrossRef] [PubMed]
- Tian, B.; Qiao, Z.; Zhang, L.; Li, H.; Pei, Y. Hydrogen sulfide and proline cooperate to alleviate cadmium stress in foxtail millet seedings. Plant Physiol. Biochem. 2016, 109, 293–299. [Google Scholar] [CrossRef]
- Chen, G.F.; Huo, Y.S.; Tan, D.X.; Liang, Z.; Zhang, W.B.; Zhang, Y.K. Melatonin in Chinese medicinal herbs. Life Sci. 2003, 73, 19–26. [Google Scholar] [CrossRef]
- Yang, J.L.; Zhu, X.F.; Peng, Y.X.; Zheng, C.; Li, G.X.; Liu, Y.; Shi, Y.Z.; Zheng, S.J. Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol. 2011, 155, 1885–1892. [Google Scholar] [CrossRef]
- Loreto, F.; Velikova, V. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol. 2001, 127, 1781–1787. [Google Scholar] [CrossRef]
- Jahan, M.S.; Guo, S.R.; Baloch, A.R.; Sun, J.; Shu, S.; Wang, Y.; Ahammed, G.J.; Kabir, K.; Roy, R. Melatonin alleviates nickel phytotoxicity by improving photosynthesis, secondary metabolism and oxidative stress tolerance in tomato seedlings. Ecotoxicol. Environ. Saf. 2020, 197, 110593. [Google Scholar] [CrossRef]
- Li, J.T.; Qiu, Z.B.; Zhang, X.W.; Wang, L.S. Exogenous hydrogen peroxide can enhance tolerance of wheat seedlings to salt stress. Acta Physiol. Plant. 2011, 33, 835–842. [Google Scholar] [CrossRef]
- Hamurcu, M.; Sekmen, A.H.; Turkan, İ.; Gezgin, S.; Demiral, T.; Bell, R.W. Induced anti-oxidant activity in soybean alleviates oxidative stress under moderate boron toxicity. Plant Growth Regul. 2013, 70, 217–226. [Google Scholar] [CrossRef]
- Campos, C.N.; Ávila, R.G.; de Souza, K.R.D.; Azevedo, L.M.; Alves, J.D. Melatonin reduces oxidative stress and promotes drought tolerance in young Coffea arabica L. plants. Agric. Water Manag. 2019, 211, 37–47. [Google Scholar] [CrossRef]
- Wu, X.X.; He, J.; Ding, H.D.; Zhu, Z.W.; Chen, J.L.; Xu, S.; Zha, D.S. Modulation of zinc-induced oxidative damage in Solanum melongena by 6-benzylaminopurine involves ascorbate–glutathione cycle metabolism. Environ. Exp. Bot. 2015, 116, 1–11. [Google Scholar] [CrossRef]
- Catala, R.; Lopez-Cobollo, R.; Castellano, M.M.; Angosto, T.; Alonso, J.M.; Ecker, J.R.; Salinas, J. The Arabidopsis 14-3-3 protein RARE COLD INDUCIBLE 1A links low-temperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimation. Plant Cell 2014, 26, 3326–3342. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yang, X.; Shi, Q.; Wang, X.; Zhang, T.; Feng, K.; Wang, G.; Zhao, J.; Yuan, X.; Ren, J. Melatonin-Induced Chromium Tolerance Requires Hydrogen Sulfide Signaling in Maize. Plants 2024, 13, 1763. https://doi.org/10.3390/plants13131763
Yang X, Shi Q, Wang X, Zhang T, Feng K, Wang G, Zhao J, Yuan X, Ren J. Melatonin-Induced Chromium Tolerance Requires Hydrogen Sulfide Signaling in Maize. Plants. 2024; 13(13):1763. https://doi.org/10.3390/plants13131763
Chicago/Turabian StyleYang, Xiaoxiao, Qifeng Shi, Xinru Wang, Tao Zhang, Ke Feng, Guo Wang, Juan Zhao, Xiangyang Yuan, and Jianhong Ren. 2024. "Melatonin-Induced Chromium Tolerance Requires Hydrogen Sulfide Signaling in Maize" Plants 13, no. 13: 1763. https://doi.org/10.3390/plants13131763
APA StyleYang, X., Shi, Q., Wang, X., Zhang, T., Feng, K., Wang, G., Zhao, J., Yuan, X., & Ren, J. (2024). Melatonin-Induced Chromium Tolerance Requires Hydrogen Sulfide Signaling in Maize. Plants, 13(13), 1763. https://doi.org/10.3390/plants13131763