Crosstalk between Melatonin and Reactive Oxygen Species in Plant Abiotic Stress Responses: An Update
Abstract
:1. Introduction
2. Melatonin Acts as an Antioxidant to Establish Redox Homeostasis through the Antioxidant System in Plants under Abiotic Stresses
3. Plant Abiotic Stress Tolerance Is Mediated by the Crosstalk between Melatonin and Signal Molecules (NO, H2S, and ROS)
4. The Roles of RBOH-Involved ROS Signaling in Melatonin-Modulated Plant Processes
5. How Melatonin Directs with the RBOH-Regulated ROS Signaling in Plant Tolerance to Abiotic Stress
6. Conclusions and Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bailey-Serres, J.; Parker, J.E.; Ainsworth, E.A.; Oldroyd, G.E.D.; Schroeder, J.I. Genetic strategies for improving crop yields. Nature 2019, 575, 109–118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.; Zhao, Y.; Zhu, J.K. Thriving under stress: How plants balance growth and the stress response. Dev. Cell 2020, 55, 529–543. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Zhu, J.; Gong, Z.; Zhu, J. Abiotic stress responses in plants. Nat. Rev. Genet. 2022, 23, 104–111. [Google Scholar] [CrossRef]
- Sachdev, S.; Ansari, S.A.; Ansari, M.I.; Fujita, M.; Hasanuzzaman, M. Abiotic stress and reactive oxygen species: Generation, signaling, and defense mechanisms. Antioxidants 2021, 10, 277. [Google Scholar] [CrossRef] [PubMed]
- Foyer, C.H.; Noctor, G. Oxidant and antioxidant signalling in plants: A re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ. 2005, 28, 1056–1071. [Google Scholar] [CrossRef]
- Qi, J.; Song, C.P.; Wang, B.; Zhou, J.; Kangasjärvi, J.; Zhu, J.K.; Gong, Z. Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J. Integr. Plant Biol. 2018, 60, 805–826. [Google Scholar] [CrossRef] [Green Version]
- Apel, K.; Hirt, H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55, 373–399. [Google Scholar] [CrossRef] [Green Version]
- Mittler, R. ROS are good. Trends Plant Sci. 2017, 22, 11–19. [Google Scholar] [CrossRef] [Green Version]
- Sun, C.; Liu, L.; Wang, L.; Li, B.; Jin, C.; Lin, X. Melatonin: A master regulator of plant development and stress responses. J. Integr. Plant Biol. 2021, 63, 126–145. [Google Scholar] [CrossRef]
- Arnao, M.B.; Cano, A.; Hernández-Ruiz, J. Phytomelatonin: An unexpected molecule with amazing performances in plants. J. Exp. Bot. 2022, erac009. [Google Scholar] [CrossRef]
- Gu, Q.; Chen, Z.; Yu, X.; Cui, W.; Pan, J.; Zhao, G.; Xu, S.; Wang, R.; Shen, W. Melatonin confers plant tolerance against cadmium stress via the decrease of cadmium accumulation and reestablishment of microRNA-mediated redox homeostasis. Plant Sci. 2017, 261, 28–37. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Xie, Y.; Gu, Q.; Zhao, G.; Zhang, Y.; Cui, W.; Xu, S.; Wang, R.; Shen, W. The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic. Biol. Med. 2017, 108, 465–477. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Gu, Q.; Yu, X.; Huang, L.; Xu, S.; Wang, R.; Shen, W.; Shen, W. Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann. Bot. 2018, 121, 1127–1136. [Google Scholar] [CrossRef] [PubMed]
- Sun, L.; Song, F.; Guo, J.; Zhu, X.; Liu, S.; Liu, F.; Li, X. Nano-ZnO-induced drought tolerance is associated with melatonin synthesis and metabolism in maize. Int. J. Mol. Sci. 2020, 21, 782. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Guo, Y.; Lan, Z.; Xu, K.; Chang, J.; Ahammed, G.J.; Ma, J.; Wei, C.; Zhang, X. Methyl jasmonate mediates melatonin-induced cold tolerance of grafted watermelon plants. Hortic. Res. 2021, 8, 57. [Google Scholar] [CrossRef]
- Haskirli, H.; Yilmaz, O.; Ozgur, R.; Uzilday, B.; Turkan, I. Melatonin mitigates UV-B stress via regulating oxidative stress response, cellular redox and alternative electron sinks in Arabidopsis thaliana. Phytochemistry 2021, 182, 112592. [Google Scholar] [CrossRef]
- Lee, H.Y.; Back, K. Mitogen-activated protein kinase pathways are required for melatonin-mediated defense responses in plants. J. Pineal Res. 2016, 60, 327–335. [Google Scholar] [CrossRef]
- Arnao, M.B.; Hernandez-Ruiz, J. Melatonin: A new plant hormone and/or a plant master regulator? Trends Plant Sci. 2019, 24, 38–48. [Google Scholar] [CrossRef]
- Gu, Q.; Wang, C.; Xiao, Q.; Chen, Z.; Han, Y. Melatonin confers plant cadmium tolerance: An update. Int. J. Mol. Sci. 2021, 22, 11704. [Google Scholar] [CrossRef]
- Tousi, S.; Zoufan, P.; Ghahfarrokhie, A.R. Alleviation of cadmium-induced phytotoxicity and growth improvement by exogenous melatonin pretreatment in mallow (Malva parviflora) plants. Ecotox. Environ. Safe. 2020, 206, 111403. [Google Scholar] [CrossRef]
- Wei, W.; Li, Q.T.; Chu, Y.N.; Reiter, R.J.; Yu, X.M.; Zhu, D.H.; Zhang, W.K.; Ma, B.; Lin, Q.; Zhang, J.S.; et al. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J. Exp. Bot. 2015, 66, 695–707. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teng, Z.; Yu, Y.; Zhu, Z.; Hong, S.B.; Yang, B.; Zang, Y. Melatonin elevated Sclerotinia sclerotiorum resistance via modulation of ATP and glucosinolate biosynthesis in Brassica rapa ssp. pekinensis. J. Proteom. 2021, 243, 104264. [Google Scholar] [CrossRef] [PubMed]
- Choudhury, F.K.; Rivero, R.M.; Blumwald, E.; Mittler, R. Reactive oxygen species, abiotic stress and stress combination. Plant J. 2017, 90, 856–867. [Google Scholar] [CrossRef] [PubMed]
- Marino, D.; Dunand, C.; Puppo, A.; Pauly, N. A burst of plant NADPH oxidases. Trends Plant Sci. 2012, 17, 9–15. [Google Scholar] [CrossRef] [PubMed]
- Sagi, M.; Fluhr, R. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 2006, 141, 336–340. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Torres, M.A.; Jones, J.D.; Dangl, J.L. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 2005, 37, 1130–1134. [Google Scholar] [CrossRef]
- Jiang, C.; Belfield, E.J.; Mithani, A.; Visscher, A.; Ragoussis, J.; Mott, R.; Smith, J.A.; Harberd, N.P. ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. EMBO J. 2012, 31, 4359–4370. [Google Scholar] [CrossRef] [Green Version]
- Ma, L.; Zhang, H.; Sun, L.; Jiao, Y.; Zhang, G.; Miao, C.; Hao, F. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J. Exp. Bot. 2012, 63, 305–317. [Google Scholar] [CrossRef]
- Gupta, D.K.; Pena, L.B.; Romero-Puertas, M.C.; Hernández, A.; Inouhe, M.; Sandalio, L.M. NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ. 2017, 40, 509–526. [Google Scholar] [CrossRef]
- Wang, L.; Guo, Y.; Jia, L.; Chu, H.; Zhou, S.; Chen, K.; Wu, D.; Zhao, L. Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol. 2014, 164, 2184–2196. [Google Scholar] [CrossRef] [Green Version]
- Zhou, J.; Wang, J.; Shi, K.; Xia, X.J.; Zhou, Y.H.; Yu, J.Q. Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol. Biochem. 2012, 60, 141–149. [Google Scholar] [CrossRef] [PubMed]
- Zandalinas, S.I.; Fichman, Y.; Devireddy, A.R.; Sengupta, S.; Azad, R.K.; Mittler, R. Systemic signaling during abiotic stress combination in plants. Proc. Natl. Acad. Sci. USA 2000, 117, 13810–13820. [Google Scholar] [CrossRef] [PubMed]
- Mukherjee, S. Insights to nitric oxide-melatonin crosstalk and N-nitrosomelatonin functioning in plants: Where do we stand? J. Exp. Bot. 2019, 70, 6035–6047. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Gao, H.; Lu, M.; Hao, C.; Pu, Z.; Guo, M.; Hou, D.; Chen, L.Y.; Huang, X. Melatonin-nitric oxide crosstalk and their roles in the redox network in plants. Int. J. Mol. Sci. 2019, 20, 6200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Su, J.; Yang, X.; Shao, Y.; Chen, Z.; Shen, W. Molecular hydrogen-induced salinity tolerance requires melatonin signalling in Arabidopsis thaliana. Plant Cell Environ. 2021, 44, 476–490. [Google Scholar] [CrossRef] [PubMed]
- Zhao, G.; Zhao, Y.; Yu, X.; Kiprotich, F.; Han, H.; Guan, R.; Wang, R.; Shen, W. Nitric oxide is required for melatonin-enhanced tolerance against salinity stress in rapeseed (Brassica napus L.) seedlings. Int. J. Mol. Sci. 2018, 19, 1912. [Google Scholar] [CrossRef] [Green Version]
- Yang, N.; Sun, K.; Wang, X.; Wang, K.; Kong, X.; Gao, J.; Wen, D. Melatonin participates in selenium-enhanced cold tolerance of cucumber seedlings. Front. Plant Sci. 2021, 12, 786043. [Google Scholar] [CrossRef]
- Jahan, M.S.; Guo, S.; Sun, J.; Shu, S.; Wang, Y.; El-Yazied, A.A.; Alabdallah, N.M.; Hikal, M.; Mohamed, M.H.M.; Ibrahim, M.F.M.; et al. Melatonin-mediated photosynthetic performance of tomato seedlings under high-temperature stress. Plant Physiol. Biochem. 2021, 167, 309–320. [Google Scholar] [CrossRef]
- Li, C.; Tan, D.X.; Liang, D.; Chang, C.; Jia, D.; Ma, F. Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress. J. Exp. Bot. 2015, 66, 669–680. [Google Scholar] [CrossRef] [Green Version]
- Zheng, X.; Tan, D.X.; Allan, A.C.; Zuo, B.; Zhao, Y.; Reiter, R.J.; Wang, L.; Wang, Z.; Guo, Y.; Zhou, J.; et al. Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress. Sci. Rep. 2017, 7, 41236. [Google Scholar] [CrossRef]
- Byeon, Y.; Back, K. Molecular cloning of melatonin 2-hydroxylase responsible for 2-hydroxymelatonin production in rice (Oryza sativa). J. Pineal Res. 2015, 58, 343–351. [Google Scholar] [CrossRef] [PubMed]
- Mukherjee, S.; David, A.; Yadav, S.; Baluška, F.; Bhatla, S.C. Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiol. Plant. 2014, 152, 714–728. [Google Scholar] [CrossRef] [PubMed]
- Ren, J.; Yang, X.; Zhang, N.; Feng, L.; Ma, C.; Wang, Y.; Yang, Z.; 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]
- Iqbal, N.; Fatma, M.; Gautam, H.; Umar, S.; Khan, N.A. The crosstalk of melatonin and hydrogen sulfide determines photosynthetic performance by regulation of carbohydrate metabolism in wheat under heat stress. Plants 2021, 10, 1778. [Google Scholar] [CrossRef]
- Wang, L.; Zhao, Y.; Reiter, R.J.; He, C.; Liu, G.; Lei, Q.; Zuo, B.; Zheng, X.; Li, Q.; Kong, J. Changes in melatonin levels in transgenic ‘Micro-Tom’ tomato overexpressing ovine AANAT and ovine HIOMT genes. J. Pineal Res. 2014, 56, 134–142. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.J.; Huang, B.; Zhao, Y.Q.; Hu, D.; Chen, T.; Ding, C.B.; Chen, Y.E.; Yuan, S.; Yuan, M. Melatonin enhanced the tolerance of Arabidopsis thaliana to high light through improving anti-oxidative system and photosynthesis. Front. Plant Sci. 2021, 12, 752584. [Google Scholar] [CrossRef]
- Tan, K.; Zheng, J.; Liu, C.; Liu, X.; Liu, X.; Gao, T.; Song, X.; Wei, Z.; Ma, F.; Li, C. Heterologous expression of the melatonin-related gene HIOMT improves salt tolerance in Malus domestica. Int. J. Mol. Sci. 2021, 22, 12425. [Google Scholar] [CrossRef]
- Pandey, V.; Dixit, V.; Shyam, R. Chromium effect on ROS generation and detoxification in pea (Pisum sativum) leaf chloroplasts. Protoplasma 2009, 236, 85–95. [Google Scholar] [CrossRef]
- Chang, R.; Jang, C.J.; Branco-Price, C.; Nghiem, P.; Bailey-Serres, J. Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol. Biol. 2012, 78, 109–122. [Google Scholar] [CrossRef]
- Corpas, F.J.; Del Río, L.A.; Palma, J.M. Plant peroxisomes at the crossroad of NO and H2O2 metabolism. J. Integr. Plant Biol. 2019, 61, 803–816. [Google Scholar]
- Hofmann, A.; Wienkoop, S.; Harder, S.; Bartlog, F.; Lüthje, S. Hypoxia-responsive class III peroxidases in maize roots: Soluble and membrane-bound isoenzymes. Int. J. Mol. Sci. 2020, 21, 8872. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Mu, X.; Chen, X.; Han, Y. Hydrogen sulfide attenuates intracellular oxidative stress via repressing glycolate oxidase activities in Arabidopsis thaliana. BMC Plant Biol. 2022, 22, 98. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Shabala, S.; Zhang, J.; Ma, G.; Chen, D.; Shabala, L.; Zeng, F.; Chen, Z.H.; Zhou, M.; Venkataraman, G. Melatonin improves rice salinity stress tolerance by NADPH oxidase-dependent control of the plasma membrane K+ transporters and K+ homeostasis. Plant Cell Environ. 2020, 43, 2591–2605. [Google Scholar] [CrossRef] [PubMed]
- Zahedi, S.M.; Hosseini, M.S.; Fahadi, H.N.; Gholami, R.; Abdelrahman, M.; Tran, L.P. Exogenous melatonin mitigates salinity-induced damage in olive seedlings by modulating ion homeostasis, antioxidant defense, and phytohormone balance. Physiol. Plant. 2021, 173, 1682–1694. [Google Scholar] [CrossRef]
- Li, C.; Wang, P.; Wei, Z.; Liang, D.; Liu, C.; Yin, L.; Jia, D.; Fu, M.; Ma, F. The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J. Pineal Res. 2012, 53, 298–306. [Google Scholar] [CrossRef] [PubMed]
- Siddiqui, M.H.; Alamri, S.; Al-Khaishany, M.Y.; Khan, M.N.; Al-Amri, A.; Ali, H.M.; Alaraidh, I.A.; Alsahli, A.A. Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. Int. J. Mol. Sci. 2019, 20, 353. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.J.; Zhang, N.; Yang, R.C.; Wang, L.; Sun, Q.Q.; Li, D.B.; Cao, Y.Y.; Weeda, S.; Zhao, B.; Ren, S.; et al. Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J. Pineal Res. 2014, 57, 269–279. [Google Scholar] [CrossRef]
- Yan, F.; Wei, H.; Ding, Y.; Li, W.; Liu, Z.; Chen, L.; Tang, S.; Ding, C.; Jiang, Y.; Li, G. Melatonin regulates antioxidant strategy in response to continuous salt stress in rice seedlings. Plant Physiol. Biochem. 2021, 165, 239–250. [Google Scholar] [CrossRef]
- Li, J.; Liu, Y.; Zhang, M.; Xu, H.; Ning, K.; Wang, B.; Chen, M. Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity. BMC Plant Biol. 2022, 22, 16. [Google Scholar] [CrossRef]
- Altaf, M.A.; Shahid, R.; Ren, M.X.; Naz, S.; Altaf, M.M.; Khan, L.U.; Tiwari, R.K.; Lal, M.K.; Shahid, M.A.; Kumar, R.; et al. Melatonin improves drought stress tolerance of tomato by modulating plant growth, root architecture, photosynthesis, and antioxidant defense system. Antioxidants 2022, 11, 309. [Google Scholar] [CrossRef]
- Jafari, M.; Shahsavar, A. The effect of foliar application of melatonin on changes in secondary metabolite contents in two Citrus species under drought stress conditions. Front. Plant Sci. 2021, 12, 692735. [Google Scholar] [CrossRef] [PubMed]
- Shamloo-Dashtpagerdi, R.; Aliakbari, M.; Lindlöf, A.; Tahmasebi, S. A systems biology study unveils the association between a melatonin biosynthesis gene, O-methyl transferase 1 (OMT1) and wheat (Triticum aestivum L.) combined drought and salinity stress tolerance. Planta 2022, 255, 99. [Google Scholar] [CrossRef] [PubMed]
- Imran, M.; Latif, K.A.; Shahzad, R.; Aaqil, K.M.; Bilal, S.; Khan, A.; Kang, S.M.; Lee, I.J. Exogenous melatonin induces drought stress tolerance by promoting plant growth and antioxidant defence system of soybean plants. AoB Plants 2021, 13, plab026. [Google Scholar] [CrossRef] [PubMed]
- Xia, H.; Ni, Z.; Hu, R.; Lin, L.; Deng, H.; Wang, J.; Tang, Y.; Sun, G.; Wang, X.; Li, H.; et al. Melatonin alleviates drought stress by a non-enzymatic and enzymatic antioxidative system in kiwifruit seedlings. Int. J. Mol. Sci. 2020, 21, 852. [Google Scholar] [CrossRef] [Green Version]
- Antoniou, C.; Chatzimichail, G.; Xenofontos, R.; Pavlou, J.J.; Panagiotou, E.; Christou, A.; Fotopoulos, V. Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. J. Pineal Res. 2017, 62, e12401. [Google Scholar] [CrossRef]
- Bajwa, V.S.; Shukla, M.R.; Sherif, S.M.; Murch, S.J.; Saxena, P.K. Role of melatonin in alleviating cold stress in Arabidopsis thaliana. J. Pineal Res. 2014, 56, 238–245. [Google Scholar] [CrossRef]
- Li, X.; Wei, J.P.; Scott, E.R.; Liu, J.W.; Guo, S.; Li, Y.; Zhang, L.; Han, W.Y. Exogenous melatonin alleviates cold stress by promoting antioxidant defense and redox homeostasis in Camellia sinensis L. Molecules 2018, 23, 165. [Google Scholar] [CrossRef] [Green Version]
- Han, Q.H.; Huang, B.; Ding, C.B.; Zhang, Z.W.; Chen, Y.E.; Hu, C.; Zhou, L.J.; Huang, Y.; Liao, J.Q.; Yuan, S.; et al. Effects of melatonin on anti-oxidative systems and photosystem II in cold-stressed rice seedlings. Front. Plant Sci. 2017, 8, 785. [Google Scholar] [CrossRef]
- Marta, B.; Szafrańska, K.; Posmyk, M.M. Exogenous melatonin improves antioxidant defense in cucumber seeds (Cucumis sativus L.) germinated under chilling stress. Front. Plant Sci. 2016, 7, 575. [Google Scholar] [CrossRef] [Green Version]
- Ding, F.; Liu, B.; Zhang, S. Exogenous melatonin ameliorates cold-induced damage in tomato plants. Sci. Horticult. 2017, 219, 264–271. [Google Scholar] [CrossRef]
- Yu, Y.; Deng, L.; Zhou, L.; Chen, G.; Wang, Y. Exogenous melatonin activates antioxidant systems to increase the ability of rice seeds to germinate under high temperature conditions. Plants 2022, 11, 886. [Google Scholar] [CrossRef] [PubMed]
- Imran, M.; Aaqil, K.M.; Shahzad, R.; Bilal, S.; Khan, M.; Yun, B.W.; Khan, A.L.; Lee, I.J. Melatonin ameliorates thermotolerance in soybean seedling through balancing redox homeostasis and modulating antioxidant defense, phytohormones and polyamines biosynthesis. Molecules 2021, 26, 5116. [Google Scholar] [CrossRef] [PubMed]
- Xing, X.; Ding, Y.; Jin, J.; Song, A.; Chen, S.; Chen, F.; Fang, W.; Jiang, J. Physiological and transcripts analyses reveal the mechanism by which melatonin alleviates heat stress in Chrysanthemum seedlings. Front. Plant Sci. 2021, 12, 673236. [Google Scholar] [CrossRef] [PubMed]
- Xia, H.; Zhou, Y.; Deng, H.; Lin, L.; Deng, Q.; Wang, J.; Lv, X.; Zhang, X.; Liang, D. Melatonin improves heat tolerance in Actinidia deliciosa via carotenoid biosynthesis and heat shock proteins expression. Physiol. Plant. 2021, 172, 1582–1593. [Google Scholar] [CrossRef]
- Li, Z.G.; Xu, Y.; Bai, L.K.; Zhang, S.Y.; Wang, Y. Melatonin enhances thermotolerance of maize seedlings (Zea mays L.) by modulating antioxidant defense, methylglyoxal detoxification, and osmoregulation systems. Protoplasma 2019, 256, 471–490. [Google Scholar] [CrossRef]
- Shi, H.; Tan, D.X.; Reiter, R.J.; Ye, T.; Yang, F.; Chan, Z. Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis. J. Pineal Res. 2015, 58, 335–342. [Google Scholar] [CrossRef]
- Xu, W.; Cai, S.Y.; Zhang, Y.; Wang, Y.; Ahammed, G.J.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Yu, J.Q.; Reiter, R.J. Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J. Pineal Res. 2016, 61, 457–469. [Google Scholar] [CrossRef]
- Posmyk, M.M.; Kuran, H.; Marciniak, K.; Janas, K.M. Presowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations. J. Pineal Res. 2008, 45, 24–31. [Google Scholar] [CrossRef]
- Sun, C.; Lv, T.; Huang, L.; Liu, X.; Jin, C.; Lin, X. 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]
- Nawaz, M.A.; Jiao, Y.; Chen, C.; Shireen, F.; Zheng, Z.; Imtiaz, M.; Bie, Z.; Huang, Y. Melatonin pretreatment improves vanadium stress tolerance of watermelon seedlings by reducing vanadium concentration in the leaves and regulating melatonin biosynthesis and antioxidant-related gene expression. J. Plant Physiol. 2018, 220, 115–127. [Google Scholar] [CrossRef]
- Wang, Y.; Cheng, P.; Zhao, G.; Li, L.; Shen, W. Phytomelatonin and gasotransmitters: A crucial combination for plant physiological functions. J. Exp. Bot. 2022, 17, erac159. [Google Scholar] [CrossRef] [PubMed]
- Tan, D.X.; Manchester, L.C.; Terron, M.P.; Flores, L.J.; Reiter, R.J. One molecule, many derivatives: A never-ending interaction of melatonin with reactive oxygen and nitrogen species? J. Pineal Res. 2007, 42, 28–42. [Google Scholar] [CrossRef] [PubMed]
- He, H.; He, L.F. Crosstalk between melatonin and nitric oxide in plant development and stress responses. Physiol. Plant. 2020, 170, 218–226. [Google Scholar] [CrossRef] [PubMed]
- Aghdam, M.S.; Luo, Z.; Jannatizadeh, A.; Sheikh-Assadi, M.; Sharafi, Y.; Farmani, B.; Fard, J.R.; Razavi, F. Employing exogenous melatonin applying confers chilling tolerance in tomato fruits by upregulating ZAT2/6/12 giving rise to promoting endogenous polyamines, proline, and nitric oxide accumulation by triggering arginine pathway activity. Food Chem. 2019, 275, 549–556. [Google Scholar] [CrossRef] [PubMed]
- Arora, D.; Bhatla, S.C. Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/ZnSOD and MnSOD. Free Radic Biol. Med. 2017, 106, 315–328. [Google Scholar] [CrossRef] [PubMed]
- Imran, M.; Shazad, R.; Bilal, S.; Imran, Q.M.; Lee, I.J. Exogenous melatonin mediates the regulation of endogenous nitric oxide in Glycine max L. to reduce effects of drought stress. Environ. Exp. Bot. 2021, 188, 104511. [Google Scholar] [CrossRef]
- Pardo-Hernández, M.; López-Delacalle, M.; Rivero, R.M. ROS and NO regulation by melatonin under abiotic stress in plants. Antioxidants 2020, 9, 1078. [Google Scholar] [CrossRef]
- Wang, T.; Song, J.; Liu, Z.; Liu, Z.; Cui, J. Melatonin alleviates cadmium toxicity by reducing nitric oxide accumulation and IRT1 expression in Chinese cabbage seedlings. Environ. Sci. Pollut. Res. Int. 2021, 28, 15394–15405. [Google Scholar] [CrossRef]
- Zhang, J.; Zhou, M.; Zhou, H.; Zhao, D.; Gotor, C.; Romero, L.C.; Shen, J.; Ge, Z.; Zhang, Z.; Shen, W.; et al. Hydrogen sulfide, a signaling molecule in plant stress responses. J. Integr. Plant Biol. 2021, 63, 146–160. [Google Scholar] [CrossRef]
- Chen, T.; Tian, M.; Han, Y. Hydrogen sulfide: A multi-tasking signal molecule in the regulation of oxidative stress responses. J. Exp. Bot. 2020, 71, 2862–2869. [Google Scholar] [CrossRef]
- Jia, H.; Wang, X.; Dou, Y.; Liu, D.; Si, W.; Fang, H.; Zhao, C.; Chen, S.; Xi, J.; Li, J. Hydrogen sulfide-cysteine cycle system enhances cadmium tolerance through alleviating cadmium-induced oxidative stress and ion toxicity in Arabidopsis roots. Sci. Rep. 2016, 6, 39702. [Google Scholar] [CrossRef] [PubMed]
- Huang, D.; Huo, J.; Liao, W. Hydrogen sulfide: Roles in plant abiotic stress response and crosstalk with other signals. Plant Sci. 2021, 302, 110733. [Google Scholar] [CrossRef] [PubMed]
- Mukherjee, S.; Bhatla, S.C. Exogenous melatonin modulates endogenous H2S homeostasis and L-cysteine desulfhydrase activity in salt-stressed tomato (Solanum lycopersicum L. var. cherry) seedling cotyledons. J. Plant Growth Regul. 2020, 40, 2502–2514. [Google Scholar] [CrossRef]
- Siddiqui, M.; Khan, M.; Mukherjee, S.; Basahi, R.; Alamri, S.; Al-Amri, A.; Alsubaie, Q.; Ali, H.; Al-Munqedhi, B.; Almohisen, I. Exogenous melatonin-mediated regulation of K+/Na+ transport, H+-ATPase activity and enzymatic antioxidative defence operate through endogenous hydrogen sulphide signalling in NaCl-stressed tomato seedling roots. Plant Biol. 2021, 23, 797–805. [Google Scholar] [CrossRef]
- Sun, Y.; Ma, C.; Kang, X.; Zhang, L.; Wang, J.; Zheng, S.; Zhang, T. Hydrogen sulfide and nitric oxide are involved in melatonin-induced salt tolerance in cucumber. Plant Physiol. Biochem. 2021, 167, 101–112. [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]
- Kaya, C.; Higgs, D.; Ashraf, M.; Alyemeni, M.N.; Ahmad, P. Integrative roles of nitric oxide and hydrogen sulfide in melatonin-induced tolerance of pepper (Capsicum annuum L.) plants to iron deficiency and salt stress alone or in combination. Physiol. Plant. 2020, 168, 256–277. [Google Scholar] [CrossRef] [Green Version]
- Chang, J.; Guo, Y.; Li, J.; Su, Z.; Wang, C.; Zhang, R.; Wei, C.; Ma, J.; Zhang, X.; Li, H. Positive interaction between H2O2 and Ca2+ mediates melatonin-induced CBF pathway and cold tolerance in watermelon (Citrullus lanatus L.). Antioxidants 2021, 10, 1457. [Google Scholar] [CrossRef]
- Gong, B.; Yan, Y.; Wen, D.; Shi, Q. Hydrogen peroxide produced by NADPH oxidase: A novel downstream signaling pathway in melatonin induced stress tolerance in Solanum lycopersicum. Physiol. Plant. 2017, 160, 396–409. [Google Scholar] [CrossRef]
- Zeng, H.; Bai, Y.; Wei, Y.; Reiter, R.J.; Shi, H. Phytomelatonin as a central molecule in plant disease resistance. J. Exp. Bot. 2022, 17, erac111. [Google Scholar] [CrossRef]
- Suzuki, N.; Miller, G.; Morales, J.; Shulaev, V.; Torres, M.A.; Mittler, R. Respiratory burst oxidases: The engines of ROS signaling. Curr. Opin. Plant Biol. 2011, 14, 691–699. [Google Scholar] [CrossRef] [PubMed]
- Chung, J.S.; Zhu, J.K.; Bressan, R.A.; Hasegawa, P.M.; Shi, H. Reactive oxygen species mediate Na-induced SOS1 mRNA stability in Arabidopsis. Plant J. 2008, 53, 554–565. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, X.H.; Zhang, H.J.; Tian, L.M.; Huang, L.; Liu, S.X.; Li, D.Y.; Song, F.M. Tomato SlRbohB, a member of the NADPH oxidase family, is required for disease resistance against Botrytis cinerea and tolerance to drought stress. Front. Plant Sci. 2015, 6, 463. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, X.; Li, Y.; Ahammed, G.J.; Zhang, X.N.; Ying, L.; Zhang, L.; Yan, P.; Zhang, L.P.; Li, Q.Y.; Han, W.Y. RBOH1-dependent apoplastic H2O2 mediates epigallocatechin- 3-gallate-induced abiotic stress tolerance in Solanum lycopersicum L. Environ. Exp. Bot. 2019, 161, 357–366. [Google Scholar] [CrossRef]
- Liu, T.; Ye, X.L.; Li, M.; Li, J.M.; Hu, X.H. H2O2 and NO are involved in trehalose-regulated oxidative stress tolerance in cold-stressed tomato plants. Environ. Exp. Bot. 2020, 171, 103961. [Google Scholar] [CrossRef]
- Xu, J.; Kang, Z.; Zhu, K.; Zhao, D.; Yuan, Y.; Yang, S.; Zhen, W.; Hu, X. RBOH1-dependent H2O2 mediates spermine-induced antioxidant enzyme system to enhance tomato seedling tolerance to salinity-alkalinity stress. Plant Physiol. Biochem. 2021, 164, 237–246. [Google Scholar] [CrossRef]
- Liu, D.; Li, Y.Y.; Zhou, Z.C.; Xiang, X.; Liu, X.; Wang, J.; Hu, Z.R.; Xiang, S.P.; Li, W.; Xiao, Q.Z.; et al. Tobacco transcription factor bHLH123 improves salt tolerance by activating NADPH oxidase NtRbohE expression. Plant Physiol. 2021, 186, 1706–1720. [Google Scholar] [CrossRef]
- Orman-Ligeza, B.; Parizot, B.; de Rycke, R.; Fernandez, A.; Himschoot, E.; Van Breusegem, F.; Bennett, M.J.; Périlleux, C.; Beeckman, T.; Draye, X. RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development 2016, 143, 3328–3339. [Google Scholar] [CrossRef] [Green Version]
- Mangano, S.; Denita-Juarez, S.P.; Choi, H.S.; Marzol, E.; Hwang, Y.; Ranocha, P.; Velasquez, S.M.; Borassi, C.; Barberini, M.L.; Aptekmann, A.A.; et al. Molecular link between auxin and ROS-mediated polar growth. Proc. Natl. Acad. Sci. USA 2017, 114, 5289–5294. [Google Scholar] [CrossRef] [Green Version]
- Jiang, C.; Belfield, E.J.; Cao, Y.; Smith, J.A.; Harberd, N.P. An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell 2013, 25, 3535–3552. [Google Scholar] [CrossRef] [Green Version]
- Arnao, M.B.; Hernández-Ruiz, J. Regulatory role of melatonin in the redox network of plants and plant hormone relationship in stress. In Hormones and Plant Response. Plant in Challenging Environments; Gupta, D.K., Corpas, F.J., Eds.; Springer: Cham, Switzerland, 2021; Volume 2, pp. 235–272. [Google Scholar]
- Chen, J.; Li, H.; Yang, K.; Wang, Y.; Yang, L.; Hu, L.; Liu, R.; Shi, Z. Melatonin facilitates lateral root development by coordinating PAO-derived hydrogen peroxide and Rboh-derived superoxide radical. Free Radic. Biol. Med. 2019, 143, 534–544. [Google Scholar] [CrossRef] [PubMed]
- Bian, L.; Wang, Y.; Bai, H.; Li, H.; Zhang, C.; Chen, J.; Xu, W. Melatonin-ROS signal module regulates plant lateral root development. Plant Signal. Behav. 2021, 16, 1901447. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.; Cao, X.; Wang, X.; Zhang, W.; Li, W.; Wang, X.; Liu, S.; Lyu, D. RBOH-dependent hydrogen peroxide signaling mediates melatonin-induced anthocyanin biosynthesis in red pear fruit. Plant Sci. 2021, 313, 111093. [Google Scholar] [CrossRef] [PubMed]
- Corpas, F.J.; Rodríguez-Ruiz, M.; Muñoz-Vargas, M.A.; González-Gordo, S.; Reiter, R.J.; Palma, J.M. Interactions of melatonin, ROS and NO during fruit ripening: An update and prospective view. J. Exp. Bot. 2022, erac128. [Google Scholar] [CrossRef]
- Wei, J.; Li, D.X.; Zhang, J.R.; Shan, C.; Rengel, Z.; Song, Z.B.; Chen, Q. Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. J. Pineal Res. 2018, 65, e12500. [Google Scholar] [CrossRef]
- Kong, M.; Sheng, T.; Liang, J.; Ali, Q.; Gu, Q.; Wu, H.; Chen, J.; Liu, J.; Gao, X. Melatonin and its homologs induce immune responses via receptors trP47363-trP13076 in Nicotiana benthamiana. Front. Plant Sci. 2021, 12, 691835. [Google Scholar] [CrossRef]
- Wang, L.F.; Li, T.T.; Zhang, Y.; Guo, J.X.; Lu, K.K.; Liu, W.C. CAND2/PMTR1 is required for melatonin-conferred osmotic stress tolerance in Arabidopsis. Int. J. Mol. Sci. 2021, 22, 4014. [Google Scholar] [CrossRef]
- Wang, L.F.; Lu, K.K.; Li, T.T.; Zhang, Y.; Guo, J.X.; Song, R.F.; Liu, W.C. Maize PHYTOMELATONIN RECEPTOR1 functions in plant osmotic and drought stress tolerance. J. Exp. Bot. 2021, erab553. [Google Scholar] [CrossRef]
- Han, Y.; Mhamdi, A.; Chaouch, S.; Noctor, G. Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione. Plant Cell Environ. 2013, 36, 1135–1146. [Google Scholar] [CrossRef]
- Han, Y.; Chaouch, S.; Mhamdi, A.; Queval, G.; Zechmann, B.; Noctor, G. Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signaling. Antioxid. Redox Signal. 2013, 18, 2106–2121. [Google Scholar] [CrossRef] [Green Version]
- Chen, J.; Zhou, H.; Xie, Y. SnRK2.6 phosphorylation/persulfidation: Where ABA and H2S signaling meet. Trends Plant Sci. 2021, 26, 1207–1209. [Google Scholar] [CrossRef] [PubMed]
- Zhou, M.; Zhang, J.; Shen, J.; Zhou, H.; Zhao, D.; Gotor, C.; Romero, L.C.; Fu, L.; Li, Z.; Yang, J.; et al. Hydrogen sulfide-linked persulfidation of ABI4 controls ABA responses through the transactivation of MAPKKK18 in Arabidopsis. Mol. Plant 2021, 14, 921–936. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.S.; Jia, H.L.; Wang, X.F.; Shi, C.; Wang, X.; Ma, P.; Wang, J.; Wang, M.J.; Li, J. Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Mol. Plant 2020, 13, 732–744. [Google Scholar] [CrossRef] [PubMed]
- de Bont, L.; Mu, X.; Wei, B.; Han, Y. Abiotic stress-triggered oxidative challenges: Where does H2S act? J. Genet. Genom. 2022; in press. [Google Scholar] [CrossRef]
- Xu, S.; Chen, T.; Tian, M.; Rahantaniaina, M.S.; Zhang, L.; Wang, R.; Xuan, W.; Han, Y. Genetic manipulation of ROS homeostasis utilizing CRISPR/Cas9-based gene editing in rice. Methods Mol. Biol. 2022; in press. [Google Scholar] [CrossRef]
- Li, S.; Shen, P.; Wang, B.; Mu, X.; Tian, M.; Chen, T.; Han, Y. Modification of chloroplast antioxidant capacity by plastid transformation. Methods Mol. Biol. 2022; in press. [Google Scholar] [CrossRef]
Abiotic Stressors | Impact on Oxidative Stress Markers and Antioxidative Defense Systems (Enzymes and Related Genes) | Plant Species | References |
---|---|---|---|
Salinity stress | H2O2, O2•–, MDA, ·OH, and EL; APX, SOD, CAT, POD, Δ1-pyrroline-5-carboxylate synthetase, ASC, GSH, proline, and total soluble carbohydrates; APX1, APX2, CAT1, FSD1, CuZnSOD, and MnSOD | Arabidopsis, Brassica napus, Malus domestica, olive, tomato, wheat, cucumber, rice, Limonium bicolor | [12,35,36,40,42,47,53,54,55,56,57,58,59] |
Drought stress | H2O2, MDA, O2•–, and EL; APX, SOD, CAT, POD, DHAR, GST, GR, MDHAR, PPO, ASC, DHA, GSH, proline, flavonoid, carotenoid, and phenolic compounds; Cu/ZnSOD, Fe/MnSOD, APX, CAT, GR, POD, GST, DHAR, and MDHAR | maize, tomato, citrus, soybean, kiwifruit, Malus | [14,39,60,61,62,63,64,65] |
Cold stress | H2O2, O2•–, MDA, and EL; APX, SOD, CAT, POD, GR, GSH, ASC, proline, polyamine; APX, CAT, SOD, GR, ZAT10, and ZAT12 | Arabidopsis, watermelon, Camellia sinensis, rice, cucumber, tomato | [15,37,66,67,68,69,70] |
Heat stress | H2O2, O2•–, MDA, and EL; APX, SOD, CAT, POD, GPX, GR, Gly I, Gly II, GSH, ASC, proline, flavonoid, proline, polyamine, and carotenoid; APX, CAT, SOD, POD, HsfA2, and Hsp90 | rice, soybean, maize, Chrysanthemum, Actinidia deliciosa | [38,44,71,72,73,74,75,76,77] |
Heavy metals stress | H2O2, O2•–, MDA, and EL; APX, SOD, CAT, POD, GPX, GR, PAL, ASC, DHA, GSH, proline, flavonoid, anthocyanins APX, CAT, POD, SOD, GR, GSH1, PCS | Tomato,Nicotiana tabacum L., Brassica napus L., rice, maize, wheat, alfalfa, Azolla imbricata, watermelon | [11,19,20,43,78,79,80] |
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Gu, Q.; Xiao, Q.; Chen, Z.; Han, Y. Crosstalk between Melatonin and Reactive Oxygen Species in Plant Abiotic Stress Responses: An Update. Int. J. Mol. Sci. 2022, 23, 5666. https://doi.org/10.3390/ijms23105666
Gu Q, Xiao Q, Chen Z, Han Y. Crosstalk between Melatonin and Reactive Oxygen Species in Plant Abiotic Stress Responses: An Update. International Journal of Molecular Sciences. 2022; 23(10):5666. https://doi.org/10.3390/ijms23105666
Chicago/Turabian StyleGu, Quan, Qingqing Xiao, Ziping Chen, and Yi Han. 2022. "Crosstalk between Melatonin and Reactive Oxygen Species in Plant Abiotic Stress Responses: An Update" International Journal of Molecular Sciences 23, no. 10: 5666. https://doi.org/10.3390/ijms23105666