Mechanisms by Which Exogenous Substances Enhance Plant Salt Tolerance through the Modulation of Ion Membrane Transport and Reactive Oxygen Species Metabolism
Abstract
:1. Introduction
2. Role of Exogenous Substances in Plant Salt Tolerance Research
2.1. Plant Hormones
2.1.1. ABA
2.1.2. MT
2.1.3. SA
2.1.4. JA
2.2. Signal Transduction Substances
2.2.1. Ca2+
2.2.2. GABA
2.3. Relationships between Exogenous Substance Application and Improvements in Salt Tolerance, Yield, and Quality
3. Role of Ion Transporters in Salt Stress Research
- (1)
- Na+ Membrane Transporters
- (2)
- K+ Membrane Transporters
- (3)
- Ca2+ transporters
- (4)
- Chloride Ion Transporters
4. Regulation of Ion Transport and Reactive Oxygen Species by Exogenous Substances
4.1. Plant Hormones Affecting Ion Transporters Involved in Regulating Reactive Oxygen Species Metabolism
4.1.1. Regulation of Ion Transport and Reactive Oxygen Species by ABA
4.1.2. Regulation of Ion Transport and Reactive Oxygen Species by MT
4.1.3. Regulation of Ion Transport and Reactive Oxygen Species by JA
4.1.4. Regulation of Ion Transport and Reactive Oxygen Species by Other Substances
4.2. Signaling Molecules Affecting Ion Transporters Involved in Regulating Reactive Oxygen Species Metabolism
4.2.1. Regulation of Ion Transport and Reactive Oxygen Species by Ca2+
4.2.2. Regulation of Ion Transport and Reactive Oxygen Species by GABA
Name | Species | Description | Family |
---|---|---|---|
NbPIP2;2 [109] | N. benthamiana | H2O2 transporter protein that guides extracellular H2O2 through the plasma membrane into cells and regulates plant immunity and ROS accumulation. | AQP |
AtPMTR1 [110] | Arabidopsis | Interacts with GPA 1, activates NADPH oxidase to produce H2O2, and promotes Ca2+ influx and K+ efflux to regulate stomatal motility. | GPCR |
NPR1 [111] | Arabidopsis | Accumulation of the SA receptor NPR 1 under salt stress reduces the accumulation of ROS in chloroplasts. | TF |
CsWAKL08 [112] | Citrus reticulata Blanco | SA- and JA-induced CsWAKL08 regulates plant resistance to pathogens by regulating ROS production and signaling. | RLK |
OsPM1 [113] | Oryza sativa L. | OsPM 1 serves as an ABA influx carrier to promote exogenous ABA introduction into cells and play a role in the response to drought stress and oxidative stress. | AWPM-19 |
CRK2 [114] | Arabidopsis | The reciprocal regulation of CRK2 and RBOHD regulates ROS generation, stomatal movement, Ca2+ influx, and MAPK activation, which are important elements involved in immunity. | RLK |
SOS1 [115] | Arabidopsis | ROS acts as a signaling molecule to mediate SOS1 mRNA stability under salt stress, and SOS1 plays a key role in the regulation of NADPH oxidase activity and ROS generation. | NHX |
5. Conclusions and Perspectives
Author Contributions
Funding
Conflicts of Interest
References
- FAO. The State of the World’s Land and Water Resources for Food and Agriculture (SOLAW)—Managing Systems at Risk; Food and Agriculture Organization of the United Nations and Earthscan: Geneva, Switzerland, 2011. [Google Scholar]
- Kesawat, M.S.; Satheesh, N.; Kherawat, B.S.; Kumar, A.; Kim, H.U.; Chung, S.M.; Kumar, M. Regulation of Reactive Oxygen Species during Salt Stress in Plants and Their Crosstalk with Other Signaling Molecules-Current Perspectives and Future Directions. Plants 2023, 12, 864. [Google Scholar] [CrossRef] [PubMed]
- Niu, J.; Chen, Z.; Guo, Z.; Xu, N.; Sui, X.; Roy, M.; Kareem, H.A.; Hassan, M.U.; Cui, J.; Wang, Q. Exogenous melatonin promotes the growth of alfalfa (Medicago sativa L.) under NaCl stress through multiple pathways. Ecotoxicol. Environ. Saf. 2022, 242, 113938. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Ji, P.; Yang, H.; Liu, X.; Ji, P.; Yang, H.; Jiang, C.; Liang, Z.; Chen, Q.; Lu, F.; et al. Priming effect of exogenous ABA on heat stress tolerance in rice seedlings is associated with the upregulation of antioxidative defense capability and heat shock-related genes. Plant Growth Regul. 2021, 98, 23–38. [Google Scholar] [CrossRef]
- Aleman, F.; Yazaki, J.; Lee, M.; Takahashi, Y.; Kim, A.Y.; Li, Z.; Kinoshita, T.; Ecker, J.R.; Schroeder, J.I. An ABA-increased interaction of the PYL6 ABA receptor with MYC2 Transcription Factor: A putative link of ABA and JA signaling. Sci. Rep. 2016, 6, 28941. [Google Scholar] [CrossRef] [PubMed]
- Wang, J. ABA and JA responses to salt stress in plants. Bioprocess 2023, 13, 33–38. [Google Scholar] [CrossRef]
- Zhao, D.; Wang, H.; Chen, S.; Yu, D.; Reiter, R.J. Phytomelatonin: An Emerging Regulator of Plant Biotic Stress Resistance. Trends Plant Sci. 2021, 26, 70–82. [Google Scholar] [CrossRef]
- Wang, M.; Wang, Y.; Zhang, Y.; Li, C.; Gong, S.; Yan, S.; Li, G.; Hu, G.; Ren, H.; Yang, J.; et al. Comparative transcriptome analysis of salt-sensitive and salt-tolerant maize reveals potential mechanisms to enhance salt resistance. Genes Genom. 2019, 41, 781–801. [Google Scholar] [CrossRef]
- Xu, X.; Sun, Y.; Sun, B.; Zhang, J.; Guo, X. Effects of exogenous melatonin on active oxygen metabolism of cucumber seedlings under high temperature stress. Chin. J. Appl. Ecol. 2010, 21, 1295–1300. [Google Scholar]
- Jiang, D.; Lu, B.; Liu, L.; Duan, W.; Meng, Y.; Li, J.; Zhang, K.; Sun, H.; Zhang, Y.; Dong, H.; et al. Exogenous melatonin improves the salt tolerance of cotton by removing active oxygen and protecting photosynthetic organs. BMC Plant Biol. 2021, 21, 331. [Google Scholar] [CrossRef]
- Ren, W.; Chen, L.; Xie, Z.; Peng, X. Combined transcriptome and metabolome analysis revealed pathways involved in improved salt tolerance of Gossypium hirsutum L. seedlings in response to exogenous melatonin application. BMC Plant Biol. 2022, 22, 552. [Google Scholar] [CrossRef]
- Wei, L.; Zhao, H.; Wang, B.; Wu, X.; Lan, R.; Huang, X.; Chen, B.; Chen, G.; Jiang, C.; Wang, J.; et al. Exogenous melatonin confers enhanced salinity tolerance in rice by blocking the ROS burst and improving Na+/K+ homeostasis. Environ. Exp. Bot. 2021, 189, 104530. [Google Scholar]
- Ma, C.; Cao, Y.; Shang, Y.; Yin, B.; Du, P.; Zhou, S.; Li, Z.; Xu, J.; Zhang, X.; Liang, B. Melatonin enhances the tolerance of apple seedlings to salt stress by regulating the microbial community structure and metabolite composition of the rhizosphere. Plant Soil 2023, 497, 467–481. [Google Scholar] [CrossRef]
- Talaat, N.B.; Todorova, D. Antioxidant Machinery and Glyoxalase System Regulation Confers Salt Stress Tolerance to Wheat (Triticum aestivum L.) Plants Treated with Melatonin and Salicylic Acid. J. Soil Sci. Plant Nutr. 2022, 22, 3527–3540. [Google Scholar] [CrossRef]
- Usman, S.; Yaseen, G.; Noreen, Z.; Rizwan, M.; Noor, H.; Elansary, H.O. Melatonin and arginine combined supplementation alleviate salt stress through physiochemical adjustments and improved antioxidant enzymes activity in Capsicum annuum L. Sci. Hortic. 2023, 321, 112270. [Google Scholar] [CrossRef]
- Yin, Z.; Lu, J.; Meng, S.; Liu, Y.; Mostafa, I.; Qi, M.; Li, T. Exogenous melatonin improves salt tolerance in tomato by regulating photosynthetic electron flux and the ascorbate–glutathione cycle. J. Plant Interact. 2019, 14, 453–463. [Google Scholar] [CrossRef]
- Huang, X.; Tanveer, M.; Min, Y.; Shabala, S. Melatonin as a regulator of plant ionic homeostasis: Implications for abiotic stress tolerance. J. Exp. Bot. 2022, 73, 5886–5902. [Google Scholar] [CrossRef] [PubMed]
- Yu, L.; Liu, Y.; Zhu, F.; Geng, X.; Yang, Y.; He, Z.; Xu, F. The enhancement of salt stress tolerance by salicylic acid pretreatment in Arabidopsis thaliana. Biol. Plant. 2020, 64, 150–158. [Google Scholar] [CrossRef]
- Pai, R.; Sharma, P.K. Exogenous supplementation of salicylic acid ameliorates salt-induced membrane leakage, ion homeostasis and oxidative damage in Sorghum seedlings. Biologia 2024, 79, 23–43. [Google Scholar] [CrossRef]
- Bukhat, S.; Manzoor, H.; Athar, H.R.; Zafar, Z.U.; Azeem, F.; Rasul, S. Salicylic Acid Induced Photosynthetic Adaptability of Raphanus sativus to Salt Stress is Associated with Antioxidant Capacity. J. Plant Growth Regul. 2020, 39, 809–822. [Google Scholar] [CrossRef]
- Yu, Z.; Duan, X.; Luo, L.; Dai, S.; Ding, Z.; Xia, G. How Plant Hormones Mediate Salt Stress Responses. Trends Plant Sci. 2020, 25, 1117–1130. [Google Scholar] [CrossRef]
- Wang, Y.; Mostafa, S.; Zeng, W.; Jin, B. Function and mechanism of jasmonic acid in plant responses to abiotic and biotic stresses. Int. J. Mol. Sci 2021, 22, 8568. [Google Scholar] [CrossRef] [PubMed]
- Mir, M.A.; Sirhindi, G.; Alyemeni, M.N.; Alam, P.; Ahmad, P. Jasmonic Acid Improves Growth Performance of Soybean Under Nickel Toxicity by Regulating Nickel Uptake, Redox Balance, and Oxidative Stress Metabolism. J. Plant Growth Regul. 2018, 37, 1195–1209. [Google Scholar] [CrossRef]
- Esmaielzadeh, S.; Fallah, H.; Niknejad, Y.; Mahmoudi, M.; Tari, D.B. Methyl jasmonate increases aluminum tolerance in rice by augmenting the antioxidant defense system, maintaining ion homeostasis, and increasing nonprotein thiol compounds. Environ. Sci. Pollut. R. 2022, 29, 46708–46720. [Google Scholar] [CrossRef] [PubMed]
- Sheteiwy, M.S.; Ulhassan, Z.; Qi, W.; Lu, H.; AbdElgawad, H.; Minkina, T.; Sushkova, S.; Rajput, V.D.; El-Keblawy, A.; Jośko, I.; et al. Association of jasmonic acid priming with multiple defense mechanisms in wheat plants under high salt stress. Front. Plant Sci. 2022, 13, 886862. [Google Scholar] [CrossRef] [PubMed]
- Bali, S.; Kaur, P.; Jamwal, V.L.; Gandhi, S.G.; Sharma, A.; Ohri, P.; Bhardwaj, R.; Ali, M.A.; Ahmad, P. Seed Priming with Jasmonic Acid Counteracts Root Knot Nematode Infection in Tomato by Modulating the Activity and Expression of Antioxidative Enzymes. Biomolecules 2020, 10, 98. [Google Scholar] [CrossRef]
- El Nahhas, N.; AlKahtani, M.D.F.; Abdelaal, K.A.A.; Al Husnain, L.; AlGwaiz, H.I.M.; Hafez, Y.M.; Attia, K.A.; El-Esawi, M.A.; Ibrahim, M.F.M.; Elkelish, A. Biochar and jasmonic acid application attenuates antioxidative systems and improves growth, physiology, nutrient uptake and productivity of faba bean (Vicia faba L.) irrigated with saline water. Plant Physiol. Biochem. 2021, 166, 807–817. [Google Scholar] [CrossRef]
- Hou, J.; Riaz, M.; Yan, L.; Lu, K.; Jiang, C. Effect of exogenous l-aspartate nano-calcium on root growth, calcium forms and cell wall metabolism of Brassica napus L. NanoImpact 2022, 27, 100415. [Google Scholar] [CrossRef]
- Zhang, X.; Bian, A.; Li, T.; Ren, L.; Li, L.; Su, Y.; Zhang, Q. ROS and calcium oscillations are required for polarized root hair growth. Plant Signal. Behav. 2022, 17, 2106410. [Google Scholar] [CrossRef]
- Rui, Z.; Huali, X.; Min, S.A.; Yang, B.; Naderi, M.; Yuanyuan, Z.; Haitao, L.; Prusky, D.; Xiaoyan, C. Mechanism of Ca2+-mediated NOX modulated in ROS metabolism induced by T-2 toxin in potato tuber. Food Chem. 2020, 317, 126416. [Google Scholar] [CrossRef]
- Li, G.; Meng, X.; Cai, J.; Dong, T.; Li, Z.; Zhu, M. Progress on the function of reactive oxygen species in plant abiotic stress response. J. Plant Physiol. 2018, 54, 951–959. [Google Scholar]
- Gao, M.; He, Y.; Yin, X.; Zhong, X.; Yan, B.; Wu, Y.; Chen, J.; Li, X.; Zhai, K.; Huang, Y.; et al. Ca2+ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector. Cell 2021, 184, 5391–5404.e17. [Google Scholar] [CrossRef] [PubMed]
- Meyer, A.; Eskandari, S.; Grallath, S.; Rentsch, D. AtGAT 1, a high affinity transporter for γ-aminobutyric acid in Arabidopsis thaliana. J. Biol. Chem. 2006, 281, 7197–7204. [Google Scholar] [CrossRef] [PubMed]
- Ansari, M.I.; Jalil, S.U.; Ansari, S.A.; Hasanuzzaman, M. GABA shunt: A key-player in mitigation of ROS during stress. Plant Growth Regul. 2021, 94, 131–149. [Google Scholar] [CrossRef]
- Kalhor, M.S.; Aliniaeifard, S.; Seif, M.; Asayesh, E.J.; Bernard, F.; Hassani, B.; Li, T. Title: Enhanced salt tolerance and photosynthetic performance: Implication of ɤ-amino butyric acid application in salt-exposed lettuce (Lactuca sativa L.) plants. Plant Physiol. Biochem. 2018, 130, 157–172. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Guo, S.; Yang, X.; Meng, Q.; Wei, X. Exogenous gamma-aminobutyric acid increases salt tolerance of wheat by improving photosynthesis and enhancing activities of antioxidant enzymes. Biol. Plant. 2016, 60, 123–131. [Google Scholar] [CrossRef]
- Wang, Y.; Gu, W.; Meng, Y.; Xie, T.; Li, L.; Li, J.; Wei, S. γ-Aminobutyric Acid Imparts Partial Protection from Salt Stress Injury to Maize Seedlings by Improving Photosynthesis and Upregulating Osmoprotectants and Antioxidants. Sci. Rep. 2017, 7, 43609. [Google Scholar] [CrossRef]
- Hu, W.; Wan, H.; He, J.; Li, J.; Yang, W.; Xiao, C.; Lei, J.; Yang, J.; Yang, Y. Effect of salt stress and exogenous substances on germination and growth physiology of synthetic wheat. J. Sichuan Agric. Univ. 2023, 41, 1065–1070+1078. [Google Scholar]
- Jia, Y.; Yang, L.; Zou, D.; Qu, Z.; Wang, J.; Liu, H.; Wang, J.; Zhao, H. Effect of exogenous material application under cold water stress on nitrogen photosynthesis efficiency and yield in cold japonica rice. Rice Sci. 2020, 34, 443–456. [Google Scholar]
- Dong, Y.; Chen, W.; He, M. Effect of slow-release exogenous nitric oxide (NO) and slow-release salicylic acid (SA) on the physiological characteristics of winter wheat under salt stress. Soil Bull. 2018, 49, 623–629. [Google Scholar]
- Guo, J.; Huang, Y.; Yang, X.; Bu, W.; Tian, J.; Zhang, M.; Huang, K.; Luo, X.; Ye, Y.; Xing, W.; et al. Effects of Three Exogenous Substances on Heat Tolerance of Peony Seedlings. Horticulturae 2023, 9, 765. [Google Scholar] [CrossRef]
- Tong, Q.; Liu, L.; Zhao, Y.; Kong, J.; Wang, Y.; Xu, X.; Hilbert, G.; Gomès, E.; Dai, Z. Transcriptome Remodeling in Response to Leaf Removal and Exogenous Abscisic Acid in Berries of Grapevine (Vitis vinifera L.) Fruit Cuttings. Horticulturae 2022, 8, 905. [Google Scholar] [CrossRef]
- Rathod, K.D.; Ahlawat, T.R.; Kumar, S.; Sarkar, M.; Chakraborty, B. Effect of Plant Growth Regulators on Growth, Yield and Quality of Strawberry (Fragaria × ananassa Duch.) Cv. Winter Dawn under Open Field Conditions of South Gujarat. Agric. Sci. Digest. 2020, 41, 323–333. [Google Scholar] [CrossRef]
- Nazir, N.; Sharma, M.; Khalil, A. Effect of exogenous application of plant growth regulators on vine growth, yield and quality attributes in kiwifruit cv. Hayward. Indian J. Hortic. 2018, 75, 153–156. [Google Scholar] [CrossRef]
- Xu, N.; Cao, N.; Guo, B.; Li, G.; Xu, Y.; Wang, C. Effects of exogenous melatonin on grape yield, quality, and microecology of the root region. Jiangsu Agric. Sci. 2024, 52, 160–165. [Google Scholar]
- Niazi, Z.; Razavi, F.; Khademi, O.; Aghdam, M. Exogenous application of hydrogen sulfide and γ-aminobutyric acid alleviates chilling injury and preserves quality of persimmon fruit (Diospyros kaki, cv. Karaj) during cold storage. Sci. Hortic. 2021, 285, 110198. [Google Scholar] [CrossRef]
- Malakar, P.; Chattopadhyay, D. Adaptation of plants to salt stress: The role of the ion transporters. J. Plant Biochem. Biotechnol. 2021, 30, 668–683. [Google Scholar] [CrossRef]
- Wang, J.; Luo, Y.; Ye, F.; Ding, Z.J.; Zheng, S.J.; Qiao, S.; Wang, Y.; Guo, J.; Yang, W.; Su, N. Structures and ion transport mechanisms of plant high-affinity potassium transporters. Mol. Plant 2024, 17, 409–422. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Sun, X.; Li, Y.; Luo, X.; Song, S.; Chen, Y.; Wang, X.; Mao, D.; Chen, L.; Luan, S. Rice Na+-Permeable Transporter OsHAK12 Mediates Shoots Na+ Exclusion in Response to Salt Stress. Front. Plant Sci. 2021, 12, 771746. [Google Scholar] [CrossRef] [PubMed]
- Saddhe, A.A.; Mishra, A.K.; Kumar, K. Molecular insights into the role of plant transporters in salt stress response. Physiol. Plant. 2021, 173, 1481–1494. [Google Scholar] [CrossRef]
- Wang, L. Progress in endosomal Na+, K+/H+ antiporter in Arabidopsis thaliana. Chin. J. Biotechnol. 2019, 35, 1424–1432. [Google Scholar]
- Liu, X.; Cai, S.; Wang, G.; Wang, F.; Dong, F.; Mak, M.; Holford, P.; Ji, J.; Salih, A.; Zhou, M.; et al. Halophytic NHXs confer salt tolerance by altering cytosolic and vacuolar K+ and Na+ in Arabidopsis root cell. Plant Growth Regul. 2017, 82, 333–351. [Google Scholar] [CrossRef]
- Assaha, D.V.M.; Ueda, A.; Saneoka, H.; Al-Yahyai, R.; Yaish, M.W. The Role of Na+ and K+ Transporters in Salt Stress Adaptation in Glycophytes. Front. Physiol. 2017, 8, 509. [Google Scholar] [CrossRef] [PubMed]
- Yao, F.Y.; Qi, G.N.; Ren, H.M.; Zhang, A.; Hussain, J.; Wang, Y.F. S-type anion channel SLAC1’s homologues inhibit inward potassium channels AKT2 and KAT2 in Arabidopsis. Sci. Bull. 2017, 62, 464–466. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Yang, F.; Sun, D.; Zhang, Y.; Zhang, M.; Liu, S.; Zhou, P.; Shi, C.; Zhang, L.; Tian, C. Cryo-EM structure of the hyperpolarization-activated inwardly rectifying potassium channel KAT1 from Arabidopsis. Cell Rrs. 2020, 30, 1049–1052. [Google Scholar] [CrossRef]
- Horie, T.; Sugawara, M.; Okada, T.; Taira, K.; Kaothien-Nakayama, P.; Katsuhara, M.; Shinmyō, A.; Nakayama, H. Rice sodium-insensitive potassium transporter, OsHAK5, confers increased salt tolerance in tobacco BY2 cells. J. Biosci. Bioeng. 2011, 111, 346–356. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Shen, L.; Shen, Z.; Jing, W.; Ge, H.; Zhao, J.; Zhang, W. The potassium transporter OsHAK21 functions in the maintenance of ion homeostasis and tolerance to salt stress in rice. Plant Cell Environ. 2015, 38, 2766–2779. [Google Scholar] [CrossRef] [PubMed]
- Zheng, S. Biological Function Studies of the AtKEA Gene Family of K+/H+ Reverse Transporters in Arabidopsis thaliana. Ph.D. Thesis, Lanzhou University, Lanzhou, China, 2014. [Google Scholar]
- Zhu, X.; Pan, T.; Zhang, X.; Fan, L.; Quintero, F.J.; Zhao, H.; Su, X.; Li, X.; Villalta, I.; Mendoza, I.; et al. K+ efflux antiporters 4, 5, and 6 mediate pH and K+ homeostasis in endomembrane compartments. Plant Physiol. 2018, 178, 1657–1678. [Google Scholar] [CrossRef] [PubMed]
- Shao, Q.; Ding, T.; Han, N.; Wang, B. High-affinity K+ transport carrier (HKT) and plant salt resistance. Plant Physiol. Commun. 2006, 32, 175–181. [Google Scholar]
- Ali, A.; Maggio, A.; Bressan, R.; Yun, D.J. Role and functional differences of HKT1-type transporters in plants under salt stress. Int. J. Mol. Sci. 2019, 20, 1059. [Google Scholar] [CrossRef]
- Tada, Y.; Ohnuma, A. Comparative Functional Analysis of Class II Potassium Transporters, SvHKT2;1, SvHKT2;2, and HvHKT2;1, on Ionic Transport and Salt Tolerance in Transgenic Arabidopsis. Plants 2020, 9, 786. [Google Scholar] [CrossRef]
- Wang, C.; Tang, R.J.; Kou, S.; Xu, X.; Lu, Y.; Rauscher, K.; Voelker, A.; Luan, S. Mechanisms of calcium homeostasis orchestrate plant growth and immunity. Nature 2024, 627, 382–388. [Google Scholar] [CrossRef] [PubMed]
- Zhai, Y.; Wen, Z.; Han, Y.; Zhuo, W.; Wang, F.; Xi, C.; Liu, J.; Gao, P.; Zhao, H.; Wang, Y.; et al. Heterogeneous expression of plasma-membrane-localised OsOSCA1.4 complements osmotic sensing based on hyperosmolality and salt stress in Arabidopsis osca1 mutant. Cell Calcium. 2020, 91, 102261. [Google Scholar] [CrossRef] [PubMed]
- Shan, F.; Wu, Y.; Du, R.; Yang, Q.; Liu, C.; Wang, Y.; Zhang, C.; Chen, Y. Evolutionary analysis of the OSCA gene family in sunflower (Helianthus annuus L) and expression analysis under NaCl stress. PeerJ 2023, 11, e15089. [Google Scholar] [CrossRef]
- Wang, P.H.; Lee, C.E.; Lin, Y.S.; Lee, M.H.; Chen, P.Y.; Chang, H.C.; Chang, I.F. The Glutamate Receptor-Like Protein GLR3.7 Interacts With 14-3-3ω and Participates in Salt Stress Response in Arabidopsis thaliana. Front. Plant Sci. 2019, 10, 1169. [Google Scholar] [CrossRef]
- Duarte-Delgado, D.; Dadshani, S.; Schoof, H.; Oyiga, B.C.; Schneider, M.; Mathew, B.; Léon, J.; Ballvora, A. Transcriptome profiling at osmotic and ionic phases of salt stress response in bread wheat uncovers trait-specific candidate genes. BMC Plant Biol. 2020, 20, 428. [Google Scholar] [CrossRef] [PubMed]
- Wang, P.; Li, Z.; Wei, J.; Zhao, Z.; Sun, D.; Cui, S. A Na+/Ca2+ Exchanger-like Protein (AtNCL) Involved in Salt Stress in Arabidopsis*. J. Biol. Chem. 2012, 287, 44062–44070. [Google Scholar] [CrossRef] [PubMed]
- Yamada, N.; Theerawitaya, C.; Cha-um, S.; Kirdmanee, C.; Takabe, T. Expression and functional analysis of putative vacuolar Ca2+-transporters (CAXs and ACAs) in roots of salt tolerant and sensitive rice cultivars. Protoplasma 2014, 251, 1067–1075. [Google Scholar] [CrossRef]
- Zhou, Y.; Xu, K.; Gao, H.; Yao, W.; Zhang, Y.; Zhang, Y.; Azhar Hussain, M.; Wang, F.; Yang, X.; Li, H. Comparative Proteomic Analysis of Two Wild Soybean (Glycine soja) Genotypes Reveals Positive Regulation of Saline-Alkaline Stress Tolerance by Tonoplast Transporters. J. Agric. Food Chem. 2023, 71, 14109–14124. [Google Scholar] [CrossRef]
- Nguyen, C.T.; Agorio, A.; Jossier, M.; Depré, S.; Thomine, S.; Filleur, S. Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol. 2016, 57, 764–775. [Google Scholar] [CrossRef]
- Nedelyaeva, O.I.; Shuvalov, A.V.; Balnokin, Y.V. Chloride Channels and Transporters of the CLC Family in Plants. Russ. J. Plant Physiol. 2020, 67, 767–784. [Google Scholar] [CrossRef]
- Liu, W.; Feng, J.; Ma, W.; Zhou, Y.; Ma, Z. GhCLCg-1, a Vacuolar Chloride Channel, Contributes to Salt Tolerance by Regulating Ion Accumulation in Upland Cotton. Front. Plant Sci. 2021, 12, 765173. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Balasubramaniam, T.; Wijewardene, I.; Hu, R.; Shen, G. Co-Overexpression of Avp1, Pp2a-C5, and Atclcc in Arabidopsis thaliana Greatly Increases Tolerance to Salt and Drought Stresses. SSRN Electron. J. 2022, 67, 767–784. [Google Scholar] [CrossRef]
- Banik, S.; Dutta, D. Membrane Proteins in Plant Salinity Stress Perception, Sensing, and Response. J. Membr. Biol. 2023, 256, 109–124. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Liu, S.; Zhang, Q.; Cui, M.; Zhao, M.; Li, N.; Wang, S.; Wu, R.; Zhang, L.; Cao, Y.; et al. The interaction of ABA and ROS in plant growth and stress resistances. Front. Plant Sci. 2022, 13, 1050132. [Google Scholar] [CrossRef] [PubMed]
- Kandhol, N.; Singh, V.P.; Wang, Y.; Chen, Z.; Tripathi, D.K. Ca2+ sensor-mediated ROS homeostasis: Defense without yield penalty. Trends Plant Sci. 2022, 27, 834–836. [Google Scholar] [CrossRef] [PubMed]
- Hong, Y.; Wang, Z.; Liu, X.; Yao, J.; Kong, X.; Shi, H.; Zhu, J.K. Two Chloroplast Proteins Negatively Regulate Plant Drought Resistance Through Separate Pathways. Plant Physiol. 2020, 182, 1007–1021. [Google Scholar] [CrossRef]
- Yu, Y.; Wang, J.; Li, S.; Kakan, X.; Zhou, Y.; Miao, Y.; Wang, F.; Qin, H.; Huang, R. Ascorbic Acid Integrates the Antagonistic Modulation of Ethylene and Abscisic Acid in the Accumulation of Reactive Oxygen Species. Plant Physiol. 2019, 179, 1861–1875. [Google Scholar] [CrossRef]
- Kim, J.H.; Lim, S.D.; Jung, K.H.; Jang, C.S. Overexpression of a C3HC4-type E3-ubiquitin ligase contributes to salinity tolerance by modulating Na+ homeostasis in rice. Physiol. Plant. 2023, 175, e14075. [Google Scholar] [CrossRef]
- Siddiqui, M.H.; Khan, M.N.; Mukherjee, S.; Basahi, R.A.; Alamri, S.; Al-Amri, A.A.; Alsubaie, Q.D.; Ali, H.M.; Al-Munqedhi, B.M.A.; Almohisen, I.A.A. 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]
- Yu, Y.; Wang, A.; Li, X.; Kou, M.; Wang, W.; Chen, X.; Xu, T.; Zhu, M.; Ma, D.; Li, Z.; et al. Melatonin-Stimulated Triacylglycerol Breakdown and Energy Turnover under Salinity Stress Contributes to the Maintenance of Plasma Membrane H+-ATPase Activity and K+/Na+ Homeostasis in Sweet Potato. Front. Plant Sci. 2018, 9, 256. [Google Scholar] [CrossRef]
- Kumar, S.; Liu, Y.; Wang, M.; Khan, M.N.; Wang, S.; Li, Y.; Chen, Y.; Zhu, G. Alleviating sweetpotato salt tolerance through exogenous glutathione and melatonin: A profound mechanism for active oxygen detoxification and preservation of photosynthetic organs. Chemosphere 2024, 350, 141120. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Lv, P.; Yan, D.; Zhang, Z.; Xu, X.; Wang, T.; Wang, Y.; Peng, Z.; Yu, C.; Gao, Y.; et al. Exogenous Melatonin Improves Seed Germination of Wheat (Triticum aestivum L.) under Salt Stress. Int. J. Mol. Sci. 2022, 23, 8436. [Google Scholar] [CrossRef] [PubMed]
- Xue, Y.; Wang, W.; Fu, J. Molecular Mechanism Research Progress of Melatonin-Mediated Abiotic/Biotic Stress Response in Plant. J. Integr. Agric. 2019, 9, 323–330. [Google Scholar]
- Gong, B.; Yan, Y.; Wen, D.; Shi, Q. Hy-drogen 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]
- Lee, H.Y.; Back, K. Melatonin Is Required for H2O2- and NO-Mediated Defense Signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana. J Pineal Res. 2017, 62, e12379. [Google Scholar] [CrossRef]
- Sood, M. Jasmonates: “The Master Switch” for Regulation of Developmental and Stress Responses in Plants. J Plant Growth Regul. 2023, 42, 5247–5265. [Google Scholar] [CrossRef]
- Liu, Q.; Li, M.; Guo, J. Regulation of Jasmonic Acid Biosynthesis and Jasmonic Acid Signaling Pathway. Plant Physiol. J. 2012, 48, 837–844. [Google Scholar]
- Li, M.; Yu, G.; Cao, C.; Liu, P. Metabolism, signaling, and transport of jasmonates. Plant Commun. 2021, 2, 100231. [Google Scholar] [CrossRef]
- Maruta, T.; Inoue, T.; Tamoi, M.; Yabuta, Y.; Yoshimura, K.; Ishikawa, T.; Shigeoka, S. Arabidopsis NADPH oxidases, AtrbohD and AtrbohF, are essential for jasmonic acid-induced expression of genes regulated by MYC2 transcription factor. Plant Sci. 2011, 180, 655–660. [Google Scholar] [CrossRef]
- Zhang, L.; Zou, C.; Zhu, T.; Du, M.; Zuo, X.; He, Y.; Chen, S.; Long, Q. The role of jasmonic acid in stress resistance of plants: A review. Chin. J. Biotechnol. 2024, 40, 15–34. [Google Scholar]
- Zeng, P.; Xie, T.; Shen, J.; Liang, T.; Yin, L.; Liu, K.; He, Y.; Chen, M.; Tang, H.; Chen, S.; et al. Potassium transporter OsHAK9 regulates seed germination under salt stress by preventing gibberellin degradation through mediating OsGA2ox7 in rice. J. Integr. Plant Biol. 2024, 66, 731–748. [Google Scholar] [CrossRef] [PubMed]
- Jayakannan, M.; Bose, J.; Babourina, O.; Shabala, S.; Massart, A.; Poschenrieder, C.; Rengel, Z. The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J. Exp. Bot. 2015, 66, 1865–1875. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Huang, R. Progress in ethylene in regulating salt tolerance in plants. J. Plant Physiol. 2015, 51, 1567–1572. [Google Scholar]
- Zhang, M.; Smith, J.A.; Harberd, N.P.; Jiang, C. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol. Biol. 2016, 91, 651–659. [Google Scholar] [CrossRef]
- Wu, Z.; Wu, S.; Wang, Y.; Zheng, L. Progress on calcium-dependent protein kinase (CDPK) in plants. J. Grass Ind. 2018, 163, 204–214. [Google Scholar]
- Zhang, Y.; Wang, Z.; Liu, Y.; Zhang, T.; Liu, J.; You, Z.; Huang, P.; Zhang, Z.; Wang, C. Plasma membrane-associated calcium signaling modulates cadmium transport. New Phytol. 2023, 238, 313–331. [Google Scholar] [CrossRef] [PubMed]
- Atif, R.M.; Shahid, L.; Waqas, M.; Ali, B.; Rashid, M.A.R.; Azeem, F.; Nawaz, M.A.; Wani, S.H.; Chung, G. Insights on Calcium-Dependent Protein Kinases (CPKs) Signaling for Abiotic Stress Tolerance in Plants. Int. J. Mol. Sci. 2019, 20, 5298. [Google Scholar] [CrossRef]
- Cheng, J.; Zhang, S.; Yi, Y.; Qin, Y.; Chen, Z.H.; Deng, F.; Zeng, F. Hydrogen peroxide reduces root cadmium uptake but facilitates root-to-shoot cadmium translocation in rice through modulating cadmium transporters. Plant Physiol. Biochem. 2023, 200, 107754. [Google Scholar] [CrossRef]
- Wu, F.; Chi, Y.; Jiang, Z.; Xu, Y.; Xie, L.; Huang, F.; Wan, D.; Ni, J.; Yuan, F.; Wu, X.; et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 2022, 578, 577–581. [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]
- Yuan, D.; Wu, X.; Jiang, X.; Gong, B.; Gao, H. Types of Membrane Transporters and the Mechanisms of Interaction between Them and Reactive Oxygen Species in Plants. Antioxidants 2024, 13, 221. [Google Scholar] [CrossRef]
- Ramesh, S.A.; Kamran, M.; Sullivan, W.; Chirkova, L.; Okamoto, M.; Degryse, F.; McLaughlin, M.; Gilliham, M.; Tyerman, S.D. Aluminum-Activated Malate Transporters Can Facilitate GABA Transport. Plant Cell 2019, 30, 1147–1164. [Google Scholar] [CrossRef] [PubMed]
- Song, H.; Xu, X.; Wang, H.; Wang, H.; Tao, Y. Exogenous gamma-aminobutyric acid alleviates oxidative damage caused by aluminium and proton stresses on barley seedlings. J. Sci. Food Agric. 2010, 90, 1410–1416. [Google Scholar] [CrossRef]
- Cao, Y.; Chen, Y.; Cheng, N.; Zhang, K.; Duan, Y.; Fang, S.; Shen, Q.; Yang, X.; Fang, W.; Zhu, X. CsCuAO1 Associated with CsAMADH1 Confers Drought Tolerance by Modulating GABA Levels in Tea Plants. Int. J. Mol. Sci. 2024, 25, 992. [Google Scholar] [CrossRef]
- Michaeli, S.; Fait, A.; Lagor, K.; Nunes-Nesi, A.; Grillich, N.; Yellin, A.; Bar, D.; Khan, M.; Fernie, A.R.; Turano, F.J.; et al. A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. Plant J. 2011, 67, 485–498. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.H.; Xu, Z.J.; Peng, J.S.; Zhao, J.; Zhang, G.B.; Xie, J.; Yi, Z.X.; Zhang, J.H.; Gong, J.M.; Ye, N.H.; et al. OsProT1 and OsProT3 Function to Mediate Proline- and γ-aminobutyric acid-specific Transport in Yeast and are Differentially Expressed in Rice (Oryza sativa L.). Rice 2019, 12, 79. [Google Scholar] [CrossRef]
- Ai, G.; Xia, Q.; Song, T.; Li, T.; Zhu, H.; Peng, H.; Liu, J.; Fu, X.; Zhang, M.; Jing, M.; et al. A Phytophthora sojae CRN effector mediates phosphorylation and degradation of plant aquaporin proteins to suppress host immune signaling. PLoS Pathog. 2021, 17, e1009388. [Google Scholar] [CrossRef] [PubMed]
- Yang, Q.; Peng, Z.; Ma, W.; Zhang, S.; Hou, S.; Wei, J.; Dong, S.; Yu, X.; Song, Y.; Gao, W.; et al. Melatonin functions in priming of stomatal immunity in Panax notoginseng and Arabidopsis thaliana. Plant Physiol. 2021, 187, 2837–2851. [Google Scholar] [CrossRef]
- Seo, S.Y.; Wi, S.J.; Park, K.Y. Functional switching of NPR1 between chloroplast and nucleus for adaptive response to salt stress. Sci. Rep. 2020, 10, 4339. [Google Scholar] [CrossRef]
- Li, Q.; Hu, A.; Qi, J.; Dou, W.; Qin, X.; Zou, X.; Xu, L.; Chen, S.; He, Y. CsWAKL08, a pathogen-induced wall-associated receptor-like kinase in sweet orange, confers resistance to citrus bacterial canker via ROS control and JA signaling. Hortic. Res. 2020, 7, 42. [Google Scholar] [CrossRef]
- Wang, W.; Quan, C.; Zheng, S.; Wang, Y.; Mo, Y.; Ma, C.; Xu, Z.; Li, L.; Huang, Z.; Jia, X.; et al. OsPM1 is a positive regulator of rice tolerance to drought stress but a negative regulator of rice tolerance to salt stress. J. Plant Interact. 2021, 16, 213–221. [Google Scholar] [CrossRef]
- Kimura, S.; Hunter, K.; Vaahtera, L.; Tran, H.C.; Citterico, M.; Vaattovaara, A.; Rokka, A.; Stolze, S.C.; Harzen, A.; Meißner, L.; et al. CRK2 and C-terminal Phosphorylation of NADPH Oxidase RBOHD Regulate Reactive Oxygen Species Production in Arabidopsis. Plant Cell 2020, 32, 1063–1080. [Google Scholar] [CrossRef]
- Chung, J.; Zhu, J.; Bressan, R.A.; Hasegawa, P.M.; Shi, H. Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J. 2007, 53, 554–565. [Google Scholar] [CrossRef]
- Pan, L.; Ma, J.; Li, J.; Yin, B.; Fu, C. Advances of salt stress-responsive transcription factors in plants. Chin. J. Biotechnol. 2022, 38, 50–65. [Google Scholar]
- Feng, D.; Gao, Q.; Liu, J.; Tang, J.; Hua, Z.; Sun, X. Categories of exogenous substances and their effect on alleviation of plant salt stress. Eur. J. Agron. 2023, 142, 126656. [Google Scholar] [CrossRef]
- Qin, H.; Huang, R. The phytohormonal regulation of Na+/K+ and reactive oxygen species homeostasis in rice salt response. Mol. Breed. 2020, 40, 47. [Google Scholar] [CrossRef]
Exogenous Additive | Varieties | Impact on Yield and Quality | |
---|---|---|---|
GA3 | S79 and S80 | Root length, root number, root weight, seedling weight, and growth rate increased by 12.82%, 9.45%, 17.84%, 7.06%, 36.73%, and 36.73%. | Hu W et al. [38] |
CGG (GABA, CaCl2 and Glu compound) | Japonica rice: Dongnong 428, Songjing 10 | Under the optimal concentration ratio (1.87 mmol/L CaCl2, 2.76 mg/mL Glu, 4.40 mmol/L GABA), the annual output of Dongnong 428 was 8340.5 kg/ha and that of Songjing 10 was 7093.5 kg/ha, which was 11.05% and 24.47% higher than the values observed under cold water stress treatment, respectively. | Jia Y et al. [39] |
SNP, SA | Wheat: “Shanon 22”, | The yield of wheat treated with SA, SNP, slow-release SA, and SNP under salt stress increased by 16.35%, 9.62%, 22.12%, and 32.69%, respectively; the chlorophyll content in the seedling leaves increased by 5.51%, 7.85%, 12.98%, and 16.83%, respectively; and the O2− content decreased by 26.78%, 34.58%, 27.65% and 39.06%, respectively, compared with CK. | Dong YJ et al. [40] |
Salicylic acid (SA), calcium chloride (CaCl2), and abscisic acid (ABA) | Peony (P. ostii ‘Fengdan’) | Treatments with 100 μmol/L SA, 40 mmol/L CaCl2, and 240 mg/L ABA could all alleviate high-temperature damage. Taking soluble protein (SPs) as an example, the SP content of SA-treated seedlings increased by 34.00%, 17.67% and 19.29% at 2, 4 and 6 d, respectively; that of CaCl2-treated seedlings increased by 15.31%, 20.03% and 41.40% at 4, 6 and 7 d, respectively; and that of ABA-treated seedlings increased by 26.36%, 12.66%, 15.23% and 35.89% at 2, 4, 6 and 7 d, respectively, during the recovery period (all are compared with HT treatment). | Guo JX et al. [41] |
Abscisic acid (ABA) | Sauvignon (Vitis vinifera cv. Cabernet) | Exogenous ABA treatment speeds up grape coloration. Colouration after ABA treatment started 5 days earlier than that in the CK group, with 10% coloration occurring per day 7 days after treatment (66 DAF) and full coloration observed at 72 DAF. Under carbon-limited ABA treatment, grapes changed color faster, at a 5.8% daily change rate, at 69 DAF compared to CK (3.3% daily). | Tong Q et al. [42] |
GA3 | Strawberry (Fragaria × ananassa Duch.) | The maximum fruit weight of 100 mgL−1 GA3-sprayed plants increased by 34.82%, the longitudinal diameter increased by 33.56%, and the total output increased by 54.84%. The yield of marketable fruit in this treatment group increased by 74.47% compared with CK, and the yield of nonmarketable fruit decreased by 14.64%. | Rathod K.D. et al. [43] |
GA3 | Kiwifruit (Actinidia deliciosa Chev.) | After 25 mgL−1 GA3 treatment, the leaf area in the first and second years increased by 11.54% and 8.48% over CK, respectively; the fruit weight increased by 30.51% and 31.43%, respectively; and the fruit hardness increased by 10.70% and 7.24%, respectively. | Nowsheen Nazir et al. [44] |
Melatonin (MT) | Sunshine rose (Vitis labrusca × vinifera ‘Shine Muscat’) | Treatment with 150 μmol/LMT increased the yield by 8.28%, 8.20%, and 8.54%, and treatment with 50 μmol/LMT increased the yield by 4.41%, 4.09%, and 3.09%. | Xu N et al. [45] |
H2S, GABA | Persimmon (Diospyros kaki) | Under 3 mM NaHS and 7.5 mM GABA treatment, persimmon peel had a low browning rate and more antioxidants (AsA, flavonoids), higher polygalacturonase (PG) and pectin methylesterase (PME) activity, and better hardness, DPPH clearance activity and membrane integrity under cold storage, allowing maintenance of better food quality. | Zohreh Niazi et al. [46] |
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
Jiang, S.; Lan, Z.; Zhang, Y.; Kang, X.; Zhao, L.; Wu, X.; Gao, H. Mechanisms by Which Exogenous Substances Enhance Plant Salt Tolerance through the Modulation of Ion Membrane Transport and Reactive Oxygen Species Metabolism. Antioxidants 2024, 13, 1050. https://doi.org/10.3390/antiox13091050
Jiang S, Lan Z, Zhang Y, Kang X, Zhao L, Wu X, Gao H. Mechanisms by Which Exogenous Substances Enhance Plant Salt Tolerance through the Modulation of Ion Membrane Transport and Reactive Oxygen Species Metabolism. Antioxidants. 2024; 13(9):1050. https://doi.org/10.3390/antiox13091050
Chicago/Turabian StyleJiang, Shiqing, Zuwen Lan, Yinkang Zhang, Xinna Kang, Liran Zhao, Xiaolei Wu, and Hongbo Gao. 2024. "Mechanisms by Which Exogenous Substances Enhance Plant Salt Tolerance through the Modulation of Ion Membrane Transport and Reactive Oxygen Species Metabolism" Antioxidants 13, no. 9: 1050. https://doi.org/10.3390/antiox13091050