Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling Roots

Potassium (K<sup>+</sup>) is one of the vital macronutrients required by plants for proper growth and blossoming harvest. In addition, K<sup>+</sup> also plays a decisive role in promoting tolerance to various stresses. Under stressful conditions, plants deploy their defense...

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Main Authors: M. Nasir Khan, Soumya Mukherjee, Asma A. Al-Huqail, Riyadh A. Basahi, Hayssam M. Ali, Bander M. A. Al-Munqedhi, Manzer H. Siddiqui, Hazem M. Kalaji
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/10/5/948
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author M. Nasir Khan
Soumya Mukherjee
Asma A. Al-Huqail
Riyadh A. Basahi
Hayssam M. Ali
Bander M. A. Al-Munqedhi
Manzer H. Siddiqui
Hazem M. Kalaji
author_facet M. Nasir Khan
Soumya Mukherjee
Asma A. Al-Huqail
Riyadh A. Basahi
Hayssam M. Ali
Bander M. A. Al-Munqedhi
Manzer H. Siddiqui
Hazem M. Kalaji
author_sort M. Nasir Khan
collection DOAJ
description Potassium (K<sup>+</sup>) is one of the vital macronutrients required by plants for proper growth and blossoming harvest. In addition, K<sup>+</sup> also plays a decisive role in promoting tolerance to various stresses. Under stressful conditions, plants deploy their defense system through various signaling molecules, including hydrogen sulfide (H<sub>2</sub>S). The present investigation was carried out to unravel the role of K<sup>+</sup> and H<sub>2</sub>S in plants under NaCl stress. The results of the study show that NaCl stress caused a reduction in K<sup>+</sup> and an increase in Na<sup>+</sup> content in the tomato seedling roots which coincided with a lower H<sup>+</sup>-ATPase activity and K<sup>+</sup>/Na<sup>+</sup> ratio. However, application of 5 mM K<sup>+</sup>, in association with endogenous H<sub>2</sub>S, positively regulated the Na<sup>+</sup>/H<sup>+</sup> antiport system that accelerated K+ influx and Na+ efflux, resulting in the maintenance of a higher K<sup>+</sup>/Na<sup>+</sup> ratio. The role of K<sup>+</sup> and H<sub>2</sub>S in the regulation of the Na<sup>+</sup>/H<sup>+</sup> antiport system was validated by applying sodium orthovanadate (plasma membrane H<sup>+</sup>-ATPase inhibitor), tetraethylammonium chloride (K<sup>+</sup> channel blocker), amiloride (Na<sup>+</sup>/H<sup>+</sup> antiporter inhibitor), and hypotaurine (HT, H<sub>2</sub>S scavenger). Application of 5 mM K<sup>+</sup> positively regulated the ascorbate–glutathione cycle and activity of antioxidant enzymes that resulted in a reduction in reactive oxygen species generation and associated damage. Under NaCl stress, K<sup>+</sup> also activated carbohydrate metabolism and proline accumulation that caused improvement in osmotic tolerance and enhanced the hydration level of the stressed seedlings. However, inclusion of the H<sub>2</sub>S scavenger HT reversed the effect of K<sup>+</sup>, suggesting H<sub>2</sub>S-dependent functioning of K<sup>+</sup> under NaCl stress. Therefore, the present findings report that K<sup>+</sup>, in association with H<sub>2</sub>S, alleviates NaCl-induced impairments by regulating the Na<sup>+</sup>/H<sup>+</sup> antiport system, carbohydrate metabolism, and antioxidative defense system.
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spelling doaj.art-56f30fa4c9e2474b8eac1f3a72b92b332023-11-21T19:00:12ZengMDPI AGPlants2223-77472021-05-0110594810.3390/plants10050948Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling RootsM. Nasir Khan0Soumya Mukherjee1Asma A. Al-Huqail2Riyadh A. Basahi3Hayssam M. Ali4Bander M. A. Al-Munqedhi5Manzer H. Siddiqui6Hazem M. Kalaji7Department of Biology, Faculty of Science, College of Haql, University of Tabuk, Tabuk 71491, Saudi ArabiaDepartment of Botany, Jangipur College, University of Kalyani, West Bengal 742213, IndiaChair of Climate Change, Environmental Development and Vegetation Cover, Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi ArabiaDepartment of Biology, Faculty of Science, College of Haql, University of Tabuk, Tabuk 71491, Saudi ArabiaChair of Climate Change, Environmental Development and Vegetation Cover, Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi ArabiaChair of Climate Change, Environmental Development and Vegetation Cover, Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi ArabiaChair of Climate Change, Environmental Development and Vegetation Cover, Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi ArabiaDepartment of Plant Physiology, Institute of Biology, Warsaw University of Life Sciences SGGW, 159 Nowoursynowska 159, 02-776 Warsaw, PolandPotassium (K<sup>+</sup>) is one of the vital macronutrients required by plants for proper growth and blossoming harvest. In addition, K<sup>+</sup> also plays a decisive role in promoting tolerance to various stresses. Under stressful conditions, plants deploy their defense system through various signaling molecules, including hydrogen sulfide (H<sub>2</sub>S). The present investigation was carried out to unravel the role of K<sup>+</sup> and H<sub>2</sub>S in plants under NaCl stress. The results of the study show that NaCl stress caused a reduction in K<sup>+</sup> and an increase in Na<sup>+</sup> content in the tomato seedling roots which coincided with a lower H<sup>+</sup>-ATPase activity and K<sup>+</sup>/Na<sup>+</sup> ratio. However, application of 5 mM K<sup>+</sup>, in association with endogenous H<sub>2</sub>S, positively regulated the Na<sup>+</sup>/H<sup>+</sup> antiport system that accelerated K+ influx and Na+ efflux, resulting in the maintenance of a higher K<sup>+</sup>/Na<sup>+</sup> ratio. The role of K<sup>+</sup> and H<sub>2</sub>S in the regulation of the Na<sup>+</sup>/H<sup>+</sup> antiport system was validated by applying sodium orthovanadate (plasma membrane H<sup>+</sup>-ATPase inhibitor), tetraethylammonium chloride (K<sup>+</sup> channel blocker), amiloride (Na<sup>+</sup>/H<sup>+</sup> antiporter inhibitor), and hypotaurine (HT, H<sub>2</sub>S scavenger). Application of 5 mM K<sup>+</sup> positively regulated the ascorbate–glutathione cycle and activity of antioxidant enzymes that resulted in a reduction in reactive oxygen species generation and associated damage. Under NaCl stress, K<sup>+</sup> also activated carbohydrate metabolism and proline accumulation that caused improvement in osmotic tolerance and enhanced the hydration level of the stressed seedlings. However, inclusion of the H<sub>2</sub>S scavenger HT reversed the effect of K<sup>+</sup>, suggesting H<sub>2</sub>S-dependent functioning of K<sup>+</sup> under NaCl stress. Therefore, the present findings report that K<sup>+</sup>, in association with H<sub>2</sub>S, alleviates NaCl-induced impairments by regulating the Na<sup>+</sup>/H<sup>+</sup> antiport system, carbohydrate metabolism, and antioxidative defense system.https://www.mdpi.com/2223-7747/10/5/948hydrogen sulfideionic homeostasisNa<sup>+</sup>/H<sup>+</sup> antiportoxidative stresspotassiumsalinity
spellingShingle M. Nasir Khan
Soumya Mukherjee
Asma A. Al-Huqail
Riyadh A. Basahi
Hayssam M. Ali
Bander M. A. Al-Munqedhi
Manzer H. Siddiqui
Hazem M. Kalaji
Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling Roots
Plants
hydrogen sulfide
ionic homeostasis
Na<sup>+</sup>/H<sup>+</sup> antiport
oxidative stress
potassium
salinity
title Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling Roots
title_full Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling Roots
title_fullStr Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling Roots
title_full_unstemmed Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling Roots
title_short Exogenous Potassium (K<sup>+</sup>) Positively Regulates Na<sup>+</sup>/H<sup>+</sup> Antiport System, Carbohydrate Metabolism, and Ascorbate–Glutathione Cycle in H<sub>2</sub>S-Dependent Manner in NaCl-Stressed Tomato Seedling Roots
title_sort exogenous potassium k sup sup positively regulates na sup sup h sup sup antiport system carbohydrate metabolism and ascorbate glutathione cycle in h sub 2 sub s dependent manner in nacl stressed tomato seedling roots
topic hydrogen sulfide
ionic homeostasis
Na<sup>+</sup>/H<sup>+</sup> antiport
oxidative stress
potassium
salinity
url https://www.mdpi.com/2223-7747/10/5/948
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