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Loss of function of the chloroplast membrane K+/H+ antiporters AtKEA1 and AtKEA2 alters the ROS and NO metabolism but promotes drought stress resilience.
Plant Physiol Biochem. 2021 Mar; 160:106-119.PP

Abstract

Potassium (K+) exerts key physiological functions such as osmoregulation, stomatal movement, membrane transport, protein synthesis and photosynthesis among others. Previously, it was demonstrated in Arabidopsis thaliana that the loss of function of the chloroplast K+Efflux Antiporters KEA1 and KEA2, located in the inner envelope membrane, provokes inefficient photosynthesis. Therefore, the main goal of this study was to evaluate the potential impact of the loss of function of those cation transport systems in the metabolism of reactive oxygen and nitrogen species (ROS and RNS). Using 14-day-old seedlings from Arabidopsis double knock-out kea1kea2 mutants, ROS metabolism and NO content in roots and green cotyledons were studied at the biochemical level. The loss of function of AtKEA1 and AtKEA2 did not cause oxidative stress but it provoked an alteration of the ROS homeostasis affecting some ROS-generating enzymes. These included glycolate oxidase (GOX) and NADPH-dependent superoxide generation activity, enzymatic and non-enzymatic antioxidants and both NADP-isocitrate dehydrogenase and NADP-malic enzyme activities. NO content, analyzed by confocal laser scanning microscopy (CLSM), was negatively affected in both photosynthetic and non-photosynthetic organs in kea1kea2 mutant seedlings. Furthermore, the S-nitrosoglutathione reductase (GSNOR) protein expression and activity were downregulated in kea1kea2 mutants, whereas the tyrosine nitrated protein profile, analyzed by immunoblot, was unaffected but the relative expression of each immunoreactive band changed. Moreover, kea1kea2 mutants showed an increased photorespiratory pathway and stomata closure, thus promoting a higher resilience to drought stress. Data suggest that the chloroplast osmotic balance and integrity maintained by AtKEA1 and AtKEA2 are necessary to keep the balance of ROS/RNS metabolism. Moreover, these data open new questions about how endogenous NO generation might be affected by the K+/H+ transport located in the chloroplasts.

Authors+Show Affiliations

Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Spain.Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Spain.Group of Ion Homeostasis, Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental Del Zaidín, CSIC, C/ Profesor Albareda, 1, 18008, Granada, Spain.Group of Ion Homeostasis, Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental Del Zaidín, CSIC, C/ Profesor Albareda, 1, 18008, Granada, Spain.Group of Ion Homeostasis, Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental Del Zaidín, CSIC, C/ Profesor Albareda, 1, 18008, Granada, Spain.Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Spain.Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Spain. Electronic address: javier.corpas@eez.csic.es.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

33485149

Citation

Sánchez-McSweeney, Antonio, et al. "Loss of Function of the Chloroplast Membrane K+/H+ Antiporters AtKEA1 and AtKEA2 Alters the ROS and NO Metabolism but Promotes Drought Stress Resilience." Plant Physiology and Biochemistry : PPB, vol. 160, 2021, pp. 106-119.
Sánchez-McSweeney A, González-Gordo S, Aranda-Sicilia MN, et al. Loss of function of the chloroplast membrane K+/H+ antiporters AtKEA1 and AtKEA2 alters the ROS and NO metabolism but promotes drought stress resilience. Plant Physiol Biochem. 2021;160:106-119.
Sánchez-McSweeney, A., González-Gordo, S., Aranda-Sicilia, M. N., Rodríguez-Rosales, M. P., Venema, K., Palma, J. M., & Corpas, F. J. (2021). Loss of function of the chloroplast membrane K+/H+ antiporters AtKEA1 and AtKEA2 alters the ROS and NO metabolism but promotes drought stress resilience. Plant Physiology and Biochemistry : PPB, 160, 106-119. https://doi.org/10.1016/j.plaphy.2021.01.010
Sánchez-McSweeney A, et al. Loss of Function of the Chloroplast Membrane K+/H+ Antiporters AtKEA1 and AtKEA2 Alters the ROS and NO Metabolism but Promotes Drought Stress Resilience. Plant Physiol Biochem. 2021;160:106-119. PubMed PMID: 33485149.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Loss of function of the chloroplast membrane K+/H+ antiporters AtKEA1 and AtKEA2 alters the ROS and NO metabolism but promotes drought stress resilience. AU - Sánchez-McSweeney,Antonio, AU - González-Gordo,Salvador, AU - Aranda-Sicilia,María Nieves, AU - Rodríguez-Rosales,María Pilar, AU - Venema,Kees, AU - Palma,José M, AU - Corpas,Francisco J, Y1 - 2021/01/12/ PY - 2020/12/09/received PY - 2021/01/08/accepted PY - 2021/1/24/pubmed PY - 2021/3/3/medline PY - 2021/1/23/entrez KW - Drought stress KW - KEA K(+)/H(+) antiporters KW - Nitric oxide KW - Photorespiration KW - Reactive nitrogen species KW - Reactive oxygen species KW - Stomata SP - 106 EP - 119 JF - Plant physiology and biochemistry : PPB JO - Plant Physiol Biochem VL - 160 N2 - Potassium (K+) exerts key physiological functions such as osmoregulation, stomatal movement, membrane transport, protein synthesis and photosynthesis among others. Previously, it was demonstrated in Arabidopsis thaliana that the loss of function of the chloroplast K+Efflux Antiporters KEA1 and KEA2, located in the inner envelope membrane, provokes inefficient photosynthesis. Therefore, the main goal of this study was to evaluate the potential impact of the loss of function of those cation transport systems in the metabolism of reactive oxygen and nitrogen species (ROS and RNS). Using 14-day-old seedlings from Arabidopsis double knock-out kea1kea2 mutants, ROS metabolism and NO content in roots and green cotyledons were studied at the biochemical level. The loss of function of AtKEA1 and AtKEA2 did not cause oxidative stress but it provoked an alteration of the ROS homeostasis affecting some ROS-generating enzymes. These included glycolate oxidase (GOX) and NADPH-dependent superoxide generation activity, enzymatic and non-enzymatic antioxidants and both NADP-isocitrate dehydrogenase and NADP-malic enzyme activities. NO content, analyzed by confocal laser scanning microscopy (CLSM), was negatively affected in both photosynthetic and non-photosynthetic organs in kea1kea2 mutant seedlings. Furthermore, the S-nitrosoglutathione reductase (GSNOR) protein expression and activity were downregulated in kea1kea2 mutants, whereas the tyrosine nitrated protein profile, analyzed by immunoblot, was unaffected but the relative expression of each immunoreactive band changed. Moreover, kea1kea2 mutants showed an increased photorespiratory pathway and stomata closure, thus promoting a higher resilience to drought stress. Data suggest that the chloroplast osmotic balance and integrity maintained by AtKEA1 and AtKEA2 are necessary to keep the balance of ROS/RNS metabolism. Moreover, these data open new questions about how endogenous NO generation might be affected by the K+/H+ transport located in the chloroplasts. SN - 1873-2690 UR - https://www.unboundmedicine.com/medline/citation/33485149/Loss_of_function_of_the_chloroplast_membrane_K+/H+_antiporters_AtKEA1_and_AtKEA2_alters_the_ROS_and_NO_metabolism_but_promotes_drought_stress_resilience_ DB - PRIME DP - Unbound Medicine ER -