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Inhibition of Shaker K+ channel activity by external Na+ was previously reported in the melon (Cucumis melo L.) inwardly rectifying K+ channel MIRK and was hypothesized to contribute to salt tolerance. In this study, two inward Shaker K+ channels, CsKAT2 from cucumber (Cucumis sativus) and ClKAT2 from watermelon (Citrullus lanatus), were identified and characterized in Xenopus oocytes. Both channels were inwardly rectifying K+ channels with higher permeability to potassium than other monovalent cations and more active when external pH was acidic. Similarly to MIRK, their activity displayed an inhibition by external Na+, thus suggesting a common feature in Cucurbitaceae (Cucumis spp., Citrullus spp.). CsKAT2 and ClKAT2 are highly expressed in guard cells. After 24 h of plant treatment with 100 mM NaCl, the three KAT2-like genes were significantly downregulated in leaves and guard cells. Reciprocal chimeras were obtained between MIRK and Na+-insensitive AtKAT2 cDNAs. The chimera where the MIRK S5-P-S6 segment was replaced by that from AtKAT2 no longer showed Na+ sensitivity, while the inverse chimera gained Na+ sensitivity. These results provide evidence that the molecular basis of the channel blockage by Na+ is located in the S5-P-S6 region. Comparison of the electrostatic property in the S5-P-S6 region in AtKAT2 and MIRK revealed four key amino acid residues potentially governing Na+ sensitivity., (© The Author(s) 2021. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

• The possible roles of K(+) channels in plant adaptation to high Na(+) conditions have not been extensively analyzed. Here, we characterize an inward Shaker K(+) channel, MIRK (melon inward rectifying K(+) channel), cloned in a salt-tolerant melon (Cucumis melo) cultivar, and show that this channel displays an unusual sensitivity to Na(+) . • MIRK expression localization was analyzed by reverse-transcription PCR (RT-PCR). MIRK functional analyses were performed in yeast (growth tests) and Xenopus oocytes (voltage-clamp). MIRK-type activity was revealed in guard cells using the patch-clamp technique. • MIRK is an inwardly rectifying Shaker channel belonging to the 'KAT' subgroup and expressed in melon leaves (especially in guard cells and vasculature), stems, flowers and fruits. Besides having similar features to its close homologs, MIRK displays a unique property: inhibition of K(+) transport by external Na(+) . In Xenopus oocytes, external Na(+) affected both inward and outward MIRK currents in a voltage-independent manner, suggesting a blocking site in the channel external mouth. • The degree of MIRK inhibition by Na(+) , which is dependent on the Na(+) /K(+) concentration ratio, is predicted to have an impact on the control of K(+) transport in planta upon salt stress. Expressed in guard cells, MIRK might control Na(+) arrival to the shoots via regulation of stomatal aperture by Na(+) ., (© 2010 The Authors. New Phytologist © 2010 New Phytologist Trust.)