Characterization of the grapevine Shaker K⁺ channel VvK3.1 supports its function in massive potassium fluxes necessary for berry potassium loading and pulvinus‐actuated leaf movements

Abstract

Summary In grapevine, climate changes lead to increased berry potassium (K+) contents that result in must with low acidity. Consequently, wines are becoming ‘flat’ to the taste, with poor organoleptic properties and low potential aging, resulting in significant economic loss. Precise investigation into the molecular determinants controlling berry K+ accumulation during its development are only now emerging. Here, we report functional characterization by electrophysiology of a new grapevine Shaker‐type K+ channel, VvK3.1. The analysis of VvK3.1 expression patterns was performed by qPCR and in situ hybridization. We found that VvK3.1 belongs to the AKT2 channel phylogenetic branch and is a weakly rectifying channel, mediating both inward and outward K+ currents. We showed that VvK3.1 is highly expressed in the phloem and in a unique structure located at the two ends of the petiole, identified as a pulvinus. From the onset of fruit ripening, all data support the role of the VvK3.1 channel in the massive K+ fluxes from the phloem cell cytosol to the berry apoplast during berry K+ loading. Moreover, the high amount of VvK3.1 transcripts detected in the pulvinus strongly suggests a role for this Shaker in the swelling and shrinking of motor cells involved in paraheliotropic leaf movements.

Grapevine Potassium Nutrition and Fruit Quality in the Context of Climate Change

“…These channels are known to dominate phloem K + conductance where they have a major role in phloem K + loading and unloading (Marten et al, 1999;Lacombe et al, 2000;Ache et al, 2001;Hafke et al, 2007). In grapevine, VvK3.1 channel mediates K + unloading in the berries and is also involved in the maintenance of transmembrane K + gradients of phloem cells, which refers to the concept of K + battery (Gajdanowicz et al, 2011;Dreyer et al, 2017;Nieves-Cordones et al, 2019). The K + battery explains how an open AKT2-like channel can compensate for the reduced pH gradient present under energy limitation and can provide additional energy stored in the K + gradient between the phloem cytosol and the berry apoplast for transmembrane transport processes (Dreyer et al, 2017).…”

“…High temperature affects the phenology of grape berry development and ripening, resulting in a shift of picking dates toward earlier periods depending on the region, the variety, and the wine type. Heat waves directly increase sugar import (Mori et al, 2007;Parker et al, 2011) and K + accumulation (Mpelasoka et al, 2003;Cuéllar et al, 2010;Kodur, 2011;Cuéllar et al, 2013;Rogiers et al, 2017;Nieves-Cordones et al, 2019). Phloem transport and berry metabolism also increase at high temperature.…”

“…Phloem transport and berry metabolism also increase at high temperature. From the onset of the ripening (veraison), berry loading is ensured from the phloem by a directional flow of water, sugar, and nutrients driven by massive K + fluxes (Nieves-Cordones et al, 2019). In addition, it is also known that vineyards grown in warmer areas give wines with low acidity.…”

“…In grapevine, K + plays an essential role in the initiation and control of massive fluxes that are necessary for berry growth during maturation (Cuéllar et al, 2013;Nieves-Cordones et al, 2019). In addition, grape acidity at harvest is a key factor to obtain wines of great quality.…”

“…malic and tartaric acids) and organic acids neutralized by K + . In the context of warmer climates, K + ion accumulation increases during grape ripening, leading to an excessive neutralization of organic acids (Cuéllar et al, 2010;Cuéllar et al, 2013;Rogiers et al, 2017;Nieves-Cordones et al, 2019). Moreover, high temperature also affects the organic acid content of berries inducing the consumption of malic acid as a respiratory substrate (Famiani et al, 2016).…”