Potassium transport in developing fleshy fruits: the grapevine inward K⁺ channel VvK1.2 is activated by CIPK–CBL complexes and induced in ripening berry flesh cells

Abstract

SUMMARYThe grape berry provides a model for investigating the physiology of non-climacteric fruits. Increased K + accumulation in the berry has a strong negative impact on fruit acidity (and quality). In maturing berries, we identified a K + channel from the Shaker family, VvK1.2, and two CBL-interacting protein kinase (CIPK)/calcineurin B-like calcium sensor (CBL) pairs, VvCIPK04-VvCBL01 and VvCIPK03-VvCBL02, that may control the activity of this channel. VvCBL01 and VvCIPK04 are homologues of Arabidopsis AtCBL1 and AtCIPK23, respectively, which form a complex that controls the activity of the Shaker K + channel AKT1 in Arabidopsis roots. VvK1.2 remained electrically silent when expressed alone in Xenopus oocytes, but gave rise to K + currents when co-expressed with the pairs VvCIPK03-VvCBL02 or VvCIPK04-VvCBL01, the second pair inducing much larger currents than the first one. Other tested CIPK-CBL pairs expressed in maturing berries were found to be unable to activate VvK1.2. When activated by its CIPK-CBL partners, VvK1.2 acts as a voltagegated inwardly rectifying K + channel that is activated at voltages more negative than -100 mV and is stimulated upon external acidification. This channel is specifically expressed in the berry, where it displays a very strong induction at veraison (the inception of ripening) in flesh cells, phloem tissues and perivascular cells surrounding vascular bundles. Its expression in these tissues is further greatly increased upon mild drought stress. VvK1.2 is thus likely to mediate rapid K + transport in the berry and to contribute to the extensive reorganization of the translocation pathways and transport mechanisms that occurs at veraison.

The Os-AKT1 Channel Is Critical for K+ Uptake in Rice Roots and Is Modulated by the Rice CBL1-CIPK23 Complex

“…Several AKT1 orthologs have been identified in other plant species, such as Os-AKT1 in rice (Oryza sativa; Fuchs et al, 2005), Zm-ZMK1 in maize (Zea mays; Philippar et al, 1999), Ta-AKT1 in wheat (Triticum aestivum; Buschmann et al, 2000), Hv-AKT1 in barley (Hordeum vulgare; Boscari et al, 2009), Sl-LKT1 in tomato (Solanum lycopersicum; Hartje et al, 2000), and St-SKT1 in potato (Solanum tuberosum; Zimmermann et al, 1998). Similar regulatory mechanisms, with CBL-CIPK complex-modulating K + channels, were also reported in barley (Boscari et al, 2009) and grape (Vitis vinifera) plants (Cuéllar et al, 2010(Cuéllar et al, , 2013.…”

“…In X. laevis oocytes, Vv-K1.2 alone could not form functional channel. However, after coexpression with Vv-CBL01-Vv-CIPK04 or Vv-CBL02-Vv-CIPK03, Vv-K1.2 was capable of mediating inward K + currents (Cuéllar et al, 2013). It seems that the regulation of AKT1-like channels via a CBL-CIPK complex might be a universal mechanism in different plant species.…”

The Basic Leucine Zipper Transcription Factor ABSCISIC ACID RESPONSE ELEMENT-BINDING FACTOR2 Is an Important Transcriptional Regulator of Abscisic Acid-Dependent Grape Berry Ripening Processes

“…These genes are known ABA targets that are also important for berry ripening . Indeed, together with sugar accumulation, K + influx might help the turgor-driven berry expansion , and the K + channel VvK1.1 may play a major role in K + loading into berry tissues, especially upon drought stress (Cuéllar et al, 2010(Cuéllar et al, , 2013.…”

Decrypting Calcium Signaling in Plants: The Kinase Way

“…When VvCIPK03-VvCBL02 were co-expressed with VvK1.2, much smaller K + currents were generated. VvCBL01 and VvCIPK04 were also found to control the activity of AKT1 in Arabidopsis roots (Cuéllar et al 2013 ). Recently, it was shown that co-expression of either AtCBL1 or AtCBL9 with AtCIPK26 strongly enhances ROS production by phosphorylating NADPH oxidase RBOHF (Sagi and Fluhr 2006 ;Kimura et al 2013 ;Drerup et al 2013 ).…”