Adjustment of K+ Fluxes and Grapevine Defense in the Face of Climate Change

Abstract

Grapevine is one of the most economically important fruit crops due to the high value of its fruit and its importance in winemaking. The current decrease in grape berry quality and production can be seen as the consequence of various abiotic constraints imposed by climate changes. Specifically, produced wines have become too sweet, with a stronger impression of alcohol and fewer aromatic qualities. Potassium is known to play a major role in grapevine growth, as well as grape composition and wine quality. Importantly, potassium ions (K⁺) are involved in the initiation and maintenance of the berry loading process during ripening. Moreover, K⁺ has also been implicated in various defense mechanisms against abiotic stress. The first part of this review discusses the main negative consequences of the current climate, how they disturb the quality of grape berries at harvest and thus ultimately compromise the potential to obtain a great wine. In the second part, the essential electrical and osmotic functions of K⁺, which are intimately dependent on K⁺ transport systems, membrane energization, and cell K⁺ homeostasis, are presented. This knowledge will help to select crops that are better adapted to adverse environmental conditions.

Keywords: climate change; fruit; potassium homeostasis; potassium transport; quality.

Figure 1

The Shaker K⁺ channel family. (A) Phylogenetic relationships in the grapevine (in green) and A. thaliana (in blue) Shaker K⁺ channel families. The Shaker family displays five groups in plants [115] named 1 to 5. Accession references are listed in Table 1. The abbreviations K_in, K_out K_weak, and K_silent are explained in the legend of Table 1. To find the conserved region, A. thaliana and grapevine Shaker polypeptide sequences were first aligned using MUSCLE 3.8.31 in full mode and then treated with Gblocks for alignment curation. The phylogenetic analyses were carried out using maximum likelihood with Phy ML 3.1/3.0 aLRT software. Tree rendering was performed using the tree drawing engine ETE 3 [116]). Bootstrap values are indicated at the corresponding nodes. The scale bar corresponds to a distance of 4,6 changes per 100 amino acid positions. (B) Functional Shaker channels are multimeric proteins formed by the assembly of four Shaker subunits. Current–voltage (I–V) curves illustrate the functional types found in the homotetrameric Shaker channels that form inwardly rectifying, weakly inwardly rectifying, or outwardly rectifying conductances. Int and ext: internal and external face of the plasma membrane. (C) Structural domains of a Shaker channel subunit. S1 to S6: transmembrane segments, CNBD: cyclic nucleotide-binding domain, ANKY: ankyrin domain (involved in protein-protein interactions, not found in all Shaker subunits), KHA: hydrophic and acidic domain. (D) Assembly of four Shaker alpha-subunit is a prerequisite for channel functioning. Three-dimensional representation of S1–S6 segments in a single subunit (left) or Shaker tetramers (right). Subunits are encoded either by the same gene (homotetrameric channel) or by different genes (heterotetrameric channel). K_in sub-units (Groups 1, 2, 3 and 4 in A) assemble as K_in channels, whereas K_out sub-units (Group 5) form K_out channels. No assembly could be detected between K_in and K_out channel subunits [117]. Stoichiometry studies have revealed the various possible combinations between the different subunits [117,118,119].

Figure 2

Schematic representation of known and expected K⁺ transport pathways in grape berries after the onset of ripening. K⁺ is delivered to berries via the phloem [15] and must cross the phloem plasma membrane barrier before accumulating in mesocarp cells [35]. This K⁺ flux to the apoplastic space involves the Shaker VvK3.1 channel. The activity of this channel can be enhanced by CIPK/CBL couples, possibly via an unusual mechanism of CBL anchoring in the plasma membrane [33]. Moreover, the depolarization-activated VvK5.1 channel present in phloem cells could control the plasma membrane potential [103]. By analogy with its GORK counterpart, VvK5.1 is expected to be modulated by CPKs [17]. Once in the apoplast, K⁺ is taken up by the flesh cells owing to the VvK1.2 Shaker channel [32], which recruits CIPK/CBL partners for its activation. CIPKs are also known to be inhibited by their interaction with PP2Cs of the ABA signaling pathway [17]. PP2Cs are, in an ABA-dependent manner, under the negative control of PYR/PYL/RCAR receptors. The VvNHX1 H⁺/K⁺ exchanger mediates K⁺ transfer to the vacuole, where this ion is accumulated [114].