Functional Characterization of VvSK Gene Family in Grapevine Revealing Their Role in Berry Ripening

Abstract

The glycogen synthase kinase 3/shaggy kinase (GSK3) is a serine/threonine kinase that plays important roles in brassinosteroid signaling, abiotic stress responses, cell division, and elongation, etc. In this study, we characterized seven grape GSK3 genes, showing high similarities with homologs from other species including Arabidopsis, white pear, apple, orange, and peach. Gene chip microarray data derived from an online database revealed very diverse developmental and tissue-specific expression patterns of VvSKs. VvSK3 and VvSK7 showed much higher expression levels in almost every tissue compared with other members. VvSK7 was highly enriched in young tissues like berries before the veraison stage, young leaves and green stems, etc., but immediately downregulated after these tissues entered maturation or senescence phases. Prediction of cis-elements in VvSK promoters indicated that VvSKs might be sensitive to light stimulation, which is further confirmed by the qPCR data. Constitutive overexpression of VvSK7 in Arabidopsis leads to dwarf plants that resembles BR-deficient mutants. The photosynthetic rate was significantly reduced in these plants, even though they accumulated more chlorophyll in leaves. Transient overexpression of VvSKs in tomatoes delayed the fruit ripening process, consistent with the observation in grapevine which blocks VvSKs by EBR- or BIKININ-promoted berry expansion and soluble solids accumulation. Data presented in the current study may serve as a theoretical basis for the future application of BRs or related compounds in quality grape production.

Versatile Physiological Functions of Plant GSK3-Like Kinases

“…The plant GSK3-like kinases might also regulate the fruit ripening process (Figure 1). A recent study showed that overexpression of a grapevine GSK3-like kinase (VvSK7 for Vitis vinifera Shaggy-like Kinase7) in tomatoes delayed fruit ripening, which seems to be consistent with the finding of that treatment of grapevines with BRs or GSK3-kinase inhibitor at the veraison stage promoted berry ripening with larger/heavier berries [94]. Interestingly, an earlier study found that another grapevine GSK3-like kinase, VvSK1, was induced by sugars and might be involved in transport and accumulation of sugars during the berry ripening process by regulating expression of several sugar transporters [95].…”

Glycogen synthase kinases in model and crop plants – From negative regulators of brassinosteroid signaling to multifaceted hubs of various signaling pathways and modulators of plant reproduction and yield

“…In a more recent study, overexpression of another grapevine homolog of GSK3, VvSK7, in tomato resulted in a delay in the fruit ripening process. On the other hand, treatment of grapevine plants with exogenous BR or inhibitor of the GSK3 kinases caused an enhancement of fruit ripening and enlargement of fruit size (Zeng et al, 2020). These results indicate that also in non-cereal crops the genes encoding the GSK3 proteins may be regarded as target for genome editing which may result in development of high-yield cultivars with improved fruit quality (Figure 7).…”

Signal transduction in non-climacteric fruit ripening

“…Moreover, individually silencing the hexokinases CsHXK1 or CsHXK2, which are thought to function as glucose sensors, in grape calli reduced the expression of sucrose synthase and cell wall invertase-encoding genes, suggesting an involvement of sugar signaling in the regulation of grape berry ripening [ 133 ]. The serine/threonine kinase, glycogen synthase kinase 3/shaggy kinase (GSK3) is involved in brassinosteroid signaling, and one study reported that transient overexpression of the grape homolog, VvSK, in tomato delayed ripening [ 134 ]. It has also been reported that a U-Box E3 Ubiquitin ligase U-box (PUB) gene, VIPUB35 , is involved in grape fruit ripening, and its heterologous expression in strawberry delayed ripening.…”