Abstract
A small set of TTG2-like homolog proteins from different species belonging to the WRKY family of transcription factors were shown to share a similar mechanism of action and to control partially conserved biochemical/developmental processes in their native species. In particular, by activating P-ATPases residing on the tonoplast, PH3 from Petunia hybrida promotes vacuolar acidification in petal epidermal cells whereas TTG2 from Arabidopsis thaliana enables the accumulation of proanthocyanidins in the seed coat. In this work we functionally characterized VvWRKY26 identified as the closest grapevine homolog of PhPH3 and AtTTG2. When constitutively expressed in petunia ph3 mutant, VvWRKY26 can fulfill the PH3 function in the regulation of vacuolar pH and restores the wild type pigmentation phenotype. By a global correlation analysis of gene expression and by transient over-expression in Vitis vinifera, we showed transcriptomic relationships of VvWRKY26 with many genes related to vacuolar acidification and transport in grapevine. Moreover, our results indicate an involvement in flavonoid pathway possibly restricted to the control of proanthocyanidin biosynthesis that is consistent with its expression pattern in grape berry tissues. Overall, the results show that, in addition to regulative mechanisms and biological roles shared with TTG2-like orthologs, VvWRKY26 can play roles in fleshy fruit development that have not been previously reported in studies from dry fruit species. This study paves the way toward the comprehension of the regulatory network controlling vacuolar acidification and flavonoid accumulation mechanisms that contribute to the final berry quality traits in grapevine.
Highlights
Grape berry needs a relatively long period to develop during which its tissues undergo several physiological and biochemical changes leading to the final composition and quality of ripe fruit
Among the genes not grouped in this category but highly coexpressed with VvWRKY26 we found the R2R3-MYB repressor MYBC2-L1 (VIT_01S0011G04760), recently demonstrated to influence pigmentation and cell vacuolar pH when expressed in petunia petals, and anthocyanin and PA biosynthesis in grapevine (Cavallini et al, 2014, 2015; Huang et al, 2014)
Two WRKY factors extremely close to AtTTG2 have recently been characterized, PH3 of P. hybrida, a novel regulator of vacuolar acidification in petals (Verweij et al, 2016), and TTG2 of Brassica napus involved in response to salt stress and in trichome development (Li et al, 2015)
Summary
Grape berry needs a relatively long period to develop during which its tissues undergo several physiological and biochemical changes leading to the final composition and quality of ripe fruit. A combined proton pumping system constituted by V-PPases and V-ATPases influences the electrochemical potential gradient and allows the active transport of sugars, ions and organic acids across the tonoplast Another mechanism recently identified in Petunia hybrida for vacuole acidification requires PhPH1 and PhPH5 encoding two interacting P-ATPase transmembrane transporters located on the tonoplast. The lack of expression of the PhPH5/AtTT13 citrus homolog was proposed as being responsible for the low acidity in the juice of Faris “sweet” lemon (Citrus limon) variety (Aprile et al, 2011) The homologs of both PhPH1 and PhPH5/AtTT13 were identified in grapevine and were shown to replace the function of the respective endogenous genes when expressed in petunia (Faraco et al, 2014; Li et al, 2016), suggesting the existence of a similar acidification mechanism in grapevine
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