Time-resolved transcriptomic of singleV. viniferafruits: membrane transports as switches of the double sigmoidal growth

Abstract

By revealing that the grape berry loses one H+ per accumulated sucrose at the inception of ripening, adopting a single fruit paradigm elucidates the fundamentals of the malate-sugar nexus, previously obscured by asynchrony in population-based models of ripening. More broadly, the development of the individual fruit was revisited from scratch to capture the simultaneous changes in gene expression and metabolic fluxes in a kinetically relevant way from flowering to overripening. Dynamics in water, tartrate, malate, hexoses, and K+ fluxes obtained by combining individual single fruit growth and concentration data allowed to define eleven sub-phases in fruit development, which distributed on a rigorous curve in RNAseq PCA. WGCNA achieved unprecedented time resolutions in exploring transcript level-metabolic rate associations. A comprehensive set of membrane transporters was found specifically expressed during the first growth phase related to vacuolar over-acidification. Unlike in slightly more acidic citrus, H+ V-PPase transcripts were predominantly expressed, followed by V-ATPase and PH5, clarifying the thermodynamic limit beyond which replacement by the PH1/PH5 complex turns compulsory. Puzzlingly, bona fide ALMT kept a low profile at this stage, possibly replaced by a predominating uncharacterized anion channel. Then, the switch role of HT6 in sugar accumulation was confirmed, electroneutralized by malate vacuolar leakage and H+ pumps activation.