The Tomato Hybrid Proline-rich Protein regulates the abscission zone competence to respond to ethylene signals

Abstract

The Tomato Hybrid Proline-rich Protein (<i>THyPRP</i>) gene was specifically expressed in the tomato (<i>Solanum lycopersicum</i>) flower abscission zone (FAZ), and its stable antisense silencing under the control of an abscission zone (AZ)-specific promoter, <i>Tomato Abscission Polygalacturonase4</i>, significantly inhibited tomato pedicel abscission following flower removal. For understanding the THyPRP role in regulating pedicel abscission, a transcriptomic analysis of the FAZ of <i>THyPRP</i>-silenced plants was performed, using a newly developed AZ-specific tomato microarray chip. Decreased expression of <i>THyPRP</i> in the silenced plants was already observed before abscission induction, resulting in FAZ-specific altered gene expression of transcription factors, epigenetic modifiers, post-translational regulators, and transporters. Our data demonstrate that the effect of <i>THyPRP</i> silencing on pedicel abscission was not mediated by its effect on auxin balance, but by decreased ethylene biosynthesis and response. Additionally, <i>THyPRP</i> silencing revealed new players, which were demonstrated for the first time to be involved in regulating pedicel abscission processes. These include: gibberellin perception, Ca²⁺-Calmodulin signaling, Serpins and Small Ubiquitin-related Modifier proteins involved in post-translational modifications, Synthaxin and SNARE-like proteins, which participate in exocytosis, a process necessary for cell separation. These changes, occurring in the silenced plants early after flower removal, inhibited and/or delayed the acquisition of the competence of the FAZ cells to respond to ethylene signaling. Our results suggest that THyPRP acts as a master regulator of flower abscission in tomato, predominantly by playing a role in the regulation of the FAZ cell competence to respond to ethylene signals.