Timing and Order of the Molecular Events Marking the Onset of Berry Ripening in Grapevine

Abstract

Grapevine () is a model for the investigation of physiological and biochemical changes during the formation and ripening of nonclimacteric fleshy fruits. However, the order and complexity of the molecular events during fruit development remain poorly understood. To identify the key molecular events controlling berry formation and ripening, we created a highly detailed transcriptomic and metabolomic map of berry development, based on samples collected every week from fruit set to maturity in two grapevine genotypes for three consecutive years, resulting in 219 samples. Major transcriptomic changes were represented by coordinated waves of gene expression associated with early development, veraison (onset of ripening)/midripening, and late-ripening and were consistent across vintages. The two genotypes were clearly distinguished by metabolite profiles and transcriptional changes occurring primarily at the veraison/midripening phase. Coexpression analysis identified a core network of transcripts as well as variations in the within-module connections representing varietal differences. By focusing on transcriptome rearrangements close to veraison, we identified two rapid and successive shared transitions involving genes whose expression profiles precisely locate the timing of the molecular reprogramming of berry development. Functional analyses of two transcription factors, markers of the first transition, suggested that they participate in a hierarchical cascade of gene activation at the onset of ripening. This study defined the initial transcriptional events that mark and trigger the onset of ripening and the molecular network that characterizes the whole process of berry development, providing a framework to model fruit development and maturation in grapevine.

Phytohormone profiles are strongly altered during induction and symptom development of the physiological ripening disorder berry shrivel in grapevine

“…3c). Recently, transcriptional biomarkers for the onset of ripening were identified in grapevine and individual ethylene response factors belonged to both negative as well as positive biomarkers (Fasoli et al 2018), which may at least partially explain the observed undetermined expression profile in our study.…”

“…IAA can either be conjugated via ester linkages to glucose by UDP-glucosyl transferases or to amino acids by the Gretchen hagen3 (GH3) family of IAA-amido synthetases, or oxidized via IAA oxidase to form oxIAA, which seems to be the major catabolic pathway (Zhang and Peer 2017). Low auxin levels are necessary to start ripening as indicated by down-regulation of several auxin related and response genes at the onset of ripening (Bottcher et al 2011;Fasoli et al 2018). Only two genes, namely VviIAA19 and VviSAUR29, were identified as positive biomarkers for the onset of ripening (Fasoli et al 2018;Palumbo et al 2014).…”

“…Low auxin levels are necessary to start ripening as indicated by down-regulation of several auxin related and response genes at the onset of ripening (Bottcher et al 2011;Fasoli et al 2018). Only two genes, namely VviIAA19 and VviSAUR29, were identified as positive biomarkers for the onset of ripening (Fasoli et al 2018;Palumbo et al 2014). Both genes, VviSAUR29 (VIT_15s0048g02860) and Vvi-IAA19 (VIT_18s0001g08090), were only slightly induced at EL36/2 in BS berries and no difference in expression was observed at veraison.…”

“…Veraison marks the initiation of sugar accumulation and the rapid pigmentation of berries by anthocyanins in red grape varieties. Grape berry ripening, especially the transition from the first growth phase to ripening related processes later in development, is very complex and just recently this complexity was revealed by applying omics techniques (Fasoli et al 2018;Pilati et al 2017). In general, it is assumed that ABA, ethylene, and brassinosteroids provide the signals for the onset of ripening although the processes are unclear as previously reviewed (Fortes et al 2015;Kuhn et al 2014b).…”

“…Apart from metabolic signals, a timeline of events leading to the onset of ripening was suggested with an initial fall of berry elasticity and turgor pressure followed by ABA and sugar accumulation and coloring pigments in skins of red grape varieties (Castellarin et al 2016). More specifically two rapid transcriptional transitions starting 14 d before veraison have been characterized in grape berries, suggesting a hierarchy of signals for the onset of ripening (Fasoli et al 2018). BS berries have low sugar contents and reduced anthocyanin biosynthesis (Griesser et al 2018), suggesting a disturbed ripening process, which is supported by the transcriptional repression of switch genes in BS berries at veraison (Savoi et al 2019).…”