(M.L.); 0000-0002-5725-885X (J.P.); 0000-0001-7707-7776 (J.-P.R.).The plant hormone ethylene plays a key role in climacteric fruit ripening. Studies on components of ethylene signaling have revealed a linear transduction pathway leading to the activation of ethylene response factors. However, the means by which ethylene selects the ripening-related genes and interacts with other signaling pathways to regulate the ripening process are still to be elucidated. Using tomato (Solanum lycopersicum) as a reference species, the present review aims to revisit the mechanisms by which ethylene regulates fruit ripening by taking advantage of new tools available to perform in silico studies at the genomewide scale, leading to a global view on the expression pattern of ethylene biosynthesis and response genes throughout ripening. Overall, it provides new insights on the transcriptional network by which this hormone coordinates the ripening process and emphasizes the interplay between ethylene and ripening-associated developmental factors and the link between epigenetic regulation and ethylene during fruit ripening.As a developmental process, fruit ripening is coordinated by a complex network of endogenous and exogenous cues. Indeed, the making of a fruit is a genetically regulated process unique to plants involving three distinct stages: fruit set, development, and ripening. Fruit development is characterized by a series of developmental transitions tightly coordinated by a network of interacting genes and signaling pathways. Among these, ripening has received the greatest attention from both geneticists and breeders. From the scientific point of view, fruit ripening is seen as a process in which the biochemistry and physiology of the organ are developmentally altered to influence the appearance, texture, flavor, and aroma (Giovannoni, 2004). Since most of the fruit sensory and nutritional quality traits are elaborated at the ripening stage, deciphering the key genetic and molecular factors regulating ripening becomes a major task toward improving overall fruit quality (Carrari and Fernie, 2006). In addition, the control of fruit ripening is also instrumental to maintain the quality attributes of the fruit during the postharvest shelf life.Based on their mode of ripening, fleshy fruits are divided into two categories, climacteric and nonclimacteric, depending on the presence or absence of the climacteric rise in respiration and of autocatalytic ethylene production (Lelièvre et al., 1997). In climacteric fruit, the plant hormone ethylene is the major cue that controls most aspects of ripening. By contrast, the ripening of nonclimacteric fruit does not strictly depend on ethylene, and the nature of the triggers of ripening in this type of fruit remains yet to be elucidated. Since the upstream components of the ethylene transduction pathway are common to all ethylene responses, the apparent simplicity of the ethylene signaling pathway cannot account for the wide diversity of ethylene responses. A plausible hypothesis is that dif...
1 2While the grape has been classified as a non-climacteric fruit whose ripening is 3 thought to be ethylene independent, we show here that a transient increase of endogenous 4 ethylene production occurs just before veraison (i.e. inception of ripening). We observed that 5 ethylene perception, at this time, is required for at least the increase of berry diameter, the 6 decrease of berry acidity and anthocyanin accumulation in the ripening berries; these latter 7 experiments were performed with 1-methylcyclopropene, a specific inhibitor of ethylene 8 receptors. The potential roles of ethylene in berry development and ripening are discussed. 9 10
Successful completion of fruit developmental programs depends on the interplay between multiple phytohormones. However, besides ethylene, the impact of other hormones on fruit quality traits remains elusive. A previous study has shown that downregulation of SlARF4, a member of the tomato (Solanum lycopersicum) auxin response factor (ARF) gene family, results in a darkgreen fruit phenotype with increased chloroplasts (Jones et al., 2002). This study further examines the role of this auxin transcriptional regulator during tomato fruit development at the level of transcripts, enzyme activities, and metabolites. It is noteworthy that the dark-green phenotype of antisense SlARF4-suppressed lines is restricted to fruit, suggesting that SlARF4 controls chlorophyll accumulation specifically in this organ. The SlARF4 underexpressing lines accumulate more starch at early stages of fruit development and display enhanced chlorophyll content and photochemical efficiency, which is consistent with the idea that fruit photosynthetic activity accounts for the elevated starch levels. SlARF4 expression is high in pericarp tissues of immature fruit and then undergoes a dramatic decline at the onset of ripening concomitant with the increase in sugar content. The higher starch content in developing fruits of SlARF4 down-regulated lines correlates with the up-regulation of genes and enzyme activities involved in starch biosynthesis, suggesting their negative regulation by SlARF4. Altogether, the data uncover the involvement of ARFs in the control of sugar content, an essential feature of fruit quality, and provide insight into the link between auxin signaling, chloroplastic activity, and sugar metabolism in developing fruit.
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