Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation

Abstract

(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...

Comprehensive Profiling of Ethylene Response Factor Expression Identifies Ripening-Associated ERF Genes and Their Link to Key Regulators of Fruit Ripening in Tomato

“…Taking advantage of the recent release of the complete annotated tomato genome sequence (Tomato Genome Consortium, 2012), 77 tomato ERF genes were identified, but knowledge of their physiological significance has been hampered by the functional redundancy among members of this vast gene family. A number of the ERF genes identified in tomato are ethylene inducible and show a ripeningrelated expression pattern that highlights their putative role in fruit ripening (Sharma et al, 2010;Pirrello et al, 2012;Liu et al, 2014Liu et al, , 2015. Consistent with this hypothesis, tomato LeERF1 was reported to mediate the ethylene response, and its overexpression resulted in a constitutive ethylene response and accelerated fruit ripening and softening (Li et al, 2007).…”

Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation

“…Many of the most important regulators of ripening-associated transcription have been identified (25,26). We examined the patterns of expression of a set of the most important TFs controlling ripening and identified several whose transcript abundance was significantly altered in response to chilling (Fig.…”

A Prunus persica genome‐wide RNA‐seq approach uncovers major differences in the transcriptome among chilling injury sensitive and non‐sensitive varieties

“…Current model states that when the ethylene is perceived, the block exerted by mitogen‐activated protein kinases on EIN2 is released, activating a transcriptional cascade (Liu et al ). Once the transcriptional cascade triggered, the primary TFs EIN/EIL are activated.…”