A novel tomato F‐box protein, SlEBF3, is involved in tuning ethylene signaling during plant development and climacteric fruit ripening

Abstract

Ethylene is instrumental to climacteric fruit ripening and EIN3 BINDING F-BOX (EBF) proteins have been assigned a central role in mediating ethylene responses by regulating EIN3/EIL degradation in Arabidopsis. However, the role and mode of action of tomato EBFs in ethylene-dependent processes like fruit ripening remains unclear. Two novel EBF genes, SlEBF3 and SlEBF4, were identified in the tomato genome, and SlEBF3 displayed a ripening-associated expression pattern suggesting its potential involvement in controlling ethylene response during fruit ripening. SlEBF3 downregulated tomato lines failed to show obvious ripening-related phenotypes likely due to functional redundancy among SlEBF family members. By contrast, SlEBF3 overexpression lines exhibited pleiotropic ethylene-related alterations, including inhibition of fruit ripening, attenuated triple-response and delayed petal abscission. Yeast-two-hybrid system and bimolecular fluorescence complementation approaches indicated that SlEBF3 interacts with all known tomato SlEIL proteins and, consistently, total SlEIL protein levels were decreased in SlEBF3 overexpression fruits, supporting the idea that the reduced ethylene sensitivity and defects in fruit ripening are due to the SlEBF3-mediated degradation of EIL proteins. Moreover, SlEBF3 expression is regulated by EIL1 via a feedback loop, which supposes its role in tuning ethylene signaling and responses. Overall, the study reveals the role of a novel EBF tomato gene in climacteric ripening, thus providing a new target for modulating fleshy fruit ripening.

The Involvement of the Banana F-Box Protein MaEBF1 in Regulating Chilling-Inhibited Starch Degradation through Interaction with a MaNAC67-Like Protein

“…In the present work, the expression of MaEBF1 was significantly induced by ETH treatment, which is similar to EBF genes in other fruits, such as SlEBF1/2/3 in tomato [17,52] and MaEBF2 in Cavendish banana fruit [53], indicating that MaEBF1 may be an important player in Fenjiao banana fruit ripening. Additionally, the expression of MaEBF1 was strongly reduced after 12 days at 7 °C, which may be closely related to the fruit ripening problem.…”

A critical evaluation of the role of ethylene and MADS transcription factors in the network controlling fleshy fruit ripening

“…Later important milestones included the identification of multiple 1‐aminocyclopropane‐1‐carboxylate ( ACC ) synthase ( ACS ) and ACC oxidase ( ACO ) genes for ethylene synthesis, first identified in fruit (see Grierson, and references therein), and seven ethylene receptors, which have similarities to those in Arabidopsis (Klee, ; Gapper et al ., ; M. C. Liu et al ., ) and other ripening genes (Davies & Grierson, ). The ethylene signal transduction chain has more components than so far revealed in Arabidopsis (Lin et al ., ; Lin & Grierson, ), with three CTRs (Adams‐Phillips et al ., ), four EIN3‐BINDING PROTEIN ( EBFs ) (Deng et al ., ) and seven EIN3‐LIKEs ( EILs ) (M. C. Liu et al ., ), which may not be functionally redundant: compare Klee & Tieman () and Chen et al . (2004a).…”

“…The view that has emerged is of an interacting network of transcription factors and hormone biosynthesis and signaling genes that orchestrate a cascade of events, culminating in the expression of many hundreds, perhaps thousands, of genes that contribute to the ripening process (M. C. Liu et al ., , ; Giovannoni et al ., ; Shinozaki et al ., ). One new twist to the story has been the demonstration that, although many ERFs do respond to ethylene (M. C. Liu et al ., , ; Deng et al ., ), others actually respond to auxin (Li et al ., ), whereas some are regulated by both hormones (Liu et al ., ).…”

“…C. Liu et al, 2015) and other ripening genes (Davies & Grierson, 1989). The ethylene signal transduction chain has more components than so far revealed in Arabidopsis (Lin et al, 2009;Lin & Grierson, 2010), with three CTRs (Adams-Phillips et al, 2004), four EIN3-BINDING PROTEIN (EBFs) (Deng et al, 2018) and seven EIN3-LIKEs (EILs) (M. C. Liu et al, 2015), which may not be functionally redundant: compare Klee & Tieman (2002) and Chen et al (2004a). These and other important ripening genes are listed in Table 1 and a general outline of the way in which these factors relate to the control of ripening is shown in Fig.…”

Transcriptome analysis provides new insight into the molecular mechanisms in regulating carotenoid accumulation in pericarp of fruits from two pummelo cultivars Citrus grandis (L.) Osbeck

“…EBF belongs to Fbox protein family and acts as a component in SCF complex, this complex could degrade EIN3 protein [54]. Recently, it has been reported that SlEBF3 could interact with all known ethylene insensitive-like proteins (EIL) in tomato fruits and overexpression of SlEBF3 reduced the total SlEIL protein levels [55].…”