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

Abstract

(E.M.); 0000-0001-7707-7776 (J.-P.R.); 0000-0002-5725-885X (J.P.).Our knowledge of the factors mediating ethylene-dependent ripening of climacteric fruit remains limited. The transcription of ethylene-regulated genes is mediated by ethylene response factors (ERFs), but mutants providing information on the specific role of the ERFs in fruit ripening are still lacking, likely due to functional redundancy among this large multigene family of transcription factors. We present here a comprehensive expression profiling of tomato (Solanum lycopersicum) ERFs in wild-type and tomato ripening-impaired tomato mutants (Never-ripe [Nr], ripening-inhibitor [rin], and non-ripening [nor]), indicating that out of the 77 ERFs present in the tomato genome, 27 show enhanced expression at the onset of ripening while 28 display a ripeningassociated decrease in expression, suggesting that different ERFs may have contrasting roles in fruit ripening. Among the 19 ERFs exhibiting the most consistent up-regulation during ripening, the expression of 11 ERFs is strongly down-regulated in rin, nor, and Nr tomato ripening mutants, while only three are consistently up-regulated. Members of subclass E, SlERF.E1, SlERF.E2, and SlERF.E4, show dramatic down-regulation in the ripening mutants, suggesting that their expression might be instrumental in fruit ripening. This study illustrates the high complexity of the regulatory network connecting RIN and ERFs and identifies subclass E members as the most active ERFs in ethylene-and RIN/NOR-dependent ripening.The plant hormone ethylene is involved in a wide range of developmental processes and physiological responses such as flowering, fruit ripening, organ senescence, abscission, root nodulation, seed germination, programmed cell death, cell expansion, and responses to abiotic stresses and pathogen attacks. In the last decades, tremendous progress has been made toward deciphering the mechanisms by which plants perceive and respond to ethylene (Benavente and Alonso, 2006;Ju et al., 2012). Studies on components of ethylene signaling have revealed a linear transduction pathway that ultimately leads to the activation of transcriptional regulators belonging to the ethylene response factor (ERF) family of transcription factors. While the upstream components of the ethylene transduction pathway are common to all ethylene responses, the apparent simplicity of the hormone signaling pathway cannot account for the wide diversity and specificity of biological responses. ERFs are one of the largest families of plant transcription factors, and in this regard, they represent a suitable step where the diversity and specificity of ethylene responses can be expressed. These downstream components of ethylene signaling are the main mediators of ethylenedependent gene transcription.Considering the importance of fleshy fruits for a healthy diet and the prominent role assigned to ethylene in the control of fruit ripening, substantial advances have been made to uncover the molecular mechanisms that control fruit development...

Tomato SlERF.A1, SlERF.B4, SlERF.C3 and SlERF.A3, Members of B3 Group of ERF Family, Are Required for Resistance to Botrytis cinerea

“…Recent genome-wide bioinformatics analyses identified a total of 146 members in the tomato AP2/ERF superfamily, of which 77 members belong to the ERF family (Sharma et al, 2010; Pirrello et al, 2012; Liu et al, 2016). Expression profiling analyses revealed that a large set of the tomato ERF genes are differentially induced by developmental cues, hormones and various stress factors (Gu et al, 2000; Tournier et al, 2003; Sharma et al, 2010; Pirrello et al, 2012).…”

“…Expression profiling analyses revealed that a large set of the tomato ERF genes are differentially induced by developmental cues, hormones and various stress factors (Gu et al, 2000; Tournier et al, 2003; Sharma et al, 2010; Pirrello et al, 2012). Functional studies have characterized a number of tomato ERF genes, e.g., SlERF1, Sl-ERF2, TSRF1, SlAP2a, Sl-ERF.B3, SlERF6, SlERF36 , and SlERF52 , that play important roles in regulating growth and developmental processes including seed germination, seedling development, stomatal density, fruit ripening, and flower pedicel abscission (Pirrello et al, 2006; Li et al, 2007; Zhang et al, 2008, 2009; Chung et al, 2010; Lee et al, 2012; Liu et al, 2013, 2016; Upadhyay et al, 2013; Liu M. et al, 2014; Nakano et al, 2014). Whereas TERF1, TERF2, TSRF1, JERF1, JERF3, LeERF3b, Sl-ERF.B.3 , and ERF5 were found to be involved in regulating abiotic stress response (Huang et al, 2004; Wang et al, 2004; Zhang et al, 2004a,b, 2007, 2010; Chen et al, 2008; Wu et al, 2008; Quan et al, 2010; Zhang and Huang, 2010; Tian et al, 2011; Pan et al, 2012; Klay et al, 2014), Pti4, Pti5, Pti6, TSRF1 , and SlERF3 have been demonstrated to play key roles in regulating defense responses against pathogens and insect pests (Zhou et al, 1997; He et al, 2001; Gu et al, 2002; Wu et al, 2002, 2015; Zhang et al, 2004b, 2007; Pan et al, 2010).…”

“…Whereas TERF1, TERF2, TSRF1, JERF1, JERF3, LeERF3b, Sl-ERF.B.3 , and ERF5 were found to be involved in regulating abiotic stress response (Huang et al, 2004; Wang et al, 2004; Zhang et al, 2004a,b, 2007, 2010; Chen et al, 2008; Wu et al, 2008; Quan et al, 2010; Zhang and Huang, 2010; Tian et al, 2011; Pan et al, 2012; Klay et al, 2014), Pti4, Pti5, Pti6, TSRF1 , and SlERF3 have been demonstrated to play key roles in regulating defense responses against pathogens and insect pests (Zhou et al, 1997; He et al, 2001; Gu et al, 2002; Wu et al, 2002, 2015; Zhang et al, 2004b, 2007; Pan et al, 2010). Among the characterized tomato ERF genes, seven of them including Pti4, Pti5, LeERF1, LeERF4 ( Sl-ERF.B3 ), TSRF1, TERF1 , and ERF5 are members of the B3 group (Zhou et al, 1997; Tournier et al, 2003; Huang et al, 2004; Zhang et al, 2004a,b, 2007; Pan et al, 2012; Liu et al, 2013, 2016; Liu M. et al, 2014). Here, we performed virus-induced gene silencing (VIGS)-based functional analyses of 18 members in the B3 group members of the tomato ERF family to explore their possible involvement in disease resistance against B. cinerea .…”

Banana Transcription Factor MaERF11 Recruits Histone Deacetylase MaHDA1 and Represses the Expression of MaACO1 and Expansins during Fruit Ripening

“…For example, there are 85 members of ERFs in tomato using raw EST data in various public repositories, among which 57 ERFs were found to be differentially expressed during temporal stages of tomato fruit development (Sharma et al, 2010). More recently, the TomExpress on-line tool revealed that 55 out of 77 ERF family genes display a ripening-associated expression pattern, with 27 being up-regulated during ripening and the remaining 28 being down-regulated, indicating that different ERFs may have diverse roles in fruit ripening (Liu et al, 2016). A recent study demonstrated that MaERF11 was down-regulated in peel and pulp of banana fruit during ripening and after being treated with ethylene (Xiao et al, 2013), suggesting that MaERF11 may play a role in fruit ripening.…”

The glycerol-3-phosphate acyltransferase GPAT6 from tomato plays a central role in fruit cutin biosynthesis

“…To our knowledge, most of these have not been associated previously with the fruit epidermis/cuticle; however, several are known to regulate early fruit development, including the MADS box gene TAGL11 (Mejía et al, 2011), or fruit ripening, such as the MADS box gene RIPENING INHIBITOR (RIN [Solyc05g012020]; Vrebalov et al, 2002;Kosma et al, 2010), as well as several ethylene-responsive TFs (Liu et al, 2016). The differentially expressed TFs included those with a possible link to the circadian clock, with two genes (Solyc01g095030 and Solyc10g084370) encoding MYB-related TFs of the REVEILLE family (Farinas and Mas, 2011), one of which was expressed at lower levels in gpat6-a, and six genes encoding CONSTANS-like TFs (Valverde, 2011), one of which (Solyc12g005660) was expressed at much lower levels.…”