The Tomato FRUITFULL Homologs TDR4/FUL1 and MBP7/FUL2 Regulate Ethylene-Independent Aspects of Fruit Ripening

Abstract

Tomato (Solanum lycopersicum) contains two close homologs of the Arabidopsis thaliana MADS domain transcription factor FRUITFULL (FUL), FUL1 (previously called TDR4) and FUL2 (previously MBP7). Both proteins interact with the ripening regulator RIPENING INHIBITOR (RIN) and are expressed during fruit ripening. To elucidate their function in tomato, we characterized single and double FUL1 and FUL2 knockdown lines. Whereas the single lines only showed very mild alterations in fruit pigmentation, the double silenced lines exhibited an orange-ripe fruit phenotype due to highly reduced lycopene levels, suggesting that FUL1 and FUL2 have a redundant function in fruit ripening. More detailed analyses of the phenotype, transcriptome, and metabolome of the fruits silenced for both FUL1 and FUL2 suggest that the genes are involved in cell wall modification, the production of cuticle components and volatiles, and glutamic acid (Glu) accumulation. Glu is responsible for the characteristic umami taste of the present-day cultivated tomato fruit. In contrast with previously identified ripening regulators, FUL1 and FUL2 do not regulate ethylene biosynthesis but influence ripening in an ethylene-independent manner. Our data combined with those of others suggest that FUL1/2 and TOMATO AGAMOUS-LIKE1 regulate different subsets of the known RIN targets, probably in a protein complex with the latter.

TomatoFRUITFULLhomologs regulate fruit ripening via ethylene biosynthesis

“…Moreover, in vivo analysis revealed that the FUL homologs bind to the promoters of the two genes that encode a rate-limiting enzyme for ripening-associated ethylene production, 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS2 and ACS4). 21,22) These results strongly suggest that the FUL homologs are involved in ripening-associated ethylene production, though this is inconsistent with a result described by Bemer et al 19) To verify the possibility that the FUL homologs regulate ethylenedependent ripening through transcriptional regulation of the 1-aminocyclopropane-1-carboxylic acid synthase (ACS) genes, we independently developed FUL1/FUL2 co-suppression lines. In this report, we describe the phenotype of the transgenic lines, which showed defects in ripening and produced ethylene at very low levels, indicating the involvement of FUL1/FUL2 in ripening-associated ethylene production.…”

“…Bemer et al 19) have conducted a co-suppression analysis of FUL1 and FUL2 in tomato, and they found that the homologs are redundantly involved in the regulation of fruit ripening, as in our study. However, substantial differences exist between the results of the two studies.…”

“…These efforts identified TAGL1, a MADSbox gene encoding a SHATTERPROOF (SHP) homolog, as a regulator of fruit ripening through ethylene production. [16][17][18] Additionally, Bemer et al 19) reported that two MADS-box genes encoding FRUITFULL homologs (FUL1 and FUL2, previously called TDR4 and SlMBP7, respectively) redundantly regulate fruit ripening. They reported that, unlike ripening regulation by RIN and TAGL1, the FUL homologs regulate only ethylene-independent ripening, because their transgenic lines, containing an RNAi construct designed to suppress FUL1 and FUL2, produced ethylene at levels equal to the wild type.…”

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

“…Reduced expression of these TFs in response to chilling would be expected to globally reduce many ripening-associated processes, permitting the organ to redirect metabolic resources into more suitable stress responses. In addition to these TFs, transcripts of FUL1, a RIN-interacting MADS domain protein affecting aspects of ripening, including volatile synthesis (42), as well as HB-1, a positive regulator of ethylene synthesis (43), are down during chilling. Expression of other TFs that regulate specific aspects of fruit development, including TAGL1 (44,45) and AP2a (46,47), increased during chilling.…”

Banana MaMADS Transcription Factors Are Necessary for Fruit Ripening and Molecular Tools to Promote Shelf-Life and Food Security

“…Banana and tomato fruit exhibit climacteric (elevated) respiration and a surge in ethylene hormone production concomitant with ripening (Seymour, 1993;Klee and Giovannoni, 2011), and tomato genes necessary for ethylene production and climacteric respiration have been identified (Alexander and Grierson, 2002;Giovannoni, 2007;Pirrello et al, 2009). Among them are several MADS box genes: SlMADS-RIN of the SEPALLATA (SEP) E function clade (Vrebalov et al, 2002;Ito et al, 2008;Zhong et al, 2013); FRUIFULL (FUL1 and FUL2) homologs (Bemer et al, 2012;Shima et al, 2014); and TAGL1, an AGAMOUS (AG)-like MADS box gene necessary for both early fruit expansion and later ripening (Itkin et al, 2009;Vrebalov et al, 2009). The SlMADS-RIN protein interacts with additional MADS box proteins, including TAGL1 and SlTAGL11 (Leseberg et al, 2008) and the tomato FUL homologs FUL1 and FUL2, to execute ripening (Martel et al, 2011;Fujisawa et al, 2014).…”