TOMATO AGAMOUS‐LIKE 1 is a component of the fruit ripening regulatory network

Abstract

SUMMARYAfter fertilization, the expanding carpel of fleshy fruit goes through a phase change to ripening. Although the role of ethylene signalling in mediating climacteric ripening has been established, knowledge regarding the regulation of ethylene biosynthesis and its association with fruit developmental programs is still lacking. A functional screen of tomato transcription factors showed that silencing of the TOMATO AGAMOUS-LIKE 1 (TAGL1) MADS box gene results in altered fruit pigmentation. Over-expressing TAGL1 as a chimeric repressor suggested a role in controlling ripening, as transgenic tomato fruit showed reduced carotenoid and ethylene levels, suppressed chlorophyll breakdown, and down-regulation of ripening-associated genes. Moreover, fruits over-expressing TAGL1 accumulated more lycopene, and their sepals were swollen, accumulated high levels of the yellow flavonoid naringenin chalcone and contained lycopene. Transient promoter-binding assays indicated that part of the TAGL1 activity in ripening is executed through direct activation of ACS2, an ethylene biosynthesis gene that has recently been reported to be a target of the RIN MADS box factor. Examination of the TAGL1 transcript and its over-expression in the rin mutant background suggested that RIN does not regulate TAGL1 or vice versa. The results also indicated RIN-dependent and -independent processes that are regulated by TAGL1. We also noted that fruit of TAGL1 loss-of-function lines had a thin pericarp layer, indicating an additional role for TAGL1 in carpel expansion prior to ripening. The results add a new component to the current model of the regulatory network that controls fleshy fruit ripening and its association with the ethylene biosynthesis pathway.

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

“…Moreover, the binding of RIN to its target promoters was shown to be dependent on CNR activity, suggesting that CNR or one of its targets is required in a functional complex with RIN (Martel et al, 2011). The SHP1 ortholog TAGL1 has been reported to play an important role in tomato fruit development and ripening (Itkin et al, 2009;Vrebalov et al, 2009). TAGL1 knockdown plants were found to produce yelloworange fruits with reduced carotenoids and thin pericarps.…”

“…However, MT plants harbor four independent mutations, including one in the brassinosteroid pathway (Martí et al, 2006), which may influence tomato development and ripening. For example, the size of MT fruits is quite variable, and silencing of TAGL1 did not lead to reduced pericarp thickness in MT, but showed this phenotype only in the nondwarf variety Ailsa Craig (Itkin et al, 2009;Vrebalov et al, 2009). To investigate if the phenotype of the MT FUL1/2 silenced fruits was reproducible in a nondwarf variety, we crossed lines R1-10 and R1-29 with Ailsa Craig plants and determined the fruit phenotype of the F1 offspring ( Figure 2G), in which the MT mutations are in a recessive state.…”

“…A number of genes involved in the carotenoid biosynthesis pathway have been shown to be induced at the MG-to-Br stage transition (Alba et al, 2005;Itkin et al, 2009;Vrebalov et al, 2009). These include PSY1, which regulates the conversion of phytoene and is highly downregulated in TAGL1 silenced plants (Itkin et al, 2009;Vrebalov et al, 2009), and DXS1 (Lois et al, 2000), which is required for the first step in the carotenoid biosynthesis pathway.…”

“…They have low ethylene levels due to decreased expression of the RIN target ACS2, and TAGL1 thus appears to regulate ripening by inducing the autocatalytic ethylene production system 2 together with RIN. Itkin et al (2009) studied TAGL1 overexpression in the rin mutant background and found evidence for RINdependent and RIN-independent functions of TAGL1.…”

Network Inference Analysis Identifies an APRR2-Like Gene Linked to Pigment Accumulation in Tomato and Pepper Fruits

“…Mutations at these loci can completely abolish normal ripening (Lanahan et al, 1994;Vrebalov et al, 2002;Manning et al, 2006). The NR, RIN, CNR, and NOR gene products, along with those from tomato HD-Zip homeobox protein1 (LeHB1), Tomato AGAMOUS-LIKE1 (TAGL1), APETALA2 (AP2; Lin et al, 2008;Itkin et al, 2009;Vrebalov et al, 2009;Chung et al, 2010;Karlova et al, 2011), and others govern the onset and progression of the ripening. Despite a growing understanding of this high-level regulatory network, the links to hormonal cues, plastid signals, and downstream effectors mediating alterations in color, texture, and flavor are still poorly understood.…”