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Abstract
Fleshy fruit ripening is governed by multiple external and internal cues and accompanied by changes in color, texture, volatiles, and nutritional quality traits. While extended shelf-life and increased phytonutrients are desired, delaying ripening via genetic or postharvest means can be accompanied by reduced nutritional value. Here we report that the high pigment 1 (hp1) mutation at the UV-DAMAGED DNA BINDING PROTEIN 1 (DDB1) locus, previously shown to influence carotenoid and additional phytonutrient accumulation via altered light signal transduction, also results in delayed ripening and firmer texture, resulting at least in part from decreased ethylene evolution. Transcriptome analysis revealed multiple ethylene biosynthesis and signaling-associated genes downregulated in hp1. Furthermore, the hp1 mutation impedes softening of the pericarp, placenta, columella as well as the whole fruit, in addition to reduced expression of the FRUITFUL2 (FUL2) MADS-box transcription factor and xyloglucan endotransglucosylase/hydrolase 5 (XTH5). These results indicate that DDB1 influences a broader range of fruit development and ripening processes than previously thought and present an additional genetic target for increasing fruit quality and shelf-life.
Highlights
As sessile organisms, plants have evolved fleshy fruits to disperse seeds by attracting animals, which consume them and release their seeds
Fruit development was monitored in the hp[1] mutant from 1 cm fruit (7 days post anthesis (DPA)) up to the initial ripening or breaker (BK) stage, showing that ripening initiation was delayed 4–5 days compared to the wild-type (WT) Ailsa Craig (AC) control (Figs. 1 and 2a)
Multiple ripening or pigmentation regulators have been identified by positional cloning of the known mutants[3,13,27,38,39,40], or through functional characterization using reverse genetics approaches[8,9,15,16,41]
Summary
Plants have evolved fleshy fruits to disperse seeds by attracting animals, which consume them and release their seeds. Tomato (Solanum lycopersicum) is a model system for fleshy fruit ripening that, like many fruits, undergoes changes in color, aroma, texture, nutrient composition, and additional quality traits. These changes are coordinated by multiple internal and external factors, including the gaseous hormone ethylene, key transcription factors, epigenetic changes, and environmental stimuli, such as light and temperature[1,2]. Additional MADS-box proteins, TOMATO AGAMOUS-LIKE 1 (TAGL1), FRUITFULL 1 (FUL1), and FRUITFULL 2 (FUL2) interact with RIN to regulate fruit development and ripening[8,9,10,11,12]. Additional MADSbox and non-MADS-box ripening transcription factors, including COLORLESS NON-RIPENING (CNR), APETALA2a (AP2a), STAY-GREEN 1 (SGR1), MADS-box transcription factor MADS1, and HD-Zip homeobox protein HB-113-17, have been characterized in tomato, suggesting multiple, and sometimes interacting, factors mediating genetic control of fruit ripening
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