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The Deubiquitinase SlOTU9 Positively Regulates Tomato Fruit Softening by Modulating the Abundance of Cell Wall-Modifying Enzymes

ABSTRACT: Fruit softening is a critical aspect of ripening that determines shelf life and quality but is mechanistically complex. While transcriptional regulation of cell wall-modifying enzymes (CWMEs) is well-studied, post-translational control remains poorly understood. Here, we identify and characterize SlOTU9, a tomato (Solanum lycopersicum) Ovarian Tumor (OTU) domain-containing deubiquitinase (DUB), as a key positive regulator of fruit softening. SlOTU9 gene expression is significantly upregulated during fruit ripening. Overexpression of SlOTU9 in tomato resulted in accelerated fruit softening and reduced shelf life, whereas its knockout via CRISPR-Cas9 led to firmer fruit. Quantitative proteomic analysis revealed that SlOTU9 overexpression significantly increased the abundance of several key CWMEs at the breaker+7 stage, including multiple pectate lyases (PLs), without a corresponding increase in their transcript levels. We further demonstrate that SlOTU9 physically interacts with a pectate lyase (SlPL16) and that both proteins co-localize at the cell wall and plasma membrane. Our findings reveal a novel post-translational regulatory layer where SlOTU9 enhances the protein abundance of CWMEs to promote cell wall disassembly. This work identifies SlOTU9 as a potential target for molecular breeding strategies aimed at precisely controlling fruit texture and improving postharvest longevity.

ORGANISM(S): Solanum Lycopersicum

SUBMITTER: Zhiping Deng

PROVIDER: PXD065934 | iProX | Wed Jul 09 00:00:00 BST 2025

REPOSITORIES: iProX

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Project description:Tomato fruit ripening is under the control of ethylene as well as a group of ethylene-independent transcription factors, including NON-RIPENING (NOR) and RIPENING INHIBITOR (RIN). During ripening, the linear carotene lycopene accumulates at the expense of cyclic carotenoids. Fruit-specific overexpression of LYCOPENE β-CYCLASE (LCYb) under the control of the PHYTOENE DESATURASE (PDS) promoter resulted in increased levels of β-carotene and ABA and in decreased ethylene levels. Genes regulated by ABA, or involved in its synthesis and signaling, were overexpressed, while those associated with ethylene and cell wall remodeling were repressed. In agreement with the transcriptional data, LCYb-overexpressing fruits exhibited increased density of cell wall material containing linear, under-methylated pectins and displayed an array of additional ripening phenotypes, including delayed softening, increased turgor, enhanced shelf life and a thicker cuticle with a higher content of cutin monomers and triterpenoids. The levels of several primary metabolites and phenylpropanoids also changed in the transgenics, which could be attributed to delayed fruit ripening and to ABA respectively. Network correlation analysis suggests that ABA, acting through NOR and RIN, is responsible for many of the above phenotypes. These data reinforce suggestions that ABA plays an important role in tomato fruit ripening and provide clues that fruit b-carotene, acting as a precursor for ABA, actively participates in controlling the ripening process rather than merely being an output thereof. Overexpression of a LCYb gene from Arabidopsis under the control of the ripening-associated PDS promoter leads to ripe tomato fruits accumulating high β-carotene levels. Using several independent transgenic lines, we conducted a system-wide study of the effect of increased β-carotene levels on tomato fruit ripening and shelf life. Our data suggest that β-carotene, acting through ABA, is involved in a regulatory loop within the network controlling tomato fruit ripening.

Dataset Information

The Deubiquitinase SlOTU9 Positively Regulates Tomato Fruit Softening by Modulating the Abundance of Cell Wall-Modifying Enzymes

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