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SUMMARY: The plant cuticle is composed of cuticular wax and cutin polymers and plays an essential role in plant tolerance to diverse abiotic and biotic stresses. Several stresses, including water deficit and salinity, regulate the synthesis of cuticular wax and cutin monomers. However, the effect of wounding on wax and cutin monomer production and the associated molecular mechanisms remain unclear. In this study, we determined that the accumulation of wax and cutin monomers in Arabidopsis leaves is positively regulated by wounding primarily through the jasmonic acid (JA) signaling pathway. Moreover, we observed that a wound‐ and JA‐responsive gene (CYP96A4) encoding an ER‐localized cytochrome P450 enzyme was highly expressed in leaves. Further analyses indicated that wound‐induced wax and cutin monomer production was severely inhibited in the cyp96a4 mutant. Furthermore, CYP96A4 interacted with CER1 and CER3, the core enzymes in the alkane‐forming pathway associated with wax biosynthesis, and modulated CER3 activity to influence aldehyde production in wax synthesis. In addition, transcripts of MYC2 and JAZ1, key genes in JA signaling pathway, were significantly reduced in cyp96a4 mutant. Collectively, these findings demonstrate that CYP96A4 functions as a cofactor of the alkane synthesis complex or participates in JA signaling pathway that contributes to cuticular wax biosynthesis and cutin monomer formation in response to wounding. Significance Statement: Plant cuticle is a lipidic barrier composed of cuticular wax and cutin polymers. Cuticle plays a critical role in protecting plants from various biotic and abiotic stresses. Wounds due to mechanical damage or insect feeding are common and are potentially harmful to plants. However, the effect of wounding on plant cuticular wax and cutin monomer biosynthesis remains unclear. In our study, the findings present the validation that the Arabidopsis cuticle development was positively regulated by wounding mainly through the jasmonic acid (JA) signaling pathway. We also characterized the wound‐ and JA‐responsive gene CYP96A4, which is required for wound‐ and JA‐induced synthesis of cuticular wax and cutin monomer. [ABSTRACT FROM AUTHOR]

The plant cuticle, consisting of wax and cutin, is involved in adaptations to various environments. β-Ketoacyl-CoA synthases (KCSs) usually serve as a component of the fatty acid elongation complex that participates in the production of very long-chain fatty acids and provides precursors for the synthesis of various lipids, including wax; however, we recently reported that KCS3 and KCS12 negatively regulate wax biosynthesis. In this current study, we observed that unlike KCS3 -overexpressing (OE) lines, KCS12 -OE lines had fused floral organs because of abnormal cuticle biosynthesis. This prompted us to compare the functions of KCS3 and KCS12 during cuticle formation. Mutation of KCS3 caused greater effects on wax production, whereas mutation of KCS12 exerted more severe effects on cutin synthesis. The double-mutant kcs3 kcs12 had significantly increased wax and cutin contents compared to either single-mutant, suggesting that KCS12 and KCS3 have additive effects on cuticle biosynthesis. Cuticle permeability was greater for the double-mutant than for the single mutants, which ultimately led to increased susceptibility to drought stress and floral-organ fusion. Taken together, our results demonstrate the regulatory roles of KCS3 and KCS12 during cuticle biosynthesis, and show that maintaining KCS3 and KCS12 expression at certain levels is essential for the formation of a functional cuticle layer. [ABSTRACT FROM AUTHOR]