Loss of DET1 in High Pigment 2 Tomato Prevents High Temperature Repression of Anthocyanin Biosynthesis in Fruit Through HY5 Stabilization

Global warming impacts several aspects of plant physiology, with important negative effects on crop yield and production of secondary metabolites, such as anthocyanins. The anthocyanin content of vegetables and fruits has attracted public interest in the last two decades due to its health benefits, leading to the development of novel anthocyanin-enriched plant varieties, including purple tomato lines. In purple tomato fruits anthocyanin biosynthesis is largely regulated by light through HY5, whose levels are in turn controlled by COP1-targeted destabilization, and increasing temperatures strongly impair anthocyanin accumulation in the fruit peel. Interestingly, two different COP1-encoding genes exist in tomato and one of them is further involved in alternative splicing, giving origin to polypeptides characterized by different lengths and, possibly, functions. High temperatures trigger HY5 degradation under light through nuclear relocation and interaction with DET1 of both COP1 tomato factors. high pigment 2 (hp2) tomato plants bear a nonfunctional det1 allele and show exacerbate photomorphogenesis due to HY5 stabilization. In this paper, we show that the COP1-DET1-HY5 switch is crucial for the high temperature-induced repression of anthocyanin synthesis in purple fruits. The loss of DET1 indeed impedes COP1 activity in degrading HY5, allowing sustained anthocyanin accumulation under light even under high temperatures. All COP1 tomato factors seem to require DET1 to target HY5 to proteolysis, but only COP1-like X1 isoform gene is also transcriptionally regulated by HY5, whereas the expression of COP1 homolog is not affected by the mutation of DET1. Furthermore, whereas the expression of COP1 homolog is stable and independent from temperature, the canonical transcript of COP1-like X1 isoform, possibly producing the polypeptide containing all the functional domains, is also enhanced by higher temperatures. The introgression of the hp2 mutation in purple tomato lines can thus counteract the high temperature-induced reduction in anthocyanin accumulation, representing a key strategy to preventing global warming-related loss of quality in tomatoes.