A SIMYB75-centred transcriptional cascade regulates trichome formation and sesquiterpene accumulation in tomato

Tomato trichomes act as a mechanical and chemical barrier against pests. An R2R3 MYB transcription factor gene, SIMYB75, is highly expressed in type II, V, and VI trichomes. SIMYB75 protein is located in the nucleus and possesses transcriptional activation activity. Down-regulation of SIMYB75 increased the formation of type II, V, and VI trichomes, accumulation of delta-elemene, beta-caryophyllene, and alpha-humulene in glandular trichomes, and tolerance to spider mites in tomato. In contrast, overexpression of SIMYB75 inhibited trichome formation and sesquiterpene accumulation, and increased plant sensitivity to spider mites. RNA-Seq analyses of the SIMYB75 RNAi line indicated massive perturbation of the transcriptome, with a significant impact on several classes of transcription factors. Expression of the MYB genes SIMYB52 and SITHM1 was strongly reduced in the RNAi line and increased in the SIMYB75-overexpressing line. SIMYB75 protein interacted with SIMYB52 and SITHM1 and activated their expression. SIMYB75 directly targeted the promoter of the cyclin gene SICycB2, increasing its activity. The auxin response factor SIARF4 directly targeted the promoter of SIMYB75 and inhibited its expression. SIMYB75 also bound to the promoters of the terpene synthase genes SITPS12, SITPS31, and SITPS35, inhibiting their transcription. Our findings indicate that SIMYB75 perturbation affects several transcriptional circuits, resulting in altered trichome density and metabolic content.

Automated summary

The SIMYB75 gene plays a crucial role in tomato trichomes, with down-regulation increasing trichome formation and tolerance to spider mites, while overexpression inhibits these processes. The perturbation of SIMYB75 affects multiple transcriptional circuits, resulting in changes in trichome density and metabolic content.