Two zinc-finger proteins control the initiation and elongation of long stalk trichomes in tomato

Abstract

Plant glandular trichomes are epidermal secretory structures that are important for plant resistance to pests. Although several regulatory genes have been characterized in trichome development, the molecular mechanisms conferring glandular trichome morphogenesis are unclear. We observed the differences in trichomes in cultivated tomato cv. ‘Moneymaker’ (MM) and the wild species Solanum pimpinellifolium PI365967 (PP), and used a recombinant inbred line (RIL) population to identify the genes that control trichome development in tomato. We found that the genomic variations in two genes, HAIR (H) and SPARSE HAIR (SH), contribute to the trichome differences between MM and PP. H and SH encode two paralogous C2H2 zinc-finger proteins that function redundantly in regulating trichome formation. Loss-of-function h/sh double mutants exhibited a significantly decreased number of Type I trichomes and complete loss of long stalk trichomes. Molecular and genetic analyses further indicate that H and SH act upstream of ZFP5. Overexpression of ZFP5 partially restored the trichome defects in NIL-hPPshPP. Moreover, H and SH expression is induced by high temperatures, and their mutations inhibit the elongation of trichomes that reduce the plant repellent to whiteflies. Our findings confirm that H and SH are two vital transcription factors controlling initiation and elongation of Type I and III multicellular trichomes in tomato.