Woolly mutation with Get02 locus overcomes the polygenic nature of trichome-based pest resistance in tomato

Abstract

ABSTRACT Type-IV glandular trichomes, which only occur in the juvenile phase of tomato development, produce acylsugars (AS) that broadly protect against arthropod herbivory. Previously, we introgressed the capacity to retain type-IV trichomes in the adult phase from Solanum galapagense into the cv. Micro-Tom (MT). The resulting MT- Get line contained five loci associated with enhancing the density of type-IV trichomes in adult plants. We genetically dissected MT- Get and obtained a sub-line containing only the locus on chromosome 2 (MT- Get02 ). This genotype displayed about half the density of type-IV trichomes compared to the wild progenitor. However, when we stacked the gain-of-function allele of WOOLLY , which codes for a HD-ZIP IV transcription factor, MT- Get02/Wo exhibited double the number of type-IV trichomes compared to S. galapagense . This discovery corroborates previous reports positioning WOOLLY as a master regulator of trichome development. AS levels in MT- Get02/Wo were comparable to the wild progenitor, although the composition of AS types differed, especially regarding less AS with medium-length acyl chains. Agronomical parameters of MT- Get02/Wo , including yield, were comparable to MT. Pest resistance assays showed enhanced protection against whitefly, caterpillar, and the fungus Septoria lycopersici . However, resistance levels did not reach that of the wild progenitor, suggesting the specificity of particulars AS types in the pest resistance mechanism. Our findings in trichome-mediated resistance advance the development of robust, naturally resistant tomato varieties, harnessing the potential of natural genetic variation. Moreover, by manipulating only two loci, we achieved exceptional results for a highly complex, polygenic trait, such as herbivory resistance in tomato.