Heat stress induces a developmental shift from type-V to type-IV trichome dependent on jasmonate signaling in tomato

Abstract

Cultivated tomato (Solanum lycopersicum) and related wild species develop several types of trichomes, both glandular and non-glandular, on their aerial parts. Among these, type-IV trichomes are responsible for the synthesis and secretion of acylsugars, which act as defense compounds against herbivores. In contrast to related wild species such as S. pennellii, type-IV trichomes are present only in the juvenile stages of cultivated tomato plants and absent in later stages of development. By submitting tomato plants to high temperatures during the day (37 {degrees}C), we observe that non-glandular type-V trichomes are replaced by type-IV trichomes. This is accompanied by a massive increase in acylsugar production. On the other hand, heat treatment does not affect type VI-trichomes, which produce mono- and sesquiterpenes, but the production of monoterpenes is increased while that of sesquiterpenes is suppressed. Furthermore, tomato jai1 mutants deficient in jasmonate (JA) perception do not exhibit this developmental switch from type-V to type-IV trichomes. The implication of JA signaling in this process was further supported by an increase in JA-isoleucine and in the expression of genes involved in JA-signalling within hours of heat stress application. These results establish a unique system to study how environmental factors affect developmental fate decisions in plants while opening opportunities to understand mechanisms controlling type-IV trichome initiation and development.