Loss of tomato geranylgeranyl diphosphate synthase 2 increases monoterpenoid levels and enhances immune responses to bacterial infection

Abstract

Many plastidial isoprenoids, including diterpenes and photosynthesis-related isoprenoids such as carotenoids and chlorophylls, derive from C20 geranylgeranyl diphosphate (GGPP), produced by GGPP synthase (GGPPS) enzymes. Heterodimers of GGPPS and non-catalytic type I small subunit (SSU-I) proteins produce C10 geranyl diphosphate (GPP), the precursor of monoterpenes. Three plastidial GGPPS isoforms, referred to as SlG1-3, are present in tomato (Solanum lycopersicum). Here we explored their contribution to the production of volatile organic compounds (VOCs) of isoprenoid origin under normal conditions and in response to infection with Pseudomonas syringae pathovar tomato (Pst). Edited lines lacking SlG2 showed a distinctive VOC profile compared to unedited (WT) plants and mutants impaired in SlG1 or SlG3. In particular, only slg2 mutants showed constitutively increased levels of GPP-derived hydroxylated monoterpenes (HMTPs). Upon Pst infection, slg2 plants accumulated higher levels of salicylic acid (SA) and exhibited increase resistance compared to WT controls, resulting in reduced levels of VOCs associated to cell death. Our findings suggest that SlG2 regulates GPP synthesis, potentially by specifically competing with other GGPPS isoforms for heterodimerization with SSU-I. Increased GPP production in slg2 plants could lead to higher HMTPs levels, which may result in elevated SA content, and subsequently enhanced protection against bacterial infection.