Jasmonic Acid and Its Precursor 12-Oxophytodienoic Acid Control Different Aspects of Constitutive and Induced Herbivore Defenses in Tomato

Abstract

The jasmonate family of growth regulators includes the isoleucine (Ile) conjugate of jasmonic acid (JA-Ile) and its biosynthetic precursor 12-oxophytodienoic acid (OPDA) as signaling molecules. To assess the relative contribution of JA/JA-Ile and OPDA to insect resistance in tomato (Solanum lycopersicum), we silenced the expression of OPDA reductase3 (OPR3) by RNA interference (RNAi). Consistent with a block in the biosynthetic pathway downstream of OPDA, OPR3-RNAi plants contained wild-type levels of OPDA but failed to accumulate JA or JA-Ile after wounding. JA/JA-Ile deficiency in OPR3-RNAi plants resulted in reduced trichome formation and impaired monoterpene and sesquiterpene production. The loss of these JA/JA-Ile -dependent defense traits rendered them more attractive to the specialist herbivore Manduca sexta with respect to feeding and oviposition. Oviposition preference resulted from reduced levels of repellant monoterpenes and sesquiterpenes. Feeding preference, on the other hand, was caused by increased production of cis-3-hexenal acting as a feeding stimulant for M. sexta larvae in OPR3-RNAi plants. Despite impaired constitutive defenses and increased palatability of OPR3-RNAi leaves, larval development was indistinguishable on OPR3-RNAi and wild-type plants, and was much delayed compared with development on the jasmonic acid-insensitive1 (jai1) mutant. Apparently, signaling through JAI1, the tomato ortholog of the ubiquitin ligase CORONATINE INSENSITIVE1 in Arabidopsis (Arabidopsis thaliana), is required for defense, whereas the conversion of OPDA to JA/JA-Ile is not. Comparing the signaling activities of OPDA and JA/JA-Ile, we found that OPDA can substitute for JA/JA-Ile in the local induction of defense gene expression, but the production of JA/JA-Ile is required for a systemic response.

Defects in Peroxisomal 6-Phosphogluconate Dehydrogenase Isoform PGD2 Prevent Gametophytic Interaction in Arabidopsis thaliana

“…After successful fertilization, NO and JA are likely also important during embryo development (Supplemental Fig. S9; Goetz et al, 2012) and defense (Bosch et al, 2014), as indicated by recent studies in tomato (Solanum lycopersicum). Therefore, it is conceivable that our findings have important implications for other plant species and conditions in which NO and/or JA act as signaling components: in the case of peroxisomal NO during abiotic stress in roots (Corpas et al, 2009;Corpas and Barroso, 2014a) and in the case of JA during herbivory/wounding or plant-pathogen interactions.…”

Plant Glandular Trichomes: Natural Cell Factories of High Biotechnological Interest

“…We chose not to review the development of trichomes in Arabidopsis, as this has been thoroughly reviewed (Balkunde et al, 2010;An et al, 2011;Tominaga-Wada et al, 2011;Pattanaik et al, 2014;Matías-Hernández et al, 2016). Unlike the situation of Arabidopsis, which contains a single type of unicellular, nonglandular trichome, our understanding of the molecular genetic aspects of glandular trichome development is still in its infancy but currently improving due to recent progress in omics and genomeediting technologies as well as to a growing focus from several research teams to characterize this process in different plant species (Li et al, 2004;Dai et al, 2010;Bosch et al, 2014;Bergau et al, 2015;Liu et al, 2016). The (draft) genome sequences of a number of plant species with glandular trichomes are now available.…”

“…In this respect, some phytohormones, especially jasmonate (JA) and possibly GAs, elicit glandular trichome development via signaling cascades and the activation of trichome-specific transcriptional regulators (Li et al, 2004;Koo and Howe, 2009;Bose et al, 2013;Bosch et al, 2014;Tian et al, 2014;Liu et al, 2017;Yan et al, 2017). In Mentha arvensis, exogenous application of GA resulted in a moderate increase in trichome density and diameter of the gland, suggesting a positive, although moderate, effect of GA on trichome initiation and development in mint (Bose et al, 2013).…”

Cell death control by matrix metalloproteinases in tomato

“…Transgenic tomato (Solanum peruvianum) cell lines were generated by particle bombardment as described (Cedzich et al, 2009;Pickel et al, 2010). Transgenic tomato plants were generated by Agrobacterium tumefaciens-mediated transformation as described (Bosch et al, 2014).…”

“…The entire expression cassette comprising the CaMV 35S promoter, Sl3-MMP-HP, and the OCS terminator was cut out with NotI and transferred into pART27 (Gleave, 1992). Transgenic tomato plants were generated by A. tumefaciens-mediated transformation as described (Bosch et al, 2014). Stable integration of the transgene and the independence of transformation events were confirmed by Southern-blot analysis.…”