The Tomato Homolog of CORONATINE-INSENSITIVE1 Is Required for the Maternal Control of Seed Maturation, Jasmonate-Signaled Defense Responses, and Glandular Trichome Development[W]

Abstract

Jasmonic acid (JA) is a fatty acid-derived signaling molecule that regulates a broad range of plant defense responses against herbivores and some microbial pathogens. Molecular genetic studies in Arabidopsis have established that JA also performs a critical role in anther and pollen development but is not essential for other developmental aspects of the plant's life cycle. Here, we describe the phenotypic and molecular characterization of a sterile mutant of tomato ( jasmonic acidinsensitive1 [ jai1 ]) that is defective in JA signaling. Although the mutant exhibited reduced pollen viability, sterility was caused by a defect in the maternal control of seed maturation, which was associated with the loss of accumulation of JAregulated proteinase inhibitor proteins in reproductive tissues. jai1 plants exhibited several defense-related phenotypes, including the inability to express JA-responsive genes, severely compromised resistance to two-spotted spider mites, and abnormal development of glandular trichomes. We demonstrate that these defects are caused by the loss of function of the tomato homolog of CORONATINE-INSENSITIVE1 (COI1), an F-box protein that is required for JA-signaled processes in Arabidopsis. These findings indicate that the JA/COI1 signaling pathway regulates distinct developmental processes in different plants and suggest a role for JA in the promotion of glandular trichome-based defenses.

Role of cis-12-Oxo-Phytodienoic Acid in Tomato Embryo Development

“…This idea was initially supported by the fact that sterility of jai1 may result from arrest in embryo/seed maturation, because jai1 ovules have still the ability to be fertilized followed by production of small aborted seeds (Li et al, 2004). It has been discussed that this mutant seems to be affected in SlCOI1/JA-dependent supply of carbon or nitrogen by the maternal tissue thereby altering embryo development and/or generation of vitamin(s) or cofactor(s) that requires transport from maternal tissues to the developing embryo (Li et al, 2004). This might be similar to the role of biotin synthesis in Arabidopsis embryogenesis (Patton et al, 1998).…”

“…The JA-insensitive tomato jai1 mutant, homologous to coi1 in Arabidopsis, is female sterile due to a block in embryo development (Li et al, 2001(Li et al, , 2004. Pollen viability is also reduced in jai1, although there is enough fertile pollen for successful cross-fertilization to wild-type flowers (Li et al, 2004;B. McCaig, unpublished data).…”

Jasmonate-induced plant defenses and prey availability impact the preference and performance of an omnivorous stink bug, Podisus maculiventris

“…Jasmonate-overexpressing plants have the highest levels of defensive proteinase inhibitors and polyphenol oxidase (Howe and Ryan 1999), wild-type plants are intermediate, and jasmonate-insensitive plants have the lowest levels (Kaplan and Thaler 2010). Jasmonate-insensitive plants have 87 % fewer total trichomes than wildtype or jasmonate-overexpressing plants and are absent of both the hair-like glandular type-1 trichome and the glandular type-VI, (Kaplan and Thaler 2010;Li et al 2004). Therefore, jasmonate insensitive are the highest quality for many herbivores that are the prey for P. maculiventris, wild-type are intermediate and jasmonate overexpressor are the lowest quality (Kaplan and Thaler 2010;Rodriguez-Saona et al 2010;Scott et al 2010).…”

“…The level of plant resistance via the jasmonate pathway was manipulated using three types of tomato plants that vary in the inducibility of the jasmonate pathway. Wild-type tomato plants (Solanum lycopersicon cv Castlemart) that induce the jasmonate pathway following wounding, jasmonateinsensitive mutant plants [jai-1; (Li et al 2004)] that do not induce the JA pathway even when damaged and jasmonateoverexpressing 35S::prosystemin plants that express the jasmonic acid pathway constitutively (McGurl et al 1994). The jasmonate-insensitive plant is a mutant defective in jasmonate perception that was backcrossed two times into the Castlemart variety, and the jasmonate overexpressor is a transgenic plant developed using agrobacterium-mediated transformation and backcrossed into the Castlemart variety.…”

“…Jasmonate-insensitive homozygous seeds were identified with a diluted methyl jasmonate and ethanol mixture, added just after germination (Li et al 2004). Seedlings of the three plant types were planted in metro mix soil in 4-inch pots a week after germination.…”