Minisymposium 14: Reproductive development

Abs # 27001: The jasmonate-COI1 signaling pathway plays a dual role in the regulation of stress responses and seed development in tomato

Presenter:	Howe, Gregg A, howeg@msu.edu
Authors	Howe, Gregg A (A)   McCaig, Bonnie C (A)   Schilmiller, Tony L (A)   Chen, Hui  (A)   Li, Lei  (A)
Affiliations:	(A): MSU-DOE Plant Research Lab, Michigan State University
Web Site:	http://www.prl.msu.edu/howe.shtml

Jasmonic acid (JA) is a fatty acid-derived signal that regulates plant responses to biotic and abiotic stress. Studies in Arabidopsis have shown 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. To obtain a more complete understanding of the role of JA in plant growth and development, we conducted a screen for JA-insensitive (jai) mutants of tomato. One fast-neutron-induced mutant, called jai1-1, was shown to harbor a deletion in the CORONATINE-INSENSITIVE1 (COI1) gene that encodes an F-box protein involved in the ubiquitin-proteosome pathway. The phenotype of jai1-1 plants indicates that loss of COI1 function disrupts JA-signaled processes in all tissues of tomato. For example, jai1-1 abrogated wound- and JA-induced expression of proteinase inhibitors and other defensive compounds in leaves. As a consequence, natural resistance of the mutant to herbivores was severely compromised. jai1 roots were insensitive to the growth inhibitory effects of exogenous JA, and also failed to express JA-regulated genes. Reproductive phenotypes resulting from loss of COI1 function included reduced pollen viability, abnormal trichome development on fruit and sepals, loss of viable seed production, and reduced fruit size. Although jai1 homozygotes were capable of self-fertilization, fruit set, and fruit ripening, reciprocal crosses showed that seedlessness is caused mainly by a defect in female reproductive development. Consistent with these results, fertilized jai1 embryos arrested early in development. This finding contrasts with the male sterile phenotype of Arabidopsis coi1 mutants and suggests differences in the hormonal control of seed development in fleshy fruit compared to dry dehiscent fruit. The strict sporophytic behavior of jai1, together with the occurrence of high JA levels in female reproductive tissues, indicates that JA-COI1 signaling regulates maternal processes that nurture the developing embryo and seed. Gene expression profiling of wild-type and mutant flowers showed that COI1 is required for constitutive expression of a specific set of genes that is induced in leaves in response to wounding, herbivore attack, and other stress conditions. These results indicate that the JA-COI1 signaling pathway in tomato plays a role in regulating biochemical processes that promote not only plant protection, but also embryo and seed development.