MANIPULATION OF LIGHT SIGNAL TRANSDUCTION AS A MEANS OF MODIFYING FRUIT NUTRITIONAL QUALITY IN TOMATO

Authors: LIU, YONGSHENG - BOYCE THOMPSON INST; ROOF, SHERRY - BOYCE THOMPSON INST; YE, ZHIBIAO - BOYCE THOMPSON INST; BARRY, CORNELIUS - BOYCE THOMPSON INST; VAN TUINEN, AGEETH - WAGENINGEN UNIVERSITY; VREBALOV, JULIA - BOYCE THOMPSON INST; BOWLER, CHRIS - STAZIONE ZOOLOGICA; Giovannoni, James

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/23/2004
Publication Date: 6/11/2004
Citation: Liu, Y., Roof, S., Ye, Z., Barry, C., Van Tuinen, A., Vrebalov, J., Bowler, C., Giovannoni, J.J. 2004. Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proceedings of the National Academy of Sciences. 26:9897-9902.

Interpretive Summary: Dietary carotenoids derived from plants serve roles as necessary nutrients (e.g. pro-vitamin A) and anti-oxidants. Epidemiological studies indicate that high dietary intake of carotenoid-rich foods can decrease the incidence of degenerative diseases including coronary heart disease, certain cancers, and macular degeneration. While the genes responsible for carotenoid biosynthesis are largely defined, little is known about the molecular mechanisms that regulate carotenoid accumulation. Indeed, prior efforts to manipulate carotenoid accumulation, particularly early in the pathway, have resulted in plant phenotypes negatively impacting crop performance as a result of consequences on phytohormones (e.g. ABA and GA) synthesized from the same precursors. While "golden rice" was a clear technical success with the potential for real-world benefit, the realization of lower than anticipated carotenoid levels may reflect uncharacterized regulatory constraints on synthesis and/or accumulation. Analysis of the tomato hp mutations suggests that light signaling mechanisms regulates the carotenoid pathway in ways that can impact total fruit carotenoid content with less negative impact on plant characteristics. Here we describe the cloning of the tomato gene altered in the hp1 mutant and demonstrate it is homologous to sequences involved in light response. We also report the isolation of two additional tomato light signal transduction genes (LeHY5 and LeCOP1LIKE) and confirm the potential for manipulation of light signaling for improved nutrient quality.

Technical Abstract: Fruit constitute a major component of human diets providing fiber, vitamins and phytonutrients. Carotenoids are a major class of compounds found in many fruit providing nutritional benefits as precursors to essential vitamins and as antioxidants. While recent gene isolation efforts and metabolic engineering have primarily targeted genes involved in carotenoid biosynthesis, factors that regulate flux through the carotenoid pathway remain largely unknown. Characterization of the tomato high-pigment mutations (hp1, hp2) suggests manipulation of light signal transduction machinery may be an effective approach toward practical manipulation of plant carotenoids. We demonstrate here that hp1 alleles represent mutations in a tomato UV-DAMAGED DNA BINDING PROTEIN 1 (DDB1) homologue. We further demonstrate that two new tomato light signal transduction genes, LeHY5 and LeCOP1LIKE, are positive and negative regulators of fruit pigmentation, respectively. Down-regulated LeHY5 plants exhibit defects in light responses, including inhibited seedling photomorphogenesis, loss of thylakoid organization, and reduced carotenoid accumulation. In contrast, repression of LeCOP1LIKE expression results in plants with exaggerated photomorphogenesis, dark green leaves, and elevated fruit carotenoid levels. These results suggest genes encoding components of light signal transduction machinery also influence fruit pigmentation and represent genetic tools for manipulation of fruit quality and nutritional value.