ARS | Publication request: Uniform ripening (U) encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development

Submitted to: Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: June 8, 2012
Publication Date: June 29, 2012
Citation: Powell, A., Nguyen, C., Hill, T., Aktas, H., Figueroa-Balderas, R., Barry, C., Liu, Y., Chetelat, R., Granell, A., Van Deynze, A., Giovannoni, J.J., Bennett, A. 2012. Uniform ripening (U) encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science. 336(6089):1711-1715. DOI: 10.1126/Science.1222218.

Interpretive Summary: For approximately 70 years, breeders have selected tomato varieties with fruit that are uniformly light green prior to ripening, a characteristic that facilitates fruit maturity determinations in large-scale commercial production. Light green fruit ripen to a red color, although in some cultivars and growing conditions, the selection improves the development of uniform red color at the stem end of the fruit. However, light green fruit lead to ripe fruit with reduced sugars. The light green fruit phenotype in most tomato cultivars is conferred by a single gene mutation called uniform ripening or u for short. We report the characterization of the gene underlying the u mutation and show that it is a transcription factor (i.e. a regulator of other genes) influencing chloroplast development and associated photosynthesis and sugar accumulation traits of the fruit. While helpful in determining harvest time, this mutation has a negative unintended effect on fruit quality in that u fruit have reduced sugars.

Technical Abstract: Modern tomato (Solanum lycopersicum) varieties are bred for recessive uniform ripening (u) light green fruit phenotypes to facilitate maturity determinations without information about the underlying gene. We show that U encodes a Golden 2-like (GLK) transcription factor, SlGLK2, which determines the pattern and intensity of green fruit color; u is a nonsense mutation. Homology and mapping identified in tomato two GLK genes, SlGLK1 and SlGLK2; both are expressed in leaves. In fruit, only SlGLK2 is expressed. Overexpressing GLKs converted u/u fruit to dark green. SlGLK2 suppression in U/U recapitulated the u/u fruit phenotype. GLK expression enhanced fruit photosynthesis gene expression and chloroplast development. Elaboration of fruit photosynthetic capacity by GLK expression elevated green fruit starch and ripe fruit sugars. Information about SlGLK2 reveals that photosynthesis in green fruit contributes to ripe fruit quality and suggests that selection of u inadvertently compromised ripe fruit sugars in exchange for desirable production traits.