Tomato golden 2-like (GLK) transcription factors reveal molecular gradients that function during fruit development and ripening

Authors: NGUYEN, CUONG - Cornell University; VREBALOV, JULIA - Boyce Thompson Institute; GAPPER, NIGEL - Boyce Thompson Institute; ZHENG, YI - Boyce Thompson Institute; ZHONG, SILIN - Boyce Thompson Institute; FEI, ZHANGJUN - Boyce Thompson Institute; Giovannoni, James

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/15/2014
Publication Date: 2/1/2014
Publication URL: http://DOI: 10.1105/tpc.113.118794
Citation: Nguyen, C., Vrebalov, J., Gapper, N., Zheng, Y., Zhong, S., Fei, Z., Giovannoni, J.J. 2014. Tomato golden 2-like (GLK) transcription factors reveal molecular gradients that function during fruit development and ripening. The Plant Cell. 26(2):585-601.

Interpretive Summary: The fruit ripening process results in a transition from physiological and biochemical activities that are protective of the developing fruit organ to those that promote attractive attributes for seed dispersing animals including humans. Many fruits develop green and chloroplast-rich and then transition to ripening, where photosynthesis and related biochemical processes diminish and flavor, aroma and nutritional metabolites increase in abundance. Here we describe the functional characterization of two related regulatory genes (transcription factors) that influence the numbers and patterns of chloroplast distribution in fruit and leaves, and further show that one regulator primarily influences fruit chloroplasts while the other chloroplast abundance in green fruit is regulated by a transcription factor of the Golden 2-like family. We further demonstrate that the number of chloroplasts in the green fruit is related to the nutrition and quality attributes of ripe fruit.

Technical Abstract: Fruit ripening is the summation of changes rendering fleshy fruit tissues attractive and palatable to seed dispersing organisms. For example, sugar content is influenced by plastid numbers and photosynthetic activity in unripe fruit and later by starch and sugar catabolism during ripening. Tomato fruit are sinks of photosynthate, yet unripe green fruit contribute significantly to the sugars that ultimately accumulate in the ripe fruit. Plastid numbers and chlorophyll content are influenced by numerous environmental and genetic factors and are positively correlated with photosynthesis and photosynthate accumulation. Golden 2-like (GLK) transcription factors regulate plastid and chlorophyll levels. Tomato, like most plants, contains two GLKs, i.e., GLK1 and GLK2/UNIFORM. Mutant and transgene analysis demonstrated that these genes encode functionally similar peptides, though differential expression renders GLK1 more important in leaves while GLK2 is predominant in fruit. A latitudinal gradient of GLK2 expression influences the typical uneven coloration of green and ripe wild-type fruit. Transcriptome profiling revealed a broader fruit gene expression gradient throughout development. The gradient influenced general ripening activities beyond plastid development and was consistent with the easily observed yet poorly studied ripening gradient present in tomato and many fleshy fruits.