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First published online October 30, 2009; 10.1105/tpc.109.066936

The Plant Cell 21:3041-3062 (2009)
© 2009 American Society of Plant Biologists

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Fleshy Fruit Expansion and Ripening Are Regulated by the Tomato SHATTERPROOF Gene TAGL1[W],[OA]

Julia Vrebalova,1, Irvin L. Panb,1,2, Antonio Javier Matas Arroyoc, Ryan McQuinna,d, MiYoung Chunga, Mervin Poolee,3, Jocelyn Rosec, Graham Seymoure, Silvana Grandillof, James Giovannonia,d,4,5 and Vivian F. Irishb,g,4

a Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York 14853
b Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520-8104
c Department of Plant Biology, Cornell University, Ithaca, New York 14853
d U.S. Department of Agriculture–Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Cornell University, Ithaca, New York 14853
e Division of Plant Sciences, University of Nottingham, Sutton Bonnington, Loughborough, Leics LE12 5RD, United Kingdom
f Consiglio Nationale delle Ricerche-Instituto Di Genetica Vegetale, 80055 Portici (Naples), Italy
g Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520-8104

5 Address correspondence to jjg33{at}cornell.edu.

The maturation and ripening of fleshy fruits is a developmental program that synchronizes seed maturation with metabolism, rendering fruit tissues desirable to seed dispersing organisms. Through RNA interference repression, we show that Tomato AGAMOUS-LIKE1 (TAGL1), the tomato (Solanum lycopersicum) ortholog of the duplicated SHATTERPROOF (SHP) MADS box genes of Arabidopsis thaliana, is necessary for fruit ripening. Tomato plants with reduced TAGL1 mRNA produced yellow-orange fruit with reduced carotenoids and thin pericarps. These fruit are also decreased in ethylene, indicating a comprehensive inhibition of maturation mediated through reduced ACC Synthase 2 expression. Furthermore, ectopic expression of TAGL1 in tomato resulted in expansion of sepals and accumulation of lycopene, supporting the role of TAGL1 in ripening. In Arabidopsis, the duplicate SHP1 and SHP2 MADS box genes regulate the development of separation layers essential for pod shatter. Expression of TAGL1 in Arabidopsis failed to completely rescue the shp1 shp2 mutant phenotypes, indicating that TAGL1 has evolved distinct molecular functions compared with its Arabidopsis counterparts. These analyses demonstrate that TAGL1 plays an important role in regulating both fleshy fruit expansion and the ripening process that together are necessary to promote seed dispersal of fleshy fruit. From this broad perspective, SHP1/2 and TAGL1, while distinct in molecular function, regulate similar activities via their necessity for seed dispersal in Arabidopsis and tomato, respectively.







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