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Plant Cell Advance Online Publication
Published on October 30, 2009; 10.1105/tpc.109.066936

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Received March 11, 2009
Returned for revision September 25, 2009
Accepted October 12, 2009

Fleshy Fruit Expansion and Ripening Are Regulated by the Tomato SHATTERPROOF Gene TAGL1

Julia Vrebalov 1, Irvin L. Pan 2, Antonio Javier Matas Arroyo 3, Ryan McQuinn 4, MiYoung Chung 1, Mervin Poole 5, Jocelyn Rose 3, Graham Seymour 5, Silvana Grandillo 6, James Giovannoni 4*, and Vivian F. Irish 7

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

* To whom correspondence should be addressed. E-mail: 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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