Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene, TAGL1

Authors: VREBALOV, JULIA - Boyce Thompson Institute; PAN, IRVIN - Yale University; ARROYO, ANTONIO - Cornell University; CHUNG, MIYOUNG - Boyce Thompson Institute; POOLE, MERVIN - University Of Nottingham; ROSE, JOCELYN - Cornell University; SEYMOUR, GRAHAM - University Of Nottingham; Giovannoni, James; IRISH, VIVIAN - Yale University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/30/2009
Publication Date: 11/29/2009
Citation: Vrebalov, J., Pan, I., Arroyo, A., Chung, M., Poole, M., Rose, J., Seymour, G., Giovannoni, J.J., Irish, V. 2009. Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene, TAGL1. The Plant Cell. 21:3041:3062.

Interpretive Summary: Across the plant kingdom, many different fruit types have evolved, including fleshy berries such as those of tomato and dry and dehiscent fruits exemplified by Arabidopsis siliques. Fossil records suggest the emergence of fleshy-fruited species from progenitors bearing dry and dehiscent fruit with examples of conversion between fruit types over evolutionary time. The existence of closely related species with dry and fleshy fruits, as in the plant family Solanaceae where tomato and pepper produce fleshy fruits while petunia and tobacco produce dry capsules, would suggest that the molecular basis of such differences are not necessarily complicated. The association of fleshy fruit development with ripening further suggests that these processes may be related. TAGL1 is a tomato gene expressed in ovules, developing carpels, and in the pericarp of developing fruits. Based on phylogenetic analyses, we demonstrate that TAGL1 is related to the duplicate Arabidopsis SHP1 and SHP2 genes which are necessary for pod shattering in Arabidopsis. RNAi repression of TAGL1 in tomato resulted in reduced pericarp thickness and ripening inhibition suggesting a molecular bridge linking fleshy pericarp development and fruit ripening. While they have evolved to have distinct molecular function it is fascinating that, in terms of necessity for normal seed dispersal, the Arabidopsis SHP1/2 and tomato TAGL1 genes retain surprisingly similar roles in plant development in terms of being necessary for seed dispersal in very different fruit types.

Technical Abstract: 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 RNAi repression we show that Tomato AGAMOUS-LIKE1 (TAGL1), the tomato ortholog of the duplicated SHATTERPROOF (SHP) MADS box genes of Arabidopsis, 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, 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 as compared to 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.