Overexpression of the class D MADS-box gene Sl-AGL11 impacts fleshy tissue differentiation and structure in tomato fruits

Baowen Huang (1, 2, 3) , Jean-Marc Routaboul (1, 2) , Mingchun Liu (1, 2) , Wei Deng (3) , Elie Maza (1, 2) , Isabelle Mila (1, 2) , Guojian Hu (1, 2) , Mohamed Zouine (1, 2) , Pierre Frasse (1, 2) , Julia T Vrebalov (4) , James J Giovannoni (4) , Zhengguo Li (3) , Benoît van Der Rest (1, 2) , Mondher Bouzayen (1, 2)

1 GBF - Génomique et Biotechnologie des Fruits
2 INRA - Institut National de la Recherche Agronomique
3 GERC - Genetic Engineering Research Center
4 Cornell University [New York]

MADS-box transcription factors are key elements of the genetic networks controlling flower and fruit development. Among these, the class D clade gathers AGAMOUS-like genes which are involved in seed, ovule, and funiculus development. The tomato genome comprises two class D genes, Sl-AGL11 and Sl-MBP3 , both displaying high expression levels in seeds and in central tissues of young fruits. The potential effects of Sl-AGL11 on fruit development were addressed through RNAi silencing and ectopic expression strategies. Sl-AGL11-down-regulated tomato lines failed to show obvious phenotypes except a slight reduction in seed size. In contrast, Sl-AGL11 overexpression triggered dramatic modifications of flower and fruit structure that include: the conversion of sepals into fleshy organs undergoing ethylene-dependent ripening, a placenta hypertrophy to the detriment of locular space, starch and sugar accumulation, and an extreme softening that occurs well before the onset of ripening. RNA-Seq transcriptomic profiling high-lighted substantial metabolic reprogramming occurring in sepals and fruits, with major impacts on cell wall-related genes. While several Sl-AGL11-related phenotypes are reminiscent of class C MADS-box genes (TAG1 and TAGL1), the modifications observed on the placenta and cell wall and the Sl-AGL11 expression pattern suggest an action of this class D MADS-box factor on early fleshy fruit development.

Mots clés: Tomato; MADS; Cell wall; Fleshy tissue; Fruit development

Domaines: Botanique; Génomique, Transcriptomique et Protéomique [q-bio.GN]

Baowen Huang, Jean-Marc Routaboul, Mingchun Liu, Wei Deng, Elie Maza, et al.. Overexpression of the class D MADS-box gene Sl-AGL11 impacts fleshy tissue differentiation and structure in tomato fruits. Journal of Experimental Botany, 2017, 68 (17), pp.4869-4884. ⟨10.1093/jxb/erx303⟩. ⟨hal-01643490⟩