Auxin response factor 2 intersects hormonal signals in the regulation of tomato fruit ripening

Dario A. Breitel (1) , Louise Chappell-Maor (1) , Sagit Meir (1) , Irina Panizel (1) , Clara Pons Puig (2) , Yanwei Hao (3) , Tamar Yifhar (1) , Hagai Yasuor (4) , Mohammed Zouine (3) , Mondher Bouzayen (3) , Antonio Granell Richart (2) , Ilana Rogachev (1) , Asaph Aharoni (1)

1 Department of Plant and Environmental Sciences
2 UPV - Universitat Politècnica de València = Universitad Politecnica de Valencia = Polytechnic University of Valencia
3 GBF - Génomique et Biotechnologie des Fruits
4 Agricultural Research Organization

The involvement of ethylene in fruit ripening is well documented, though knowledge regarding the crosstalk between ethylene and other hormones in ripening is lacking. We discovered that AUXIN RESPONSE FACTOR 2A (ARF2A), a recognized auxin signaling component, functions in the control of ripening. ARF2A expression is ripening regulated and reduced in the rin, nor and nr ripening mutants. It is also responsive to exogenous application of ethylene, auxin and abscisic acid (ABA). Over-expressing ARF2A in tomato resulted in blotchy ripening in which certain fruit regions turn red and possess accelerated ripening. ARF2A over-expressing fruit displayed early ethylene emission and ethylene signaling inhibition delayed their ripening phenotype, suggesting ethylene dependency. Both green and red fruit regions showed the induction of ethylene signaling components and master regulators of ripening. Comprehensive hormone profiling revealed that altered ARF2A expression in fruit significantly modified abscisates, cytokinins and salicylic acid while gibberellic acid and auxin metabolites were unaffected. Silencing of ARF2A further validated these observations as reducing ARF2A expression let to retarded fruit ripening, parthenocarpy and a disturbed hormonal profile. Finally, we show that ARF2A both homodimerizes and interacts with the ABA STRESS RIPENING (ASR1) protein, suggesting that ASR1 might be linking ABA and ethylene-dependent ripening. These results revealed that ARF2A interconnects signals of ethylene and additional hormones to co-ordinate the capacity of fruit tissue to initiate the complex ripening process.

Mots clés: cytokinin-activating enzyme; asr gene family; abscisic-acid; lycopersicon-esculentum; microarray analysis; down-regulation

Mots clés: bimolecular fluorescence complementation; protein-protein interactions; transcription factor

Domaines: Sciences du Vivant [q-bio]; Biologie végétale

Dario A. Breitel, Louise Chappell-Maor, Sagit Meir, Irina Panizel, Clara Pons Puig, et al.. Auxin response factor 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLoS Genetics, 2016, 12 (3), pp.1-34. ⟨10.1371/journal.pgen.1005903⟩. ⟨hal-02634787⟩