Arabidopsis CDF3 transcription factor increases carbon and nitrogen assimilation and yield in trans-grafted tomato plants

Grafting in tomato (Solanum lycopersicum L.) has mainly been used to prevent damage by soil-borne pathogens and the negative effects of abiotic stresses, although productivity and fruit quality can also be enhanced using high vigor rootstocks. In the context of a low nutrients input agriculture, the grafting of elite cultivars onto rootstocks displaying higher Nitrogen Use Efficiency (NUE) supports a direct strategy for yield maximization. In this study we assessed the use of plants overexpressing the Arabidopsis (AtCDF3) or tomato (SlCDF3) CDF3 genes, previously reported to increase NUE in tomato, as rootstocks to improve yield in the grafted scion under low N inputs. We found that the AtCDF3 gene induced greater production of sugars and amino acids, which allowed for greater biomass and fruit yield under both sufficient and limiting N supplies. Conversely, no positive impact was found with the SlCDF3 gene. Hormone analyses suggest that gibberellins (GA₄), auxin and cytokinins (tZ) might be involved in the AtCDF3 responses to N. The differential responses triggered by the two genes could be related, at least in part, to the mobility of the AtCDF3 transcript through the phloem to the shoot. Consistently, a higher expression of the target genes of the transcription factor, such as glutamine synthase 2 (SlGS2) and GA oxidase 3 (SlGA3ox), involved in amino acid and gibberellin biosynthesis, respectively, was observed in the leaves of this graft combination. Altogether, our results provided further insights into the mode of action of CDF3 genes and their biotechnology potential for transgrafting approaches.