Evolution and Diversification of FRUITFULL Genes in Solanaceae

Ecologically and economically important fleshy edible fruits have evolved from dry fruit numerous times during angiosperm diversification. However, the molecular mechanisms that underlie these shifts are unknown. In the Solanaceae there has been a major shift to fleshy fruits in the subfamily Solanoideae. Evidence suggests that an ortholog of FRUITFULL (FUL), a transcription factor that regulates cell proliferation and limits the dehiscence zone in the silique of Arabidopsis, plays a similar role in dry-fruited Solanaceae. However, studies have shown that FUL orthologs have taken on new functions in fleshy fruit development, including regulating elements of tomato ripening such as pigment accumulation. FUL belongs to the core eudicot euFUL clade of the angiosperm AP1/FUL gene lineage. The euFUL genes fall into two paralogous clades, euFULI and euFULII. While most core eudicots have one gene in each clade, Solanaceae have two: FUL1 and FUL2 in the former, and MBP10 and MBP20 in the latter. We characterized the evolution of the euFUL genes to identify changes that might be correlated with the origin of fleshy fruit in Solanaceae. Our analyses revealed that the Solanaceae FUL1 and FUL2 clades probably originated through an early whole genome multiplication event. By contrast, the data suggest that the MBP10 and MBP20 clades are the result of a later tandem duplication event. MBP10 is expressed at weak to moderate levels, and its atypical short first intron lacks putative transcription factor binding sites, indicating possible pseudogenization. Consistent with this, our analyses show that MBP10 is evolving at a faster rate compared to MBP20. Our analyses found that Solanaceae euFUL gene duplications, evolutionary rates, and changes in protein residues and expression patterns are not correlated with the shift in fruit type. This suggests deeper analyses are needed to identify the mechanism underlying the change in FUL ortholog function.