Evolution and Diversification of FRUITFULL Genes in Solanaceae

Abstract

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 <i>FRUITFULL</i> (<i>FUL</i>), a transcription factor that regulates cell proliferation and limits the dehiscence zone in the silique of <i>Arabidopsis</i>, plays a similar role in dry-fruited Solanaceae. However, studies have shown that <i>FUL</i> orthologs have taken on new functions in fleshy fruit development, including regulating elements of tomato ripening such as pigment accumulation. <i>FUL</i> belongs to the core eudicot <i>euFUL</i> clade of the angiosperm <i>AP1</i>/<i>FUL</i> gene lineage. The <i>euFUL</i> genes fall into two paralogous clades, <i>euFULI</i> and <i>euFULII</i>. While most core eudicots have one gene in each clade, Solanaceae have two: <i>FUL1</i> and <i>FUL2</i> in the former, and <i>MBP10</i> and <i>MBP20</i> in the latter. We characterized the evolution of the <i>euFUL</i> genes to identify changes that might be correlated with the origin of fleshy fruit in Solanaceae. Our analyses revealed that the Solanaceae <i>FUL1</i> and <i>FUL2</i> clades probably originated through an early whole genome multiplication event. By contrast, the data suggest that the <i>MBP10</i> and <i>MBP20</i> clades are the result of a later tandem duplication event. <i>MBP10</i> 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 <i>MBP10</i> is evolving at a faster rate compared to <i>MBP20.</i> Our analyses found that Solanaceae <i>euFUL</i> 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 <i>FUL</i> ortholog function.