Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato

Abstract

Auxin response factors (ARFs) are involved in auxin-mediated transcriptional regulation in plants. In this study, we performed functional characterization of SlARF6A in tomato. SlARF6A is located in the nucleus and exhibits transcriptional activator activity. Overexpression of <i>SlARF6A</i> increased chlorophyll contents in the fruits and leaves of tomato plants, whereas downregulation of <i>SlARF6A</i> decreased chlorophyll contents compared with those of wild-type (WT) plants. Analysis of chloroplasts using transmission electron microscopy indicated increased sizes of chloroplasts in <i>SlARF6A</i>-overexpressing plants and decreased numbers of chloroplasts in <i>SlARF6A</i>-downregulated plants. Overexpression of <i>SlARF6A</i> increased the photosynthesis rate and accumulation of starch and soluble sugars, whereas knockdown of <i>SlARF6A</i> resulted in opposite phenotypes in tomato leaves and fruits. RNA-sequence analysis showed that regulation of <i>SlARF6A</i> expression altered the expression of genes involved in chlorophyll metabolism, photosynthesis and sugar metabolism. <i>SlARF6A</i> directly bound to the promoters of <i>SlGLK1</i>, <i>CAB</i>, and <i>RbcS</i> genes and positively regulated the expression of these genes. Overexpression of <i>SlARF6A</i> also inhibited fruit ripening and ethylene production, whereas downregulation of <i>SlARF6A</i> increased fruit ripening and ethylene production. <i>SlARF6A</i> directly bound to the <i>SAMS1</i> promoter and negatively regulated <i>SAMS1</i> expression. Taken together, these results expand our understanding of ARFs with regard to photosynthesis, sugar accumulation and fruit development and provide a potential target for genetic engineering to improve fruit nutrition in horticulture crops.