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

Auxin response factors (ARFs) are involved in auxin-mediated transcriptional regulation in plants. In this study, we performed functional characterization of SIARF6A in tomato. SIARF6A is located in the nucleus and exhibits transcriptional activator activity. Overexpression of SIARF6A increased chlorophyll contents in the fruits and leaves of tomato plants, whereas downregulation of SIARF6A decreased chlorophyll contents compared with those of wild-type (WT) plants. Analysis of chloroplasts using transmission electron microscopy indicated increased sizes of chloroplasts in SIARF6A-overexpressing plants and decreased numbers of chloroplasts in SIARF6A-downregulated plants. Overexpression of SIARF6A increased the photosynthesis rate and accumulation of starch and soluble sugars, whereas knockdown of SIARF6A resulted in opposite phenotypes in tomato leaves and fruits. RNA-sequence analysis showed that regulation of SIARF6A expression altered the expression of genes involved in chlorophyll metabolism, photosynthesis and sugar metabolism. SIARF6A directly bound to the promoters of SIGLK1, CAB, and RbcS genes and positively regulated the expression of these genes. Overexpression of SIARF6A also inhibited fruit ripening and ethylene production, whereas downregulation of SIARF6A increased fruit ripening and ethylene production. SIARF6A directly bound to the SAMS1 promoter and negatively regulated SAMS1 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.