Auxin Response Gene SlARF3 Plays Multiple Roles in Tomato Development and is Involved in the Formation of Epidermal Cells and Trichomes.

The auxin response factor (ARF) genes encode a large family of proteins involved in auxin signaling transduction. SlARF3, a member of the ARF gene family, encodes a protein containing two conserved domains, B3 and ARF, and lacking an Aux/IAA domain. Expression analysis showed that SlARF3 has a particularly high expression level in trichomes. In situ hybridization also detected the SlARF3 transcripts in epidermal pavement cells of leaves. The physiological function of SlARF3 was studied by using the RNA interference (RNAi) strategy. SlARF3-down-regulated plants exhibited decreased density of epidermal pavement cells and obviously reduced density of type I, V and VI trichomes of leaves, which indicates the important role of SlARF3 in the formation of trichomes and epidermal cells in tomato. The number of shoot xylem cells was also decreased in SlARF3-down-regulated lines. Furthermore, RNA-sequencing (RNA-Seq) analysis identified 51 differentially expressed genes (DEGs) belonging to 14 transcription factor (TF) families, such as MYB, bHLH, WD40 and C2H2 zinc finger. Twenty-seven DEGs were involved in the metabolism and signaling transduction of phytohormones, such as auxin, ethylene and gibberellin. These results indicated the important roles of the TFs and hormones in auxin-dependent transcriptional regulation of trichome formation in tomato. Taken together, our results demonstrate that SlARF3 plays an important role in the formation of epidermal cells and trichomes and reveal novel and specific functions for ARFs in tomato developmental processes.