Red and blue light antagonistically regulate tomato root system architecture by the auxin-mediated SlARF18-SlDRO1 module.

Root system architecture (RSA) is critical for water and nutrients uptake and is affected by light. However, the precise mechanisms by which light quality regulates RSA remain obscure. Here, we showed that red light (R) caused shorter primary root, larger lateral root angle and lower expression of DEEPER ROOTING 1 (SlDRO1), while blue light (B) led to the opposite trend compared to white light. Integrative analyses of hormone quantification, gene expression, GUS staining and auxin transport inhibitor 1-N-naphthylphthalamic acid (NPA) application revealed that the antagonistic effects of R and B on RSA depended on long distance transport of leaf-synthesized auxin from shoot to root. Transcriptome analysis identified a novel auxin response factor (ARF) transcription factor, SlARF18, whose expression paralleled light quality-induced changes in auxin content. Subcellular localization and transcriptional activation assays showed that SlARF18 protein was a nucleus-localized transcriptional repressor. The functions of SlARF18 and SlDRO1 in RSA were verified by virus-induced gene silencing. Yeast one-hybrid, dual-luciferase reporter assays and electrophoretic mobility shift assays revealed that SlARF18 inhibited SlDRO1 transcription by binding to its promoter. Collectively, our results demonstrate that R and B antagonistically regulate tomato RSA by the auxin-mediated SlARF18-SlDRO1 module, providing a novel mechanism for light quality-regulated RSA.