Arabidopsis SPEECHLESS drives de novo expression of PIN1-FORMED 3 in the stomatal lineage via a Brassicaceae-specific intronic enhancer

Zimin Zhou, On Sun Lau
Department of Biological Sciences, National University of Singapore,14 Science Drive 4, Singapore 5 117557

The master stomatal regulator SPEECHLESS (SPCH) specifies the stomatal precursors and controls their self-renewing activity through regulating genes in diverse pathways, but how it gained control of these existing genes remains unexplored. Here we report that Arabidopsis SPCH is recruited by an intronic element of PIN-FORMED 3 (PIN3) to promote the expression of the auxin transporter gene in the stomatal lineage. We showed that PIN3, together with its homologs, limits the self-renewing phase of the stomatal lineage and this function depends on the SPCH binding motif within the intronic element. Intriguingly, the intronic element of PIN3 is specific to the Brassicaceae family and it can work with a monocot PIN3 homolog and heterologous promoters in mediating the de novo gene expression in the stomatal lineage and the epidermis. Overall, through probing into the regulation and importance of PINs in the stomatal precursors, our study reveals a new mode of action of SPCH as an enhancer-binding transcription factor and suggests that the incorporation of a master regulator-binding intragenic element during evolution is sufficient to generate cell-type-specific gene expression in plants.