MIR319C and its target JAW-TCPs repress each other and establish cell proliferation pattern in incipient leaf primordia in Arabidopsis thaliana

Abstract

The microRNA miR319 and its target JAW-TCP transcription factors regulate leaf morphogenesis in diverse plant species. In young Arabidopsis leaf primordia, JAW-TCPs are detected towards the distal region whereas MIR319C is expressed at the base. Little is known about how this complementary expression pattern of MIR319C and JAW-TCPs is generated. Here, we show that MIR319C is initially expressed uniformly throughout the incipient primordia and is later abruptly down-regulated at the distal region, with concomitant distal appearance of JAW-TCPs, when leaves grow to [~]100 {micro}m long. Loss of JAW-TCPs causes distal extension of MIR319C expression domain, whereas ectopic TCP activity restricts MIR319C more proximally. JAW-TCPs are recruited to and are capable of depositing histone H3K27me3 repressive marks on the MIR319C chromatin. JAW-TCPs fail to repress MIR319C in transgenic seedlings where the TCP-binding cis-elements on MIR319C are mutated, causing miR319 gain-of-function-like phenotype. Based on these results, we propose a model for growth patterning in leaf primordia wherein MIR319C and JAW-TCPs repress each other and divide the uniformly growing primordia into distal differentiation zone and proximal proliferation domain. Summary statementJAW-TCPs transcriptionally repress the microRNA319 encoding gene MIR319C to generate their mutually exclusive expression pattern and establish growth polarity during early stages of Arabidopsis leaf primordia.