A double-negative feedback loop between miR319c and JAW-TCPs establishes growth pattern in incipient leaf primordia in Arabidopsis thaliana

The microRNA miR319 and its target JAW-TCP transcription factors regulate the proliferation-to-differentiation transition of leaf pavement cells in diverse plant species. In young Arabidopsis leaf primordia, JAW-TCPs are detected towards the distal region whereas the major mRNA319-encoding gene MIR3...

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Bibliographic Details
Published in:PLoS genetics 2023-09, Vol.19 (9), p.e1010978-e1010978
Main Authors: Shankar, Naveen, Sunkara, Preethi, Nath, Utpal
Format: Article
Language:English
Subjects:
Analysis
Arabidopsis thaliana
Biology and Life Sciences
Cell differentiation
Cell growth
Cell proliferation
Chromatin
DNA binding proteins
Genes
Genetic aspects
Genetic engineering
Genetic transcription
Growth
Growth patterns
Histones
Identification and classification
Leaves
Localization
MicroRNA
MicroRNAs
miRNA
Morphogenesis
Phenotypes
Plant cells
Primordia
Proteins
Research and Analysis Methods
Transcription factors
Transmission Control Protocol/Internet Protocol (Computer network protocol)
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Summary:The microRNA miR319 and its target JAW-TCP transcription factors regulate the proliferation-to-differentiation transition of leaf pavement cells in diverse plant species. In young Arabidopsis leaf primordia, JAW-TCPs are detected towards the distal region whereas the major mRNA319-encoding gene 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 [mu]m long. Loss of JAW-TCPs causes distal extension of the 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 in the embryonic leaves. 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.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1010978