Pattern dynamics in adaxial-abaxial specific gene expression are modulated by a plastid retrograde signal during Arabidopsis thaliana leaf development.

Toshiaki Tameshige,Ryuji Tsugeki,Mikio Nishimura,Noritaka Matsumoto,Keiro Watanabe,Hironori Fujita,Maki Kondo,Kiyotaka Okada,Kiyoshi Tatematsu,Koichi Toyokura,Masayoshi Kawaguchi,Xuemei Chen

doi:10.1371/journal.pgen.1003655

Abstract

The maintenance and reformation of gene expression domains are the basis for the morphogenic processes of multicellular systems. In a leaf primordium of Arabidopsis thaliana, the expression of FILAMENTOUS FLOWER (FIL) and the activity of the microRNA miR165/166 are specific to the abaxial side. This miR165/166 activity restricts the target gene expression to the adaxial side. The adaxial and abaxial specific gene expressions are crucial for the wide expansion of leaf lamina. The FIL-expression and the miR165/166-free domains are almost mutually exclusive, and they have been considered to be maintained during leaf development. However, we found here that the position of the boundary between the two domains gradually shifts from the adaxial side to the abaxial side. The cell lineage analysis revealed that this boundary shifting was associated with a sequential gene expression switch from the FIL-expressing (miR165/166 active) to the miR165/166-free (non-FIL-expressing) states. Our genetic analyses using the enlarged fil expression domain2 (enf2) mutant and chemical treatment experiments revealed that impairment in the plastid (chloroplast) gene expression machinery retards this boundary shifting and inhibits the lamina expansion. Furthermore, these developmental effects caused by the abnormal plastids were not observed in the genomes uncoupled1 (gun1) mutant background. This study characterizes the dynamic nature of the adaxial-abaxial specification process in leaf primordia and reveals that the dynamic process is affected by the GUN1-dependent retrograde signal in response to the failure of plastid gene expression. These findings advance our understanding on the molecular mechanism linking the plastid function to the leaf morphogenic processes.

Highlights

The expansion of a flat organ from an undifferentiated organ primordium provides an excellent model for studying the dynamics of formation and maintenance of gene expression domains
Development of the planar lamina requires the specific expression of several key genes in the foreside and backside of the tiny leaf primordium
We characterized that the expression of FIL and the activity of miR165/166 are induced in all cells of initiating leaf primordia, and repressed sequentially from the adaxial cells, gradually restricted to the abaxial cells

Summary

Introduction

The expansion of a flat organ from an undifferentiated organ primordium provides an excellent model for studying the dynamics of formation and maintenance of gene expression domains. In the case of wing development in Drosophila, the wing primordium (wing disc) is subdivided into dorsal and ventral compartments. In the case of leaf development in the model plant Arabidopsis thaliana, previous studies have revealed that several genes are expressed in an adaxial- or abaxial- specific manner. Their specific expression patterns are required for lamina expansion with adaxial-abaxial asymmetric cell differentiation (see [5,6,7,8] for review). Previous studies have not focused on whether the gene expression states are maintained in each cell lineage as in the case of the fly wing. The abaxial-specific genes are four YABBY family genes, including FILAMENTOUS FLOWER (FIL) [13,14,15,16], three KANADI genes (KANs) [17,18] and two AUXIN

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Conclusion