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

PLoS Genet. 2013;9(7):e1003655. doi: 10.1371/journal.pgen.1003655. Epub 2013 Jul 25.


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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Lineage
  • DNA-Binding Proteins / genetics
  • Flowers / genetics*
  • Flowers / metabolism
  • Gene Expression Regulation, Plant
  • MicroRNAs / genetics
  • Morphogenesis / genetics
  • Mutation
  • Plant Leaves / genetics
  • Plant Leaves / growth & development*
  • Plastids / genetics*
  • Plastids / metabolism


  • Arabidopsis Proteins
  • DNA-Binding Proteins
  • GUN1 protein, Arabidopsis
  • MicroRNAs

Grant support

This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas from the Ministry for Education, Culture, Sports, Science, and Technology (MEXT) of Japan (No. 19060004) and a Grant-in-Aid for Creative Scientific Research from the Japan Society for the Promotion of Science (No. 19GS0315) to KOk. TTa and KTo were supported by a JSPS Fellowship from the Japan Society for the Promotion of Science (TTa, No. 21-1024; KTo, No. 20-2221). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.