Members of the DEAL subfamily of the DUF1218 gene family are required for bilateral symmetry but not for dorsoventrality in Arabidopsis leaves

New Phytol. 2018 Feb;217(3):1307-1321. doi: 10.1111/nph.14898. Epub 2017 Nov 15.

Abstract

Most plant leaves exhibit bilateral symmetry, which has been hypothesized as an inevitable consequence of the existence of the proximodistal and dorsoventral axes. No gene has been described that affects leaf bilateral symmetry but not dorsoventrality in Arabidopsis thaliana. We screened for viable insertional mutations that affect leaf morphology, and out of more than 700 mutants found only one, desigual1-1 (deal1-1), that exhibited bilateral symmetry breaking but no obvious defects in dorsoventrality. We found that deal1-1 is an allele of VASCULATURE COMPLEXITY AND CONNECTIVITY (VCC). Several overlapping regulatory pathways establish the interspersed lobes and indentations along the margin of Arabidopsis thaliana leaves. These pathways involve feedback loops of auxin, the PIN-FORMED1 (PIN1) auxin efflux carrier, and the CUP-SHAPED COTYLEDON2 (CUC2) transcriptional regulator. Early vcc (deal1) leaf primordia fail to acquire bilateral symmetry and instead form ectopic lobes and sinuses. The vcc leaves show aberrant recruitment of marginal cells expressing properly polarized PIN1, resulting in misplaced auxin maxima. Normal PIN1 polarization requires CUC2 expression and CUC2 genetically interacts with VCC; VCC also affects CUC2 expression. VCC has a domain of unknown function, DUF1218, and localizes to the endoplasmic reticulum membrane. VCC acts partially redundantly with its two closest paralogs, DEAL2 and DEAL3, in early leaf margin patterning and is required for bilateral symmetry, but its loss of function does not visibly affect dorsoventrality.

Keywords: Arabidopsis thaliana; CUC2; PIN1; auxin; cell proliferation; development; leaf margin; symmetry.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / anatomy & histology*
  • Arabidopsis / genetics*
  • Body Patterning / genetics*
  • Cell Proliferation
  • Endoplasmic Reticulum / metabolism
  • Epistasis, Genetic
  • Gene Expression Regulation, Plant
  • Genes, Plant*
  • Indoleacetic Acids / metabolism
  • Multigene Family*
  • Mutation / genetics
  • Phenotype
  • Plant Leaves / anatomy & histology*
  • Plant Leaves / genetics*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Subcellular Fractions / metabolism

Substances

  • Indoleacetic Acids
  • Plant Proteins