A nuclear gene encoding the iron-sulfur subunit of mitochondrial complex II is regulated by B3 domain transcription factors during seed development in Arabidopsis

Plant Physiol. 2009 May;150(1):84-95. doi: 10.1104/pp.109.136531. Epub 2009 Mar 4.

Abstract

Mitochondrial complex II (succinate dehydrogenase) is part of the tricarboxylic acid cycle and the respiratory chain. Three nuclear genes encode its essential iron-sulfur subunit in Arabidopsis (Arabidopsis thaliana). One of them, SUCCINATE DEHYDROGENASE2-3 (SDH2-3), is specifically expressed in the embryo during seed maturation, suggesting that SDH2-3 may have a role as the complex II iron-sulfur subunit during embryo maturation and/or germination. Here, we present data demonstrating that three abscisic acid-responsive elements and one RY-like enhancer element, present in the SDH2-3 promoter, are involved in embryo-specific SDH2-3 transcriptional regulation. Furthermore, we show that ABSCISIC ACID INSENSITIVE3 (ABI3), FUSCA3 (FUS3), and LEAFY COTYLEDON2, three key B3 domain transcription factors involved in gene expression during seed maturation, control SDH2-3 expression. Whereas ABI3 and FUS3 interact with the RY element in the SDH2-3 promoter, the abscisic acid-responsive elements are shown to be a target for bZIP53, a member of the basic leucine zipper (bZIP) family of transcription factors. We show that group S1 bZIP53 protein binds the promoter as a heterodimer with group C bZIP10 or bZIP25. To the best of our knowledge, the SDH2-3 promoter is the first embryo-specific promoter characterized for a mitochondrial respiratory complex protein. Characterization of succinate dehydrogenase activity in embryos from two homozygous sdh2-3 mutant lines permits us to conclude that SDH2-3 is the major iron-sulfur subunit of mature embryo complex II. Finally, the absence of SDH2-3 in mutant seeds slows down their germination, pointing to a role of SDH2-3-containing complex II at an early step of germination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / embryology
  • Arabidopsis / genetics*
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Arabidopsis Proteins / physiology
  • Base Sequence
  • Binding Sites
  • Gene Expression Regulation, Plant*
  • Germination / genetics
  • Iron-Sulfur Proteins / chemistry
  • Iron-Sulfur Proteins / genetics*
  • Iron-Sulfur Proteins / metabolism
  • Molecular Sequence Data
  • Promoter Regions, Genetic
  • Protein Structure, Tertiary
  • Protein Subunits / chemistry
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Seeds / genetics*
  • Seeds / growth & development
  • Seeds / metabolism
  • Succinate Dehydrogenase / chemistry
  • Succinate Dehydrogenase / genetics*
  • Succinate Dehydrogenase / metabolism
  • Transcription Factors / chemistry
  • Transcription Factors / physiology*

Substances

  • ABI3 protein, Arabidopsis
  • Arabidopsis Proteins
  • FUSCA3 protein, Arabidopsis
  • Iron-Sulfur Proteins
  • LEC2 protein, Arabidopsis
  • Protein Subunits
  • SDH2-3 protein, Arabidopsis
  • Transcription Factors
  • Succinate Dehydrogenase