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.
Highlights
Mitochondrial complex II is part of the tricarboxylic acid cycle and the respiratory chain
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 SUCCINATE DEHYDROGENASE2-3 (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 family of transcription factors
Summary
Mitochondrial complex II (succinate dehydrogenase) is part of the tricarboxylic acid cycle and the respiratory chain. Succinate:ubiquinone oxidoreductase (succinate dehydrogenase [SDH]; EC 1.3.5.1), commonly referred to as mitochondrial complex II, has a central role in mitochondrial metabolism as a member of both the electron transport chain and the tricarboxylic acid (TCA) cycle. Whereas SDH2-1 and SDH2-2 have similar expression patterns, being expressed in all organs from adult plants (Figueroa et al, 2001; Elorza et al, 2004), SDH2-3 is highly expressed in the embryo during the maturation phase of seed development and SDH2-3 transcripts are abundant in dry seeds and decline during germination (Elorza et al, 2006) These data suggest that SDH2-1 and SDH2-2 are probably redundant and that SDH2-3 may have a specific role as the complex II iron-sulfur protein-coding gene during embryo maturation and/or germination
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