A Nuclear Gene Encoding the Iron-Sulfur Subunit of Mitochondrial Complex II Is Regulated by B3 Domain Transcription Factors during Seed Development in Arabidopsis    

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 INSENSI-TIVE3 (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.

Control of stomatal aperture

“…Finally, it is interesting to note that although neither malate nor fumarate exert their effects on stomata by affecting ABA, the phytohormone could, conditionally, act upstream of the organic acids, given that a recent study in Arabidopsis revealed the SDH2-3 gene to be upregulated by ABA. 98 It will be important to establish the functional significance of this observation in future studies. Further genetic, molecular biological and biochemical analyses will be required to identify other components of the signal transduction pathway(s) and the corresponding effectors that are involved in the stomatal responses in order to obtain a deeper understanding of the biochemical mechanisms and the precise factors and environmental cues underlying this phenomenon.…”

How do plants make mitochondria?

“…For example, a detailed study on the regulation of COX5b-1 revealed AP2/ERF, ABF4, bZIP and trihelix transcription factors as involved in the transcriptional regulation of COX5b-1 (Comelli et al 2012). Three B3 domain transcription factors (ABI3, FUS3 and LEAFY COTYLE-DON2) have also been shown to regulate the expression of the iron-sulphur subunit of complex II during seed development in Arabidopsis (Roschzttardtz et al 2009). Analysis of the promoters of nuclear genes encoding mitochondrial proteins reveals an enrichment of elements called site II (Gonzalez et al 2007), that have been subsequently shown to play a key role in the regulation of a variety of nuclear genes encoding mitochondrial proteins.…”

Antisense Inhibition of the Iron-Sulphur Subunit of Succinate Dehydrogenase Enhances Photosynthesis and Growth in Tomato via an Organic Acid–Mediated Effect on Stomatal Aperture

“…In plants, complex II has been demonstrated to contain four additional subunits (Eubel et al, 2003;Millar et al, 2004); however, no clear biological function of these additional subunits has been described. Moreover, in contrast with the situation for complexes I, III, and IV, for which multiple gene functional analyses have allowed direct evaluation of the physiological functions of their constituent subunits (Newton et al, 1990;Marienfeld and Newton, 1994;Pla et al, 1995;Howad and Kempken, 1997;Dutilleul et al, 2005;Vidal et al, 2007), as yet only two forward or reverse genetic strategies have been employed to study the function of complex II in plants (Leó n et al, 2007;Roschzttardtz et al, 2009). These studies revealed that disruption of the expression of the SDH1-1 gene results in alterations in gametophyte development, pollen abortion, and reduced seed set (Leó n et al, 2007) and that the absence of SDH2-3 in Arabidopsis thaliana seeds appears to slow their germination (Roschzttardtz et al, 2009).…”

“…Moreover, in contrast with the situation for complexes I, III, and IV, for which multiple gene functional analyses have allowed direct evaluation of the physiological functions of their constituent subunits (Newton et al, 1990;Marienfeld and Newton, 1994;Pla et al, 1995;Howad and Kempken, 1997;Dutilleul et al, 2005;Vidal et al, 2007), as yet only two forward or reverse genetic strategies have been employed to study the function of complex II in plants (Leó n et al, 2007;Roschzttardtz et al, 2009). These studies revealed that disruption of the expression of the SDH1-1 gene results in alterations in gametophyte development, pollen abortion, and reduced seed set (Leó n et al, 2007) and that the absence of SDH2-3 in Arabidopsis thaliana seeds appears to slow their germination (Roschzttardtz et al, 2009). Furthermore, again by contrast with the other complexes of the inner mitochondrial membrane (see for example, Millar et al, 1993;Raghavendra et al, 1994;Sweetlove et al, 2002;Garmier et al, 2008), relatively few specific inhibitors of this complex have been found (Miyadera et al, 2003;Horsefield et al, 2006;Mogi et al, 2009).…”