Mitochondrial Complex II Is Essential for Gametophyte Development in Arabidopsis

Abstract

Mitochondrial complex II (succinate dehydrogenase [SDH]) is part of the tricarboxylic acid cycle and the respiratory electron transport chain. Its flavoprotein subunit is encoded by two nuclear genes, SDH1-1 and SDH1-2, in Arabidopsis (Arabidopsis thaliana). The SDH1-2 gene is significantly expressed only in roots, albeit at very low level, and its disruption has no effect on growth and development of homozygous mutant plants. In contrast, SDH1-1 transcripts are ubiquitously expressed, with highest expression in flowers. Disruption of the SDH1-1 gene results in alterations in gametophyte development. Indeed, heterozygous SDH1-1/sdh1-1 mutant plants showed normal vegetative growth, yet a reduced seed set. In the progeny of selfed SDH1-1/sdh1-1 plants, distorted segregation ratios were observed, and no homozygous mutant plants were obtained. Reciprocal test crosses with the wild type demonstrated that the mutated sdh1-1 allele is not transmitted through the male gametophyte and is only partially transmitted through the female gametophyte. Consistently, microscopic analysis showed that mutant microspores develop normally until the vacuolated microspore stage, but fail to undergo mitosis I, and then cell structures are degraded and cell content disappears. On the other hand, half the mutant embryo sacs showed arrested development, either at the two-nucleate stage or before polar nuclei fusion. Down-regulation of SDH1-1 by RNA interference results in pollen abortion and a reduced seed set, as in the insertional mutant. Altogether, our results show that SDH1-1, and therefore complex II, are essential for gametophyte development.

Comparison of global responses to mild deficiency and excess copper levels in Arabidopsis seedlings

“…According to the oxidative stress that Cu has been proposed to induce, one of the best representatives in this category was CSD1, which was already reported to respond to Cu status, and was confirmed by qPCR under our conditions. Moreover, the expression of a nuclear gene encoding the flavoprotein subunit of succinate dehydrogenase, SDH1-2, 39 was also checked and confirmed (Fig. 2), indicating the mitochondrial involvement in the perception/ signalling of these oxidative stress conditions.…”

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

“…S5). TTFA and carboxin are generally described as complex II inhibitors in mammalian and plant systems, causing decreased SQR activity and mitochondrial respiration rates at high micromolar to millimolar concentrations (Byun et al, 2008;JardimMesseder et al, 2015;León et al, 2007;Miyadera et al, 2003;Ramsay et al, 1981). As noted previously, sensitivity of SQR to these inhibitors varies between different species; mammals show a very high sensitivity with IC 50 values in micromolar concentrations (Miyadera et al, 2003), whereas Arabidopsis SQR is less sensitive, showing inhibitory effects at millimolar concentrations (Supplemental Fig.…”

“…As noted previously, sensitivity of SQR to these inhibitors varies between different species; mammals show a very high sensitivity with IC 50 values in micromolar concentrations (Miyadera et al, 2003), whereas Arabidopsis SQR is less sensitive, showing inhibitory effects at millimolar concentrations (Supplemental Fig. S5; León et al (2007); Jardim-Messeder et al (2015). It has also been shown that TTFA binds to a site within SDH3/4 based on x-ray crystallography (Sun et al, 2005).…”

“…While this effect was linked to SDH1 through a complementation assay, it could not be independently confirmed with knockout plants, because loss of SDH1 is embryo lethal in Arabidopsis León et al, 2007). To independently investigate the link between SDH and SA-induced GSTF8 response, we therefore crossed an SDH assembly factor knockdown line, sdhaf2, that has lower SDH activity with Col-0 containing the GSTF8:luciferase (GSTF8:luc) reporter gene (JC66, referred to as wild type in this manuscript; Gleason et al (2011).…”

“…In mammals, complex II influences reperfusion injury through mtROS production via reverse electron transport after succinate accumulation (Chouchani et al, 2014). However, the relative importance of mtROS generated from complex II in plants has been unclear, and knockout of the SDH complex or its assembly factors in plants is lethal, largely preventing its direct study through gene deletion in plants León et al, 2007). This limitation changed when a point mutation of SDH1-1 (dsr1) was identified that did not knockout SDH, but instead lowered SDH activity and decreased mitochondrial ROS production.…”