The Plant Mitochondrial TAT Pathway Is Essential for Complex III Biogenesis

Abstract

Highlights d The plant mitochondrial TATB protein is required for complex III biogenesis d mttatb truncation mutants accumulate a late-stage complex III assembly intermediate d Plant mitochondria contain a functional twin arginine translocation pathway

Dual targeting of TatA points to a chloroplast-like Tat pathway in plant mitochondria

“…In this case, TatA has a bifunctional role, i.e., it provides both, TatA and TatB activity (Blaudeck et al, 2005; Barnett et al, 2008; Jongbloed et al, 2006). A comparable, bifunctional role was recently suggested also for the mitochondrial TatB-like protein to explain the presumed lack of a TatA component in mitochondria (Schäfer et al, 2020). This cannot finally be excluded at this point but appears less likely, considering the import of TatA into mitochondria observed here.…”

“…As yet, this machinery is assumed to consist of a mitochondrially encoded TatC-orthologue (OrfX, Sünkel et al, 1994) and a nuclearly encoded TatB-like protein, a structural analogue of thylakoidal TatB (Carrie et al, 2016). The latter was recently shown to be essential for the biogenesis of complex III of the respiratory electron transport chain, which strongly suggests that a Tat-like transport pathway is operating also in plant mitochondria (Schäfer et al, 2020).…”

“…The apparent lower efficiency of TatA transport into mitochondria vs. chloroplasts might point to a low demand for Tat translocase in this organelle. To date, solely a single substrate of this pathway has been identified which is the mitochondrial Rieske Fe/S protein (Schäfer et al, 2020). Further substrates might be detected in the future but it appears unlikely that the number will raise very much considering that in bacteria Tat transport is largely restricted to proteins that demand for cytoplasmic insertion of metal ions or complex cofactors prior to membrane translocation (Palmer and Berks, 2012), like NADPH (Halbig et al, 1999) or Fe/S clusters (Molik et al, 2001).…”

“…Moreover, a TatB-like protein was recently identified which shows considerable structural homology to TatB (Carrie et al, 2016), although sequence analyses suggest that the two genes are not derived from a common ancestor. Recently, it was shown that this TatB-like protein is in fact essential for the topogenesis of plant mitochondrial Rieske proteins (Schäfer et al, 2020).…”

Gene atlas of iron‐containing proteins in Arabidopsis thaliana

“…The insertion of Fe‐S clusters into proteins of these respiratory chain complexes necessitate additional assembly factors, as reviewed recently (Meyer et al ., 2019). Notably, the translocation of the Rieske Fe‐S protein (Figure 1b) present in complex III uses a mitochondrial twin arginine transport (Tat) pathway formed by TAT A and TAT B proteins (Schäfer et al ., 2020), similar to the Tat transport system of the plastid Rieske Fe‐S protein (PetC) across the thylakoid membrane. Concerning cytosol, Fe‐S proteins intervene in translation (e.g.…”