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Institut für Pflanzengenetik
Logo Leibniz Universität Hannover
Institut für Pflanzengenetik
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Research Projects

Research of the Plant Proteomics department is focused on the energy metabolism of plants, particularly on investigating mitochondrial functions in the context of photosynthesis. Compared to animal mitochondria, the mitochondria of plants have much extended functions. Plant mitochondria are involved in managing stress situations, they stabilize the redox balance of the plant cell and they metabolically interact with chloroplasts to maintain photosynthesis. Our department is currently active in investigation the following research topics:

1. Supramolecular structure of the respiratory chain in the mitochondria of plants

Prerequisite for oxidative phosphorylation (OXPHOS) in mitochondria are five protein complexes termed NADH dehydrogenase (complex I), succinate dehydrogenase (complex II), cytochrome c reductase (complex III), cytochrome c oxidase (complex IV), and ATP synthase (complex V). Mounting evidence has been presented that these complexes form defined supramolecular assemblies designated “respiratory supercomplexes” or “respirasomes”. Using gentle membrane solubilization and native gel electrophoresis procedures, several types of supercomplexes have been identified in higher plants and green alga: (i) a I+III2 supercomplex, (ii) III2+IV1-2 supercomplexes, (iii) I+III2+IV1-4 supercomplexes and (iv) dimeric ATP synthase ([1]-[4]). The structures of several of these supercomplexes were characterized for the first time using electron microscopy in combination with single particle analysis ([5]-[12]). ATP synthase monomers were shown to interact within the dimeric ATP synthase supercomplex in a way that bends the inner mitochondrial membrane. This bending contributes to cristae formation of the inner mitochondrial membrane ([13]-[15]). The physiological roles of respiratory supercomplexes are currently investigated in our research department.

2. Special functions of respiratory chain complexes in the mitochondria of plants

The respiratory chain of plant mitochondria has several special features: (i) respiratory electron transport is very much branched due to the presence of numerous so-called “alternative” oxidoreductases, (ii) the mitochondrial genomes of plants code for more subunits of respiratory protein complexes than those of heterotrophic eukaryotes, which requires special assembly pathways for these protein complexes and (iii) the protein complexes of the respiratory chain contain additional subunits that allow them to carry out secondary or modified functions. A project was started to systematically characterize the subunits of OXPHOS complexes in plants, which is based on protein separations by two-dimensional Blue-native / SDS polyacrylamide gel electrophoresis and protein identifications by Edman degradation and mass spectrometry and more recently by Complexome profiling ([16]-[19]). Numerous plant-specific subunits of respiratory protein complexes were discovered. The functions of these extra-proteins are studied by physiological analyses and by reverse genetics. Complex III of plants includes the two subunits mitochondrial processing peptidase, which cleaves off presequences of imported proteins after their transport into mitochondria has been completed ([20]-[31]). Complex I includes proteins resembling gamma-type carbonic anhydrases and associates with a galactono lactone dehydrogenase ([32]-[45]). Evidence has been presented that the carbonic anhydrases are involved in a CO2 recycling pathway between mitochondria and chloroplasts, which is especially important during photorespiration ([46][47]). Also, complexes II and IV include additional subunits in the mitochondria of plants [48]. Experimental data have been presented that some of the extra complex II subunits represent pieces of conserved subunits of this protein complex [49]. The reason for the fragmentation of complex II subunits during plant evolution is not understood so far. The stability of complex IV has been shown to depend on the presence of cytochrome c [50].  

3. Proteomic approach to discover novel mitochondrial functions in plants: from Gel-based analyses towards Complexome profiling

Proteome projects have been carried out to systematically characterize mitochondrial functions in the model plants Arabidopsis thaliana and Medicago truncatula. In a first attempt, mitochondrial proteins were separated by two-dimensional IEF / SDS polyacrylamide gel electrophoresis (PAGE) and identified by mass spectrometry ([51]-[53]). In parallel, mitochondrial protein complexes were systematically characterized based on protein separations by two-dimensional Blue native/ SDS PAGE in combination with mass spectrometry ([54]-[58]). The GelMap internet platform has been created to promote accession of the experimental data sets (https://gelmap.de/). More recently, a Complexome profiling strategy has been employed for in depth analysis of mitochondrial protein complexes in plants [59]. This experimental approach is based on protein separation by a one-dimensional Blue native PAGE. The resulting gel is dissected into 70 slices, which are finally used for shotgun proteome analyses. By this approach, more than 1,300 proteins have been described, most of which form part of protein complexes. A new internet portal has been developed for data accession (https://complexomemap.de/).

4. Amino acid catabolism in plants

Plant cells can synthesize all 20 proteinogenic amino acids. The biochemical synthesis pathways mainly reside in the plastids. At the same time, plant cells can degrade all amino acids [60]. This especially takes place in the mitochondria. The degradation of amino acids is especially relevant at defined developmental stages of plants, like during germination (breakdown of storage proteins) and senescence (recycling of organic compounds). Plants also use amino acids as compatible osmolytes in the course of their responses towards abiotic stress factors like drought or salt. Especially proline is of key importance in this context. Upon stress release (for instance watering of plants after a period of drought), proline has to be rapidly degraded. The function and regulation of proline dehydrogenase, which catalyzes the first step of the mitochondrial proline degradation pathway, has been recently characterized in plants ([61][62]). Finally, plants also use amino acid breakdown to fuel the respiratory chain under carbohydrate shortage conditions (e.g. short day conditions or extended darkness). In this context, branched chain amino acid catabolism is especially important because it efficiently provides electrons for the respiratory chain, either via NADH formation or directly via the ETF/ETFQO system [63][64]. A new enzyme involved in valine and isoleucine metabolism has recently been discovered and functionally characterized in plants [65]. Furthermore, cysteine catabolism has been found to be relevant for the plant stress response as well as the plant response with respect to extended darkness [66][67]. The enzymes involved in this pathway are currently investigated by Dr. Tatjana Hildebrandt in our research department.

5. Protein transport into plant mitochondria

Import of proteins into the mitochondrial compartment is a complex process, which involves the coordinated action of a variety of different components including receptors, translocases, chaperones and proteases (reviewed in [68]). This so-called mitochondrial protein import apparatus of plant cells differs from the one of heterotrophic cells in many respects, which most likely is a consequence of the occurrence of plastids. Our research focuses on the mitochondrial processing peptidase, which in plants forms part of complex III of the respiratory chain ([69]-[73]), and on the preprotein translocase of the outer mitochondrial membrane, which includes plant specific preprotein receptors ([74]-[76]).

6. Supramolecular structure of photosystems in higher plants

In parallel to the characterization of mitochondrial protein complexes, our department is studying the structure and function of the thylakoid membrane of higher plants by two-dimensional Blue-native / SDS-PAGE. This method was optimized for the analysis of chloroplast proteins and protein complexes [77][78]. Further improvement of native gel electrophoresis procedures allowed insights into the supramolecular structure of the protein complexes involved in photosynthesis in higher plants [79][80]. Finally, a 2D GelMap (https://gelmap.de/) has been created for the chloroplast proteins of Arabidopsis thaliana [81].

7. New methods and method developments

Blue native (BN) polyacrylamide gel electrophoresis (PAGE) has been developed by Hermann Schägger in the early 1990th. The procedure resembles SDS PAGE but SDS is substituted by the protein dye Coomassie blue. It allows separating proteins and protein complexes according to molecular mass in a native state. If BN PAGE is combined with SDS PAGE, subunits of protein complexes can be separated (they form characteristic vertical rows of spots on the resulting 2D gels). In cooperation with Hermann Schägger, our research department contributed to standardizing and further developing Blue native PAGE [82]. Several of our publications report the optimization of BN PAGE for analyzing biochemical fractions from plants ([83]-[87]). A biochemical method was introduced to investigate the subunit topology of protein complexes which is based on BN PAGE in the presence of very low concentrations of SDS [88]. Furthermore, protocols have been developed to combine BN PAGE and protein labeling by fluorophores (BN DIGE, [89][90]). Our research department developed internet platforms for optimal accession of gel-based protoeme data (www.gelmap.de, [91][92]) and of Complexome profiling data (www.complexomeprofiling.de).

 

Publications cited

1. Supramolecular structure of the respiratory chain in the mitochondria of plants

[1] Eubel, H., Jänsch, L. and Braun, H.P. (2003) New insights into the respiratory chain of plant mitochondria: supercomplexes and a unique composition of complex II. Plant Physiol. 133, 274-286.

[2] Eubel, H., Heinemeyer, J. and Braun, H.P. (2004) Identification and characterization of respirasomes in potato mitochondria. Plant Physiol. 134, 1450-1459.

[3] Eubel, H., Heinemeyer, J., Sunderhaus, S., and Braun, H.P. (2004) Respiratory chain supercomplexes in plant mitochondria. Plant Physiology and Biochemistry 42, 937-942.

[4] Sunderhaus, S., Klodmann, J., Lenz, C. and Braun, H.P. (2010) Supramolecular structure of the OXPHOS system in highly thermogenic tissue of Arum maculatum. Plant Physiol. Biochem. 48, 265-272.

[5] Dudkina, N.V., Eubel, H., Keegstra, W., Boekema, E.J. and Braun, H.P. (2005) Structure of a mitochondrial supercomplex formed by respiratory chain complexes I and III. Proc. Natl. Acad. Sci. USA 102, 3225-3229.

[6] Dudkina, N.V., Heinemeyer, J., Sunderhaus, S., Boekema, E.J. and Braun, H.P. (2006) Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends in Plant Science 11, 232-240.

[7] Heinemeyer, J., Braun, H.P., Boekema, E.J. and Kuril, R. (2007) A structural model of the cytochrome c reductase / oxidase supercomplex from yeast mitochondria. J. Biol. Chem. 282, 12240-12248.

[8] Boekema, E.J. and Braun, H.P. (2007) Supramolecular structure of the mitochondrial Oxidative Phosphorylation System. J. Biol. Chem. 282, 1-4.

[9] Peters, K., Dudkina, N.V., Jänsch, L., Braun, H.P. & Boekema, E.J. (2008) A structural investigation of complex I and I+III2 supercomplex from Zea mays at 11-13 Å resolution: assignment of the carbonic anhydrase domain and evidence for structural heterogeneity within complex I. Biochim. Biophys. Acta (Bioenergetics) 1777, 84-93.

[10] Dudkina, N.V., Sunderhaus, S., Boekema, E.J. & Braun, H.P. (2008) The higher level of the oxidative phosphorylation system: mitochondrial supercomplexes. J. Bioenerg. Biomembr. 40, 419–424.

[11] Bultema, J.B., Braun, H.P., Boekema, E.J. and Kouril, R. (2009) Megacomplex organization of the oxidative phosphorylation system by structural analysis of respiratory supercomplexes from potato. Biochim. Biophys. Acta (Bioenergetics) 1787, 60-67.

[12] Dudkina, N.V., Kouřil, R., Peters, K., Braun, H.P. and Boekema, E.J. (2010) Structure and function of mitochondrial supercomplexes. Biochim. Biophys. Acta (Bioenergetics) 1797, 664-670.

[13] Dudkina, N.V., Heinemeyer, H., Keegstra, W., Boekema, E.J. and Braun, H.P. (2005) Structure of dimeric ATP synthase from mitochondria: An angular association of monomers induces the strong curvature of the inner membrane. FEBS Lett. 579, 5769-5772.  

[14] Dudkina, N.V., Sunderhaus, S., Braun, H.P. and Boekema, E.J. (2006) Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria. FEBS Lett. 580, 3427-3432.

[15] Dudkina, N.V., Oostergetel, G. Lewejohann, D., Braun, H.P. and Boekema, E.J. (2010) Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography. Biochim. Biophys. Acta (Bioenergetics) 1797, 272–277.

2. Special functions of respiratory chain complexes in the mitochondria of plants

[16] Jänsch, L., Kruft, V., Schmitz, U.K. and Braun, H.P. (1996) New insights into the composition, molecular mass and stoichiometry of the protein complexes of plant mitochondria. Plant J. 9, 357-368.

[17] Eubel, H., Jänsch, L. and Braun, H.P. (2003) New insights into the respiratory chain of plant mitochondria: supercomplexes and a unique composition of complex II. Plant Physiol. 133, 274-286.

[18] Klodmann, J., Rode, C., Senkler, M., and Braun, H.P. (2011) The protein complex proteome of plant mitochondria. Plant Physiol. 157, 587-598.

[19] Senkler, J., Senkler, M., Eubel, H., Hildebrandt, T., Lengwenus, C., Schertl, P., Schwarzländer, M., Wagner, S., Wittig, I., and Braun, H.P. (2017) The mitochondrial complexome of Arabidopsis thaliana. Plant J. 89, 1079-1092.

Complex III

[20] Braun, H.P. and Schmitz, U.K. (1992) Affinity purification of cytochrome c reductase from plant mitochondria. Eur. J. Biochem. 208, 761-767.

[21] Braun, H.P., Emmermann, M., Kruft, V. and Schmitz, U.K. (1992) The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. EMBO J. 11, 3219-3227.

[22] Emmermann, M., Braun H.P. and Schmitz, U.K. (1993) The two high molecular weight subunits of cytochrome c reductase from potato are immunologically related to the mitochondrial processing enhancing protein. Biochim. Biophys. Acta 1142, 306-310.

[23] Emmermann, M., Braun, H.P., Arretz, M. and Schmitz, U.K. (1993) Characterization of the bifunctional cytochrome c reductase / processing peptidase complex from potato mitochondria. J. Biol. Chem. 268, 18936-18942.

[24] Braun, H.P., Kruft, V. and Schmitz, U.K. (1994) Molecular identification of the ten subunits of cytochrome c reductase from potato mitochondria. Planta 193, 99-106.

[25] Emmermann, M., Braun, H.P. and Schmitz, U.K. (1994) The mitochondrial processing peptidase from potato: A self-processing enzyme encoded by two differentially expressed genes. Mol. Gen. Genet. 245, 237-245.

[26] Braun, H.P., Emmermann, M., Kruft, V., Bödicker, M. and Schmitz, U.K. (1995) The general mitochondrial processing peptidase from wheat is integrated into the cytochrome bc1 complex of the respiratory chain. Planta 195, 396-402.

[27] Braun, H.P. and Schmitz, U.K. (1995) Are the "core" proteins of the mitochondrial bc1 complex evolutionary relics of a processing peptidase? Trends Biochem. Sci. 20, 171-175.

[28] Braun, H.P. and Schmitz, U.K. (1995) The bifunctional cytochrome c reductase / processing peptidase complex from plant mitochondria. J. Bioenerg. Biomembr. 27, 423-436.

[29] Jänsch, L., Kruft, V., Schmitz, U.K. and Braun, H.P. (1995) Cytochrome c reductase from potato does not comprise three core proteins but contains an additional low molecular weight subunit. Eur. J. Biochem. 228, 878-885.

[30] Braun, H.P. and Schmitz, U.K. (1997) Molecules In Focus: The cytochrome c reductase / mitochondrial processing peptidase complex. Int. J. Biochem. Cell Biol. 29, 1043-1045.

[31] Brumme, S., Kruft, V., Schmitz, U.K. and Braun, H.P. (1998) New insights into the co-evolution of cytochrome c reductase and the mitochondrial processing peptidase. J. Biol. Chem. 273, 13143-13149.

Complex I

[32] Perales, M., Parisi, G., Fornasari, M.S., Colaneri, A., Villarreal, F., Gonzalez-Schain, N., Gómez-Casati, D., Braun, H.P., Araya, A., Echave, J. and Zabaleta, E. (2004) Gamma carbonic anhydrase subunits physically interact within complex I of plant mitochondria. Plant Mol. Biol. 56, 947-957.

[33] Perales, M., Eubel, H. Heinemeyer, H., Colaneri, A., Zabaleta, E. and Braun, H.P. (2005) Disruption of a nuclear gene encoding a mitochondrial gamma carbonic anhydrase reduces complex I and supercomplex I+III2 levels and alters mitochondrial physiology in Arabidopsis. J. Mol. Biol. 350, 263-277.

[34] Sunderhaus, S., Dudkina, N., Jänsch, L., Klodmann, J., Heinemeyer, J., Perales, M., Zabaleta, E., Boekema, E. and Braun, H.P. (2006) Carbonic anhydrase subunits form a matrix-exposed domain attached to the membrane arm of mitochondrial complex I in plants. J. Biol. Chem. 281, 6482-6488.

[35] Klodmann, J. Sunderhaus, S., Nimtz, M., Jänsch, L. and Braun, H.P. (2010) Internal architecture of mitochondrial complex I from Arabidopsis thaliana. The Plant Cell 22, 797–810.

[36] Klodmann, J. and Braun, H.P. (2011) Proteomic approach to characterize mitochondrial complex I from plants. Phytochemistry 72, 1071-1080.

[37] Schertl, P., Sunderhaus, S., Klodmann, J., Gergoff, G., Bartoli, C.G. and Braun, H.P. (2012) L-galactono-1,4-lactone dehydrogenase (GLDH) forms part of three subcomplexes of mitochondrial complex I in Arabidopsis thaliana. J. Biol. Chem. 287, 14412–14419.

[38] Peters K., Belt, K. and Braun, H.P. (2013) 3D gel map of Arabidopsis complex I. Frontiers in Plant Proteomics, doi: 10.2289/fpls.2013.00153.

[39] Peters, K., Nießen, M., Peterhänsel, C. Späth, B., Hölzle, A., Binder, S., Marchfelder, A. and Braun, H.P. (2012) Complex I - complex II ratio strongly differs in various organs of Arabidopsis thaliana. Plant Mol. Biol. 79, 273–284.

[40] Braun, H.P., Binder, S., Brennicke, A., Eubel, H., Fernie, A.R., Finkemeier, I., Klodmann, J., König, A.C., Kühn, K., Meyer, E., Obata, T., Schwarzländer, M., Takenaka, M. and Zehrmann, A. (2014) The life of plant mitochondrial complex I. Mitochondrion 19, 295–313.

[41] Fromm, S., Senkler, J., Eubel, H., Peterhänsel, C. and Braun, H.P. (2016) Life without complex I: Proteome analyses of an Arabidopsis mutant lacking the mitochondrial NADH dehydrogenase complex. J. Exp. Botany 67, 3079–3093.

[42] Fromm, S., Braun, H.P. and Peterhänsel, C. (2016) Mitochondrial gamma carbonic anhydrases are required for complex I assembly and plant reproductive development. New Phytologist 211, 194–207.

[43] Fromm, S., Senkler, J., Peterhänsel, C. and Braun, H.P. (2016) The carbonic anhydrase domain of plant mitochondrial complex I. Physiologia Plantarum 157, 289-296.

[44] Fromm, S., Göing, J., Lorenz, C, Peterhänsel, C. and Braun, H.P. (2016) Depletion of the “gamma-type carbonic anhydrase-like” subunits of complex I specifically affects central mitochondrial metabolism in Arabidopsis thaliana. BBA Bioenergetics 1857, 60-71.

[45] Senkler, J., Senkler, M. and Braun, H.P. (2017) Structure and function of complex I in animals and plants – A comparative view. Physiologia Plantarum 161, 6-15.

[46] Braun, H.P. and Zabaleta, E. (2006) Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (complex I) in plants. Physiologia Plantarum 129, 114-122.

[47] Zabaleta, E., Martin, M.V. and Braun, H.P. (2012) A basal carbon concentrating mechanism in plants? Plant Science 187, 97-104.

Complexes II and IV

[48] Millar, A.H., Eubel, H., Jänsch, L., Kruft, V., Heazlewood, L. and Braun, H.P. (2004) Mitochondrial cytochrome c oxidase and succinate dehydrogenase contain plant-specific subunits. Plant Mol. Biol. 56, 77-89.

[49] Schikowsky, C., Senkler, J. and Braun, H.P. (2017) SDH6 and SDH7 contribute to anchoring succinate dehydrogenase to the inner mitochondrial membrane in Arabidopsis thaliana. Plant Physiology 173, 1094-1108.

[50] Welchen, E., Hildebrandt, T., Lewejohann, D., Gonzalez, D. and Braun, H.P. (2012) Lack of cytochrome c in Arabidopsis decreases stability of Complex IV and modifies redox metabolism without affecting Complexes I and III. Biochim. Biophys. Acta (Bioenergetics) 1817, 990–1001.

3. Proteomic approach to discover novel mitochondrial functions in plants: from Gel-based analyses towards Complexome profiling

[51] Kruft, V., Eubel, H., Werhahn, W.H., Jänsch, L. and Braun, H.P. (2001) Proteomic approach to identify novel mitochondrial functions in Arabidopsis thaliana. Plant Physiology 127, 1694-1710.

[52] Werhahn, W.H. and Braun, H.P. (2002) Biochemical dissection of the mitochondrial proteome of Arabidopsis thaliana by three-dimensional gel electrophoresis. Electrophoresis 23, 640-646.

[53] Millar, A.H., Heazlewood, L., Kristense, B.K., Braun, H.P. and Møller, IA (2005) The plant mitochondrial proteome. Trends in Plant Science 10, 36-43.

[54] Jänsch, L., Kruft, V., Schmitz, U.K. and Braun, H.P. (1996) New insights into the composition, molecular mass and stoichiometry of the protein complexes of plant mitochondria. Plant J. 9, 357-368.

[55] Eubel, H., Jänsch, L. and Braun, H.P. (2003) New insights into the respiratory chain of plant mitochondria: supercomplexes and a unique composition of complex II. Plant Physiol. 133, 274-286.

[56] Klodmann, J., Rode, C., Senkler, M., and Braun, H.P. (2011) The protein complex proteome of plant mitochondria. Plant Physiology 157, 587-598.

[57] Dubinin, J., Braun, H.P., Schmitz, U.K. and Colditz, F. (2011) The mitochondrial proteome of the model legume Medicago truncatula. Biochim. Biophys. Acta (Proteins and Proteomics) 1814, 1658-1668.

[58] Kiirika, L.M., Behrens, C., Braun, H.P. and Colditz, F. (2013) The mitochondrial complexome of Medicago truncatula. Frontiers in Plant Proteomics, doi: 10.3389/fpls.2013.00084.

[59] Senkler, J., Senkler, M., Eubel, H., Hildebrandt, T., Lengwenus, C., Schertl, P., Schwarzländer, M., Wagner, S., Wittig, I., and Braun, H.P. (2017) The mitochondrial complexome of Arabidopsis thaliana. Plant J. 89, 1079-1092.

4. Amino acid catabolism in plants

[60] Hildebrandt, T., Nunes Nesi, A., Araujo, W.L. and Braun, H.P. (2015) Amino acid catabolism in plants. Mol. Plant 8, 1563-1579.

[61] Schertl, P., Cabassa, C., Saadallah, K., Bordenave, M., Savouré, A. and Braun, H.P. (2014) Integration of proline dehydrogenase into mitochondrial metabolism in Arabidopsis thaliana. FEBS J. 281 (2014) 2794–2804.

[62] Cabassa-Hourton, C., Schertl, P., Bordenave-Jacquemin, M., Saadallah, K., Guivarc’h, A., Planchais, S., Klodmann, J., Eubel, H., Lefebvre-De Vos, D., Ghelis, T., Richard, L., Lebreton, S., Abdelly, C., Carol, P.,  Braun, H.P. and Savouré, A. (2016) Proteomic and functional analysis of proline dehydrogenase 1 link proline catabolism to mitochondrial electron transport in Arabidopsis thaliana. Biochem J. 473, 2623–2634.

[63] Schertl, P. and Braun, H.P. (2014) Respiratory electron transfer pathways in plant mitochondria. Frontiers in Plant Science 5:163, doi: 10.3389/fpls.2014.00163.

[64] Cavalcanti J.H., Quinhones, C.G., Schertl, P., Brito, D.S., Hildebrandt, T., Nunes-Nesi, A., Braun, H.P. and Araújo, WL (2017) The differential impact of amino acids on OXPHOS system activity following carbohydrate starvation in Arabidopsis cell suspensions. Physiologia Plantarum, in press

[65] Schertl, P., Danne, L. and Braun, H.P. (2017) 3-Hydroxyisobutyrate Dehydrogenase is involved in both, Valine and Isoleucine degradation in Arabidopsis thaliana. Plant Physiology, in press

[66] Krüßel, L., Junemann, J., Wirtz, M., Birke, H., Thornton, JD, Browning, L.W., Poschet, G., Hell, R., Balk, J., Braun, H.P. and Hildebrandt, T.M. (2014) The mitochondrial sulfur dioxygenase ETHE1 is required for amino acid catabolism during carbohydrate starvation and embryo development in Arabidopsis thaliana. Plant Physiol. 165, 92-104.

[67] Höfler, S., Lorenz, C., Busch, T., Brinkkötter, M., Tohge, T., Fernie, A., Braun, H.P. and Hildebrandt, T. (2016) Dealing with the sulfur part of cysteine: four enzymatic steps degrade l-cysteine to pyruvate and thiosulfate in Arabidopsis mitochondria. Physiologia Plantarum 157, 352-366.

5. Protein transport into plant mitochondria

[68] Braun, H.P. and Schmitz, U.K. (1999) The protein import apparatus of plant mitochondria. Planta 209, 267-274.

[69] Braun, H.P., Emmermann, M., Kruft, V. and Schmitz, U.K. (1992) The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. EMBO J. 11, 3219-3227.

[70] Braun, H.P. and Schmitz, U.K. (1995) Are the "core" proteins of the mitochondrial bc1 complex evolutionary relics of a processing peptidase? Trends Biochem. Sci. 20, 171-175.

[71] Braun, H.P. and Schmitz, U.K. (1995) The bifunctional cytochrome c reductase / processing peptidase complex from plant mitochondria. J. Bioenerg. Biomembr. 27, 423-436.

[72] Braun, H.P. and Schmitz, U.K. (1997) Molecules In Focus: The cytochrome c reductase / mitochondrial processing peptidase complex. Int. J. Biochem. Cell Biol. 29, 1043-1045.

[73] Brumme, S., Kruft, V., Schmitz, U.K. and Braun, H.P. (1998) New insights into the co-evolution of cytochrome c reductase and the mitochondrial processing peptidase. J. Biol. Chem. 273, 13143-13149.

[74] Jänsch, L., Kruft, V., Schmitz, U.K. and Braun, H.P. (1998) Unique composition of the preprotein translocase of the outer mitochondrial membrane from plants. J. Biol. Chem. 273, 17251-17257.

[75] Werhahn, W.H., Niemeyer, A., Jänsch, L., Kruft, V., Schmitz, U.K. and Braun, H.P. (2001) Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis thaliana: identification of multiple forms of TOM20. Plant Physiol. 125, 943-954.

[76] Werhahn, W., Jänsch, L. and Braun, H.P. (2003) Identification of novel subunits of the TOM complex from Arabidopsis thaliana. Plant Physiol. Biochem. 41, 407-416.

6. Supramolecular structure of photosystems in higher plants

[77] Kügler, M., Jänsch, L., Kruft, V., Schmitz, U.K. and Braun, H.P. (1997) Analysis of the chloroplast protein complexes by blue-native polyacrylamide gel electrophoresis. Photosynthesis Research 53, 35-44.

[78] Kügler, M., Kruft, V., Schmitz, U.K. and Braun, H.P. (1998) Characterization of the PetM subunit of the b6f complex from higher plants. J. Plant Physiol. 153, 581-586.

[79] Heinemeyer, J., Eubel, H., Wehmhöner, D., Jänsch, L. and Braun, H.P. (2004) Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. Phytochemistry 65, 1683-1692.

[80] Behrens, C., Hartmann, K., Sunderhaus, S., Braun, H.P. and Eubel, H. (2013) Theoretical and experimental analysis of native isoelectric points of membrane protein complexes of Arabidopsis chloroplasts and mitochondria. Biochim. Biophy. Acta (Biomembranes) 1828, 1036–1046.

[81] Behrens, C., Blume, C., Senkler, M., Eubel, H., Peterhänsel, C. and Braun, H.P. (2013) the ‘protein complex proteome’ of chloroplasts in Arabidopsis thaliana. J. Proteomics 91, 73-83.

7. New methods and method developments

[82] Wittig, I., Braun, H.P. and Schägger, H. (2006) Blue-Native PAGE. NATURE Protocols 1, 418-428.

[83] Werhahn, W.H. and Braun, H.P. (2002) Biochemical dissection of the mitochondrial proteome of Arabidopsis thaliana by three-dimensional gel elelctrophoresis. Electrophoresis 23, 640-646.

[84] Eubel, H., Braun, H.P. and Millar, A.H. (2005) Blue-Native PAGE in Plants: a Tool in Analysis of Protein-Protein Interactions. BMC Plant Methods 1, 11 (p 1-13); doi:10.1186/1746-4811-1-11.

[85] Heinemeyer, J., Lewejohann, D. and Braun, H.P. (2007) Blue-native gel electrophoresis for the characterization of protein complexes in plants. Meth. Mol. Biol. 335, 343-352.

[86] Sunderhaus, S., Eubel, H. and Braun, H.P. (2007) Two dimensional blue native / blue native polyacrylamide gel electrophoresis for the characterization of mitochondrial protein complexes and supercomplexes. Meth. Mol. Biol. 372, 315-324.

[87] Schertl, P. and Braun, H.P. (2015) Activity measurements of mitochondrial enzymes in native gels. Meth. Mol. Biol. 1305, 131-138.

[88] Klodmann, J., Lewejohann, D. and Braun, H.P. (2011) Low-SDS Blue native PAGE. Proteomics 11, 1834-1839.

[89] Heinemeyer, J., Scheibe, B., Schmitz, U.K. and Braun, H.P. (2009) Blue native DIGE as a tool for comparative analyses of protein complexes. J. of Proteomics 72, 539–544.

[90] Peters, K. and Braun, H.P. (2012) Comparative analyses of protein complexes by Blue Native DIGE. Meth. Mol. Biol. 854, 145-154.

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[92] Senkler, M. and Braun, H.P. (2012) Functional annotation of 2D protein maps: The GelMap portal. Frontiers in Plant Science, doi: 10.3389/fpls.2012.00087.

 

Cooperations

  • Prof. Dr. Wagner Luiz Araújo, Universidade Federal de Viçosa, Brazil
  • Prof. Dr. E. Boekema, University of Groningen, The Netherlands
  • PD Dr. Ahmed Debez, Centre de Biotechnol, Borj-Cédria, Tunisia
  • Dr. Natalia Dudkina, University of Groningen, The Netherlands
  • Prof. Dr. W. Horst, Hannover University, Germany
  • Prof. Dr. Iris Finkemeier, Münster University, Germany
  • Prof. Dr. L. Jänsch, Gesellschaft for Biotechnol. Research, Braunschweig, Germany
  • Dr. V. Kruft, AB Sciex, Darmstadt, Germany
  • Prof. Dr. A.H. Millar, Perth University, Australia
  • Prof. Dr. Adriano Nunes Nesi, Universidade Federal de Viçosa, Brazil
  • Prof. Dr. Christoph Peterhänsel, Leibniz Universität Hannover, Germany
  • Prof. Dr. Ralf Rabus, Oldenburg University, Germany
  • Prof. Dr. Hardy Rolletschek, IPK Gatersleben, Germany
  • Prof. Dr. H. Schägger, Frankfurt University, Germany
  • Prof. Dr. Markus Schwarzländer, Münster University, Germany
  • Prof. Dr. Arnould Savouré, Paris University, France
  • Prof. Dr. Traud Winkelmann, Leibniz Universität Hannover, Germany
  • Dr. Lars Wöhlbrand, Oldenburg University, Germany
  • Dr. Ilka Wittig, Frankfurt University, Germany
  • Prof. Dr. E. Zabaleta, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina

 

Financial Support

  • Deutsche Forschungsgemeinschaft (DFG)
  • Deutscher Akademischer Austauschdienst (DAAD)
  • Volkswagenstiftung
  • Bayer Crop Science
  • Deutscher Akademischer Austauschdienst (DAAD)
  • Federation of European Biochemical Societies (FEBS)
  • European Molecular Biology Organization (EMBO)
  • Alexander von Humboldt Foundation (AvH)