Protein transport into complex plastids
Prof. Dr. Uwe-G. Maier
Laboratory for Cell Biology
Karl-von-Frisch Str. 8
Phone: +49 6421 28 21547
Complex plastids are surrounded by three or four membranes and evolved after the engulfment and intracellular reduction of a phototrophic cell containing a primary plastid surrounded by two membranes within another eukaryote (secondary endosymbiosis). Important algal groups harbor complex plastids: peridinin-containing dinoflagellates and phototrophic euglenoids possess plastids surrounded by three membranes, whereas heterokont algae, haptophytes and apicomplexa have a four-membrane bound plastid. Further groups are the cryptophytes and chlorarachniophytes, which are morphological intermediates in that these groups a remnant of the cytoplasm of the secondary endosymbiont is maintained between the outer and inner membrane pair of the complex plastid. This cytoplasm, the periplastidal compartment (PPC), is devoid of typical eukaryotic compartments such as e.g. a mitochondrion or a Golgi apparatus, but it still harbors 80S ribosomes and a pigmy nucleus, the nucleomorph.
We are studying protein import of nucleus-encoded plastid proteins into complex plastids of a heterokont alga, the diatom Phaeodactylum tricornutum. In our work in the CRC593, we have identified a translocon machinery, called SELMA (symbiont specific ERAD-like machinery) embedded in the second outermost plastid membrane. For this modified ERAD-like system, we have isolated at least most of the components and characterized important players in respect to their localization and their binding partners. In addition, we demonstrated that SELMA is not restricted to diatoms, instead present in other secondary-evolved organisms at the same cellular localization.
Aims of the project:
Although the characterization of some SELMA-components is still underway, we have started to determine other factors of the second outermost plastid membrane. For this, we separate the respective membrane from other cellular compartments and determine the protein component via mass spectroscopy. In addition, we will analyze how proteins are directed to the second outermost membrane. Further important issues are membrane proteins. We will study how these proteins find their individual cellular targets.
Figure 1: Current model of preprotein import into the complex plastid of P. tricornutum: Nucleus-encoded plastid-destined proteins are co-translationally imported into the ER lumen via Sec61. Import across the 2nd outermost membrane is mediated by SELMA with the sDer proteins presumably forming the protein-conducting pore. Once protruding into the PPC, preproteins are ubiquitinated by the catalytic triad composed of sUba1, sUbc4 and ptE3P. sCdc48 aided by sUfd1 pulls the preprotein into the PPC. For proper maturation and further import preproteins have to be deconjugated, which is carried out by the ubiquitin isopeptidase ptDUP.
Simone Stork, wiss. Mitarbeiterin, firstname.lastname@example.org, Phone: 282 1542
Julia Lau, wiss. Mitarbeiterin, email@example.com, Phone: 282 1542
Bolte K, Gruenheit N, Felsner G, Sommer MS, Maier UG, Hempel F (2011) Making new out of old: Recycling and modification of an ancient protein translocation system during eukaryotic evolution. BioEssays Published Online: 21 MAR 2011, DOI : 10.1002/bies.201100007
Felsner G, Sommer MS, Gruenheit N, Hempel F, Moog D, Zauner S, Martin W, Maier UG (2010) ERAD components in organisms with complex red plastids suggest recruitment of a preexisting protein transport pathway for the periplastid membrane. Genome Biol. Evol. 3, 140-150.
Felsner G, Sommer MS, Maier UG (2010) The physical and functional borders of transit peptide-like sequences in secondary endosymbionts. BMC Plant Biol. 10, 223.
Hempel F, Felsner G, Maier UG (2010) New mechanistic insights into pre-protein transport across the second outermost plastid membrane of diatoms. Mol. Microbiol. 76, 793-801.
Bullmann L, Haarmann R, Mirus O, Bredemeier R, Hempel F, Maier UG, Schleiff E (2010) Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J. Biol. Chem. 285, 6848-6856.
Tillich M, Sy VL, Schulerowitz K, von Haeseler A, Maier UG, Schmitz-Linneweber C (2009) Loss of matK RNA editing in seed plant chloroplasts. BMC Evol. Biol. 13, 201.
Spork S, Hiss JA, Mandel K, Sommer M, Kooij TW, Chu T, Schneider G, Maier UG, Przyborski JM (2009) An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Eukaryot. Cell. 8, 1134-1145.
Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic Footprints of a Cryptic Plastid Endosymbiosis in Diatoms. Science 324, 1724-1726.
Hempel F, Bullmann L, Lau J, Zauner S, Maier UG (2009) s-ERAD dependent pre-protein transport across the 2nd outermost plastid membrane of diatoms. Mol. Biol. Evol. 26, 1781-1790.
Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, Maier UG (2009) Protein Targeting into Secondary Plastids. J. Eukaryot. Microbiol. 56, 9–15.
Geissinger O, Herlemann DP, Mörschel E, Maier UG, Brune A (2009) The ultramicrobacterium Elusimicrobium minutum gen. nov., sp. nov., the first cultivated representative of the Termite Group 1 phylum. Appl. Environ. Microbiol. 75, 2831-2840.
Rüdinger M, Funk HT, Rensing SA, Maier UG, Knoop V (2009) RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol. Genet. Genomics. 281, 473-481.
Bozarth A, Maier UG, Zauner S (2009) Diatoms in biotechnology: modern tools and applications. Appl. Microbiol. Biotechnol. 82, 195-201.
Kleine T, Maier UG, Leister D (2008) DNA Transfer From Organelles to the Nucleus: The Idiosyncratic Genetics of Endosymbiosis. Annu. Rev. Plant. Biol. 60, 115-138.
Frommolt R, Werner S, Paulsen H, Goss R, Wilhelm C, Zauner S, Maier UG, Grossman AR, Bhattacharya D, Lohr M (2008) Ancient recruitment by chromists of green algal genes encoding enzymes for carotenoid biosynthesis. Mol. Biol. Evol. 25, 2653-2667.
Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, Schmitz-Linneweber C, Börner T, Tillich M (2008) Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol. 6, 36.
Bolte K, Kawach O, Prechtl J, Gruenheit N, Nyalwidhe J, Maier UG (2008) Complementation of a phycocyanin-bilin lyase from Synechocystis sp. PCC 6803 with a nucleomorph-encoded open reading frame from the cryptophyte Guillardia theta. BMC Plant Biol. 8, 56.
Kneip C, Voss C, Lockhart PJ, Maier UG (2008) The cyanobacterial endosymbiont of the unicellular algae Rhopalodia gibba shows reductive genome evolution. BMC Evol Biol. 8, 30.
Oreb M, Zoryan M, Vojta A, Maier UG, Eichacker LA, Schleiff E (2007) Phospho-mimicry mutant of atToc33 affects early development of Arabidopsis thaliana. FEBS Lett. 581, 5945-5951.
Funk HT, Berg S, Krupinska K, Maier UG, Krause K (2007) Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biology 7, 45.
Gould SB, Fan E, Hempel F, Maier U-G, Kloesgen RB (2007) Translocation of a phycoerythrin alpha subunitacross five biological membranes. J Biol Chem. 282, 30295-30302.
Hempel F, Bozarth A, Sommer MS, Zauner S, Przyborski JM, Maier UG. (2007) Transport of nuclear-encoded proteins into secondarily evolved plastids. Biol Chem. 388, 899-906.
Gruber A, Vugrinec S, Hempel F, Gould SB, Maier UG, Kroth PG (2007) Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol. Biol. 64, 519–530.
Kneip C, Lockhart P, Voss C, Maier U-G. (2007) Nitrogen fixation in eukaryotes--new models for symbiosis. BMC Evol Biol. 7, 55.
Sommer MS, Gould SB, Lehmann P, Gruber A, Przyborski JM, Maier U-G (2007) Der1-Mediated Pre-Protein Import into the Periplastid Compartment of Chromalveolates? Mol. Biol. Evol. 24, 918–928.
Teich R, Zauner S, Baurain D, Brinkmann H, Petersen J (2007) Origin and Distribution of Calvin Cycle Fructose and Sedoheptulose Bisphosphatases in Plantae and Complex Algae. A Single Secondary Origin of Complex Red Plastids and Subsequent Propagation via Tertiary Endosymbioses. Protist. 158, 263-276.