Advertisement

Planta

, Volume 242, Issue 3, pp 733–746 | Cite as

The extreme Albino3 (Alb3) C terminus is required for Alb3 stability and function in Arabidopsis thaliana

  • Manuela Urbischek
  • Sabine Nick von Braun
  • Thomas Brylok
  • Irene L. Gügel
  • Andreas Richter
  • Minna Koskela
  • Bernhard Grimm
  • Paula Mulo
  • Bettina Bölter
  • Jürgen Soll
  • Elisabeth Ankele
  • Serena SchwenkertEmail author
Original Article

Abstract

Main conclusion

The extreme Alb3 C terminus is important for Alb3 stability in a light dependent manner, but is dispensable for LHCP insertion or D1 synthesis.

YidC/Oxa1/Alb3 dependent insertion of membrane proteins is evolutionary conserved among bacteria, mitochondria and chloroplasts. Chloroplasts are challenged by the need to coordinate membrane integration of nuclear encoded, post-translationally targeted proteins into the thylakoids as well as of proteins translated on plastid ribosomes. The pathway facilitating post-translational targeting of the light-harvesting chlorophyll a/b binding proteins involves the chloroplast signal recognition particle, cpSRP54 and cpSRP43, as well as its membrane receptor FtsY and the translocase Alb3. Interaction of cpSRP43 with Alb3 is mediated by the positively charged, stromal exposed C terminus of Alb3. In this study, we utilized an Alb3 T-DNA insertion mutant in Arabidopsis thaliana lacking the last 75 amino acids to elucidate the function of this domain (alb3∆C). However, the truncated Alb3 protein (Alb3∆C) proved to be unstable under standard growth conditions, resulting in a reduction of Alb3∆C to 20 % of wild-type levels. In contrast, accumulation of Alb3∆C was comparable to wild type under low light growth conditions. Alb3∆C mutants grown under low light conditions were only slightly paler than wild type, accumulated almost wild-type levels of light harvesting proteins and were not affected in D1 synthesis, therefore showing that the extreme Alb3 C terminus is dispensable for both, co- and post-translational, protein insertion into the thylakoid membrane. However, reduction of Alb3∆C levels as observed under standard growth conditions resulted not only in a severely diminished accumulation of all thylakoid complexes but also in a strong defect in D1 synthesis and membrane insertion.

Keywords

Chloroplast Thylakoid membrane Light harvesting complex Photosystem II Chlorophyll 

Notes

Acknowledgments

Michaela Häusler is greatly acknowledged for excellent technical assistance. We would further like to thank Ralph Krafczyk for help with genotyping experiments. Alb3 antisera were a kind gift from Danja Schünemann as well as HCF136 antisera from Peter Westhoff. ATP synthase antisera were kindly provided by Stephan Greiner. Financial support from the German Research Council (DFG, SFB1035, project A4, to JS., SS), the Munich Center for Integrated Protein Science (CiPSM, Exc114/2) to JS, BB and SS, as well as the Academy of Finland Centre of Excellence in Molecular Biology of Primary Producers 271832 to PM and MK and the DFG Research Unit FOR2092 (Gr936 18-1) to BG is acknowledged.

References

  1. Arnon DJ (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15PubMedCentralCrossRefPubMedGoogle Scholar
  2. Bals T, Dunschede B, Funke S, Schunemann D (2010) Interplay between the cpSRP pathway components, the substrate LHCP and the translocase Alb3: an in vivo and in vitro study. FEBS Lett 584:4138–4144CrossRefPubMedGoogle Scholar
  3. Bellafiore S, Ferris P, Naver H, Gohre V, Rochaix JD (2002) Loss of Albino3 leads to the specific depletion of the light-harvesting system. Plant Cell 14:2303–2314PubMedCentralCrossRefPubMedGoogle Scholar
  4. Benz M, Bals T, Gugel IL, Piotrowski M, Kuhn A, Schunemann D, Soll J, Ankele E (2009) Alb4 of Arabidopsis promotes assembly and stabilization of a non chlorophyll-binding photosynthetic complex, the CF1CF0-ATP synthase. Mol Plant 2:1410–1424CrossRefPubMedGoogle Scholar
  5. Cai W, Ma J, Chi W, Zou M, Guo J, Lu C, Zhang L (2010) Cooperation of LPA3 and LPA2 is essential for photosystem II assembly in Arabidopsis. Plant Physiol 154:109–120PubMedCentralCrossRefPubMedGoogle Scholar
  6. Chidgey JW, Linhartova M, Komenda J, Jackson PJ, Dickman MJ, Canniffe DP, Konik P, Pilny J, Hunter CN, Sobotka R (2014) A cyanobacterial chlorophyll synthase-HliD complex associates with the Ycf39 protein and the YidC/Alb3 insertase. Plant Cell 26:1267–1279PubMedCentralCrossRefPubMedGoogle Scholar
  7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  8. Czarnecki O, Grimm B (2012) Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. J Exp Bot 63:1675–1687CrossRefPubMedGoogle Scholar
  9. Czarnecki O, Hedtke B, Melzer M, Rothbart M, Richter A, Schroter Y, Pfannschmidt T, Grimm B (2011) An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell 23:4476–4491PubMedCentralCrossRefPubMedGoogle Scholar
  10. Dalbey RE, Kuhn A, Zhu L, Kiefer D (2014) The membrane insertase YidC. Biochim Biophys Acta 1843:1489–1496CrossRefPubMedGoogle Scholar
  11. Dunschede B, Bals T, Funke S, Schunemann D (2011) Interaction studies between the chloroplast signal recognition particle subunit cpSRP43 and the full-length translocase Alb3 reveal a membrane-embedded binding region in Alb3 protein. J Biol Chem 286:35187–35195PubMedCentralCrossRefPubMedGoogle Scholar
  12. Falk S, Sinning I (2010) The C terminus of Alb3 interacts with the chromodomains 2 and 3 of cpSRP43. J Biol Chem 285:le25–le26 (author reply le26–28) PubMedCentralCrossRefPubMedGoogle Scholar
  13. Falk S, Ravaud S, Koch J, Sinning I (2010) The C terminus of the Alb3 membrane insertase recruits cpSRP43 to the thylakoid membrane. J Biol Chem 285:5954–5962PubMedCentralCrossRefPubMedGoogle Scholar
  14. Gohre V, Ossenbuhl F, Crevecoeur M, Eichacker LA, Rochaix JD (2006) One of two alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas. Plant Cell 18:1454–1466PubMedCentralCrossRefPubMedGoogle Scholar
  15. Granvogl B, Reisinger V, Eichacker LA (2006) Mapping the proteome of thylakoid membranes by de novo sequencing of intermembrane peptide domains. Proteomics 6:3681–3695CrossRefPubMedGoogle Scholar
  16. Jarvi S, Suorsa M, Aro EM (2015) Photosystem II repair in plant chloroplasts—regulation, assisting proteins and shared components with photosystem II biogenesis. Biochim Biophys Acta. doi: 10.1016/j.bbabio.2015.01.006
  17. Jia L, Dienhart M, Schramp M, McCauley M, Hell K, Stuart RA (2003) Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1. EMBO J 22:6438–6447PubMedCentralCrossRefPubMedGoogle Scholar
  18. Jiang F, Yi L, Moore M, Chen M, Rohl T, Van Wijk KJ, De Gier JW, Henry R, Dalbey RE (2002) Chloroplast YidC homolog Albino3 can functionally complement the bacterial YidC depletion strain and promote membrane insertion of both bacterial and chloroplast thylakoid proteins. J Biol Chem 277:19281–19288CrossRefPubMedGoogle Scholar
  19. Klostermann E, Droste Gen Helling I, Carde JP, Schunemann D (2002) The thylakoid membrane protein ALB3 associates with the cpSecY-translocase in Arabidopsis thaliana. Biochem J 368:777–781PubMedCentralCrossRefPubMedGoogle Scholar
  20. Kovacs-Bogdan E, Benz JP, Soll J, Bolter B (2011) Tic20 forms a channel independent of Tic110 in chloroplasts. BMC Plant Biol 11:133PubMedCentralCrossRefPubMedGoogle Scholar
  21. Kumazaki K, Chiba S, Takemoto M, Furukawa A, Nishiyama K, Sugano Y, Mori T, Dohmae N, Hirata K, Nakada-Nakura Y, Maturana AD, Tanaka Y, Mori H, Sugita Y, Arisaka F, Ito K, Ishitani R, Tsukazaki T, Nureki O (2014) Structural basis of Sec-independent membrane protein insertion by YidC. Nature 509:516–520CrossRefPubMedGoogle Scholar
  22. Lewis NE, Marty NJ, Kathir KM, Rajalingam D, Kight AD, Daily A, Kumar TK, Henry RL, Goforth RL (2010) A dynamic cpSRP43-Albino3 interaction mediates translocase regulation of chloroplast signal recognition particle (cpSRP)-targeting components. J Biol Chem 285:34220–34230PubMedCentralCrossRefPubMedGoogle Scholar
  23. Ma J, Peng L, Guo J, Lu Q, Lu C, Zhang L (2007) LPA2 is required for efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 19:1980–1993PubMedCentralCrossRefPubMedGoogle Scholar
  24. Meurer J, Plucken H, Kowallik KV, Westhoff P (1998) A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J 17:5286–5297PubMedCentralCrossRefPubMedGoogle Scholar
  25. Moore M, Harrison MS, Peterson EC, Henry R (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275:1529–1532CrossRefPubMedGoogle Scholar
  26. Moore M, Goforth RL, Mori H, Henry R (2003) Functional interaction of chloroplast SRP/FtsY with the ALB3 translocase in thylakoids: substrate not required. J Cell Biol 162:1245–1254PubMedCentralCrossRefPubMedGoogle Scholar
  27. Mulo P, Sirpio S, Suorsa M, Aro EM (2008) Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth Res 98:489–501CrossRefPubMedGoogle Scholar
  28. Nickelsen J, Rengstl B (2013) Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol 64:609–635CrossRefPubMedGoogle Scholar
  29. Ossenbuhl F, Gohre V, Meurer J, Krieger-Liszkay A, Rochaix JD, Eichacker LA (2004) Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. Plant Cell 16:1790–1800PubMedCentralCrossRefPubMedGoogle Scholar
  30. Ossenbuhl F, Inaba-Sulpice M, Meurer J, Soll J, Eichacker LA (2006) The synechocystis sp PCC 6803 oxa1 homolog is essential for membrane integration of reaction center precursor protein pD1. Plant Cell 18:2236–2246PubMedCentralCrossRefPubMedGoogle Scholar
  31. Pasch JC, Nickelsen J, Schunemann D (2005) The yeast split-ubiquitin system to study chloroplast membrane protein interactions. Appl Microbiol Biotechnol 69:440–447CrossRefPubMedGoogle Scholar
  32. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficientsand simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394CrossRefGoogle Scholar
  33. Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208PubMedCentralCrossRefPubMedGoogle Scholar
  34. Saaf A, Monne M, de Gier JW, von Heijne G (1998) Membrane topology of the 60-kDa Oxa1p homologue from Escherichia coli. J Biol Chem 273:30415–30418CrossRefPubMedGoogle Scholar
  35. Saller MJ, Wu ZC, de Keyzer J, Driessen AJ (2012) The YidC/Oxa1/Alb3 protein family: common principles and distinct features. Biol Chem 393:1279–1290CrossRefPubMedGoogle Scholar
  36. Schneider A, Steinberger I, Strissel H, Kunz HH, Manavski N, Meurer J, Burkhard G, Jarzombski S, Schunemann D, Geimer S, Flugge UI, Leister D (2014) The Arabidopsis Tellurite resistance C protein together with ALB3 is involved in photosystem II protein synthesis. Plant J 78:344–356CrossRefPubMedGoogle Scholar
  37. Schonberg A, Bergner E, Helm S, Agne B, Dunschede B, Schunemann D, Schutkowski M, Baginsky S (2014) The peptide microarray “ChloroPhos1.0” identifies new phosphorylation targets of plastid casein kinase II (pCKII) in Arabidopsis thaliana. PLoS One 9:e108344PubMedCentralCrossRefPubMedGoogle Scholar
  38. Schuenemann D, Gupta S, Persello-Cartieaux F, Klimyuk VI, Jones JD, Nussaume L, Hoffman NE (1998) A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc Natl Acad Sci USA 95:10312–10316PubMedCentralCrossRefPubMedGoogle Scholar
  39. Schwenkert S, Umate P, Dal Bosco C, Volz S, Mlcochova L, Zoryan M, Eichacker LA, Ohad I, Herrmann RG, Meurer J (2006) PsbI affects the stability, function, and phosphorylation patterns of photosystem II assemblies in tobacco. J Biol Chem 281:34227–34238CrossRefPubMedGoogle Scholar
  40. Spence E, Bailey S, Nenninger A, Moller SG, Robinson C (2004) A homolog of Albino3/OxaI is essential for thylakoid biogenesis in the cyanobacterium Synechocystis sp. PCC6803. J Biol Chem 279:55792–55800CrossRefPubMedGoogle Scholar
  41. Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43CrossRefPubMedGoogle Scholar
  42. Stengel KF, Holdermann I, Cain P, Robinson C, Wild K, Sinning I (2008) Structural basis for specific substrate recognition by the chloroplast signal recognition particle protein cpSRP43. Science 321:253–256CrossRefPubMedGoogle Scholar
  43. Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, Coupland G (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9:717–730PubMedCentralPubMedGoogle Scholar
  44. Szyrach G, Ott M, Bonnefoy N, Neupert W, Herrmann JM (2003) Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria. EMBO J 22:6448–6457PubMedCentralCrossRefPubMedGoogle Scholar
  45. Wada M (2013) Chloroplast movement. Plant Sci 210:177–182CrossRefPubMedGoogle Scholar
  46. Walter B, Hristou A, Nowaczyk MM, Schunemann D (2015) In vitro reconstitution of cotranslational D1 insertion reveals a role of the cpSec/Alb3 translocase and Vipp1 in photosystem II biogenesis. Biochem J 468(2):315–324. doi: 10.1042/BJ20141425 CrossRefPubMedGoogle Scholar
  47. Wang P, Dalbey RE (2011) Inserting membrane proteins: the YidC/Oxa1/Alb3 machinery in bacteria, mitochondria, and chloroplasts. Biochim Biophys Acta 1808:866–875CrossRefPubMedGoogle Scholar
  48. Woolhead CA, Thompson SJ, Moore M, Tissier C, Mant A, Rodger A, Henry R, Robinson C (2001) Distinct Albino3-dependent and -independent pathways for thylakoid membrane protein insertion. J Biol Chem 276:40841–40846CrossRefPubMedGoogle Scholar
  49. Zhao A, Fang Y, Chen X, Zhao S, Dong W, Lin Y, Gong W, Liu L (2014) Crystal structure of Arabidopsis glutamyl-tRNA reductase in complex with its stimulator protein. Proc Natl Acad Sci USA 111:6630–6635PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Manuela Urbischek
    • 1
    • 2
  • Sabine Nick von Braun
    • 1
    • 2
  • Thomas Brylok
    • 1
    • 2
  • Irene L. Gügel
    • 1
    • 2
  • Andreas Richter
    • 4
  • Minna Koskela
    • 3
  • Bernhard Grimm
    • 4
  • Paula Mulo
    • 3
  • Bettina Bölter
    • 1
    • 2
  • Jürgen Soll
    • 1
    • 2
  • Elisabeth Ankele
    • 1
    • 2
  • Serena Schwenkert
    • 1
    • 2
    Email author
  1. 1.Department Biologie I, BotanikLudwig-Maximilians-UniversitätPlanegg-MartinsriedGermany
  2. 2.Munich Center for Integrated Protein Science CiPSMLudwig-Maximilians-UniversitätMunichGermany
  3. 3.Molecular Plant Biology, Department of BiochemistryUniversity of TurkuTurkuFinland
  4. 4.Institute of Biology/Plant PhysiologyHumboldt UniversityBerlinGermany

Personalised recommendations