Journal of Plant Research

, Volume 128, Issue 2, pp 317–325 | Cite as

The Omp85-type outer membrane protein p36 of Arabidopsisthaliana evolved by recent gene duplication

  • Kerstin Nicolaisen
  • Sandra Missbach
  • Yi-Ching Hsueh
  • Franziska Ertel
  • Hrvoje Fulgosi
  • Maik S. Sommer
  • Enrico Schleiff
Regular Paper

Abstract

Proteins of the Omp85 family are involved in the insertion of β-barrel shaped outer membrane proteins in bacteria and mitochondria, and—at least—in the transfer of preproteins across the chloroplast outer envelope. In general these proteins consist of up to five N-terminal “polypeptide transport associated” (POTRA) domains and a C-terminal, membrane embedded β-barrel domain. In Arabidopsisthaliana two plastidic gene families coding for Omp85-like proteins exist, namely the Toc75-III and the Toc75-V/Oep80 sub-family. The latter is composed of three genes, of which two do not contain POTRA domains. These are annotated as P39 and P36. However, P36 resulted from a very recent gene duplication of P39 and appears to be specific to Arabidopsisthaliana. Furthermore, we show that P39 is specifically expressed in vein tissues, while P36 is expressed at early and late developmental stages. T-DNA insertion in P36 causes a mild phenotype with reduced starch accumulation in chloroplasts of sepals pointing towards a yet to be described plastid function.

Keywords

β-Barrel membrane protein Omp85 Chloroplasts Gene duplication 

Abbreviations

TOC

Translocon on the outer envelope of chloroplasts

Toc75

Translocon on the outer envelope of chloroplasts subunit of 75 kDa

OEP80

Outer envelope protein of 80 kDa

Omp85

Outer membrane protein of 85 kDa

POTRA

Polypeptide transport associated domain

PTB

Polypeptide-transporting β-barrel channels

Supplementary material

10265_2014_693_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1305 kb)

References

  1. Baldwin A, Wardle A, Patel R, Dudley P, Park SK, Twell D, Inoue K, Jarvis P (2005) A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol 138:715–733CrossRefPubMedCentralPubMedGoogle Scholar
  2. Bohnsack MT, Schleiff E (2010) The evolution of protein targeting and translocation systems. Biochim Biophys Acta 1803:1115–1130CrossRefPubMedGoogle Scholar
  3. Bohnsack MT, Kos M, Tollervey D (2008) Quantitative analysis of snoRNA association with pre-ribosomes and release of snR30 by Rok1 helicase. EMBO Rep 9:1230–1236CrossRefPubMedCentralPubMedGoogle Scholar
  4. Borner GH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol 132:568–577CrossRefPubMedCentralPubMedGoogle Scholar
  5. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Gorlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510CrossRefPubMedCentralPubMedGoogle Scholar
  6. Bredemeier R, Schlegel T, Ertel F, Vojta A, Borissenko L, Bohnsack MT, Groll M, von Haeseler A, Schleiff E (2007) Functional and phylogenetic properties of the pore-forming beta-barrel transporters of the Omp85 family. J Biol Chem 282:1882–1890CrossRefPubMedGoogle 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. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  9. Eckart K, Eichacker L, Sohrt K, Schleiff E, Heins L, Soll J (2002) A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep 3:557–562CrossRefPubMedCentralPubMedGoogle Scholar
  10. Gechev TS, Minkov IN, Hille J (2005) Hydrogen peroxide-induced cell death in Arabidopsis: transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process. IUBMB Life 57:181–188CrossRefPubMedGoogle Scholar
  11. Gu ZL, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH (2003) Role of duplicate genes in genetic robustness against null mutations. Nature 421:63–66CrossRefPubMedGoogle Scholar
  12. Guan S, Lu Y (2013) Dissecting organ-specific transcriptomes through RNA-sequencing. Plant Methods 9:42CrossRefPubMedCentralPubMedGoogle Scholar
  13. Heinz E, Lithgow T (2014) A comprehensive analysis of the Omp85/TpsB protein superfamily structural diversity, taxonomic occurrence, and evolution. Front Microbiol 5:370CrossRefPubMedCentralPubMedGoogle Scholar
  14. Hsu SC, Inoue K (2009) Two evolutionarily conserved essential beta-barrel proteins in the chloroplast outer envelope membrane. Biosci Trends 3:168–178PubMedGoogle Scholar
  15. Hu TT, Pattyn P, Bakker EG et al (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nature Gen 43:476–481CrossRefGoogle Scholar
  16. Huang WH, Ling QH, Bedard J, Lilley K, Jarvis P (2011) In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane. Plant Physiol 157:147–159CrossRefPubMedCentralPubMedGoogle Scholar
  17. Inoue K, Potter D (2004) The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms. Plant J 39:354–365CrossRefPubMedGoogle Scholar
  18. Jackson-Constan D, Keegstra K (2001) Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol 125:1567–1576CrossRefPubMedCentralPubMedGoogle Scholar
  19. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907PubMedCentralPubMedGoogle Scholar
  20. Kai K, Mizutani M, Kawamura N, Yamamoto R, Tamai M, Yamaguchi H, Sakata K, Shimizu B (2008) Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant J 55:989–999CrossRefPubMedGoogle Scholar
  21. Kissen R, Bones AM (2009) Nitrile-specifier proteins involved in glucosinolate hydrolysis in Arabidopsis thaliana. J Biol Chem 284:12057–12070CrossRefPubMedCentralPubMedGoogle Scholar
  22. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR (2009) Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat Rev Microbiol 7:206–214CrossRefPubMedGoogle Scholar
  23. Li L, Foster CM, Gan QL, Nettleton D, James MG, Myers AM, Wurtele ES (2009) Identification of the novel protein QQS as a component of the starch metabolic network in Arabidopsis leaves. Plant J 58:485–498CrossRefPubMedGoogle Scholar
  24. Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43:900–914CrossRefPubMedGoogle Scholar
  25. Löffelhardt W, von Haeseler A, Schleiff E (2007) The beta-barrel shaped polypeptide transporter, an old concept for precursor protein transfer across membranes. Symbiosis 44:33–42Google Scholar
  26. Long MY, Langley CH (1993) Natural-selection and the origin of Jingwei, a chimeric processed functional gene in Drosophila. Science 260:91–95CrossRefPubMedGoogle Scholar
  27. Luesse DR, DeBlasio SL, Hangarter RP (2006) Plastid movement impaired 2, a new gene involved in normal blue-light-induced chloroplast movements in Arabidopsis. Plant Physiol 141:1328–1337CrossRefPubMedCentralPubMedGoogle Scholar
  28. Missbach S, Weis BL, Martin R, Simm S, Bohnsack MT, Schleiff E (2013) 40S ribosome biogenesis co-factors are essential for gametophyte and embryo development. PLoS ONE 8:e54084CrossRefPubMedCentralPubMedGoogle Scholar
  29. Moslavac S, Mirus O, Bredemeier R, Soll J, von Haeseler A, Schleiff E (2005) Conserved pore-forming regions in polypeptide-transporting proteins. FEBS J 272:1367–1378CrossRefPubMedGoogle Scholar
  30. Oreb M, Reger K, Schleiff E (2006) Chloroplast protein import: reverse genetic approaches. Curr Genomics 7:235–244CrossRefGoogle Scholar
  31. 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 581:5945–5951CrossRefPubMedGoogle Scholar
  32. Ossowski S, Schneeberger K, Lucas-Lledó JI, Warthmann N, Clark RM, Shaw RG, Weigel D, Lynch M (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:92–94CrossRefPubMedGoogle Scholar
  33. Patel R, Hsu SC, Bedard J, Inoue K, Jarvis P (2008) The Omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis. Plant Physiol 148:235–245CrossRefPubMedCentralPubMedGoogle Scholar
  34. Schlegel T, Mirus O, von Haeseler A, Schleiff E (2007) The tetratricopeptide repeats of receptors involved in protein translocation across membranes. Mol Biol Evol 24:2763–2774CrossRefPubMedGoogle Scholar
  35. Schleiff E, Becker T (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat Rev Mol Cell Bio 12:48–59CrossRefGoogle Scholar
  36. Schleiff E, Soll J (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6:1023–1027CrossRefPubMedCentralPubMedGoogle Scholar
  37. Schleiff E, Maier UG, Becker T (2011) Omp85 in eukaryotic systems: one protein family with distinct functions. Biol Chem 392:21–27CrossRefPubMedGoogle Scholar
  38. Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124:1477–1480CrossRefPubMedCentralPubMedGoogle Scholar
  39. Takeda S, Tadele Z, Hofmann I, Probst AV, Angelis KJ, Kaya H, Araki T, Mengiste T, Mittelsten Scheid O, Shibahara K, Scheel D, Paszkowski J (2004) BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Gene Dev 18:782–793CrossRefPubMedCentralPubMedGoogle Scholar
  40. Thole V, Alves SC, Worland B, Bevan MW, Vain P (2009) A protocol for efficiently retrieving and characterizing flanking sequence tags (FSTs) in Brachypodium distachyon T-DNA insertional mutants. Nature Prot 4:650–661CrossRefGoogle Scholar
  41. Vicient CM, Delseny M (1999) Isolation of total RNA from Arabidopsis thaliana seeds. Anal Biochem 268:412–413CrossRefPubMedGoogle Scholar
  42. Vojta A, Alavi M, Becker T, Hörmann F, Küchler M, Soll J, Thomson R, Schleiff E (2004) The protein translocon of the plastid envelopes. J Biol Chem 279:21401–21405CrossRefPubMedGoogle Scholar
  43. Wright SI, Lauga B, Charlesworth D (2002) Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol Biol Evol 19:1407–1420CrossRefPubMedGoogle Scholar
  44. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genom Proteom Bioinf 4:259–263CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  • Kerstin Nicolaisen
    • 1
    • 2
  • Sandra Missbach
    • 1
    • 6
  • Yi-Ching Hsueh
    • 1
  • Franziska Ertel
    • 1
    • 7
  • Hrvoje Fulgosi
    • 5
  • Maik S. Sommer
    • 1
  • Enrico Schleiff
    • 1
    • 2
    • 3
    • 4
  1. 1.Department of Molecular Cell Biology of PlantsGoethe UniversityFrankfurtGermany
  2. 2.Center of Membrane ProteomicsGoethe UniversityFrankfurtGermany
  3. 3.Cluster of Excellence FrankfurtGoethe UniversityFrankfurtGermany
  4. 4.Buchman Institute of Molecular Life SciencesGoethe UniversityFrankfurtGermany
  5. 5.Institute Ruđer BoškovićZavod za molekularnu biologyZagrebCroatia
  6. 6.Novartis Vaccines and Diagnostics GmbHMarburgGermany
  7. 7.Department of BiochemistryMcGill University MontrealMontrealCanada

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