Alternative Transcription Initiation and the AUG Context Configuration Control Dual-Organellar Targeting and Functional Competence of Arabidopsis Lon1 Protease

Molecular Plant

Volumn 7, Issue 6, 2014, Pages 989-1005

  Daras, Gerasimos ^a   Rigas, Stamatis ^a   Tsitsekian, Dikran ^a   Zur, Hadas ^b   Tuller, Tamir ^b   Hatzopoulos, Polydefkis ^a  

^a AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

alternative transcription; alternative translation; ambiguous and twin presequences; chloroplasts; Lon; mitochondria; protein dual targeting

Indexed keywords

ARABIDOPSIS PROTEIN; LON1 PROTEIN, ARABIDOPSIS; SERINE PROTEINASE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEQUENCE ALIGNMENT; TRANSCRIPTION INITIATION SITE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SERINE ENDOPEPTIDASES; TRANSCRIPTION INITIATION SITE;

EID: 84901017612     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssu030     Document Type: Article

References (53)

1. Adam Z., Adamska I., Nakabayashi K., Ostersetzer O., Haussuhl K., Manuell A., Zheng B., Vallon O., Rodermel S.R., Shinozaki K. et al. Chloroplast and mitochondrial proteases in Arabidopsis: a proposed nomenclature Plant Physiol 125 2001 1912 1918
2. Baginsky S., Siddique A., Gruissem W. Proteome analysis of tobacco bright yellow-2 (BY-2) cell culture plastids as a model for undifferentiated heterotrophic plastids J. Proteome Res 3 2004 1128 1137
3. Berglund A.K., Pujol C., Duchene A.M., Glaser E. Defining the determinants for dual targeting of amino acyl-tRNA synthetases to mitochondria and chloroplasts J. Mol. Biol 393 2009 803 814
4. Bota D.A., Ngo J.K., Davies K.J Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death Free Radic. Biol. Med 38 2005 665 677
5. Bradford M.M A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem 72 1976 248 254
6. Carrie C., Small I. A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts Biochim. Biophys. Acta 1833 2013 253 259
7. Carrie C., Giraud E., Whelan J. Protein transport in organelles: dual targeting of proteins to mitochondria and chloroplasts FEBS J 276 2009 1187 1195
8. Christensen A.C., Lyznik A., Mohammed S., Elowsky C.G., Elo A., Yule R., Mackenzie S.A Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons Plant Cell 17 2005 2805 2816
9. Danpure C.J How can the products of a single gene be localized to more than one intracellular compartment? Trends. Cell Biol 5 1995 230 238
10. Daras G., Rigas S., Penning B., Milioni D., McCann M.C., Carpita N.C., Fasseas C., Hatzopoulos P. The thanatos mutation in Arabidopsis thaliana cellulose synthase 3 (AtCesA3) has a dominant-negative effect on cellulose synthesis and plant growth New Phytol 184 2009 114 126
11. Day D.A., Neuburger M., Douce R. Biochemical characterization of chlorophyll-free mitochondria from pea leaves Aust. J. Plant Physiol 12 1985 219 228
12. Degenhardt J., Tobin E.M A DNA binding activity for one of two closely defined phytochrome regulatory elements in an Lhcb promoter is more abundant in etiolated than in green plants Plant Cell 8 1996 31 41
13. Ferro M., Salvi D., Brugière S., Miras S., Kowalski S., Louwagie M., Garin J., Joyard J., Rolland N. Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana Mol. Cell Proteomics 2 2003 325 345
14. Hamilton R., Watanabe C.K., de Boer H.A Compilation and comparison of the sequence context around the AUG start codons in Saccharomyces cerevisiae mRNAs Nucleic Acids Res 15 1987 3581 3593
15. Huang J., Hack E., Thornburg R.W., Myers A.M A yeast mitochondrial leader peptide functions in vivo as a dual targeting signal for both chloroplasts and mitochondria Plant Cell 2 1990 1249 1260
16. Ingolia N.T., Ghaemmaghami S., Newman J.R., Weissman J.S Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling Science 324 2009 218 223
17. Ivanov I.P., Loughran G., Sachs M.S., Atkins J.F Initiation context modulates autoregulation of eukaryotic translation initiation factor 1 (eIF1) Proc. Natl Acad. Sci. U S A 107 2010 18056 18060
18. Janska H., Piechota J., Kwasniak M. ATP-dependent proteases in biogenesis and maintenance of plant mitochondria Biochim. Biophys. Acta 1797 2010 1071 1075
19. Joshi C.P., Zhou H., Huang X., Chiang V.L Context sequences of translation initiation codon in plants Plant Mol. Biol 35 1997 993 1001
20. Kim Y., Lee G., Jeon E., Sohn E.J., Lee Y., Kang H., Lee D.W., Kim D.H., Hwang I. The immediate upstream region of the 5′-UTR from the AUG start codon has a pronounced effect on the translational efficiency in Arabidopsis thaliana Nucleic Acids Res 42 2014 485 498
21. Kozak M. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs Nucleic Acids Res 15 1987 8125 8148
22. Kozak M. Pushing the limits of the scanning mechanism for initiation of translation Gene 299 2002 1 34
23. Kozak M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes Gene 361 2005 13 37
24. Lister R., Chew O., Lee M.N., Heazlewood J.L., Clifton R., Parker K.L., Millar A.H., Whelan J. A transcriptomic and proteomic characterization of Arabidopsis mitochondrial protein import apparatus and its response to mitochondrial dysfunction Plant Physiol 134 2004 777 789
25. Lütcke H.A., Chow K.C., Mickel F.S., Moss K.A., Kern H.F., Scheele G.A Selection of AUG initiation codons differs in plants and animals EMBO J 6 1987 43 48
26. Lynch M., Conery J.S The evolutionary fate and consequences of duplicate genes Science 290 2000 1151 1155
27. Mackenzie S.A Plant organellar protein targeting: a traffic plan still under construction Trends Cell Biol 15 2005 548 554
28. Maeda M., Ohashi K., Ohashi-Kobayashi A. Further extension of mammalian GATA-6 Dev. Growth Differ 47 2005 591 600
29. Mauro V.P., Chappell S.A., Dresios J. Analysis of ribosomal shunting during translation initiation in eukaryotic mRNAs Meth. Enzymol 429 2007 323 354
30. Millar A.H., Whelan J., Small I. Recent surprises in protein targeting to mitochondria and plastids Curr. Opin. Plant Biol 9 2006 610 615
31. Miura F., Kawaguchi N., Sese J., Toyoda A., Hattori M., Morishita S., Ito T. A large-scale full-length cDNA analysis to explore the budding yeast transcriptome Proc. Natl Acad. Sci. U S A 103 2006 17846 17851
32. Ostersetzer O., Kato Y., Adam Z., Sakamoto W. Multiple intracellular locations of Lon protease in Arabidopsis: evidence for the localization of AtLon4 to chloroplasts Plant Cell Physiol 48 2007 881 885
33. Peeters N., Small I. Dual targeting to mitochondria and chloroplasts Biochim. Biophys. Acta 1541 2001 54 63
34. Pestova T.V, Kolupaeva V.G The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection Genes Dev 16 2002 2906 2922
35. Rigas S., Daras G., Laxa M., Marathias N., Fasseas C., Sweetlove L.J., Hatzopoulos P. The role of Lon1 protease in post-germinative growth and maintenance of mitochondrial function in Arabidopsis thaliana New Phytol 181 2009 588 600
36. Rigas S., Daras G., Sweetlove L.J., Hatzopoulos P. Mitochondria biogenesis via Lon1 selective proteolysis: who dares to live for ever? Plant Signal. Behav 4 2009 221 224
37. Rigas S., Daras G., Tsitsekian D., Hatzopoulos P. The multifaceted role of Lon proteolysis in seedling establishment and maintenance of plant organelle function: living from protein destruction Physiol. Plant 145 2012 215 223
38. Ryabova L.A., Pooggin M.M., Hohn T. Translation reinitiation and leaky scanning in plant viruses Virus Res 119 2006 52 62
39. Sakamoto W. Protein degradation machineries in plastids Annu. Rev. Plant Biol 57 2006 599 621
40. Sarria R., Lyznik A., Vallejos C.E., Mackenzie S.A A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated Plant Cell 10 1998 1217 1228
41. Silva-Filho M.C One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations Curr. Opin. Plant Biol 6 2003 589 595
42. Simpson G.G., Laurie R.E., Dijkwel P.P., Quesada V., Stockwell P.A., Dean C., Macknight R.C Noncanonical translation initiation of the Arabidopsis flowering time and alternative polyadenylation regulator FCA Plant Cell 22 2010 3764 3777
43. Sinvany-Villalobo G., Davydov O., Ben-Ari G., Zaltsman A., Raskind A., Adam Z. Expression in multigene families: analysis of chloroplast and mitochondrial proteases Plant Physiol 135 2004 1336 1345
44. Smalle J., Vierstra R.D The ubiquitin 26S proteasome proteolytic pathway Annu. Rev. Plant Physiol. Plant Mol. Biol 55 2004 555 590
45. Solheim C., Li L., Hatzopoulos P., Millar A.H Loss of Lon1 in Arabidopsis changes the mitochondrial proteome leading to altered metabolite profiles and growth retardation without an accumulation of oxidative damage Plant Physiol 160 2012 1187 1203
46. Souciet G., Menand B., Ovesna J., Cosset A., Dietrich A., Wintz H. Characterization of two bifunctional Arabidopsis thaliana genes coding for mitochondrial and cytosolic forms of valyl-tRNA synthetase and threonyl-tRNA synthetase by alternative use of two in-frame AUGs Eur. J. Biochem 266 1999 848 854
47. Suzuki C.K., Suda K., Wang N., Schatz G. Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration Science 264 1994 273 276
48. Sweetlove L.J., Heazlewood J.L., Herald V., Holtzapffel R.H., Day D.A., Leaver C.J., Millar A.H The impact of oxidative stress on Arabidopsis mitochondria Plant J 32 2002 891 904
49. Thön M., Al, Abdallah Q., Hortschansky P., Scharf D.H., Eisendle M., Haas H., Brakhage A.A The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes Nucleic Acids Res 38 2010 1098 1113
50. van Dyck L., Pearce D.A., Sherman F. PIM1 encodes a mitochondrial ATP-dependent protease that is required for mitochondrial function in the yeast Saccharomyces cerevisiae J. Biol. Chem 269 1994 238 242
51. Vijayraghavan U., Company M., Abelson J. Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae Genes Dev 3 1989 1206 1216
52. Wamboldt Y., Mohammed S., Elowsky C., Wittgren C., de Paula W.B., Mackenzie S.A Participation of leaky ribosome scanning in protein dual targeting by alternative translation initiation in higher plants Plant Cell 21 2009 157 167
53. Watanabe N., Che F.S., Iwano M., Takayama S., Yoshida S., Isogai A. Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons J. Biol. Chem 276 2001 20474 20481