Plant Molecular Biology

, Volume 93, Issue 4–5, pp 355–368 | Cite as

The PPR protein SLOW GROWTH 4 is involved in editing of nad4 and affects the splicing of nad2 intron 1

Article

Abstract

Key message

SLO4 is a mitochondrial PPR protein that is involved in editing nad4, possibly required for the efficient splicing of nad2 intron1.

Abstract

Pentatricopeptide repeat (PPR) proteins constitute a large protein family in flowering plants and are thought to be mostly involved in organellar RNA metabolism. The subgroup of PLS-type PPR proteins were found to be the main specificity factors of cytidine to uridine RNA editing. Identifying the targets of PLS-type PPR proteins can help in elucidating the molecular function of proteins encoded in the organellar genomes. In this study, plants lacking the SLOW GROWTH 4 PPR protein were characterized. Slo4 mutants were characterized as having restricted root growth, being late flowering and displaying an overall delayed growth phenotype. Protein levels and activity of mitochondrial complex I were decreased and putative complex I assembly intermediates accumulated in the mutant plants. An editing defect, leading to an amino acid change, in the mitochondrial nad4 transcript, encoding for a complex I subunit, was identified. Furthermore, the splicing efficiency of the first intron of nad2, encoding for another complex I subunit, was also decreased. The change in splicing efficiency could however not be linked to any editing defects in the nad2 transcript.

Keywords

Mitochondria Complex I RNA editing Splicing Pentatricopeptide repeat 

Supplementary material

11103_2016_566_MOESM1_ESM.pdf (51 kb)
Supplementary material 1 (PDF 51 KB)
11103_2016_566_MOESM2_ESM.pdf (1.2 mb)
Supplementary material 2 (PDF 1181 KB)
11103_2016_566_MOESM3_ESM.pdf (6 mb)
Supplementary material 3 (PDF 6142 KB)
11103_2016_566_MOESM4_ESM.pdf (71 kb)
Supplementary material 4 (PDF 70 KB)
11103_2016_566_MOESM5_ESM.pdf (45 kb)
Supplementary material 5 (PDF 45 KB)

References

  1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al (2003) Genome-Wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657CrossRefPubMedGoogle Scholar
  2. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298–305CrossRefPubMedGoogle Scholar
  3. Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494:443–448CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442CrossRefPubMedGoogle Scholar
  5. Barkan A, Rojas M, Fujii S, Yap A, Chong YS, Bond CS, Small I (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 8:e1002910CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bentolila S, Oh J, Hanson MR, Bukowski R (2013) Comprehensive high-resolution analysis of the role of an Arabidopsis gene family in RNA editing. PLoS Genet 9:e1003584CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bonen L (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8:26–34CrossRefPubMedGoogle Scholar
  8. Bosco CD, Lezhneva L, Biehl A, Leister D, Strotmann H, Wanner G, Meurer J (2004) Inactivation of the chloroplast ATP synthase γ subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. J Biol Chem 279:1060–1069CrossRefGoogle Scholar
  9. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510CrossRefPubMedPubMedCentralGoogle Scholar
  10. Braun H-P, Binder S, Brennicke A, Eubel H, Fernie AR, Finkemeier I, Klodmann J, König A-C, Kühn K, Meyer E et al (2014) The life of plant mitochondrial complex I. Mitochondrion 19(Part B):295–313CrossRefPubMedGoogle Scholar
  11. Brown GG, Colas des Francs-Small C, Ostersetzer-Biran O (2014) Group II intron splicing factors in plant mitochondria. Front Plant Sci 5:35CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cardol P, Matagne RF, Remacle C (2002) Impact of mutations affecting ND mitochondria-encoded subunits on the activity and assembly of complex I in Chlamydomonas. Implication for the structural organization of the enzyme. J Mol Biol 319:1211–1221CrossRefPubMedGoogle Scholar
  13. Cardol P, Boutaffala L, Memmi S, Devreese B, Matagne RF, Remacle C (2008) In Chlamydomonas, the loss of ND5 subunit prevents the assembly of whole mitochondrial complex I and leads to the formation of a low abundant 700 kDa subcomplex. Biochim Biophys Acta 1777:388–396CrossRefPubMedGoogle Scholar
  14. Carrie C, Giraud E, Duncan O, Xu L, Wang Y, Huang S, Clifton R, Murcha M, Filipovska A, Rackham O et al (2010) Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. J Biol Chem 285:36138–36148CrossRefPubMedPubMedCentralGoogle Scholar
  15. Colcombet J, Lopez-Obando M, Heurtevin L, Bernard C, Martin K, Berthomé R, Lurin C (2013) Systematic study of subcellular localization of Arabidopsis PPR proteins confirms a massive targeting to organelles. RNA Biol 10:1557–1575CrossRefPubMedPubMedCentralGoogle Scholar
  16. de Longevialle AF, Meyer EH, Andrés C, Taylor NL, Lurin C, Millar AH, Small ID (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 Intron 1 in Arabidopsis thaliana. Plant Cell 19:3256–3265CrossRefPubMedPubMedCentralGoogle Scholar
  17. des Francs-Small CC, Falcon de Longevialle A, Li Y, Lowe E, Tanz SK, Smith C, Bevan MW, Small I (2014) The Pentatricopeptide Repeat proteins TANG2 and ORGANELLE TRANSCRIPT PROCESSING439 are involved in the splicing of the multipartite nad5 transcript encoding a subunit of mitochondrial complex I1[W][OPEN]. Plant Physiol 165:1409–1416CrossRefGoogle Scholar
  18. Doniwa Y, Ueda M, Ueta M, Wada A, Kadowaki K, Tsutsumi N (2010) The involvement of a PPR protein of the P subfamily in partial RNA editing of an Arabidopsis mitochondrial transcript. Gene 454:39–46CrossRefPubMedGoogle Scholar
  19. Duncan O, Carrie C, Wang Y, Murcha MW (2015) In vitro and in vivo protein uptake studies in plant mitochondria. Methods Mol Biol 1305:61–81CrossRefPubMedGoogle Scholar
  20. Elthon TE, Nickels RL, McIntosh L (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol 89:1311–1317CrossRefPubMedPubMedCentralGoogle Scholar
  21. Eubel H, Millar AH (2009) Systematic Monitoring of protein complex composition and abundance by blue-native PAGE. Cold Spring Harb Protoc 2009:pdb.prot5221CrossRefPubMedGoogle Scholar
  22. Eubel H, Jänsch L, Braun H-P (2003) New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II. Plant Physiol 133:274–286CrossRefPubMedPubMedCentralGoogle Scholar
  23. Francs-Small des CC, Kroeger T, Zmudjak M, Ostersetzer-Biran O, Rahimi N, Small I, Barkan A (2012) A PORR domain protein required for rpl2 and ccmF(C) intron splicing and for the biogenesis of c-type cytochromes in Arabidopsis mitochondria. Plant J Cell Mol Biol 69:996–1005CrossRefGoogle Scholar
  24. Fujii S, Small I (2011) The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol 191:37–47CrossRefPubMedGoogle Scholar
  25. Garmier M, Carroll AJ, Delannoy E, Vallet C, Day DA, Small ID, Millar AH (2008) Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol 148:1324–1341CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gualberto JM, Le Ret M, Beator B, Kühn K (2015) The RAD52-like protein ODB1 is required for the efficient excision of two mitochondrial introns spliced via first-step hydrolysis. Nucleic Acids Res 43:6500–6510CrossRefPubMedPubMedCentralGoogle Scholar
  27. Haïli N, Arnal N, Quadrado M, Amiar S, Tcherkez G, Dahan J, Briozzo P, Colas des Francs-Small C, Vrielynck N, Mireau H (2013) The pentatricopeptide repeat MTSF1 protein stabilizes the nad4 mRNA in Arabidopsis mitochondria. Nucleic Acids Res 41:6650–6663CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hammani K, Giegé P (2014) RNA metabolism in plant mitochondria. Trends Plant Sci 19:380–389CrossRefPubMedGoogle Scholar
  29. He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, Chen Z, Han L, Qu L-J, Gong Z (2012) DEXH Box RNA Helicase–mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between Abscisic acid and Auxin signaling [C][W][OA]. Plant Cell 24:1815–1833CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hölzle A, Jonietz C, Törjek O, Altmann T, Binder S, Forner J (2011) A RESTORER OF FERTILITY-like PPR gene is required for 5′-end processing of the nad4 mRNA in mitochondria of Arabidopsis thaliana. Plant J Cell Mol Biol 65:737–744CrossRefGoogle Scholar
  31. Hsieh W-Y, Liao J-C, Chang C-Y, Harrison T, Boucher C, Hsieh M-H (2015) The SLOW GROWTH3 pentatricopeptide repeat protein is required for the splicing of mitochondrial NADH dehydrogenase subunit 7 Intron 2 in Arabidopsis. Plant Physiol 168:490–501CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jacoby RP, Li L, Huang S, Pong Lee C, Millar AH, Taylor NL (2012) Mitochondrial composition, function and stress response in plants. J Integr Plant Biol 54:887–906PubMedGoogle Scholar
  33. Juszczuk IM, Rychter AM (2009) BN-PAGE analysis of the respiratory chain complexes in mitochondria of cucumber MSC16 mutant. Plant Physiol Biochem 47:397–406CrossRefPubMedGoogle Scholar
  34. Juszczuk IM, Flexas J, Szal B, Dabrowska Z, Ribas-Carbo M, Rychter AM (2007) Effect of mitochondrial genome rearrangement on respiratory activity, photosynthesis, photorespiration and energy status of MSC16 cucumber (Cucumis sativus) mutant. Physiol Plant 131:527–541CrossRefPubMedGoogle Scholar
  35. Juszczuk IM, Szal B, Rychter AM (2012) Oxidation–reduction and reactive oxygen species homeostasis in mutant plants with respiratory chain complex I dysfunction. Plant Cell Environ 35:296–307CrossRefPubMedGoogle Scholar
  36. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195CrossRefPubMedGoogle Scholar
  37. Karpova OV, Newton KJ (1999) A partially assembled complex I in NAD4-deficient mitochondria of maize. Plant J 17:511–521CrossRefGoogle Scholar
  38. Keren I, Bezawork-Geleta A, Kolton M, Maayan I, Belausov E, Levy M, Mett A, Gidoni D, Shaya F, Ostersetzer-Biran O (2009) AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA 15:2299–2311CrossRefPubMedPubMedCentralGoogle Scholar
  39. Keren I, Tal L, des Francs-Small CC, Araújo WL, Shevtsov S, Shaya F, Fernie AR, Small I, Ostersetzer-Biran O (2012) nMAT1, a nuclear-encoded maturase involved in the trans-splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function. Plant J Cell Mol Biol 71:413–426Google Scholar
  40. Köhler D, Schmidt-Gattung S, Binder S (2009) The DEAD-box protein PMH2 is required for efficient group II intron splicing in mitochondria of Arabidopsis thaliana. Plant Mol Biol 72:459–467CrossRefPubMedGoogle Scholar
  41. Koop HU, Steinmuller K, Wagner H, Rossler C, Eibl C, Sacher L (1996) Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta 199:193–201CrossRefPubMedGoogle Scholar
  42. Koprivova A, Francs-Small des CC, Calder G, Mugford ST, Tanz S, Lee B-R, Zechmann B, Small I, Kopriva S (2010) Identification of a pentatricopeptide repeat protein implicated in splicing of Intron 1 of mitochondrial nad7 transcripts. J Biol Chem 285:32192–32199CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lee CP, Taylor NL, Millar AH (2013) Recent advances in the composition and heterogeneity of the Arabidopsis mitochondrial proteome. Front Plant Sci 4:4PubMedPubMedCentralGoogle Scholar
  44. Leu K-C, Hsieh M-H, Wang H-J, Hsieh H-L, Jauh G-Y (2016) Distinct role of Arabidopsis mitochondrial P-type pentatricopeptide repeat protein-modulating editing protein, PPME, in nad1 RNA editing. RNA Biol 13:593–604CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lister R, Carrie C, Duncan O, Ho LHM, Howell KA, Murcha MW, Whelan J (2007) Functional definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell 19:3739–3759CrossRefPubMedPubMedCentralGoogle Scholar
  46. Meyer EH, Solheim C, Tanz SK, Bonnard G, Millar AH (2011) Insights into the composition and assembly of the membrane arm of plant complex I through analysis of subcomplexes in Arabidopsis mutant lines. J Biol Chem 286:26081–26092CrossRefPubMedPubMedCentralGoogle Scholar
  47. Murcha MW, Millar AH, Whelan J (2005) The N-terminal cleavable extension of plant carrier proteins is responsible for efficient insertion into the inner mitochondrial membrane. J Mol Biol 351:16–25CrossRefPubMedGoogle Scholar
  48. Nakagawa N, Sakurai N (2006) A mutation in At-nMat1a, which encodes a nuclear gene having high similarity to group II intron maturase, causes impaired splicing of mitochondrial NAD4 transcript and altered carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol 47:772–783CrossRefPubMedGoogle Scholar
  49. Perales M, Parisi G, Fornasari MS, Colaneri A, Villarreal F, González-Schain N, Echave J, Gómez-Casati D, Braun H-P, Araya A et al (2004) Gamma carbonic anhydrase like complex interact with plant mitochondrial complex I. Plant Mol Biol 56:947–957CrossRefPubMedGoogle Scholar
  50. Pfalz J, Liere K, Kandlbinder A, Dietz K-J, Oelmüller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197CrossRefPubMedPubMedCentralGoogle Scholar
  51. Pineau B, Layoune O, Danon A, De Paepe R (2008) l-galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J Biol Chem 283:32500–32505CrossRefPubMedGoogle Scholar
  52. Prikryl J, Rojas M, Schuster G, Barkan A (2011) Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc Natl Acad Sci 108:415–420CrossRefPubMedGoogle Scholar
  53. Rivals E, Bruyère C, Toffano-Nioche C, Lecharny A (2006) Formation of the Arabidopsis pentatricopeptide repeat family. Plant Physiol 141:825–839CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sabar M, De Paepe R, de Kouchkovsky Y (2000) Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol 124:1239–1250CrossRefPubMedPubMedCentralGoogle Scholar
  55. Schertl P, Braun H-P (2015) Activity measurements of mitochondrial enzymes in native gels. Method Mol Biol Clifton NJ 1305:131–138CrossRefGoogle Scholar
  56. Schimmeyer J, Bock R, Meyer EH (2016) l-Galactono-1,4-lactone dehydrogenase is an assembly factor of the membrane arm of mitochondrial complex I in Arabidopsis. Plant Mol Biol 90:117–126CrossRefPubMedGoogle Scholar
  57. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefPubMedGoogle Scholar
  58. Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124:1477–1480CrossRefPubMedPubMedCentralGoogle Scholar
  59. Schweiger R, Muller NC, Schmitt MJ, Soll J, Schwenkert S (2012) AtTPR7 is a chaperone-docking protein of the Sec translocon in Arabidopsis. J Cell Sci 125:5196–5207CrossRefPubMedGoogle Scholar
  60. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14:2985–2994CrossRefPubMedPubMedCentralGoogle Scholar
  61. Shikanai T (2015) RNA editing in plants: machinery and flexibility of site recognition. Biochim Biophys Acta 1847:779–785CrossRefPubMedGoogle Scholar
  62. Soole KL, Menz RI (1995) Functional molecular aspects of the NADH dehydrogenases of plant mitochondria. J Bioenerg Biomembr 27:397–406CrossRefPubMedGoogle Scholar
  63. Sung T-Y, Tseng C-C, Hsieh M-H (2010) The SLO1 PPR protein is required for RNA editing at multiple sites with similar upstream sequences in Arabidopsis mitochondria. Plant J Cell Mol Biol 63:499–511CrossRefGoogle Scholar
  64. Takenaka M, Zehrmann A, Brennicke A, Graichen K (2013) Improved computational target site prediction for pentatricopeptide repeat RNA editing factors. PloS One 8:e65343CrossRefPubMedPubMedCentralGoogle Scholar
  65. Takenaka M, Verbitskiy D, Zehrmann A, Härtel B, Bayer-Császár E, Glass F, Brennicke A (2014) RNA editing in plant mitochondria—connecting RNA target sequences and acting proteins. Mitochondrion 19(Pt B):191–197CrossRefPubMedGoogle Scholar
  66. Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, Millar HA (2013) SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res 41:D1185–D1191CrossRefPubMedGoogle Scholar
  67. Vidal G, Ribas-Carbo M, Garmier M, Dubertret G, Rasmusson AG, Mathieu C, Foyer CH, De Paepe R (2007) Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signaling during elicitor-induced cell death in tobacco. Plant Cell 19:640–655CrossRefPubMedPubMedCentralGoogle Scholar
  68. Whelan J, Hugosson M, Glaser E, Day DA (1995) Studies on the import and processing of the alternative oxidase precursor by isolated soybean mitochondria. Plant Mol Biol 27:769–778CrossRefPubMedGoogle Scholar
  69. Williams-Carrier R, Kroeger T, Barkan A (2008) Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA 14:1930–1941CrossRefPubMedPubMedCentralGoogle Scholar
  70. Xie T, Chen D, Wu J, Huang X, Wang Y, Tang K, Li J, Sun M, Peng X (2016) Growing Slowly 1 locus encodes a PLS-type PPR protein required for RNA editing and plant development in Arabidopsis. J Exp Bot 67:5687–5698CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zehrmann A, Verbitskiy D, van der Merwe JA, Brennicke A, Takenaka M (2009) A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell 21:558–567CrossRefPubMedPubMedCentralGoogle Scholar
  72. Zhu Q, Meyer EH, Van Der Straeten D (2012) Functional analysis of SLO2 provides new insight into the role of plant PPR proteins. Plant Signal Behav 7:1209–1211CrossRefPubMedPubMedCentralGoogle Scholar
  73. Zmudjak M, Colas des Francs-Small C, Keren I, Shaya F, Belausov E, Small I, Ostersetzer-Biran O (2013) mCSF1, a nucleus-encoded CRM protein required for the processing of many mitochondrial introns, is involved in the biogenesis of respiratory complexes I and IV in Arabidopsis. New Phytol 199:379–394CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Biology IBotany, Ludwig-Maximilians-Universität MünchenPlanegg-MartinsriedGermany
  2. 2.Munich Center for Integrated Protein ScienceCiPSM, Ludwig-Maximilians-Universität MünchenMunichGermany

Personalised recommendations