Skip to main content
Log in

Maize contains a Lon protease gene that can partially complement a yeast pim1-deletion mutant

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have identified a gene in maize that encodes a product belonging to the Lon protease family. In yeast and mammals, Lon-type proteases catalyze the ATP-dependent degradation of mitochondrial matrix proteins. The maize gene, which we have designated LON1, is predicted to encode a protein with a molecular mass of 97.7 kDa. Lon1p is more similar in sequence to bacterial Lon proteases than to the yeast and human mitochondrial Lon proteases. LON1 transcripts are present in shoots of 4-day-old etiolated maize seedlings, and transcript levels decrease when these seedlings are heat-shocked. LON1 transcripts are also present at comparable levels in leaves and roots of 2-week-old greenhouse-grown seedlings. In yeast, the mitochondrial Lon-type protease, Pim1p, has been implicated in mitochondrial protein turnover, the assembly of mitochondrial enzyme complexes, and mitochondrial DNA maintenance, and it is essential for respiratory function. We show that maize Lon1p can replace the Pim1p function in yeast for maintaining mitochondrial DNA integrity, but not in the assembly of cytochrome a _ a3 complexes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Arlt H, Tauer R, Feldmann H, Neupert W, Langer H: The YTA1012 complex, an AAA protease with chaperonelike activity in the inner membrane of mitochondria. Cell 85: 875–885 (1996).

    Google Scholar 

  2. Ausubel FM, Brent R, Kingston RG, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology. Green Publishing Associates/Wiley Interscience, New York (1990).

    Google Scholar 

  3. Beers EP, Moreno TN, Callis J: Subcellular localization of ubiquitin and ubiquitinated proteins in Arabidopsis thaliana. J Biol Chem 267: 15432–15439 (1992).

    Google Scholar 

  4. Beltzer JP, Morris SR, Kohlhaw G: Yeast LEU4 encodes mitochondrial and nonmitochondrial forms of α-isopropylmalate synthase. J Biol Chem 263: 368–374 (1988).

    Google Scholar 

  5. Bushnell TP, Bushnell D, Jagendorf AT: A purified zinc protease of pea chloroplasts, EP1, degrades the large subunit of ribulose1,5bisphosphate carboxylase/oxygenase. Plant Physiol 103: 585–591 (1993).

    Google Scholar 

  6. Callis J: Regulation of protein degradation. Plant Cell 7: 845–857 (1995).

    Google Scholar 

  7. Chin DT, Goff SA, Webster T, Smith T, Goldberg AL: Sequence of the lon gene in Escherichia coli. J Biol Chem 263: 11718–11728 (1988).

    Google Scholar 

  8. Chung CH, Goldberg AL: DNA stimulates ATPdependent proteolysis and proteindependent ATPase activity of protease La from Escherichia coli. Proc Natl Acad Sci USA 79: 795–799 (1982).

    Google Scholar 

  9. Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1: 19–22 (1983).

    Google Scholar 

  10. Desautels M, Goldberg AL: Livermitohondria contain anATPdependent, vanadatesensitive pathway for the degradation of proteins. Proc Natl Acad Sci USA 79: 1869–1873 (1982).

    Google Scholar 

  11. Desautels M, Goldberg AL: Demonstration of an ATPdependent, vanadatesensitive endoprotease in the matrix of rat liver mitochondria. J Biol Chem 257: 11673–11679 (1982).

    Google Scholar 

  12. Diffley JFX, Stillman B: A close relative of the nuclear, chromosomal highmobility group protein HMG1 in yeast mitochondria. Proc Natl Acad Sci USA 88: 7864–7868 (1991).

    Google Scholar 

  13. Fisher H, Glockshuber R: A point mutation within the ATPbinding site inactivates both catalytic functions of the ATPdependent protease La (Lon) from Escherichia coli. FEBS Lett 356: 101–103 (1994).

    Google Scholar 

  14. Fu GK, Smith MJ, Markovitz DM: Bacterial protease Lon is a sitespecific DNAbinding protein. J Biol Chem 272: 534–538 (1997).

    Google Scholar 

  15. Genga A, Bianchi L, Foury F: A nuclear mutant of Saccharomyces cerevisiae deficient in mitochondrial DNA replication and polymerase activity. J Biol Chem 261: 9328–9332 (1986).

    Google Scholar 

  16. Giannattasio S, Marra E, Vacca RA, Iannace G, Quagliariello E: Import of mutant forms of mitochondrial aspartate aminotransferase into isolated mitochondria. Arch Biochem Biophys 298: 532–537 (1992).

    Google Scholar 

  17. Gill RE, Cull MG: Control of developmental gene expression by celltocell interactions in Myxococcus xanthus. J Bact 168: 341–347 (1986).

    Google Scholar 

  18. Gill RE, Karlok M, Benton D: Myxococcus xanthus encodes an ATPdependent protease which is required for developmental gene transcription and intercellular signaling. J Bact 175: 4538–4544 (1993).

    Google Scholar 

  19. Goff SA, Casson LP, Goldberg AL: The heat shock regulatory gene, htpR, influences rates of protein degradation and expression of the lon gene in Escherichia coli. Proc Natl Acad Sci USA 81: 6647–6651 (1984).

    Google Scholar 

  20. Goldberg AL: Themechanismand functions ofATPdependent proteases in bacterial and animal cells. Eur J Biochem 203: 9–23 (1992).

    Google Scholar 

  21. Goldberg AL, Moerschell RP, Chung CH, Maurizi MR: ATPdependent protease La (Lon) from Escherichia coli. Meth Enzymol 244: 350–375 (1994).

    Google Scholar 

  22. Gottesman S, Maurizi M: Regulation by proteolysis: energy dependent proteases and their targets. Microbiol Rev 56: 592–621 (1992).

    Google Scholar 

  23. Greenleaf AL, Kelly JL, Lehman IR:Yeast RP041 gene product is required for transcription and maintenance of the mitochondrial genome. Proc Natl Acad Sci USA 83: 3391–3394 (1986).

    Google Scholar 

  24. Guelin E, Rep M, Grivell LA: Afg3p, a mitochondrial ATPdependent metalloprotease, is involved in degradation of mitochondriallyencoded Cox1, Cox3, Cob, Su6, Su8 and Su9 subunits of the inner membrane complexes III, IV and V. FEBS Lett 381: 42–46 (1996).

    Google Scholar 

  25. Hampsey DM, Lewin AS, Kohlhaw GB: Submitochondrial localization, cellfree synthesis, and mitochondrial import of 2isopropylmalate synthase of yeast. Proc Natl Acad Sci USA 80: 1270–1274 (1983).

    Google Scholar 

  26. Hickey DR, Jayaraman K, Goodhue CT, Shah J, Clements JM, Tsunasawa S, Sherman F: Synthesis and expression of genes encoding tuna, pigeon, and horse cytochromes c in the yeast Saccharomyces cerevisiae. Gene 105: 73–81 (1991).

    Google Scholar 

  27. Kaiser C, Michaelis S, Mitchell A: Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Manual. CSHL Press, Plainview, NY (1994).

    Google Scholar 

  28. Kao LR, Megraw TL, Chae CB: Essential role of the HMG domain in the function of yeast mitochondrial histone HM: functional complementation of HM by the nuclear nonhistone protein NHP6A. Proc Natl Acad Sci USA 90: 5598–5602 (1993).

    Google Scholar 

  29. Kroos L, Kaiser D: Expression of many developmentally regulated genes in Myxococcus xanthus depends on a sequence of cell interactions. Genes Devel 1: 840–854 (1987).

    Google Scholar 

  30. Kutejová E, Durcova G, Surovkova E, Kuzela S: Yeast mitochondrial ATPdependent protease: purification and comparison with the homologous rat enzyme and bacterial ATPdependent protease La. FEBS Lett 329: 47–50 (1993).

    Google Scholar 

  31. Langer T, Neupert W: Regulated protein degradation in mitochondria. Experientia 52: 1069–1076 (1996).

    Google Scholar 

  32. Liu XQ, Jagendorf AT: ATPdependent proteolysis in pea chloroplasts. FEBS Lett 166: 248–252 (1984).

    Google Scholar 

  33. Malek L, Bogorad L, Ayers AR, Goldberg AL: Newly synthesized proteins are degraded by an ATPstimulated proteolytic process in isolated pea chloroplasts. FEBS Lett 166: 253–257 (1984).

    Google Scholar 

  34. Mattoo AK, HoffmanFalk H, Marder JB, Edelman M: Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81: 1380–1384 (1984).

    Google Scholar 

  35. Maurizi MR, Clark WP, Kim SH, Gottesman S: Clp P represents a unique family of serine proteases. J Biol Chem 256: 12546–12552 (1990).

    Google Scholar 

  36. Megraw TL, Chae CB: Functional complementarity between the HMG1like yeast mitochondrial histone HM and the bacterial histonelike protein HU. J Biol Chem 268: 12758–12763 (1993).

    Google Scholar 

  37. Merchant S, Bogorad L: Rapid degradation of apoplastocyanin in Cu(II)deficient cells of Chlamydomonas reinhardtii. J Biol hem 261: 15850–15853 (1986).

    Google Scholar 

  38. Mullet JE, Klein PG, Klein RR: Chlorophyll regulates accumulation of the plastidencoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Proc Natl Acad Sci USA 87: 4038–4042 (1990).

    Google Scholar 

  39. Myers AM, Pape LK, Tzagoloff A: Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J 4: 2087–2092 (1985).

    Google Scholar 

  40. Nakai T, Yasuhara T, Fujiki Y, Ohashi A: Multiple genes, including a member of the AAA family, are essential for the degradation of unassembled subunit 2 of cytochrome c oxidase in yeast mitochondria. Mol Cell Biol 15: 4441–4452 (1995).

    Google Scholar 

  41. Neckelmann N, Li K, Wade RP, Shuster R, Wallace DC: cDNA sequence of a human skeletal muscle ADP/ATP translocator: lack of a leader peptide, divergence from a fibroblast translocator cDNA, and coevolution with mitochondrial DNA genes. Proc Natl Acad Sci USA 84: 7580–7584 (1987).

    Google Scholar 

  42. NietoSotelo J, Vierling E, Ho THD: Cloning, sequence analysis and expression of a cDNA encoding a plastidlocalized heat shock protein in maize. Plant Physiol 93: 1321–1328 (1990).

    Google Scholar 

  43. Pearce DA, Sherman F: Degradation of cytochrome oxidase subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1. J Biol Chem 270: 20879–20882 (1995).

    Google Scholar 

  44. Phillips TA, Van Bogelen RA, Neidhardt FC: The lon(CapR) gene product of Escherichia coli is a heatshock protein. J Bact 159: 283–287 (1984).

    Google Scholar 

  45. Rep M, Grivell LA: The role of protein degradation in mitochondrial function and biogenesis. Curr Genet 30: 367–380 (1996).

    Google Scholar 

  46. Rep M, Nooy J, Guélin E, Grivell LA: Three genes for mitochondrial proteins suppress nullmutations in both Afg3 and Rca1 when overexpressed. Curr Genet 30: 206–211 (1996).

    Google Scholar 

  47. Rep M, Van Dijl JM, Suda K, Schatz G, Grivell LA, Suzuki CK: Promotion ofmitochondrial membrane complex assembly by a proteolytically inactive yeast Lon. Science 274: 103–106 (1996).

    Google Scholar 

  48. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D, Goldberg AL: Inhibitors of the proteasome block the degradation ofmost cell proteins and the generation of peptides presented on MHCclass Imolecules. Cell 78: 761–771 (1994).

    Google Scholar 

  49. Schmidt GW, Mishkind ML: Rapid degradation of unassembled ribulose 1,5bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci USA 80: 2632–2636 (1983).

    Google Scholar 

  50. Shanklin J, DeWitt ND, Flanagan JM: The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: an archetypal twocomponent ATPdependent protease. Plant Cell 7: 1713–1722 (1995).

    Google Scholar 

  51. Sherman F, Stewart JW, Jackson M, Gilmore RA, Parker JH: Mutants of yeast defective in iso1cytochrome c. Genetics 77: 255–284 (1974).

    Google Scholar 

  52. Shimkets LJ: Social and developmental biology of the myxobacteria. Microbiol Rev 54: 473–501 (1990).

    Google Scholar 

  53. Suzuki CK, Suda K, Wang N, Schatz G: Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration. Science 264: 273–276 (1994).

    Google Scholar 

  54. Teichmann U, Van Dyck L, Guiard B, Fischer H, Glockshuber R, Neupert W, Langer T: Substitution of PIM1 protease in mitochondria by Escherichia coli Lon protease. J Biol Chem 271: 10137–10142 (1996).

    Google Scholar 

  55. Tojo N, Inouye S, Komano T: Cloning and nucleotide sequence of the Myxococcus xanthus lon gene: indispensability of lon for vegetative growth. J Bact 175: 2271–2277 (1993).

    Google Scholar 

  56. Tojo N, Inouye S, Komano T: The lonD gene is homologous to the lon gene encoding an ATPdependent protease and is essential for the development of Myxococcus xanthus. J Bact 175: 4545–4549 (1993).

    Google Scholar 

  57. Valens M, Rinaldi T, Daignan-Fornier B, Bolotin-Fukuhara M: Identification of nuclear genes which participate to mitochondrial translation in Saccharomyces cerevisiae. Biochimie 73: 1525–1532 (1991).

    Google Scholar 

  58. Van Dyck E, Foury F, Stillman B, Brill SJ: A singlestranded DNA binding protein required for mitochondrial DNA replication in Saccharomyces cerevisiae is homologous to Escherichia coli SSB. EMBO J 11: 3421–3430 (1992).

    Google Scholar 

  59. Van Dyck L, Pearce DA, Sherman F: PIM1 encodes a mitochondrial ATPdependent protease that is required for mitochondrial function in the yeast Saccharomyces cerevisiae. J Biol Chem 269: 238–242 (1994).

    Google Scholar 

  60. Vierstra RD: Protein degradation in plants. Annu Rev Plant Physiol Plant Mol Biol 44: 385–410 (1993).

    Google Scholar 

  61. Wagner I, Arlt H, Van Dyck L, Langer T, Neupert W: Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J 13: 5135–5145 (1994).

    Google Scholar 

  62. Wang N, Gottesman S, Willingham MC, Gottesman MM, Maurizi MR: A humanmitochondrial ATPdependent protease that is highly homologous to bacterial Lon protease. Proc Natl Acad Sci USA 90: 11247–11251 (1993).

    Google Scholar 

  63. Wang N, Maurizi MR, Emmert-Buck L, Gottesman MM: Synthesis, processing, and localization of human Lon protease. J Biol Chem 269: 29308–29313 (1994).

    Google Scholar 

  64. Watabe S, Kimura T: Adrenal cortex mitochondrial enzyme with ATPdependent protease and proteindependent ATPase activities. J Biol Chem 260: 14498–14504 (1985).

    Google Scholar 

  65. Watabe S, Kimura T: ATPdependent protease in bovine adrenal cortex. Tissue specificity, subcellular localization, and partial characterization. J Biol Chem 260: 5511–5517 (1985).

    Google Scholar 

  66. Wickner S, Gottesman S, Skowyra D, Hoskins J, McKenney K, Maurizi M: A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc Natl Acad Sci USA 91: 12218–12222 (1994).

    Google Scholar 

  67. Zimmerman R, Paluch U, Sprinzl M, Neupert W: Cellfree synthesis of the mitochondrial ADP/ATP carrier protein of Neurospora crassa. Eur J Biochem 99: 247–252 (1979).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barakat, S., Pearce, D.A., Sherman, F. et al. Maize contains a Lon protease gene that can partially complement a yeast pim1-deletion mutant. Plant Mol Biol 37, 141–154 (1998). https://doi.org/10.1023/A:1005912831051

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005912831051

Navigation