1932

Abstract

The N-degron pathway, formerly the N-end rule pathway, regulates functions of regulatory proteins. It impacts protein half-life and therefore directs the actual presence of target proteins in the cell. The current concept holds that the N-degron pathway depends on the identity of the amino (N)-terminal amino acid and many other factors, such as the follow-up sequence at the N terminus, conformation, flexibility, and protein localization. It is evolutionarily conserved throughout the kingdoms. One possible entry point for substrates of the N-degron pathway is oxidation of N-terminal Cys residues. Oxidation of N-terminal Cys is decisive for further enzymatic modification of various neo–N termini by arginylation that generates potentially neofunctionalized or instable proteoforms. Here, I focus on the posttranslational modifications that are encompassed by protein degradation via the Cys/Arg branch of the N-degron pathway—part of the PROTEOLYSIS 6 (PRT6)/N-degron pathway—as well as the underlying physiological principles of this branch and its biological significance in stress response.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050718-095937
2019-04-29
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/arplant/70/1/annurev-arplant-050718-095937.html?itemId=/content/journals/10.1146/annurev-arplant-050718-095937&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Abbas M, Berckhan S, Rooney DJ, Gibbs DJ, Vicente Conde J et al. 2015. Oxygen sensing coordinates photomorphogenesis to facilitate seedling survival. Curr. Biol. 25:1483–88
    [Google Scholar]
  2. 2.  Abbruzzetti S, Faggiano S, Spyrakis F, Bruno S, Mozzarelli A et al. 2011. Oxygen and nitric oxide rebinding kinetics in nonsymbiotic hemoglobin AHb1 from Arabidopsis thaliana. IUBMB Life 63:1094–100
    [Google Scholar]
  3. 3.  Alberts B 1989. Molecular Biology of the Cell New York: Garland
  4. 4.  Akter S, Fu L, Jung Y, Conte ML, Lawson JR et al. 2018. Chemical proteomics reveals new targets of cysteine sulfinic acid reductase. Nat. Chem. Biol. 14:995–1004
    [Google Scholar]
  5. 5.  Apel W, Schulze WX, Bock R 2010. Identification of protein stability determinants in chloroplasts. Plant J 63:636–50
    [Google Scholar]
  6. 6.  Bachmair A, Becker F, Schell J 1993. Use of a reporter transgene to generate Arabidopsis mutants in ubiquitin-dependent protein degradation. PNAS 90:418–21
    [Google Scholar]
  7. 7.  Bachmair A, Finley D, Varshavsky A 1986. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234:179–86
    [Google Scholar]
  8. 8.  Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC et al. 2012. Making sense of low oxygen sensing. Trends Plant Sci 17:129–38
    [Google Scholar]
  9. 9.  Bailey-Serres J, Lee SC, Brinton E 2012. Waterproofing crops: effective flooding survival strategies. Plant Physiol 160:1698–709
    [Google Scholar]
  10. 10.  Baker RT, Varshavsky A 1991. Inhibition of the N-end rule pathway in living cells. PNAS 88:1090–94
    [Google Scholar]
  11. 11.  Baker RT, Varshavsky A 1995. Yeast N-terminal amidase: a new enzyme and component of the N-end rule pathway. J. Biol. Chem. 270:12065–74
    [Google Scholar]
  12. 12.  Balzi E, Choder M, Chen W, Varshavsky A, Goffeau A 1990. Cloning and functional analysis of the arginyl-tRNA-protein transferase gene ATE1 of Saccharomyces cerevisiae. J. Biol. Chem 265:7464–71
    [Google Scholar]
  13. 13.  Bienvenut WV, Giglione C, Meinnel T 2015. Proteome-wide analysis of the amino terminal status of Escherichia coli proteins at the steady-state and upon deformylation inhibition. Proteomics 15:2503–18
    [Google Scholar]
  14. 14.  Boehm CR, Bock R 2019. Recent advances and current challenges in synthetic biology of the plastid genetic system and metabolism. Plant Physiol 179:794–802
    [Google Scholar]
  15. 15.  Bohley P, Kopitz J, Adam G 1988. Arginylation, surface hydrophobicity and degradation of cytosol proteins from rat hepatocytes. Adv. Exp. Med. Biol. 240:159–69
    [Google Scholar]
  16. 16.  Bohley P, Kopitz J, Adam G 1988. Surface hydrophobicity, arginylation and degradation of cytosol proteins from rat hepatocytes. Biol. Chem. Hoppe Seyler 369:Suppl.307–10Arginylated proteins are more rapidly degraded by endopeptidases, suggesting that arginylation might function in the N-degron pathway.
    [Google Scholar]
  17. 17.  Bohley P, Kopitz J, Adam G, Rist B, von Appen F, Urban S 1991. Post-translational arginylation and intracellular proteolysis. Biomed. Biochim. Acta 50:343–46
    [Google Scholar]
  18. 18.  Bonissone S, Gupta N, Romine M, Bradshaw R, Pevzner P 2013. N-terminal protein processing: a comparative proteogenomic analysis. Mol. Cell Proteom. 12:14–28
    [Google Scholar]
  19. 19.  Bui LT, Giuntoli B, Kosmacz M, Parlanti S, Licausi F 2015. Constitutively expressed ERF-VII transcription factors redundantly activate the core anaerobic response in Arabidopsis thaliana. Plant Sci 236:37–43
    [Google Scholar]
  20. 20.  Cha-Molstad H, Kwon YT, Kim BY 2015. Amino-terminal arginylation as a degradation signal for selective autophagy. BMB Rep 48:487–88
    [Google Scholar]
  21. 21.  Cha-Molstad H, Sung KS, Hwang J, Kim KA, Yu JE et al. 2015. Amino-terminal arginylation targets endoplasmic reticulum chaperone BiP for autophagy through p62 binding. Nat. Cell Biol. 17:917–29
    [Google Scholar]
  22. 22.  Ciechanover A, Ferber S, Ganoth D, Elias S, Hershko A, Arfin S 1988. Purification and characterization of arginyl-tRNA-protein transferase from rabbit reticulocytes: its involvement in post-translational modification and degradation of acidic NH2 termini substrates of the ubiquitin pathway. J. Biol. Chem. 263:11155–67
    [Google Scholar]
  23. 23.  Colombo CV, Rosano GL, Mogk A, Ceccarelli EA 2018. A gatekeeper residue of ClpS1 from Arabidopsis thaliana chloroplasts determines its affinity towards substrates of the bacterial N-end rule. Plant Cell Physiol 59:624–36
    [Google Scholar]
  24. 24.  Davydov IV, Varshavsky A 2000. RGS4 is arginylated and degraded by the N-end rule pathway in vitro. J. Biol. Chem. 275:22931–41First report where an N-terminal initiator Met of a Met-Cys-starting protein was replaced with Arg.
    [Google Scholar]
  25. 25.  de Marchi R, Sorel M, Mooney B, Fudal I, Goslin K et al. 2016. The N-end rule pathway regulates pathogen responses in plants. Sci. Rep. 6:26020
    [Google Scholar]
  26. 26.  Dissmeyer N 2017. Conditional modulation of biological processes by low-temperature degrons. Methods Mol. Biol. 1669:407–16
    [Google Scholar]
  27. 27.  Dissmeyer N, Coux O, Rodriguez M, Barrio R 2019. PROTEOSTASIS: a European network to break barriers and integrate science on protein homeostasis. Trends Biochem. Sci. https://doi.org/10.1016/j.tibs.2019.01.007
  28. 28.  Dissmeyer N, Graciet E, Holdsworth MJ, Gibbs DJ 2017. N-term 2017: proteostasis via the N-terminus. Trends Biochem. Sci. https://doi.org/10.1016/j.tibs.2017.11.006
    [Crossref]
  29. 29.  Dissmeyer N, Rivas S, Graciet E 2018. Life and death of proteins after protease cleavage: protein degradation by the N-end rule pathway. New Phytol 218:929–35
    [Google Scholar]
  30. 30.  Dissmeyer N, Schnittger A 2011. The age of protein kinases. Methods Mol. Biol. 779:7–52
    [Google Scholar]
  31. 31.  Dissmeyer N, Schnittger A 2011. Use of phospho-site substitutions to analyze the biological relevance of phosphorylation events in regulatory networks. Methods Mol. Biol. 779:93–138
    [Google Scholar]
  32. 32.  Dong H, Dumenil J, Lu FH, Na L, Vanhaeren H et al. 2017. Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis. Genes Dev 31:197–208
    [Google Scholar]
  33. 33.  Eldeeb MA, Ragheb MA 2018. Post-translational N-terminal arginylation of protein fragments: a pivotal portal to proteolysis. Curr. Protein Pept. Sci. 19:1214–23
    [Google Scholar]
  34. 34.  Emanuelsson O, Nielsen H, Brunak S, von Heijne G 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300:1005–16
    [Google Scholar]
  35. 35.  Faden F, Mielke S, Dissmeyer N 2018. Switching toxic protein function in life cells. bioRxiv 430439. https://doi.org/10.1101/430439
    [Crossref]
  36. 36.  Faden F, Mielke S, Dissmeyer N 2019. Modulating protein stability to switch toxic protein function on and off in living cells. Plant Physiol 179:929–42
    [Google Scholar]
  37. 37.  Faden F, Mielke S, Lange D, Dissmeyer N 2014. Generic tools for conditionally altering protein abundance and phenotypes on demand. Biol. Chem. 395:737–62
    [Google Scholar]
  38. 38.  Faden F, Ramezani T, Mielke S, Almudi I, Nairz K et al. 2016. Phenotypes on demand via switchable target protein degradation in multicellular organisms. Nat. Commun. 7:12202
    [Google Scholar]
  39. 39.  Frottin F, Martinez A, Peynot P, Mitra S, Holz R et al. 2006. The proteomics of N-terminal methionine cleavage. Mol. Cell Proteom. 5:2336–49
    [Google Scholar]
  40. 40.  Garzón M, Eifler K, Faust A, Scheel H, Hofmann K et al. 2007. PRT6/At5g02310 encodes an Arabidopsis ubiquitin ligase of the N-end rule pathway with arginine specificity and is not the CER3 locus. FEBS Lett 581:3189–96
    [Google Scholar]
  41. 41.  Gasch P, Fundinger M, Müller JT, Lee T, Bailey-Serres J, Mustroph A 2016. Redundant ERF-VII transcription factors bind to an evolutionarily conserved cis-motif to regulate hypoxia-responsive gene expression in Arabidopsis. Plant Cell 28:160–80
    [Google Scholar]
  42. 42.  Gibbs DJ 2015. Emerging functions for N-terminal protein acetylation in plants. Trends Plant Sci 20:599–601
    [Google Scholar]
  43. 43.  Gibbs DJ, Bacardit J, Bachmair A, Holdsworth MJ 2014a. The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends Cell Biol 24:603–11
    [Google Scholar]
  44. 44.  Gibbs DJ, Bailey M, Tedds HM, Holdsworth MJ 2016. From start to finish: amino-terminal protein modifications as degradation signals in plants. New Phytol 211:1188–94
    [Google Scholar]
  45. 45.  Gibbs DJ, Lee SC, Md Isa N, Gramuglia S, Fukao T et al. 2011. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 479:415–18First description of the N-degron pathway–mediated degradation of plant proteins depending on N-terminal amino acid and oxygen levels.
    [Google Scholar]
  46. 46.  Gibbs DJ, Md Isa N, Movahedi M, Lozano-Juste J, Mendiondo GM et al. 2014b. Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol. Cell 53:369–79Cys-initiated proteins of group VII of the B-2 subfamily of ETHYLENE RESPONSE FACTORs act as sensors for NO, which renders them instable.
    [Google Scholar]
  47. 47.  Gibbs DJ, Tedds HM, Labandera AM, Bailey M, White MD et al. 2018. Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2. Nat. Commun. 9:5438
    [Google Scholar]
  48. 48.  Giglione C, Boularot A, Meinnel T 2004. Protein N-terminal methionine excision. Cell Mol. Life Sci. 61:1455–74
    [Google Scholar]
  49. 49.  Giglione C, Fieulaine S, Meinnel T 2015. N-terminal protein modifications: bringing back into play the ribosome. Biochimie 114:134–46
    [Google Scholar]
  50. 50.  Giglione C, Meinnel T 2001. Organellar peptide deformylases: universality of the N-terminal methionine cleavage mechanism. Trends Plant Sci 6:566–72
    [Google Scholar]
  51. 51.  Giglione C, Serero A, Pierre M, Boisson B, Meinnel T 2000. Identification of eukaryotic peptide deformylases reveals universality of N-terminal protein processing mechanisms. EMBO J 19:5916–29
    [Google Scholar]
  52. 52.  Giglione C, Vallon O, Meinnel T 2003. Control of protein life-span by N-terminal methionine excision. EMBO J 22:13–23
    [Google Scholar]
  53. 53.  Giuntoli B, Perata P 2018. Group VII ethylene response factors in Arabidopsis: regulation and physiological roles. Plant Physiol 176:1143–55
    [Google Scholar]
  54. 54.  Gonda D, Bachmair A, Wunning I, Tobias J, Lane W, Varshavsky A 1989. Universality and structure of the N-end rule. J. Biol. Chem. 264:16700–12
    [Google Scholar]
  55. 55.  Graciet E, Mesiti F, Wellmer F 2010. Structure and evolutionary conservation of the plant N-end rule pathway. Plant J 61:741–51
    [Google Scholar]
  56. 56.  Graciet E, Walter F, Ó'Maoiléidigh DS, Pollmann S, Meyerowitz EM et al. 2009. The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development. PNAS 106:13618–23First report of an in vitro arginylation of a highly purified wild-type plant extract, which was lacking if prepared from an ate1 ate2 double mutant.
    [Google Scholar]
  57. 57.  Graciet E, Wellmer F 2010. The plant N-end rule pathway: structure and functions. Trends Plant Sci 15:447–53
    [Google Scholar]
  58. 58.  Gravot A, Richard G, Lime T, Lemarie S, Jubault M et al. 2016. Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot. BMC Plant Biol 16:251
    [Google Scholar]
  59. 59.  Grigoryev S, Stewart AE, Kwon YT, Arfin SM, Bradshaw RA et al. 1996. A mouse amidase specific for N-terminal asparagine: the gene, the enzyme, and their function in the N-end rule pathway. J. Biol. Chem. 271:28521–32
    [Google Scholar]
  60. 60.  Have M, Balliau T, Cottyn-Boitte B, Derond E, Cueff G et al. 2018. Increases in activity of proteasome and papain-like cysteine protease in Arabidopsis autophagy mutants: back-up compensatory effect or cell-death promoting effect?. J. Exp. Bot. 69:1369–85
    [Google Scholar]
  61. 61.  Hoernstein SN, Mueller SJ, Fiedler K, Schuelke M, Vanselow JT et al. 2016. Identification of targets and interaction partners of arginyl-tRNA protein transferase in the moss Physcomitrella patens.Mol. Cell Proteom 15:1808–22
    [Google Scholar]
  62. 62.  Holdsworth MJ 2017. First hints of new sensors. Nat. Plants 3:767–68
    [Google Scholar]
  63. 63.  Holman TJ, Jones PD, Russell L, Medhurst A, Úbeda Tomás S et al. 2009. The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. PNAS 106:4549–54
    [Google Scholar]
  64. 64.  Hu RG, Brower CS, Wang H, Davydov IV, Sheng J et al. 2006. Arginyltransferase, its specificity, putative substrates, bidirectional promoter, and splicing-derived isoforms. J. Biol. Chem. 281:32559–73
    [Google Scholar]
  65. 65.  Hu RG, Sheng J, Qi X, Xu Z, Takahashi TT, Varshavsky A 2005. The N-end rule pathway as a nitric oxide sensor controlling the levels of multiple regulators. Nature 437:981–86
    [Google Scholar]
  66. 66.  Huesgen PF, Lange PF, Rogers LD, Solis N, Eckhard U et al. 2015. LysargiNase mirrors trypsin for protein C-terminal and methylation-site identification. Nat. Methods 12:55–58
    [Google Scholar]
  67. 67.  Hwang C, Shemorry A, Varshavsky A 2010. N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327:973–77
    [Google Scholar]
  68. 68.  Ida S, Kuriyama K 1983. Simultaneous determination of cysteine sulfinic acid and cysteic acid in rat brain by high-performance liquid chromatography. Anal. Biochem. 130:95–101
    [Google Scholar]
  69. 69.  Imsand EM, Njeri CW, Ellis HR 2012. Addition of an external electron donor to in vitro assays of cysteine dioxygenase precludes the need for exogenous iron. Arch. Biochem. Biophys. 521:10–17
    [Google Scholar]
  70. 70.  Jelenska J, Davern SM, Standaert RF, Mirzadeh S, Greenberg JT 2017. Flagellin peptide flg22 gains access to long-distance trafficking in Arabidopsis via its receptor, FLS2. J. Exp. Bot. 68:1769–83
    [Google Scholar]
  71. 71.  Jiang Y, Choi WH, Lee JH, Han DH, Kim JH et al. 2014. A neurostimulant para-chloroamphetamine inhibits the arginylation branch of the N-end rule pathway. Sci. Rep. 4:6344
    [Google Scholar]
  72. 72.  Kaji H, Novelli GD, Kaji A 1963. A soluble amino acid-incorporating system from rat liver. Biochim. Biophys. Acta 76:474–77
    [Google Scholar]
  73. 73.  Kashina AS 2015. Protein arginylation: over 50 years of discovery. Methods Mol. Biol. 1337:1–11
    [Google Scholar]
  74. 74.  Kashina AS, Yates JR 3rd 2015. Identification of arginylated proteins by mass spectrometry. Methods Mol. Biol. 1337:93–104
    [Google Scholar]
  75. 75.  Klecker M, Dissmeyer N 2016. Peptide arrays for binding studies of E3 ubiquitin ligases. Methods Mol. Biol. 1450:85–94
    [Google Scholar]
  76. 76.  Köhler D, Dobritzsch D, Hoehenwarter W, Helm S, Steiner JM, Baginsky S 2015. Identification of protein N-termini in Cyanophora paradoxa cyanelles: transit peptide composition and sequence determinants for precursor maturation. Front. Plant Sci. 6:559
    [Google Scholar]
  77. 77.  Kolata G 1986. New rule proposed for protein degradation. Science 234:151–52
    [Google Scholar]
  78. 78.  Kopitz J, Rist B, Bohley P 1990. Post-translational arginylation of ornithine decarboxylase from rat hepatocytes. Biochem. J. 267:343–48
    [Google Scholar]
  79. 79.  Kwon YT, Balogh SA, Davydov IV, Kashina AS, Yoon JK et al. 2000. Altered activity, social behavior, and spatial memory in mice lacking the NTAN1p amidase and the asparagine branch of the N-end rule pathway. Mol. Cell Biol. 20:4135–48
    [Google Scholar]
  80. 80.  Kwon YT, Kashina AS, Davydov IV, Hu RG, An JY et al. 2002. An essential role of N-terminal arginylation in cardiovascular development. Science 297:96–99
    [Google Scholar]
  81. 81.  Lee MJ, Kim DE, Zakrzewska A, Yoo YD, Kim SH et al. 2012. Characterization of arginylation branch of N-end rule pathway in G-protein-mediated proliferation and signaling of cardiomyocytes. J. Biol. Chem. 287:24043–52
    [Google Scholar]
  82. 82.  Lee MJ, Tasaki T, Moroi K, An JY, Kimura S et al. 2005. RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. PNAS 102:15030–35
    [Google Scholar]
  83. 83.  Li L, Nelson CJ, Trosch J, Castleden I, Huang S, Millar AH 2017. Protein degradation rate in Arabidopsis thaliana leaf growth and development. Plant Cell 29:207–28
    [Google Scholar]
  84. 84.  Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM et al. 2011. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479:419–22First description of oxygen-dependent degradation of proteins dependent on the N terminus and PROTEOLYSIS 6 or ARGINYLTRANSFERASEs in vivo.
    [Google Scholar]
  85. 85.  Lo Conte M, Carroll KS 2013. The redox biochemistry of protein sulfenylation and sulfinylation. J. Biol. Chem. 288:26480–88
    [Google Scholar]
  86. 86.  Majovsky P, Naumann C, Lee CW, Lassowskat I, Trujillo M et al. 2014. Targeted proteomics analysis of protein degradation in plant signaling on an LTQ-Orbitrap mass spectrometer. J. Proteome Res. 13:4246–58
    [Google Scholar]
  87. 87.  Manahan CO, App AA 1973. An arginyl-transfer ribonucleic acid protein transferase from cereal embryos. Plant Physiol 52:13–16First report of a general and obscure activity of aminoacyl transfer in plants.
    [Google Scholar]
  88. 88.  Mendiondo GM, Gibbs DJ, Szurman-Zubrzycka M, Korn A, Marquez J et al. 2016. Enhanced waterlogging tolerance in barley by manipulation of expression of the N-end rule pathway E3 ligase PROTEOLYSIS6. Plant Biotechnol. J 14:40–50
    [Google Scholar]
  89. 89.  Millar AH, Heazlewood JL, Giglione C, Holdsworth MJ, Bachmair A, Schulze WX 2019. The scope, functions, and dynamics of posttranslational protein modifications. Annu. Rev. Plant Biol. 70:119–51
    [Google Scholar]
  90. 90.  Mot AC, Prell E, Klecker M, Naumann C, Faden F et al. 2018. Real-time detection of N-end rule-mediated ubiquitination via fluorescently labeled substrate probes. New Phytol 217:613–24
    [Google Scholar]
  91. 91.  Mot AC, Puscas C, Miclea P, Naumova-Letia G, Dorneanu S et al. 2018. Redox control and autoxidation of class 1, 2 and 3 phytoglobins from Arabidopsis thaliana.Sci. Rep 8:13714
    [Google Scholar]
  92. 92.  Naumann C, Mot AC, Dissmeyer N 2016. Generation of artificial N-end rule substrate proteins in vivo and in vitro. Methods Mol. Biol. 1450:55–83
    [Google Scholar]
  93. 93.  Nelson CJ, Millar AH 2015. Protein turnover in plant biology. Nat. Plants 1:15017
    [Google Scholar]
  94. 94.  Nguyen KT, Kim JM, Park SE, Hwang CS 2019. N-terminal methionine excision of proteins creates tertiary destabilizing N-degrons of the Arg/N-end rule pathway. J. Biol. Chem In press. https://doi.org/10.1074/jbc.RA118.006913
    [Crossref]
  95. 95.  Nishimura K, Asakura Y, Friso G, Kim J, Oh S et al. 2013. ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. Plant Cell 25:2276–301
    [Google Scholar]
  96. 96.  Papdi C, Pérez-Salamó I, Joseph M, Giuntoli B, Bögre L et al. 2015. The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12, RAP2.2 and RAP2.3. Plant J 82:772–84
    [Google Scholar]
  97. 97.  Paulus JK, van der Hoorn RAL 2019. Do proteolytic cascades exist in plants?. J. Exp. Bot In press. https://doi.org/10.1093/jxb/erz016
    [Crossref]
  98. 98.  Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J et al. 2004. Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16:2785–94
    [Google Scholar]
  99. 99.  Perrar A, Dissmeyer N, Huesgen PF 2019. New beginnings and new ends—methods for large-scale characterization of protein termini and their use in plant biology. J. Exp. Bot https://doi.org/10.1093/jxb/erz104
    [Crossref]
  100. 100.  Piatkov K, Brower C, Varshavsky A 2012. The N-end rule pathway counteracts cell death by destroying proapoptotic protein fragments. PNAS 109:E1839–47
    [Google Scholar]
  101. 101.  Poole LB, Klomsiri C, Knaggs SA, Furdui CM, Nelson KJ et al. 2007. Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. Bioconjug. Chem. 18:2004–17
    [Google Scholar]
  102. 102.  Poole LB, Zeng BB, Knaggs SA, Yakubu M, King SB 2005. Synthesis of chemical probes to map sulfenic acid modifications on proteins. Bioconjug. Chem. 16:1624–28
    [Google Scholar]
  103. 103.  Potuschak T, Stary S, Schlogelhofer P, Becker F, Nejinskaia V, Bachmair A 1998. PRT1 of Arabidopsis thaliana encodes a component of the plant N-end rule pathway. PNAS 95:7904–8
    [Google Scholar]
  104. 104.  Pusch S, Dissmeyer N, Schnittger A 2011. Bimolecular-fluorescence complementation assay to monitor kinase-substrate interactions in vivo. Methods Mol. Biol. 779:245–57
    [Google Scholar]
  105. 105.  Reddie KG, Carroll KS 2008. Expanding the functional diversity of proteins through cysteine oxidation. Curr. Opin. Chem. Biol. 12:746–54
    [Google Scholar]
  106. 106.  Reichman P, Dissmeyer N 2017. In vivo reporters for protein half-life. Methods Mol. Biol. 1669:387–406
    [Google Scholar]
  107. 107.  Riber W, Müller JT, Visser EJW, Sasidharan R, Voesenek LACJ, Mustroph A 2015. The greening after extended darkness1 is an N-end rule pathway mutant with high tolerance to submergence and starvation. Plant Physiol 167:1616–29
    [Google Scholar]
  108. 108.  Roos G, Messens J 2011. Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic. Biol. Med. 51:314–26
    [Google Scholar]
  109. 109.  Rowland E, Kim J, Bhuiyan NH, van Wijk KJ 2015. The Arabidopsis chloroplast stromal N-terminome: complexities of amino-terminal protein maturation and stability. Plant Physiol 169:1881–96
    [Google Scholar]
  110. 110.  Sasidharan R, Mustroph A 2011. Plant oxygen sensing is mediated by the N-end rule pathway: a milestone in plant anaerobiosis. Plant Cell 23:4173–83
    [Google Scholar]
  111. 111.  Schuessele C, Hoernstein SN, Mueller SJ, Rodriguez-Franco M, Lorenz T et al. 2016. Spatio-temporal patterning of arginyl-tRNA protein transferase (ATE) contributes to gametophytic development in a moss. New Phytol 209:1014–27
    [Google Scholar]
  112. 112.  Soffer RL 1971. Enzymatic modification of proteins: V. Protein acceptor specificity in the arginine-transfer reaction. J. Biol. Chem. 246:1602–6
    [Google Scholar]
  113. 113.  Spremulli L 2000. Protein synthesis, assembly, and degradation. Biochemistry & Molecular Biology of Plants B Buchanan, W Gruissem, R Jones 412–54 Rockville, MD: Am. Soc. Plant Physiol.
    [Google Scholar]
  114. 114.  Sriram SM, Kim BY, Kwon YT 2011. The N-end rule pathway: emerging functions and molecular principles of substrate recognition. Nat. Rev. Mol. Cell Biol. 12:735–47
    [Google Scholar]
  115. 115.  Stary S, Yin X, Potuschak T, Schlogelhofer P, Nizhynska V, Bachmair A 2003. PRT1 of Arabidopsis is a ubiquitin protein ligase of the plant N-end rule pathway with specificity for aromatic amino-terminal residues. Plant Physiol 133:1360–66
    [Google Scholar]
  116. 116.  Tasaki T, Sriram SM, Park KS, Kwon YT 2012. The N-end rule pathway. Annu. Rev. Biochem. 81:261–89
    [Google Scholar]
  117. 117.  Tsiatsiani L, Timmerman E, De Bock PJ, Vercammen D, Stael S et al. 2013. The Arabidopsis METACASPASE9 degradome. Plant Cell 25:2831–47
    [Google Scholar]
  118. 118.  van Dongen JT, Licausi F 2015. Oxygen sensing and signaling. Annu. Rev. Plant Biol. 66:345–67
    [Google Scholar]
  119. 119.  van Wijk KJ 2015. Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes. Annu. Rev. Plant Biol. 66:75–111
    [Google Scholar]
  120. 120.  Varshavsky A 2011. The N-end rule pathway and regulation by proteolysis. Protein Sci 20:1298–345
    [Google Scholar]
  121. 121.  Varshavsky A 2019. N-degron and C-degron pathways of protein degradation. PNAS 116:358–66Introduction of new N-degron pathway nomenclature according to the actual N-degrons or N-recognins.
    [Google Scholar]
  122. 122.  Venne AS, Solari FA, Faden F, Paretti T, Dissmeyer N, Zahedi RP 2015. An improved workflow for quantitative N-terminal charge-based fractional diagonal chromatography (ChaFRADIC) to study proteolytic events in Arabidopsis thaliana. Proteomics 15:2458–69
    [Google Scholar]
  123. 123.  Venne AS, Vogtle FN, Meisinger C, Sickmann A, Zahedi RP 2013. Novel highly sensitive, specific, and straightforward strategy for comprehensive N-terminal proteomics reveals unknown substrates of the mitochondrial peptidase Icp55. J. Proteome Res. 12:3823–30
    [Google Scholar]
  124. 124.  Vicente J, Mendiondo GM, Movahedi M, Peirats-Llobet M, Juan YT et al. 2017. The Cys-Arg/N-end rule pathway is a general sensor of abiotic stress in flowering plants. Curr. Biol. 27:3183–90.e4First report on physiological, biochemical, and metabolic responses mediated by the N-degron pathway in plant immunity.
    [Google Scholar]
  125. 125.  Vicente J, Mendiondo GM, Pauwels J, Pastor V, Izquierdo Y et al. 2018. Distinct branches of the N-end rule pathway modulate the plant immune response. New Phytol 17:15387
    [Google Scholar]
  126. 126.  Wadas B, Piatkov KI, Brower CS, Varshavsky A 2016. Analyzing N-terminal arginylation through the use of peptide arrays and degradation assays. J. Biol. Chem. 291:20976–92
    [Google Scholar]
  127. 127.  Walia A, Waadt R, Jones AM 2018. Genetically encoded biosensors in plants: pathways to discovery. Annu. Rev. Plant Biol. 69:497–524
    [Google Scholar]
  128. 128.  Wang H, Piatkov K, Brower C, Varshavsky A 2009. Glutamine-specific N-terminal amidase, a component of the N-end rule pathway. Mol. Cell 34:686–95
    [Google Scholar]
  129. 129.  Waszczak C, Akter S, Eeckhout D, Persiau G, Wahni K et al. 2014. Sulfenome mining in Arabidopsis thaliana. PNAS 111:11545–50
    [Google Scholar]
  130. 130.  Weits D, Giuntoli B, Kosmacz M, Parlanti S, Hubberten H et al. 2014. Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat. Commun. 5:3425Identification of PLANT CYSTEINE OXIDASEs mediating the oxidation of N-terminal Cys residues using O2 as a cosubstrate.
    [Google Scholar]
  131. 131.  White MD, Kamps JJAG, East S, Taylor Kearney LJ, Flashman E 2018. The plant cysteine oxidases from Arabidopsis thaliana are kinetically tailored to act as oxygen sensors. J. Biol. Chem. 293:11786–95
    [Google Scholar]
  132. 132.  White MD, Klecker M, Hopkinson RJ, Weits DA, Mueller C et al. 2017. Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. Nat. Commun. 8:14690First evidence of enzymatic Cys oxidation in the presence of O2 by PLANT CYSTEINE OXIDASEs enabling N-terminal arginylation by ARGINYLTRANSFERASE 1.
    [Google Scholar]
  133. 133.  Worley CK, Ling R, Callis J 1998. Engineering in vivo instability of firefly luciferase and Escherichia coli β-glucuronidase in higher plants using recognition elements from the ubiquitin pathway. Plant Mol. Biol. 37:337–47
    [Google Scholar]
  134. 134.  Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA 2006. The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. PNAS 103:14631–36
    [Google Scholar]
  135. 135.  Yarnell A 2009. New chemical tools are poised to help scientists explore the roles oxidized cysteine residues might play in biology. Chem. Eng. News 87:38–40
    [Google Scholar]
  136. 136.  Yoo YD, Mun SR, Ji CH, Sung KW, Kang KY et al. 2018. N-terminal arginylation generates a bimodal degron that modulates autophagic proteolysis. PNAS 115:E2716–24
    [Google Scholar]
  137. 137.  Yoshida S, Ito M, Callis J, Nishida I, Watanabe A 2002. A delayed leaf senescence mutant is defective in arginyl-tRNA:protein arginyltransferase, a component of the N-end rule pathway in Arabidopsis. Plant J 32:129–37
    [Google Scholar]
  138. 138.  Zhang H, Deery MJ, Gannon L, Powers SJ, Lilley KS, Theodoulou FL 2015. Quantitative proteomics analysis of the Arg/N-end rule pathway of targeted degradation in Arabidopsis roots. Proteomics 15:2447–57
    [Google Scholar]
  139. 139.  Zhang H, Gannon L, Hassall KL, Deery MJ, Gibbs DJ et al. 2018. N-terminomics reveals control of Arabidopsis seed storage proteins and proteases by the Arg/N-end rule pathway. New Phytol 218:1106–26
    [Google Scholar]
  140. 140.  Goslin K, Eschen-Lippold L, Naumann C, Linster E, Sorel M et al. 2019. Differential N-end rule degradation of RIN4/NOI fragments generated by the AvrRpt2 effector protease. bioRxiv 583054. https://doi.org/10.1101/583054
    [Crossref]
/content/journals/10.1146/annurev-arplant-050718-095937
Loading
/content/journals/10.1146/annurev-arplant-050718-095937
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error