Abstract
Proteolysis is an essential process to maintain cellular homeostasis. One pathway that mediates selective protein degradation and which is in principle conserved throughout the kingdoms of life is the N-degron pathway, formerly called the ‘N-end rule’. In the cytosol of eukaryotes and prokaryotes, N-terminal residues can be major determinants of protein stability. While the eukaryotic N-degron pathway depends on the ubiquitin proteasome system, the prokaryotic counterpart is driven by the Clp protease system. Plant chloroplasts also contain such a protease network, which suggests that they might harbor an organelle specific N-degron pathway similar to the prokaryotic one. Recent discoveries indicate that the N-terminal region of proteins affects their stability in chloroplasts and provides support for a Clp-mediated entry point in an N-degron pathway in plastids. This review discusses structure, function and specificity of the chloroplast Clp system, outlines experimental approaches to test for an N-degron pathway in chloroplasts, relates these aspects into general plastid proteostasis and highlights the importance of an understanding of plastid protein turnover.
Funding source: Deutsche Forschungsgemeinschaft
Award Identifier / Grant number: DI 1794/3-1
Award Identifier / Grant number: DI 1794/6-1
Funding source: European Regional Development Fund (EFRE)
Award Identifier / Grant number: INDUCEPROT - Induced Accumulation of Recombinant P
Award Identifier / Grant number: LSP-TP2-1 of the Research Focus Program “Molecul
Acknowledgements
This work was supported by a grant for setting up the junior research group of the ScienceCampus Halle—Plant-based Bioeconomy to N. D., by DI 1794/3-1 and DI 1794/6-1 of the German Research Foundation (DFG) to N. D., and by grant LSP-TP2-1 of the Research Focus Program “Molecular Biosciences as a Motor for a Knowledge-Based Economy” from the European Regional Development Fund (EFRE) to N. D. as well as EFRE grant INDUCEPROT – Induced Accumulation of Recombinant Proteins in Barley Endosperm of the SCH to N.D. Subsequent financial support came from the ministry for science and culture (MWK) of the state of Lower Saxony.
-
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
-
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Adam, Z., Adamska, I., Nakabayashi, K., Ostersetzer, O., Haussuhl, K., Manuell, A., Zheng, B., Vallon, O., Rodermel, S.R., Shinozaki, K., et al.. (2001). Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiol. 125: 1912–1918, https://doi.org/10.1104/pp.125.4.1912.Search in Google Scholar PubMed PubMed Central
Aguilar Lucero, D., Cantoia, A., Sanchez-Lopez, C., Binolfi, A., Mogk, A., Ceccarelli, E.A., and Rosano, G.L. (2021). Structural features of the plant N-recognin ClpS1 and sequence determinants in its targets that govern substrate selection. FEBS Lett. 595: 1525–1541, https://doi.org/10.1002/1873-3468.14081.Search in Google Scholar PubMed
Ahyoung, A.P., Koehl, A., Vizcarra, C.L., Cascio, D., and Egea, P.F. (2016). Structure of a putative ClpS N-end rule adaptor protein from the malaria pathogen Plasmodium falciparum. Protein Sci. 25: 689–701, https://doi.org/10.1002/pro.2868.Search in Google Scholar PubMed PubMed Central
Apel, W., Schulze, W.X., and Bock, R. (2010). Identification of protein stability determinants in chloroplasts. Plant J. 63: 636–650, https://doi.org/10.1111/j.1365-313x.2010.04268.x.Search in Google Scholar PubMed PubMed Central
Apitz, J., Nishimura, K., Schmied, J., Wolf, A., Hedtke, B., Van Wijk, K.J., and Grimm, B. (2016). Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiol. 170: 2040–2051, https://doi.org/10.1104/pp.15.01945.Search in Google Scholar PubMed PubMed Central
Bachmair, A., Becker, F., and Schell, J. (1993). Use of a reporter transgene to generate arabidopsis mutants in ubiquitin-dependent protein degradation. Proc. Natl. Acad. Sci. U. S. A. 90: 418–421, https://doi.org/10.1073/pnas.90.2.418.Search in Google Scholar PubMed PubMed Central
Bachmair, A., Finley, D., and Varshavsky, A. (1986). In vivo half-life of a protein is a function of its amino-terminal residue. Science 234: 179–186, https://doi.org/10.1126/science.3018930.Search in Google Scholar PubMed
Barreto, P., Dambire, C., Sharma, G., Vicente, J., Osborne, R., Yassitepe, J., Gibbs, D.J., Maia, I.G., Holdsworth, M.J., and Arruda, P. (2022). Mitochondrial retrograde signaling through UCP1-mediated inhibition of the plant oxygen-sensing pathway. Curr. Biol. 32: 1403–1411.e1404, https://doi.org/10.1016/j.cub.2022.01.037.Search in Google Scholar PubMed PubMed Central
Baumler, J., Riber, W., Klecker, M., Muller, L., Dissmeyer, N., Weig, A.R., and Mustroph, A. (2019). AtERF#111/ABR1 is a transcriptional activator involved in the wounding response. Plant J. 100: 969–990, https://doi.org/10.1111/tpj.14490.Search in Google Scholar PubMed
Bellucci, M., De Marchis, F., Mannucci, R., Bock, R., and Arcioni, S. (2005). Cytoplasm and chloroplasts are not suitable subcellular locations for beta-zein accumulation in transgenic plants. J. Exp. Bot. 56: 1205–1212, https://doi.org/10.1093/jxb/eri114.Search in Google Scholar PubMed
Birch-Machin, I., Newell, C.A., Hibberd, J.M., and Gray, J.C. (2004). Accumulation of rotavirus VP6 protein in chloroplasts of transplastomic tobacco is limited by protein stability. Plant Biotechnol. J. 2: 261–270, https://doi.org/10.1111/j.1467-7652.2004.00072.x.Search in Google Scholar PubMed
Bock, R. (2014). Engineering chloroplasts for high-level foreign protein expression. Methods Mol. Biol. 1132: 93–106, https://doi.org/10.1007/978-1-62703-995-6_5.Search in Google Scholar PubMed
Bouchnak, I. and Van Wijk, K.J. (2019). N-degron pathways in plastids. Trends Plant Sci. 24: 917–926, https://doi.org/10.1016/j.tplants.2019.06.013.Search in Google Scholar PubMed
Bouchnak, I. and Van Wijk, K.J. (2021). Structure, function, and substrates of Clp AAA+ protease systems in cyanobacteria, plastids, and apicoplasts: a comparative analysis. J. Biol. Chem. 296: 100338, https://doi.org/10.1016/j.jbc.2021.100338.Search in Google Scholar PubMed PubMed Central
Bruch, E.M., Rosano, G.L., and Ceccarelli, E.A. (2012). Chloroplastic Hsp100 chaperones ClpC2 and ClpD interact in vitro with a transit peptide only when it is located at the N-terminus of a protein. BMC Plant Biol. 12: 57, https://doi.org/10.1186/1471-2229-12-57.Search in Google Scholar PubMed PubMed Central
Calvo, S.E., Julien, O., Clauser, K.R., Shen, H., Kamer, K.J., Wells, J.A., and Mootha, V.K. (2017). Comparative analysis of mitochondrial N-termini from mouse, human, and yeast. Mol. Cell. Proteomics 16: 512–523, https://doi.org/10.1074/mcp.m116.063818.Search in Google Scholar PubMed PubMed Central
Chen, P.J., Senthilkumar, R., Jane, W.N., He, Y., Tian, Z., and Yeh, K.W. (2014). Transplastomic Nicotiana benthamiana plants expressing multiple defence genes encoding protease inhibitors and chitinase display broad-spectrum resistance against insects, pathogens and abiotic stresses. Plant Biotechnol. J. 12: 503–515, https://doi.org/10.1111/pbi.12157.Search in Google Scholar PubMed
Clarke, A.K. (2012). The chloroplast ATP-dependent Clp protease in vascular plants – new dimensions and future challenges. Physiol. Plantarum 145: 235–244, https://doi.org/10.1111/j.1399-3054.2011.01541.x.Search in Google Scholar PubMed
Colombo, C.V., Ceccarelli, E.A., and Rosano, G.L. (2014). Characterization of the accessory protein ClpT1 from Arabidopsis thaliana: oligomerization status and interaction with Hsp100 chaperones. BMC Plant Biol. 14: 228, https://doi.org/10.1186/s12870-014-0228-0.Search in Google Scholar PubMed PubMed Central
Colombo, C.V., Rosano, G.L., Mogk, A., and Ceccarelli, E.A. (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: 624–636, https://doi.org/10.1093/pcp/pcy016.Search in Google Scholar PubMed
Constan, D., Froehlich, J.E., Rangarajan, S., and Keegstra, K. (2004). A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol. 136: 3605–3615, https://doi.org/10.1104/pp.104.052928.Search in Google Scholar PubMed PubMed Central
Daniell, H., Lin, C.S., Yu, M., and Chang, W.J. (2016). Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 17: 134, https://doi.org/10.1186/s13059-016-1004-2.Search in Google Scholar PubMed PubMed Central
Daniell, H., Rai, V., and Xiao, Y. (2019). Cold chain and virus-free oral polio booster vaccine made in lettuce chloroplasts confers protection against all three poliovirus serotypes. Plant Biotechnol. J. 17: 1357–1368, https://doi.org/10.1111/pbi.13060.Search in Google Scholar PubMed PubMed Central
De Cosa, B., Moar, W., Lee, S.B., Miller, M., and Daniell, H. (2001). Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat. Biotechnol. 19: 71–74, https://doi.org/10.1038/83559.Search in Google Scholar PubMed PubMed Central
Dissmeyer, N. (2017). Conditional modulation of biological processes by low-temperature degrons. Methods Mol. Biol. 1669: 407–416, https://doi.org/10.1007/978-1-4939-7286-9_30.Search in Google Scholar PubMed
Dissmeyer, N., Rivas, S., and Graciet, E. (2018). Life and death of proteins after protease cleavage: protein degradation by the N-end rule pathway. New Phytol. 218: 929–935, https://doi.org/10.1111/nph.14619.Search in Google Scholar PubMed
Dissmeyer, N. (2019). Conditional protein function via N-degron pathway-mediated proteostasis in stress physiology. Annu. Rev. Plant Biol. 70: 83–117, https://doi.org/10.1146/annurev-arplant-050718-095937.Search in Google Scholar PubMed
Dissmeyer, N. (2022). Oxygen sensing: protein degradation meets retrograde signaling. Curr. Biol. 32: R281–R284, https://doi.org/10.1016/j.cub.2022.02.047.Search in Google Scholar PubMed
Dong, H., Fei, G.L., Wu, C.Y., Wu, F.Q., Sun, Y.Y., Chen, M.J., Ren, Y.L., Zhou, K.N., Cheng, Z.J., Wang, J.L., et al.. (2013). A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants. Plant Physiol. 162: 1867–1880, https://doi.org/10.1104/pp.113.217604.Search in Google Scholar PubMed PubMed Central
Dougan, D.A., Truscott, K.N., and Zeth, K. (2010). The bacterial N-end rule pathway: expect the unexpected. Mol. Microbiol. 76: 545–558, https://doi.org/10.1111/j.1365-2958.2010.07120.x.Search in Google Scholar PubMed
El Bakkouri, M., Pow, A., Mulichak, A., Cheung, K.L., Artz, J.D., Amani, M., Fell, S., De Koning-Ward, T.F., Goodman, C.D., Mcfadden, G.I., et al.. (2010). The Clp chaperones and proteases of the human malaria parasite Plasmodium falciparum. J. Mol. Biol. 404: 456–477, https://doi.org/10.1016/j.jmb.2010.09.051.Search in Google Scholar PubMed
Erbse, A., Schmidt, R., Bornemann, T., Schneider-Mergener, J., Mogk, A., Zahn, R., Dougan, D.A., and Bukau, B. (2006). ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439: 753–756, https://doi.org/10.1038/nature04412.Search in Google Scholar PubMed
Faden, F., Mielke, S., and Dissmeyer, N. (2019). Modulating protein stability to switch toxic protein function on and off in living cells. Plant Physiol. 179: 929–942, https://doi.org/10.1104/pp.18.01215.Search in Google Scholar PubMed PubMed Central
Faden, F., Mielke, S., Lange, D., and Dissmeyer, N. (2014). Generic tools for conditionally altering protein abundance and phenotypes on demand. Biol. Chem. 395: 737–762, https://doi.org/10.1515/hsz-2014-0160.Search in Google Scholar PubMed
Faden, F., Ramezani, T., Mielke, S., Almudi, I., Nairz, K., Froehlich, M.S., Hockendorff, J., Brandt, W., Hoehenwarter, W., Dohmen, R.J., et al.. (2016). Phenotypes on demand via switchable target protein degradation in multicellular organisms. Nat. Commun. 7: 12202, https://doi.org/10.1038/ncomms12202.Search in Google Scholar PubMed PubMed Central
Giglione, C., Fieulaine, S., and Meinnel, T. (2009). Cotranslational processing mechanisms: towards a dynamic 3D model. Trends Biochem. Sci. 34: 417–426, https://doi.org/10.1016/j.tibs.2009.04.003.Search in Google Scholar PubMed
Goslin, K., Eschen-Lippold, L., Naumann, C., Linster, E., Sorel, M., Klecker, M., De Marchi, R., Kind, A., Wirtz, M., Lee, J., et al.. (2019). Differential N-end rule degradation of RIN4/NOI fragments generated by the AvrRpt2 effector protease. Plant Physiol. 180: 2272–2289, https://doi.org/10.1104/pp.19.00251.Search in Google Scholar PubMed PubMed Central
Graciet, E., Hu, R.G., Piatkov, K., Rhee, J.H., Schwarz, E.M., and Varshavsky, A. (2006). Aminoacyl-transferases and the N-end rule pathway of prokaryotic/eukaryotic specificity in a human pathogen. Proc. Natl. Acad. Sci. U. S. A. 103: 3078–3083, https://doi.org/10.1073/pnas.0511224103.Search in Google Scholar PubMed PubMed Central
Hirel, P.H., Schmitter, M.J., Dessen, P., Fayat, G., and Blanquet, S. (1989). Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Proc. Natl. Acad. Sci. U. S. A. 86: 8247–8251, https://doi.org/10.1073/pnas.86.21.8247.Search in Google Scholar PubMed PubMed Central
Jarvis, P. and Lopez-Juez, E. (2013). Biogenesis and homeostasis of chloroplasts and other plastids. Nat. Rev. Mol. Cell Biol. 14: 787–802, https://doi.org/10.1038/nrm3702.Search in Google Scholar PubMed
Jin, S., Kanagaraj, A., Verma, D., Lange, T., and Daniell, H. (2011). Release of hormones from conjugates: chloroplast expression of β-glucosidase results in elevated phytohormone levels associated with significant increase in biomass and protection from aphids or whiteflies conferred by sucrose esters. Plant Physiol. 155: 222–235, https://doi.org/10.1104/pp.110.160754.Search in Google Scholar PubMed PubMed Central
Kapust, R.B., Tozser, J., Copeland, T.D., and Waugh, D.S. (2002). The P1′ specificity of tobacco etch virus protease. Biochem. Biophys. Res. Commun. 294: 949–955, https://doi.org/10.1016/s0006-291x(02)00574-0.Search in Google Scholar
Khan, M.S., Kanwal, B., and Nazir, S. (2015). Metabolic engineering of the chloroplast genome reveals that the yeast ArDH gene confers enhanced tolerance to salinity and drought in plants. Front. Plant Sci. 6: 725, https://doi.org/10.3389/fpls.2015.00725.Search in Google Scholar PubMed PubMed Central
Kim, J., Kimber, M.S., Nishimura, K., Friso, G., Schultz, L., Ponnala, L., and Van Wijk, K.J. (2015). Structures, functions, and interactions of ClpT1 and ClpT2 in the Clp protease system of Arabidopsis chloroplasts. Plant Cell 27: 1477–1496, https://doi.org/10.1105/tpc.15.00106.Search in Google Scholar PubMed PubMed Central
Kim, J., Rudella, A., Ramirez Rodriguez, V., Zybailov, B., Olinares, P.D.B., and Van Wijk, K.J. (2009). Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cel 21: 1669–1692, https://doi.org/10.1105/tpc.108.063784.Search in Google Scholar PubMed PubMed Central
Kim, J., Olinares, P.D., Oh, S.H., Ghisaura, S., Poliakov, A., Ponnala, L., and Van Wijk, K.J. (2013). Modified Clp protease complex in the ClpP3 null mutant and consequences for chloroplast development and function in Arabidopsis. Plant Physiol. 162: 157–179, https://doi.org/10.1104/pp.113.215699.Search in Google Scholar PubMed PubMed Central
Kim, L., Heo, J., Kwon, D.H., Shin, J.S., Jang, S.H., Park, Z.Y., and Song, H.K. (2021). Structural basis for the N-degron specificity of ClpS1 from Arabidopsis thaliana. Protein Sci. 30: 700–708, https://doi.org/10.1002/pro.4018.Search in Google Scholar PubMed PubMed Central
Koussevitzky, S., Stanne, T.M., Peto, C.A., Giap, T., Sjogren, L.L., Zhao, Y., Clarke, A.K., and Chory, J. (2007). An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development. Plant Mol. Biol. 63: 85–96, https://doi.org/10.1007/s11103-006-9074-2.Search in Google Scholar PubMed
Kovacheva, S., Bedard, J., Patel, R., Dudley, P., Twell, D., Rios, G., Koncz, C., and Jarvis, P. (2005). In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J. 41: 412–428, https://doi.org/10.1111/j.1365-313x.2004.02307.x.Search in Google Scholar PubMed
Kovacheva, S., Bedard, J., Wardle, A., Patel, R., and Jarvis, P. (2007). Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J. 50: 364–379, https://doi.org/10.1111/j.1365-313x.2007.03060.x.Search in Google Scholar
Lee, S., Lee, D.W., Lee, Y., Mayer, U., Stierhof, Y.D., Lee, S., Jurgens, G., and Hwang, I. (2009). Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 21: 3984–4001, https://doi.org/10.1105/tpc.109.071548.Search in Google Scholar PubMed PubMed Central
Li, W., Wu, C., Hu, G., Xing, L., Qian, W., Si, H., Sun, Z., Wang, X., Fu, Y., and Liu, W. (2013). Characterization and fine mapping of a novel rice narrow leaf mutant nal9. J. Integr. Plant Biol. 55: 1016–1025, https://doi.org/10.1111/jipb.12098.Search in Google Scholar PubMed
Li, L., Nelson, C.J., Trosch, J., Castleden, I., Huang, S., and Millar, A.H. (2017). Protein degradation rate in Arabidopsis thaliana leaf growth and development. Plant Cell 29: 207–228, https://doi.org/10.1105/tpc.16.00768.Search in Google Scholar PubMed PubMed Central
Liao, J.R., Friso, G., Kim, J., and Van Wijk, K.J. (2018). Consequences of the loss of catalytic triads in chloroplast CLPPR protease core complexes in vivo. Plant Direct 2: e00086, https://doi.org/10.1002/pld3.86.Search in Google Scholar PubMed PubMed Central
Lin, M.T., Occhialini, A., Andralojc, P.J., Parry, M.A., and Hanson, M.R. (2014). A faster Rubisco with potential to increase photosynthesis in crops. Nature 513: 547–550, https://doi.org/10.1038/nature13776.Search in Google Scholar PubMed PubMed Central
Ling, Q., Huang, W., Baldwin, A., and Jarvis, P. (2012). Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system. Science 338: 655–659, https://doi.org/10.1126/science.1225053.Search in Google Scholar PubMed
Ling, Q., Broad, W., Trosch, R., Topel, M., Demiral Sert, T., Lymperopoulos, P., Baldwin, A., and Jarvis, R.P. (2019). Ubiquitin-dependent chloroplast-associated protein degradation in plants. Science 363: eaav4467, https://doi.org/10.1126/science.aav4467.Search in Google Scholar PubMed
Lu, Y., Rijzaani, H., Karcher, D., Ruf, S., and Bock, R. (2013). Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc. Natl. Acad. Sci. U. S. A. 110: E623–E632, https://doi.org/10.1073/pnas.1216898110.Search in Google Scholar PubMed PubMed Central
Lupas, A.N. and Koretke, K.K. (2003). Bioinformatic analysis of ClpS, a protein module involved in prokaryotic and eukaryotic protein degradation. J. Struct. Biol. 141: 77–83, https://doi.org/10.1016/s1047-8477(02)00582-8.Search in Google Scholar PubMed
Majsec, K., Bhuiyan, N.H., Sun, Q., Kumari, S., Kumar, V., Ware, D., and Van Wijk, K.J. (2017). The plastid and mitochondrial peptidase network in Arabidopsis thaliana: a foundation for testing genetic interactions and functions in organellar proteostasis. Plant Cell 29: 2687–2710, https://doi.org/10.1105/tpc.17.00481.Search in Google Scholar PubMed PubMed Central
Millar, A.H., Heazlewood, J.L., Giglione, C., Holdsworth, M.J., Bachmair, A., and Schulze, W.X. (2019). The scope, functions, and dynamics of post-translational protein modifications. Annu. Rev. Plant Biol. 70: 119–151, https://doi.org/10.1146/annurev-arplant-050718-100211.Search in Google Scholar PubMed
Montandon, C., Dougan, D.A., and Van Wijk, K.J. (2019a). N-degron specificity of chloroplast ClpS1 in plants. FEBS Lett. 593: 962–970, https://doi.org/10.1002/1873-3468.13378.Search in Google Scholar PubMed
Montandon, C., Friso, G., Liao, J.R., Choi, J., and Van Wijk, K.J. (2019b). In vivo trapping of proteins interacting with the chloroplast CLPC1 chaperone: potential substrates and adaptors. J. Proteome Res. 18: 2585–2600, https://doi.org/10.1021/acs.jproteome.9b00112.Search in Google Scholar PubMed
Moreno, J.C., Tiller, N., Diez, M., Karcher, D., Tillich, M., Schottler, M.A., and Bock, R. (2017). Generation and characterization of a collection of knock-down lines for the chloroplast Clp protease complex in tobacco. J. Exp. Bot. 68: 2199–2218, https://doi.org/10.1093/jxb/erx066.Search in Google Scholar PubMed PubMed Central
Moreno, J.C., Martinez-Jaime, S., Schwartzmann, J., Karcher, D., Tillich, M., Graf, A., and Bock, R. (2018). Temporal proteomics of inducible RNAi lines of Clp protease subunits identifies putative protease substrates. Plant Physiol. 176: 1485–1508, https://doi.org/10.1104/pp.17.01635.Search in Google Scholar PubMed PubMed Central
Mot, A.C., Prell, E., Klecker, M., Naumann, C., Faden, F., Westermann, B., and Dissmeyer, N. (2018). Real-time detection of N-end rule-mediated ubiquitination via fluorescently labeled substrate probes. New Phytol. 217: 613–624, https://doi.org/10.1111/nph.14497.Search in Google Scholar PubMed PubMed Central
Naumann, C., Mot, A.C., and Dissmeyer, N. (2016). Generation of artificial N-end rule substrate proteins in vivo and in vitro. Methods Mol. Biol. 1450: 55–83, https://doi.org/10.1007/978-1-4939-3759-2_6.Search in Google Scholar PubMed
Nishimura, K., Asakura, Y., Friso, G., Kim, J., Oh, S.H., Rutschow, H., Ponnala, L., and Van Wijk, K.J. (2013). ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. Plant Cell 25: 2276–2301, https://doi.org/10.1105/tpc.113.112557.Search in Google Scholar PubMed PubMed Central
Nishimura, K., Apitz, J., Friso, G., Kim, J., Ponnala, L., Grimm, B., and Van Wijk, K.J. (2015). Discovery of a unique Clp component, ClpF, in chloroplasts: a proposed binary ClpF-ClpS1 adaptor complex functions in substrate recognition and delivery. Plant Cell 27: 2677–2691, https://doi.org/10.1105/tpc.15.00574.Search in Google Scholar PubMed PubMed Central
Nishimura, K., Kato, Y., and Sakamoto, W. (2016). Chloroplast proteases: updates on proteolysis within and across suborganellar compartments. Plant Physiol. 171: 2280–2293, https://doi.org/10.1104/pp.16.00330.Search in Google Scholar PubMed PubMed Central
Nishimura, K., Kato, Y., and Sakamoto, W. (2017). Essentials of proteolytic machineries in chloroplasts. Mol. Plant 10: 4–19, https://doi.org/10.1016/j.molp.2016.08.005.Search in Google Scholar PubMed
Nishimura, K. and Van Wijk, K.J. (2015). Organization, function and substrates of the essential Clp protease system in plastids. Biochim. Biophys. Acta 1847: 915–930, https://doi.org/10.1016/j.bbabio.2014.11.012.Search in Google Scholar PubMed
Oey, M., Lohse, M., Kreikemeyer, B., and Bock, R. (2009). Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J. 57: 436–445, https://doi.org/10.1111/j.1365-313x.2008.03702.x.Search in Google Scholar PubMed
Oh, J.H., Hyun, J.Y., Chen, S.J., and Varshavsky, A. (2020). Five enzymes of the Arg/N-degron pathway form a targeting complex: the concept of superchanneling. Proc. Natl. Acad. Sci. U. S. A. 117: 10778–10788, https://doi.org/10.1073/pnas.2003043117.Search in Google Scholar PubMed PubMed Central
Olinares, P.D., Kim, J., Davis, J.I., and Van Wijk, K.J. (2011a). Subunit stoichiometry, evolution, and functional implications of an asymmetric plant plastid ClpP/R protease complex in. Arabidopsis Plant Cell 23: 2348–2361, https://doi.org/10.1105/tpc.111.086454.Search in Google Scholar PubMed PubMed Central
Olinares, P.D., Kim, J. and Van Wijk, K.J. (2011b). The Clp protease system; a central component of the chloroplast protease network. Biochim. Biophys. Acta 1807: 999–1011, https://doi.org/10.1016/j.bbabio.2010.12.003.Search in Google Scholar PubMed
Ortega, J., Lee, H.S., Maurizi, M.R., and Steven, A.C. (2004). ClpA and ClpX ATPases bind simultaneously to opposite ends of ClpP peptidase to form active hybrid complexes. J. Struct. Biol. 146: 217–226, https://doi.org/10.1016/j.jsb.2003.11.023.Search in Google Scholar PubMed
Park, J., Yan, G., Kwon, K.C., Liu, M., Gonnella, P.A., Yang, S., and Daniell, H. (2020). Oral delivery of novel human IGF-1 bioencapsulated in lettuce cells promotes musculoskeletal cell proliferation, differentiation and diabetic fracture healing. Biomaterials 233: 119591, https://doi.org/10.1016/j.biomaterials.2019.119591.Search in Google Scholar PubMed PubMed Central
Peltier, J.B., Ripoll, D.R., Friso, G., Rudella, A., Cai, Y., Ytterberg, J., Giacomelli, L., Pillardy, J., and Van Wijk, K.J. (2004). Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications. J. Biol. Chem. 279: 4768–4781, https://doi.org/10.1074/jbc.m309212200.Search in Google Scholar PubMed
Perrar, A., Dissmeyer, N., and Huesgen, P.F. (2019). New beginnings and new ends: methods for large-scale characterization of protein termini and their use in plant biology. J. Exp. Bot. 70: 2021–2038, https://doi.org/10.1093/jxb/erz104.Search in Google Scholar PubMed PubMed Central
Pulido, P., Llamas, E., Llorente, B., Ventura, S., Wright, L.P., and Rodriguez-Concepcion, M. (2022). Correction: specific Hsp100 chaperones determine the fate of the first enzyme of the plastidial isoprenoid pathway for either refolding or degradation by the stromal clp protease in Arabidopsis. PLoS Genet. 18: e1010216, https://doi.org/10.1371/journal.pgen.1010216.Search in Google Scholar PubMed PubMed Central
Rei Liao, J.Y., Friso, G., Forsythe, E.S., Michel, E.J.S., Williams, A.M., Boguraev, S.S., Ponnala, L., Sloan, D.B., and Van Wijk, K.J. (2022). Proteomics, phylogenetics, and coexpression analyses indicate novel interactions in the plastid CLP chaperone-protease system. J. Biol. Chem. 298: 101609, https://doi.org/10.1016/j.jbc.2022.101609.Search in Google Scholar PubMed PubMed Central
Rei Liao, J.Y. and Van Wijk, K.J. (2019). Discovery of AAA+ protease substrates through trapping approaches. Trends Biochem. Sci. 44: 528–545, https://doi.org/10.1016/j.tibs.2018.12.006.Search in Google Scholar PubMed
Reichman, P. and Dissmeyer, N. (2017). In vivo reporters for protein half-life. Methods Mol. Biol. 1669: 387–406, https://doi.org/10.1007/978-1-4939-7286-9_29.Search in Google Scholar PubMed
Rodriguez-Concepcion, M., D’andrea, L., and Pulido, P. (2019). Control of plastidial metabolism by the Clp protease complex. J. Exp. Bot. 70: 2049–2058, https://doi.org/10.1093/jxb/ery441.Search in Google Scholar PubMed
Rosano, G.L., Bruch, E.M., and Ceccarelli, E.A. (2011). Insights into the Clp/HSP100 chaperone system from chloroplasts of Arabidopsis thaliana. J. Biol. Chem. 286: 29671–29680, https://doi.org/10.1074/jbc.m110.211946.Search in Google Scholar
Rowland, E., Kim, J., Bhuiyan, N.H., and Van Wijk, K.J. (2015). The Arabidopsis chloroplast stromal N-terminome: complexities of amino-terminal protein maturation and stability. Plant Physiol. 169: 1881–1896, https://doi.org/10.1104/pp.15.01214.Search in Google Scholar PubMed PubMed Central
Ruf, S., Forner, J., Hasse, C., Kroop, X., Seeger, S., Schollbach, L., Schadach, A., and Bock, R. (2019). High-efficiency generation of fertile transplastomic Arabidopsis plants. Native Plants 5: 282–289, https://doi.org/10.1038/s41477-019-0359-2.Search in Google Scholar PubMed PubMed Central
Sako, K., Yanagawa, Y., Kanai, T., Sato, T., Seki, M., Fujiwara, M., Fukao, Y., and Yamaguchi, J. (2014). Proteomic analysis of the 26S proteasome reveals its direct interaction with transit peptides of plastid protein precursors for their degradation. J. Proteome Res. 13: 3223–3230, https://doi.org/10.1021/pr401245g.Search in Google Scholar PubMed
Schmidt, A., Kochanowski, K., Vedelaar, S., Ahrne, E., Volkmer, B., Callipo, L., Knoops, K., Bauer, M., Aebersold, R., and Heinemann, M. (2016). The quantitative and condition-dependent Escherichia coli proteome. Nat. Biotechnol. 34: 104–110, https://doi.org/10.1038/nbt.3418.Search in Google Scholar PubMed PubMed Central
Shen, G., Adam, Z., and Zhang, H. (2007a). The E3 ligase AtCHIP ubiquitylates FtsH1, a component of the chloroplast FtsH protease, and affects protein degradation in chloroplasts. Plant J. 52: 309–321, https://doi.org/10.1111/j.1365-313x.2007.03239.x.Search in Google Scholar
Shen, G., Yan, J., Pasapula, V., Luo, J., He, C., Clarke, A.K., and Zhang, H. (2007b). The chloroplast protease subunit ClpP4 is a substrate of the E3 ligase AtCHIP and plays an important role in chloroplast function. Plant J. 49: 228–237, https://doi.org/10.1111/j.1365-313x.2006.02963.x.Search in Google Scholar
Shikanai, T., Shimizu, K., Ueda, K., Nishimura, Y., Kuroiwa, T., and Hashimoto, T. (2001). The chloroplast clpP gene, encoding a proteolytic subunit of ATP-dependent protease, is indispensable for chloroplast development in tobacco. Plant Cell Physiol. 42: 264–273, https://doi.org/10.1093/pcp/pce031.Search in Google Scholar PubMed
Sjogren, L.L. and Clarke, A.K. (2011). Assembly of the chloroplast ATP-dependent Clp protease in Arabidopsis is regulated by the ClpT accessory proteins. Plant Cell 23: 322–332, https://doi.org/10.1105/tpc.110.082321.Search in Google Scholar PubMed PubMed Central
Sjogren, L.L., Macdonald, T.M., Sutinen, S., and Clarke, A.K. (2004). Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiol. 136: 4114–4126, https://doi.org/10.1104/pp.104.053835.Search in Google Scholar PubMed PubMed Central
Sjogren, L.L., Stanne, T.M., Zheng, B., Sutinen, S., and Clarke, A.K. (2006). Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis. Plant Cell 18: 2635–2649, https://doi.org/10.1105/tpc.106.044594.Search in Google Scholar PubMed PubMed Central
Stanne, T.M., Sjogren, L.L., Koussevitzky, S., and Clarke, A.K. (2009). Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis. Biochem. J. 417: 257–268, https://doi.org/10.1042/bj20081146.Search in Google Scholar PubMed
Stein, B.J., Grant, R.A., Sauer, R.T., and Baker, T.A. (2016). Structural basis of an N-degron adaptor with more stringent specificity. Structure 24: 232–242, https://doi.org/10.1016/j.str.2015.12.008.Search in Google Scholar PubMed PubMed Central
Su, J., Zhu, L., Sherman, A., Wang, X., Lin, S., Kamesh, A., Norikane, J.H., Streatfield, S.J., Herzog, R.W., and Daniell, H. (2015). Low cost industrial production of coagulation factor IX bioencapsulated in lettuce cells for oral tolerance induction in hemophilia B. Biomaterials 70: 84–93, https://doi.org/10.1016/j.biomaterials.2015.08.004.Search in Google Scholar PubMed PubMed Central
Sun, Y., Yao, Z., Chen, H., Ye, Y., Lyu, Y., Broad, W., Fournier, M., Chen, G., Hu, Y., Mohammed, S., et al. (2022). Ubiquitin-based pathway acts inside chloroplasts to regulate photosynthesis. Sci. Adv. 8: eabq7352, https://doi.org/10.1126/sciadv.abq7352.Search in Google Scholar PubMed PubMed Central
Tan, J.L., Ward, L., Truscott, K.N., and Dougan, D.A. (2016). The N-end rule adaptor protein ClpS from Plasmodium falciparum exhibits broad substrate specificity. FEBS Lett. 590: 3397–3406, https://doi.org/10.1002/1873-3468.12382.Search in Google Scholar PubMed
Tapken, W., Kim, J., Nishimura, K., Van Wijk, K.J., and Pilon, M. (2015). The Clp protease system is required for copper ion-dependent turnover of the PAA2/HMA8 copper transporter in chloroplasts. New Phytol. 205: 511–517, https://doi.org/10.1111/nph.13093.Search in Google Scholar PubMed
Tobias, J.W., Shrader, T.E., Rocap, G., and Varshavsky, A. (1991). The N-end rule in bacteria. Science 254: 1374–1377, https://doi.org/10.1126/science.1962196.Search in Google Scholar PubMed
Van Wijk, K.J. (2015). Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes. Annu. Rev. Plant Biol. 66: 75–111, https://doi.org/10.1146/annurev-arplant-043014-115547.Search in Google Scholar PubMed
Vandervere, P.S., Bennett, T.M., Oblong, J.E., and Lamppa, G.K. (1995). A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases. Proc. Natl. Acad. Sci. U. S. A. 92: 7177–7181, https://doi.org/10.1073/pnas.92.16.7177.Search in Google Scholar PubMed PubMed Central
Varshavsky, A. (2019). N-degron and C-degron pathways of protein degradation. Proc. Natl. Acad. Sci. U. S. A. 116: 358–366, https://doi.org/10.1073/pnas.1816596116.Search in Google Scholar PubMed PubMed Central
Wang, K.H., Roman-Hernandez, G., Grant, R.A., Sauer, R.T., and Baker, T.A. (2008). The molecular basis of N-end rule recognition. Mol. Cell 32: 406–414, https://doi.org/10.1016/j.molcel.2008.08.032.Search in Google Scholar PubMed PubMed Central
Wang, Y., Wei, Z., and Xing, S. (2018). Stable plastid transformation of rice, a monocot cereal crop. Biochem. Biophys. Res. Commun. 503: 2376–2379, https://doi.org/10.1016/j.bbrc.2018.06.164.Search in Google Scholar PubMed
Welsch, R., Zhou, X., Yuan, H., Alvarez, D., Sun, T., Schlossarek, D., Yang, Y., Shen, G., Zhang, H., Rodriguez-Concepcion, M., et al.. (2018). Clp protease and OR directly control the proteostasis of phytoene synthase, the crucial enzyme for carotenoid biosynthesis in Arabidopsis. Mol. Plant 11: 149–162, https://doi.org/10.1016/j.molp.2017.11.003.Search in Google Scholar PubMed
Winckler, L.I. and Dissmeyer, N. (2022). Engineering destabilizing N-termini in plastids. Methods Mol. Biol. 2379: 171–181, https://doi.org/10.1007/978-1-0716-1791-5_10.Search in Google Scholar PubMed
Winckler, L.I. and Dissmeyer, N. (2023). TEV protease cleavage in artificial substrate generation. Methods Enzymol. https://doi.org/10.1016/bs.mie.2023.02.015.Search in Google Scholar
Wu, G.Z., Chalvin, C., Hoelscher, M., Meyer, E.H., Wu, X.N., and Bock, R. (2018). Control of retrograde signaling by rapid turnover of GENOMES UNCOUPLED1. Plant Physiol. 176: 2472–2495, https://doi.org/10.1104/pp.18.00009.Search in Google Scholar PubMed PubMed Central
Wurbs, D., Ruf, S., and Bock, R. (2007). Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. Plant J. 49: 276–288, https://doi.org/10.1111/j.1365-313x.2006.02960.x.Search in Google Scholar PubMed
Xing, A., Williams, M.E., Bourett, T.M., Hu, W., Hou, Z., Meeley, R.B., Jaqueth, J., Dam, T., and Li, B. (2014). A pair of homoeolog ClpP5 genes underlies a virescent yellow-like mutant and its modifier in maize. Plant J. 79: 192–205, https://doi.org/10.1111/tpj.12568.Search in Google Scholar PubMed
Yu, A.Y. and Houry, W.A. (2007). ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett. 581: 3749–3757, https://doi.org/10.1016/j.febslet.2007.04.076.Search in Google Scholar PubMed
Yu, Q., Barkan, A., and Maliga, P. (2019). Engineered RNA-binding protein for transgene activation in non-green plastids. Native Plants 5: 486–490, https://doi.org/10.1038/s41477-019-0413-0.Search in Google Scholar PubMed
Zhang, J., Khan, S.A., Hasse, C., Ruf, S., Heckel, D.G., and Bock, R. (2015). Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347: 991–994, https://doi.org/10.1126/science.1261680.Search in Google Scholar PubMed
Zhou, F., Badillo-Corona, J.A., Karcher, D., Gonzalez-Rabade, N., Piepenburg, K., Borchers, A.M., Maloney, A.P., Kavanagh, T.A., Gray, J.C., and Bock, R. (2008). High-level expression of human immunodeficiency virus antigens from the tobacco and tomato plastid genomes. Plant Biotechnol. J 6: 897–913, https://doi.org/10.1111/j.1467-7652.2008.00356.x.Search in Google Scholar PubMed
Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodriguez, V.R., Asakura, Y., Sun, Q., and Van Wijk, K.J. (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol. Cell. Proteomics 8: 1789–1810, https://doi.org/10.1074/mcp.m900104-mcp200.Search in Google Scholar
Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and Van Wijk, K.J. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3: e1994, https://doi.org/10.1371/journal.pone.0001994.Search in Google Scholar PubMed PubMed Central
© 2023 Walter de Gruyter GmbH, Berlin/Boston
