Clp Protease and OR Directly Control the Proteostasis of Phytoene Synthase, the Crucial Enzyme for Carotenoid Biosynthesis in Arabidopsis

Molecular Plant

Volumn 11, Issue 1, 2018, Pages 149-162

  Welsch, Ralf ^a   Zhou, Xiangjun ^b   Yuan, Hui ^b   Álvarez, Daniel ^a   Sun, Tianhu ^b   Schlossarek, Dennis ^a   Yang, Yong ^b   Shen, Guoxin ^c   Zhang, Hong ^d   Rodriguez Concepcion, Manuel ^e   Thannhauser, Theodore W ^b   Li, Li ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Department of Obstetrics Gynecology   (United States)

^c INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^d TEXAS TECH UNIVERSITY   (United States)

^e UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Arabidopsis; carotenoid; clp protease; OR; phytoene synthase; post translational regulation

Indexed keywords

ARABIDOPSIS PROTEIN; CAROTENOID; ENDOPEPTIDASE CLP; HEAT SHOCK PROTEIN 40; ORANGE PROTEIN, ARABIDOPSIS; PHYTOENE SYNTHASE;

ARABIDOPSIS; GENETICS; HOMEOSTASIS; METABOLISM; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN STABILITY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CAROTENOIDS; ENDOPEPTIDASE CLP; GERANYLGERANYL-DIPHOSPHATE GERANYLGERANYLTRANSFERASE; HOMEOSTASIS; HSP40 HEAT-SHOCK PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEOLYSIS;

EID: 85039043638     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2017.11.003     Document Type: Article

References (76)

1. Al-Babili, S., von Lintig, J., Haubruck, H., Beyer, P., A novel, soluble form of phytoene desaturase from Narcissus pseudonarcissus chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association and enzymatic activation. Plant J. 9 (1996), 601–612.
2. Alvarez, D., Voß B., Maass, D., Wüst, F., Schaub, P., Beyer, P., Welsch, R., Carotenogenesis is regulated by 5′UTR-mediated translation of phytoene synthase splice variants. Plant Physiol. 172 (2016), 2314–2326.
3. Apel, W., Schulze, W.X., Bock, R., Identification of protein stability determinants in chloroplasts. Plant J. 63 (2010), 636–650.
4. Apitz, J., Nishimura, K., Schmied, J., Wolf, A., Hedtke, B., van Wijk, K.J., Grimm, B., Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiol. 170 (2016), 2040–2051.
5. Bonk, M., Hoffmann, B., Von Lintig, J., Schledz, M., Al-Babili, S., Hobeika, E., Kleinig, H., Beyer, P., Chloroplast import of four carotenoid biosynthetic enzymes in vitro reveals differential fates prior to membrane binding and oligomeric assembly. Eur. J. Biochem. 247 (1997), 942–950.
6. Carol, P., Stevenson, D., Bisanz, C., Breitenbach, J., Sandmann, G., Mache, R., Coupland, G., Kuntz, M., Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11 (1999), 57–68.
7. Chayut, N., Yuan, H., Ohali, S., Meir, A., Sa'ar, U., Tzuri, G., Zheng, Y., Mazourek, M., Gepstein, S., Zhou, X., et al. Distinct mechanisms of the ORANGE protein in controlling carotenoid flux. Plant Physiol. 173 (2017), 376–389.
8. Clarke, A.K., The chloroplast ATP-dependent Clp protease in vascular plants—new dimensions and future challenges. Physiol. Plant 145 (2012), 235–244.
9. Desimone, M., Weiß-Wichert, C., Wagner, E., Altenfeld, U., Johanningmeier, U., Immunochemical studies on the clp-protease in chloroplasts: evidence for the formation of a ClpC/P complex. Bot. Acta 110 (1997), 234–239.
10. Falk, S., Sinning, I., cpSRP43 is a novel chaperone specific for light-harvesting chlorophyll a,b-binding proteins. J. Biol. Chem. 285 (2010), 21655–21661.
11. Fraser, P.D., Kiano, J.W., Truesdale, M.R., Schuch, W., Bramley, P.M., Phytoene synthase-2 enzyme activity in tomato does not contribute to carotenoid synthesis in ripening fruit. Plant Mol. Biol. 40 (1999), 687–698.
12. Fraser, P.D., Schuch, W., Bramley, P.M., Phytoene synthase from tomato (Lycopersicon esculentum) chloroplasts—partial purification and biochemical properties. Planta 211 (2000), 361–369.
13. Flores-Pérez, U., Sauret-Güeto, S., Gas, E., Jarvis, P., Rodríguez-Concepción, M., A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20 (2008), 1303–1315.
14. Hemmerlin, A., Tritsch, D., Hartmann, M., Pacaud, K., Hoeffler, J.F., van Dorsselaer, A., Rohmer, M., Bach, T.J., A cytosolic Arabidopsis D-xylulose kinase catalyzes the phosphorylation of 1-deoxy-D-xylulose into a precursor of the plastidial isoprenoid pathway. Plant Physiol. 142 (2006), 441–457.
15. Hirschberg, J., Production of high-value compounds: carotenoids and vitamin E. Curr. Opin. Biotechnol. 10 (1999), 186–191.
16. Jarvis, P., Chen, L.J., Li, H., Peto, C.A., Fankhauser, C., Chory, J., An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282 (1998), 100–103.
17. Kachanovsky, D.E., Filler, S., Isaacson, T., Hirschberg, J., Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids. Proc. Natl. Acad. Sci. USA 109 (2012), 19021–19026.
18. Kato, Y., Sakamoto, W., New insights into the types and function of proteases in plastids. Int. Rev. Cell Mol. Biol. 280 (2010), 185–218.
19. Kim, J., Rudella, A., Ramirez Rodriguez, V., Zybailov, B., Olinares, P.D., van Wijk, K.J., Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 21 (2009), 1669–1692.
20. Kim, J., Olinares, P.D., Oh, S.H., Ghisaura, S., Poliakov, A., Ponnala, L., van Wijk, K.J., Modified Clp protease complex in the ClpP3 null mutant and consequences for chloroplast development and function in Arabidopsis. Plant Physiol. 162 (2013), 157–179.
21. Kim, J., Kimber, M.S., Nishimura, K., Friso, G., Schultz, L., Ponnala, L., van Wijk, K.J., Structures, functions, and interactions of ClpT1 and ClpT2 in the Clp protease system of Arabidopsis chloroplasts. Plant Cell 27 (2015), 1477–1496.
22. Koussevitzky, S., Stanne, T.M., Peto, C.A., Giap, T., Sjögren, L.L., Zhao, Y., Clarke, A.K., Chory, J., An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development. Plant Mol. Biol. 63 (2007), 85–96.
23. Liang, F.C., Kroon, G., McAvoy, C.Z., Chi, C., Wright, P.E., Shan, S.O., Conformational dynamics of a membrane protein chaperone enables spatially regulated substrate capture and release. Proc. Natl. Acad. Sci. USA 113 (2016), E1615–E1624.
24. Lu, S., Van Eck, J., Zhou, X., Lopez, A.B., O'Halloran, D.M., Cosman, K.M., Conlin, B.J., Paolillo, D.J., Garvin, D.F., Vrebalov, J., et al. The cauliflower or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of beta-carotene accumulation. Plant Cell 18 (2006), 3594–3605.
25. Luo, Z., Zhang, J., Li, J., Yang, C., Wang, T., Ouyang, B., Li, H., Giovannoni, J., Ye, Z., A STAY-GREEN protein SlSGR1 regulates lycopene and β-carotene accumulation by interacting directly with SlPSY1 during ripening processes in tomato. New Phytol. 198 (2013), 442–452.
26. Lätari, K., Wüst, F., Hübner, M., Schaub, P., Beisel, K.G., Matsubara, S., Beyer, P., Welsch, R., Tissue-specific apocarotenoid glycosylation contributes to carotenoid homeostasis in Arabidopsis leaves. Plant Physiol. 168 (2015), 1550–1562.
27. McDonald, A.E., Ivanov, A.G., Bode, R., Maxwell, D.P., Rodermel, S.R., Hüner, N.P., Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim. Biophys. Acta 1807 (2011), 954–967.
28. 6f complex. Plant Cell 12 (2000), 137–150.
29. Martel, C., Vrebalov, J., Tafelmeyer, P., Giovannoni, J.J., The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol. 157 (2011), 1568–1579.
30. Moreno, J.C., Tiller, N., Diez, M., Karcher, D., Tillich, M., Schöttler, M.A., Bock, R., Generation and characterization of a collection of knock-down lines for the chloroplast Clp protease complex in tobacco. J. Exp. Bot. 68 (2017), 2199–2218.
31. Nakagawara, E., Sakuraba, Y., Yamasato, A., Tanaka, R., Tanaka, A., Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J. 49 (2007), 800–809.
32. Nisar, N., Li, L., Lu, S., Khin, N.C., Pogson, B.J., Carotenoid metabolism in plants. Mol. Plant 8 (2015), 68–82.
33. Nishimura, K., van Wijk, K.J., Organization, function and substrates of the essential Clp protease system in plastids. Biochim. Biophys. Acta 1847 (2015), 915–930.
34. Nishimura, K., Apitz, J., Friso, G., Kim, J., Ponnala, L., Grimm, B., van Wijk, K.J., 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 (2015), 2677–2691.
35. Nishimura, K., Asakura, Y., Friso, G., Kim, J., Oh, S.H., Rutschow, H., Ponnala, L., van Wijk, K.J., ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. Plant Cell 25 (2013), 2276–2301.
36. Norris, S.R., Barrette, T.R., DellaPenna, D., Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7 (1995), 2139–2149.
37. + channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proc. Natl. Acad. Sci. USA 101 (2004), 12242–12247.
38. Olinares, P.D., Kim, J., van Wijk, K.J., The Clp protease system; a central component of the chloroplast protease network. Biochim. Biophys. Acta 1807 (2011), 999–1011.
39. Park, S., Rodermel, S.R., Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis. Proc. Natl. Acad. Sci. USA 101 (2004), 12765–12770.
40. Park, S., Kim, H.S., Jung, Y.J., Kim, S.H., Ji, C.Y., Wang, Z., Jeong, J.C., Lee, H.S., Lee, S.Y., Kwak, S.S., Orange protein has a role in phytoene synthase stabilization in sweet potato. Sci. Rep., 6, 2016, 33563.
41. Peltier, J.B., Ripoll, D.R., Friso, G., Rudella, A., Cai, Y., Ytterberg, J., Giacomelli, L., Pillardy, J., van Wijk, K.J., 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 (2004), 4768–4781.
42. Pulido, P., Toledo-Ortiz, G., Phillips, M.A., Wright, L.P., Rodríguez-Concepción, M., Arabidopsis J-protein J20 delivers the first enzyme of the plastidial isoprenoid pathway to protein quality control. Plant Cell 25 (2013), 4183–4194.
43. Pulido, P., Llamas, E., Llorente, B., Ventura, S., Wright, L.P., Rodríguez-Concepción, M., 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., 12, 2016, e1005824.
44. Rodríguez-Villalón, A., Gas, E., Rodríguez-Concepción, M., Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant J. 60 (2009), 424–435.
45. Rowland, E., Kim, J., Bhuiyan, N.H., van Wijk, K.J., The Arabidopsis chloroplast stromal N-terminome: complexities of amino-terminal protein maturation and stability. Plant Physiol. 169 (2015), 1881–1896.
46. Ruiz-Sola, M., Rodríguez-Concepción, M., Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book, 10, 2012, e0158.
47. Ruiz-Sola, M., Coman, D., Beck, G., Barja, M.V., Colinas, M., Graf, A., Welsch, R., Rütimann, P., Bühlmann, P., Bigler, L., et al. Arabidopsis GERANYLGERANYL DIPHOSPHATE SYNTHASE 11 is a hub isozyme required for the production of most photosynthesis-related isoprenoids. New Phytol. 209 (2016), 252–264.
48. Schledz, M., al-Babili, S., von Lintig, J., Haubruck, H., Rabbani, S., Kleinig, H., Beyer, P., Phytoene synthase from Narcissus pseudonarcissus: functional expression, galactolipid requirement, topological distribution in chromoplasts and induction during flowering. Plant J. 10 (1996), 781–792.
49. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9 (2012), 671–675.
50. Shumskaya, M., Bradbury, L.M.T., Monaco, R.R., Wurtzel, E.T., Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity. Plant Cell 24 (2012), 3725–3741.
51. Sjögren, L.L., MacDonald, T.M., Sutinen, S., Clarke, A.K., 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 (2004), 4114–4126.
52. Sjögren, L.L., Tanabe, N., Lymperopoulos, P., Khan, N.Z., Rodermel, S.R., Aronsson, H., Clarke, A.K., Quantitative analysis of the chloroplast molecular chaperone ClpC/Hsp93 in Arabidopsis reveals new insights into its localization, interaction with the Clp proteolytic core, and functional importance. J. Biol. Chem. 289 (2014), 11318–11330.
53. Stanne, T.M., Sjögren, L.L., Koussevitzky, S., Clarke, A.K., Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis. Biochem. J. 417 (2009), 257–268.
54. Sun, T., Yuan, H., Cao, H., Yazdani, M., Tadmor, Y., Li, L., Carotenoid metabolism in plants: the role of plastids. Mol. Plant, 2017, 10.1016/j.molp.2017.09.010.
55. Tapken, W., Kim, J., Nishimura, K., van Wijk, K.J., Pilon, M., The Clp protease system is required for copper ion-dependent turnover of the PAA2/HMA8 copper transporter in chloroplasts. New Phytol. 205 (2015), 511–517.
56. Toledo-Ortiz, G., Huq, E., Rodríguez-Concepción, M., Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc. Natl. Acad. Sci. USA 107 (2010), 11626–11631.
57. Toledo-Ortiz, G., Johansson, H., Lee, K.P., Bou-Torrent, J., Stewart, K., Steel, G., Rodríguez-Concepción, M., Halliday, K.J., The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet., 10, 2014, e1004416.
58. van Wijk, K.J., Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes. Annu. Rev. Plant Biol. 66 (2015), 75–111.
59. van Wijk, K.J., Peltier, J.B., Giacomelli, L., Isolation of chloroplast proteins from Arabidopsis thaliana for proteome analysis. Methods Mol. Biol. 355 (2007), 43–48.
60. Voss, I., Koelmann, M., Wojtera, J., Holtgrefe, S., Kitzmann, C., Backhausen, J.E., Scheibe, R., Knockout of major leaf ferredoxin reveals new redox-regulatory adaptations in Arabidopsis thaliana. Physiol. Plant 133 (2008), 584–598.
61. Waadt, R., Schmidt, L.K., Lohse, M., Hashimoto, K., Bock, R., Kudla, J., Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56 (2008), 505–516.
62. Wang, Y.Q., Yang, Y., Fei, Z., Yuan, H., Fish, T., Thannhauser, T.W., Mazourek, M., Kochian, L.V., Wang, X., Li, L., Proteomic analysis of chromoplasts from six crop species reveals insights into chromoplast function and development. J. Exp. Bot. 64 (2013), 949–961.
63. Waters, M.T., Moylan, E.C., Langdale, J.A., GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J. 56 (2008), 432–444.
64. Welsch, R., Beyer, P., Hugueney, P., Kleinig, H., von Lintig, J., Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211 (2000), 846–854.
65. Welsch, R., Wüst, F., Bär, C., Al-Babili, S., Beyer, P., A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol. 147 (2008), 367–380.
66. Wurtzel, E.T., Cuttriss, A., Vallabhaneni, R., Maize provitamin a carotenoids, current resources, and future metabolic engineering challenges. Front. Plant Sci., 3, 2012, 29.
67. Yang, Y., Zhang, S., Howe, K., Wilson, D.B., Moser, F., Irwin, D., Thannhauser, T.W., A comparison of nLC-ESI-MS/MS and nLC-MALDI-MS/MS for GeLC-based protein identification and iTRAQ-based shotgun quantitative proteomics. J. Biomol. Tech. 18 (2007), 226–237.
68. Yuan, H., Zhang, J., Nageswaran, D., Li, L., Carotenoid metabolism and regulation in horticultural crops. Hortic. Res., 2, 2015, 15036.
69. Yuan, H., Owsiany, K., Sheeja, T.E., Zhou, X., Rodriguez, C., Li, Y., Welsch, R., Chayut, N., Yang, Y., Thannhauser, T.W., et al. A single amino acid substitution in an ORANGE protein promotes carotenoid overaccumulation in Arabidopsis. Plant Physiol. 169 (2015), 421–431.
70. Zhang, J., Yuan, H., Yang, Y., Fish, T., Lyi, S.M., Thannhauser, T.W., Zhang, L., Li, L., Plastid ribosomal protein S5 is involved in photosynthesis, plant development, and cold stress tolerance in Arabidopsis. J. Exp. Bot. 67 (2016), 2731–2744.
71. Zheng, B., Halperin, T., Hruskova-Heidingsfeldova, O., Adam, Z., Clarke, A.K., Characterization of Chloroplast Clp proteins in Arabidopsis: localization, tissue specificity and stress responses. Physiol. Plant 114 (2002), 92–101.
72. Zhou, X., McQuinn, R., Fei, Z., Wolters, A.A., Van Eck, J., Brown, C., Giovannoni, J.J., Li, L., Regulatory control of high levels of carotenoid accumulation in potato tubers. Plant Cell Environ. 34 (2011), 1020–1030.
73. Zhou, X., Fei, Z., Thannhauser, T.W., Li, L., Transcriptome analysis of ectopic chloroplast development in green curd cauliflower (Brassica oleracea L. var. botrytis). BMC Plant Biol., 11, 2011, 169.
74. Zhou, F., Wang, C.-Y., Gutensohn, M., Jiang, L., Zhang, P., Zhang, D., Dudareva, N., Lu, S., A recruiting protein of geranylgeranyl diphosphate synthase controls metabolic flux toward chlorophyll biosynthesis in rice. Proc. Natl. Acad. Sci.USA 114 (2017), 6866–6871.
75. Zhou, X., Welsch, R., Yang, Y., Álvarez, D., Riediger, M., Yuan, H., Fish, T., Liu, J., Thannhauser, T.W., Li, L., Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc. Natl. Acad. Sci. USA 112 (2015), 3558–3563.
76. Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodríguez, V.R., Asakura, Y., Sun, Q., van Wijk, K.J., 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 (2009), 1789–1810.