CURVATURE THYLAKOID 1 (CURT1) 家族為類囊體膜蛋白，主要位於葉綠餅邊緣。它們具有兩個跨膜 α 螺旋，胺基和羧基端皆朝向葉綠體基質，能形成寡聚體並參與植物於光照環境變化下類囊體膜塑性的調控。目前對 CURT1 的派送及寡聚合的機制所知甚少。本研究利用菸草短暫表達系統表現阿拉伯芥 CURT1 亞型 A (CURT1A)，並以三分子螢光互補技術和共免疫沉澱法證明 CURT1A 能和類囊體膜嵌膜酶 Albino 3 (Alb3) 及類囊體膜生合成相關的蛋白 VESICLE-INDUCING PROTEIN IN PLASTIDS 1 (VIPP1) 產生蛋白質交互作用。我們也製作刪除 CURT1A 胺基末端完整基質區域、部分胺基末端、第四個 α 螺旋、以及同時刪除胺基與羧基末端完整基質區域的一系列缺失突變蛋白。藉由同樣的檢測方法，我們發現 CURT1A 可能使用跨膜域 與 Alb3 產生交互作用以及使用胺基末端基質區域與 VIPP1 產生交互作用。不僅如此，CURT1A 缺失突變蛋白的自相互作用能力也顯著下降。藉由次細胞分餾法，我們也發現，除了只含跨膜域的 CURT1A 缺失突變蛋白外，其餘的缺失突變蛋白仍然可以被派送至葉綠體的膜系統。不同於 CURT1A 全長蛋白，短暫大量表現 CURT1A 缺失突變蛋白於菸草並不會改變類囊體的微細構造。綜合以上結果，我們推測 CURT1A 跨膜域包含一個必要但不足以使其被派送至類囊體膜的訊息序列。CURT1A 的胺基與羧基末端基質區域可能皆參與了其進行寡聚合的機制，進而影響類囊體膜的構造。基於三分子螢光互補技術幾乎無法探測到 CURT1A 與 chloroplast signal recognition particle 43 (cpSRP43) 的蛋白交互作用，且 CURT1A 不具有一段被 cpSRP43 辨識的 DPLG 序列，我們認為 CURT1A 不是藉由傳統的 cpSRP 途徑進行派送。

The CURVATURE THYLAKOID 1 (CURT1) family are thylakoid membrane proteins mainly located at the grana margins and contain two transmembrane helices with amino (N) and carboxyl (C) termini facing to the stroma. They can form oligomers and modulate the thylakoid plasticity under challenging light conditions. So far, little is known about the mechanisms of targeting and oligomerization of the CURT1. Using tripartite split-GFP association and co-immunoprecipitation methods, we showed that in agro-infiltrated tobacco (Nicotiana benthamiana) leaves, the transiently expressed Arabidopsis CURT1 isoform A (CURT1A) interacts with the thylakoid membrane insertase Albino 3 (Alb3) and the thylakoid biogenesis-related protein VESICLE-INDUCING PROTEIN IN PLASTIDS 1 (VIPP1). We generated a series of CURT1A mutants with deletion of the N-terminal region containing the stromal tail and helix 1, the N-terminal stromal tail, the helix 4, and both the N-and C- terminal regions. Using the same protein-protein interaction assays, we found that the transmembrane domains of CURT1A may contribute to its interaction with Alb3, the N-terminal stromal region is important for its interaction with VIPP1, and all the CURT1A deletion mutants have reduced abilities to self-interact. Sub-organelle localization analysis suggested that all CURT1A mutants, except the one containing only the two transmembrane helices, are largely targeted to the chloroplast membranes. Unlike the full-length CURT1A, overexpression of the deletion mutants does not alter the grana ultrastructure. Our results suggested that a putative signal in the transmembrane domains of CURT1A is required but insufficient for its thylakoid targeting. In addition, both the N-and C-terminal stromal regions of CURT1A may mediate its oligomerization and thus affect the thylakoid structure. Because of a merely weak interaction between CURT1A and the chloroplast signal recognition particle 43 (cpSRP43) as detected by the tripartite split-GFP association assay and the absence of a putative DPLG motif in CURT1A recognized by cpSRP43, we proposed that CURT1A is not transported by the classical cpSRP pathway.

摘要 ............................................................. i
ABSTRACT ........................................................ ii
ACKNOWLEDGEMENTS ............................................... iii
CONTENTS ........................................................ iv
1. Introduction ............................................. 1
1.1. Post-translational targeting of thylakoid membrane proteins .................................................................. 1
1.1.1. Chloroplast signal recognition particle (cpSRP) pathway .. 1
1.1.2. Spontaneous pathway ...................................... 3
1.1.3. Chloroplast vesicle transport ............................ 3
1.2. CURVATURE THYLAKOID 1A (CURT1A) .......................... 5
1.3. Aims of the study ........................................ 7
2. Results .................................................. 9
2.1. Tripartite split-GFP association and split-GFP tagging assays in the chloroplasts of agro-infiltrated tobacco (Nicotiana benthamiana) leaves .............................................. 9
2.2. Examination of the interaction of CURT1A with cpRabA5e in agro-infiltrated tobacco leaves ................................. 10
2.3. Search for a putative DPLG motif in the Arabidopsis CURT1A ................................................................. 10
2.4. Examination of the interactions of CURT1A with cpSRP43, Alb3, and VIPP1 in agro-infiltrated tobacco leaves .............. 10
2.5. Role of different structural domains of CURT1A in targeting and oligomerization of CURT1A in agro-infiltrated tobacco leaves ................................................................. 13
2.6. Examination of the interactions of truncated CURT1A variants with VIPP1 and Alb3 in agro-infiltrated tobacco leaves .......... 15
2.7. Analysis of curt1a transgenic lines expressing full-length or truncated CURT1A variants .................................... 16
3. Discussion .............................................. 17
3.1. Pathways involved in the CURT1A targeting to the thylakoids ................................................................. 17
3.2. Links between the oligomeric state of CURT1A and the structural plasticity of grana responding to environmental cues . 18
3.3. Interaction of cpSRP43 with Lhcb1 ....................... 19
3.4. Promoter selection for high expression of CURT1A suitable for co-IP and complementation analyses .......................... 20
4. Materials and Methods ................................... 21
4.1. Surface-sterilization and germination of tobacco (N. benthamiana) seed ............................................... 21
4.2. Surface-sterilization and germination of A. thaliana seed ................................................................. 21
4.3. Soil and hydroponic cultivations ........................ 22
4.4. Agrobacterium tumefaciens-mediated transient gene expression in tobacco ...................................................... 22
4.5. Arabidopsis transformation .............................. 23
4.6. Construct design for gene expression .................... 24
4.7. Bioinformatics analyses ................................. 24
4.8. Confocal microscopy and fluorescence image analyses ..... 25
4.9. Isolation of intact chloroplasts from tobacco and Arabidopsis leaves .............................................. 25
4.10. Sub-fractionation of isolated chloroplasts .............. 26
4.11. Extraction of chloroplast and shoot total proteins ...... 27
4.12. Co-IP analysis .......................................... 27
4.13. Determination of protein concentration .................. 28
4.14. SDS-PAGE and immunoblot analyses ........................ 28
4.15. Immunoblot image analyses ............................... 29
5. Figures and Tables ...................................... 30
Figure 1. Application of tripartite split-GFP association and split-GFP tagging assays in chloroplasts .............................. 30
Figure 2. Detection of S11-tagged CURT1A, cpSRP43, Alb3, VIPP1, and cpSecA by cTP-GFP1–10 in agro-infiltrated tobacco leaves ........ 31
Figure 3. Interactions of CURT1A with CURT1A, cpSRP43, Alb3, VIPP1, and cpSecA by tripartite split-GFP association assay in agro-infiltrated tobacco leaves ...................................... 32
Figure 4. Interactions of Lhcb1 with cpSRP43, Alb3, VIPP1, and cpSecA by tripartite split-GFP association assay in agro-infiltrated tobacco leaves .................................................. 33
Figure 5. Interactions of cpSRP43 with CURT1A and Lhcb1 in the chloroplasts of agro-infiltrated tobacco leaves ................. 34
Figure 6. Co-IP analysis of the CURT1A interactions in agro-infiltrated tobacco leaves ...................................... 35
Figure 7. Co-IP analysis of the Lhcb1 interactions in agro-infiltrated tobacco leaves ...................................... 36
Figure 8. Conserved structural domains in the N- and C-terminal tails of CURT1 family proteins .................................. 37
Figure 9. Comparison of schematic model and localization of truncated CURT1A variants ....................................... 38
Figure 10. Localizations of S10-tagged full-length and truncated CURT1A variants and Lhcb1 in the chloroplasts of agro-infiltrated tobacco leaves .................................................. 39
Figure 11. Detection of S10- or S11-tagged full-length and truncated CURT1A variants by split-GFP tagging assay in agro-infiltrated tobacco leaves .................................................. 40
Figure 12. Analysis of oligomerization of full-length and truncated CURT1A variants by tripartite split-GFP association assay in agro-infiltrated tobacco leaves ...................................... 41
Figure 13. Detection of S10-tagged full-length and truncated CURT1A variants and cpSecA by cTP-S11-GFP1–9 in agro-infiltrated tobacco leaves .......................................................... 42
Figure 14. Interactions of VIPP1 with full-length and truncated CURT1A variants and cpSecA by tripartite split-GFP association assay in agro-infiltrated tobacco leaves .............................. 43
Figure 15. Interactions of Alb3 with full-length and truncated CURT1A variants and cpSecA by tripartite split-GFP association assay in agro-infiltrated tobacco leaves .............................. 44
Figure S1. Principle of the tripartite split-GFP association and split-GFP tagging assays in chloroplasts ........................ 45
Figure S2. CURT1A does not interact with cpRabA5e in agro-infiltrated tobacco leaves ...................................... 46
Figure S3. Sequences alignment of Arabidopsis mature CURT1A (N63–164) and loop2-TMD3 of Lhcb1 (N173–241) ......................... 47
Figure S4. Expression of cpSRP43-3 × HA, Alb3-3 × HA, and VIPP1-3 × HA in T2 transgenic lines ....................................... 48
Figure S5. Expression of cpSRP43-3 × HA, Alb3-3 × HA, and VIPP1-3 × HA in the chloroplasts isolated from T2 transgenic lines ........ 49
Figure S6. Expression of CURT1A-3 × HA, cTP-CURT1A (N63–145)-3 × HA, cTP-CURT1A (N86–164)-3 × HA, and cTP-CURT1A (N74–164)-3 × HA in the shoots of T2 transgenic lines (curtla background) ............... 50
Figure S7. Expression of CURT1A-3 × HA in the chloroplasts isolated from T2 transgenic lines (curtla background) .................... 51
Table S1. List of the constructs used in this study ............. 52
Table S2. List of the oligonucleotides used for gene cloning .... 54
6. References .............................................. 58

Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004) Image Processing with ImageJ. Biophotonics Int. 11: 36–42.
Aldridge, C., Cain, P., and Robinson, C. (2009) Protein transport in organelles: Protein transport into and across the thylakoid membrane. FEBS J. 276: 1177–1186.
Armbruster, U., Labs, M., Pribil, M., Viola, S., Xu, W., Scharfenberg, M., Hertle, A. P., Rojahn, U., Jensen, P. E., Rappaport, F., Joliot, P., Dörmann, P., Wanner, G., and Leister, D. (2013) Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell 25: 2661–2678.
Aseeva, E., Ossenbühl, F., Eichacker, L. A., Wanner, G., Soll, J., and Vothknecht, U. C. (2004) Complex formation of Vipp1 depends on its α-helical PspA-like domain. J. Biol. Chem. 279: 35535–35541.
Bals, T., Dünschede, B., Funke, S., and Schünemann, D. (2010) Interplay between the cpSRP pathway components, the substrate LHCP and the translocase Alb3: An in vivo and in vitro study. FEBS Lett. 584: 4138–4144.
Bienvenut, W. V., Sumpton, D., Martinez, A., Lilla, S., Espagne, C., Meinnel, T., and Giglione, C. (2012) Comparative large scale characterization of plant versus mammal proteins reveals similar and idiosyncratic N-α-acetylation features. Mol. Cell Proteomics 11: M111.015131.
Bryan, S. J., Burroughs, N. J., Shevela, D., Yu, J., Rupprecht, E., Liu, L. N., Mastroianni, G., Xue, Q., Llorente-Garcia, I., Leake, M. C., Eichacker, L. A., Schneider, D., Nixon, P. J., and Mullineaux, C. W. (2014) Localisation and interactions of the Vipp1 protein in cyanobacteria. Mol. Microbiol. 94: 1179–1195.
Büchel, C. (2015) Evolution and function of light harvesting proteins. J. Plant Physiol. 172: 62–75.
Cabantous, S., Nguyen, H. B., Pedelacq, J. D., Koraichi, F., Chaudhary, A., Ganguly, K., Lockard, M.A., Favre, G., Terwilliger, T. C., and Waldo, G. S. (2013) A new protein-protein interaction sensor based on tripartite split-GFP association. Sci. Rep. 3: 2854.
Cabantous, S., Terwilliger, T. C., and Waldo, G. S. (2005) Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat. Biotechnol. 23: 102–107.
Cain, P., Holdermann, I., Sinning, I., Johnson, A. E., and Robinson, C. (2011) Binding of chloroplast signal recognition particle to a thylakoid membrane protein substrate in aqueous solution and delineation of the cpSRP43-substrate interaction domain. Biochem. J. 437: 149–155.
DeLille, J., Peterson, E. C., Johnson, T., Moore, M., Kight, A., and Henry, R. (2000) A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplasts. Proc. Natl. Acad. Sci. U.S.A. 97: 1926–1931.
Drozdetskiy, A., Cole, C., Procter, J., and Barton, G. J. (2015) JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 43: W389–394.
Dünschede, B., Bals, T., Funke, S., and Schünemann, D. (2011) Interaction studies between the chloroplast signal recognition particle subunit cpSRP43 and the full-length translocase Alb3 reveal a membrane-embedded binding region in Alb3 protein. J. Biol. Chem. 286: 35187–35195.
Falk, S., Ravaud, S., Koch, J., and Sinning, I. (2010) The C terminus of the Alb3 membrane insertase recruits cpSRP43 to the thylakoid membrane. J. Biol. Chem. 285: 5954–5962.
Fucile, G., Biase, D. D., Nahal, H., La, G., Khodabandeh, S., Chen, Y., Easley, K., Christendat, D., Kelley, L., and Provart, N. J. (2011) ePlant and the 3D data display initiative: Integrative systems biology on the world wide web. PLoS ONE 6: e15237.
Garcia, C., Khan, N. Z., Nannmark, U., and Aronsson, H. (2010) The chloroplast protein CPSAR1, dually located in the stroma and the inner envelope membrane, is involved in thylakoid biogenesis. Plant J. 63: 73–85.
Gómez, S. M., Bil’, K. Y., Rodrigo Aguilera, R., Nishio, J. N., Faull, K. F., and Whitelegge, J. P. (2003) Transit peptide cleavage sites of integral thylakoid membrane proteins. Mol. Cell Proteomics 2: 1068–1085.
Groves, M. R., Mant, A., Kuhn, A., Koch, J., Dübel, S., Robinson, C., and Sinning, I. (2001) Functional characterization of recombinant chloroplast signal recognition particle. J. Biol. Chem. 276: 27778–27786.
Gutu, A., Chang, F., and O’Shea, E. K. (2018) Dynamical localization of a thylakoid membrane binding protein is required for acquisition of photosynthetic competency. Mol. Microbiol. 108: 16–31.
Hansson, M., and Vener, A. V. (2003) Identification of three previously unknown in vivo protein phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Mol. Cell Proteomics 2: 550–559.
Heinz, S., Rast, A., Shao, L., Gutu, A., Gügel, I. L., Heyno, E., Labs, M., Rengstl, B., Viola, S., Nowaczyk, M. M., Leister, D., and Nickelsen, J. (2016) Thylakoid membrane architecture in Synechocystis depends on CurT, a homolog of the granal CURVATURE THYLAKOID1 proteins. Plant Cell 28: 2238–2260.
Henderson, R. C., Gao, F., Jayanthi, S., Kight, A., Sharma, P., Goforth, R. L., Heyes, C. D., Henry, R. L. (2016) Domain organization in the 54-kDa subunit of the chloroplast signal recognition particle. Biophys. J. 111:1151–1162.
High, S., Henry, R. Mould, R. M., Valent, Q., Meacock, S., Cline, K., Gray, J. C., and Luirink, J. (1997) Chloroplast SRP54 interacts with a specific subset of thylakoid precursor proteins. J. Biol. Chem. 272: 11622–11628.
Hoshiyasu, S., Kohzuma, K., Yoshida, K., Fujiwara, M., Fukao, Y., Yokota, A., and Akashi, K. (2013) Potential involvement of N-terminal acetylation in the quantitative regulation of the ɛ subunit of chloroplast ATP synthase under drought stress. Biosci. Biotechnol. Biochem. 77: 998–1007.
Hurlock, A. K., Roston, R. L., Wang, K., and Benning, C. (2014) Lipid trafficking in plant cells. Traffic 15: 915–932.
Ingelsson, B., and Vener, A. V. (2012) Phosphoproteomics of Arabidopsis chloroplasts reveals involvement of the STN7 kinase in phosphorylation of nucleoid protein pTAC16. FEBS Lett. 586: 1265–1271.
Jarsch, I. K., Daste, F., and Gallop, J. L. (2016) Membrane curvature in cell biology: An integration of molecular mechanisms. J. Cell Biol. 214: 375–387.
Jarvis, P. (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179: 257–285.
Junglas, B., and Schneider, D. (2018) What is Vipp1 good for? Mol. Microbiol. 108: 1–5.
Kley, J., Heil, M., Muck, A., Svatoš, A., and Boland, W. (2010) Isolating intact chloroplasts from small Arabidopsis samples for proteomic studies. Anal. Biochem. 398: 198–202.
Klinkenberg, J. (2014) Extraction of chloroplast proteins from transiently transformed Nicotiana benthamiana leaves. Bio-protocol 4: e1238.
Klinkenberg, J., Faist, H., Saupe, S., Lambertz, S., Krischke, M., Stingl, N., Fekete, A., Mueller, M. J., Feussner, I., Hedrich, R., and Deeken, R. (2014) Two fatty acid desaturases, STEAROYL-ACYL CARRIER PROTEIN Δ9-DESATURASE6 and FATTY ACID DESATURASE3, are involved in drought and hypoxia stress signaling in Arabidopsis crown galls. Plant Physiol. 164: 570–583.
Karim, S., Alezzawi, M., Garcia-Petit, C., Solymosi, K., Khan, N. Z., Lindquist, E., Dahl, P., Hohmann, S., and Aronsson, H. (2014) A novel chloroplast localized Rab GTPase protein CPRabA5e is involved in stress, development, thylakoid biogenesis and vesicle transport in Arabidopsis. Plant Mol. Biol. 84: 675–692.
Katoh, K., and Standley, D. M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772–780.
Khan, N. Z., Lindquist, E., and Aronsson, H. (2013) New putative chloroplast vesicle transport components and cargo proteins revealed using a bioinformatics approach: an Arabidopsis model. PLoS ONE 8: e59898.
Köhler, R. H., Cao, J., Zipfel, W. R., Webb, W. W., and Hanson, M. R. (1997) Exchange of protein molecules through connections between higher plant plastids. Science 276: 2039–2042.
Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305: 567–580.
Króliczewski, J., Bartoszewski, R., and Króliczewska, B. (2017) Chloroplast PetD protein: evidence for SRP/Alb3-dependent insertion into the thylakoid membrane. BMC Plant Biol. 17: 1–15.
Lehtimäki, N., Koskela, M. M., Dahlström, K. M., Pakula, E., Lintala, M., Scholz, M., Hippler, M., Hanke, G. T., Rokka, A., Battchikova, N., Salminen, T. A., and Mulo, P. (2014) Posttranslational modifications of FERREDOXIN-NADP+ OXIDOREDUCTASE in Arabidopsis chloroplasts. Plant Physiol. 166: 1764–1776.
Lehtimäki, N., Koskela, M. M., and Mulo, P. (2015) Posttranslational modifications of chloroplast proteins: An emerging field. Plant Physiol. 168: 768–775.
Leister, D. (2003) Chloroplast research in the genomic age. Trends Genet. 19: 47–56.
Lewis, N. E., Marty, N. J., Kathir, K. M., Rajalingam, D., Kight, A. D., Daily, A., Kumar, T. K. S., Henry, R. L., and Goforth, R. L. (2010) A dynamic cpSRP43-Albino3 interaction mediates translocase regulation of chloroplast signal recognition particle (cpSRP)-targeting components. J. Biol. Chem. 285: 34220–34230.
Liang, F. C., Kroon, G., McAvoy, C. Z., Chi, C., Wright, P. E., and Shan, S. O. (2016) Conformational dynamics of a membrane protein chaperone enables spatially regulated substrate capture and release. Proc. Natl. Acad. Sci. U.S.A. 113: E1615–E1624.
Li, H. M., and Chiu, C. C. (2010) Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61: 157–180.
Lindquist, E., Alezzawi, M., and Aronsson, H. (2014) Bioinformatic indications that COPI- and clathrin-based transport systems are not present in chloroplasts: an Arabidopsis model. PLoS ONE 9: e104423.
Lindquist, E., and Aronsson, H. (2018) Chloroplast vesicle transport. Photosyn. Res. 138: 361–371.
Liu, T. Y., Chou, W. H., Chen, W. Y., Chu, C. Y., Dai, C. Y., and Wu, P. Y. (2018) Detection of membrane protein–protein interaction in planta based on dual-intein-coupled tripartite split-GFP association. Plant J. 94: 426–438.
Michl, D., Robinson, C., Shackleton, J. B., Herrmann, R. G., and Klösgen, R. B. (1994) Targeting of proteins to the thylakoids by bipartite presequences: CFoII is imported by a novel, third pathway. EMBO J. 13: 1310–1317.
Millner, P. D., and Kitt, D. G. (1992) The Beltsville method for soilless production of vesicular-arbuscular mycorrhizal fungi. Mycorrhiza 2: 9–15.
Mól, A. R., Castro, M. S., and Fontes, W. (2018) NetWheels: A web application to create high quality peptide helical wheel and net projections. bioRxiv 416347.
Moore, M., Harrison, M. S., Peterson, E. C., Henry, R. (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J. Biol. Chem. 275: 1529–1532.
Morré, D. J., Selldén, G., Sundqvist, C., and Sandelius, A. S. (1991) Stromal low temperature compartment derived from the inner membrane of the chloroplast envelope. Plant Physiol. 97: 1558–1564.
Murashige, T., and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15: 473–497.
Mustárdy, L., and Garab, G. (2003) Granum revisited. A three-dimensional model – where things fall into place. Trends Plant Sci. 8: 117–122.
Pribil, M., Labs, M., and Leister, D. (2014) Structure and dynamics of thylakoids in land plants. J. Exp. Bot. 65: 1955–1972.
Pribil, M., Sandoval-Ibáñez, O., Xu, W., Sharma, A., Labs, M., Liu, Q., Galgenmüller, C., Schneider, T., Wessels, M., Matsubara, S., Jansson, S., Wanner, G., and Leister, D. (2018) Fine-tuning of photosynthesis requires CURVATURE THYLAKOID1-mediated thylakoid plasticity. Plant Physiol. 176: 2351–2364.
Rantala, M., Rantala, S., and Aro, E. M. (2020) Composition, phosphorylation and dynamic organization of photosynthetic protein complexes in plant thylakoid membrane. Photochem. Photobiol. Sci. 19: 604–619.
Richter, C. V., Bals, T., and Schünemann, D. (2010) Component interactions, regulation and mechanisms of chloroplast signal recognition particle-dependent protein transport. Eur. J. Cell Biol. 89: 965–973.
Rochaix, J. D. (2014) Regulation and dynamics of the light-harvesting system. Annu. Rev. Plant Biol. 65: 287–309.
Schlücking, K., Edel, K. H., Drerup, M. M., Köster, P., Eckert, C., Steinhorst, L., Waadt, R., Batistič, O., and Kudla, J. (2013) A new β-estradiol-inducible vector set that facilitates easy construction and efficient expression of transgenes reveals CBL3-dependent cytoplasm to tonoplast translocation of CIPK5. Mol. Plant 6: 1814–1829.
Shimoni, E., Rav-Hon, O., Ohad, I., Brumfeld, V., and Reich, Z. (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17: 2580–2586.
Stengel, K. F., Holdermann, I., Cain, P., Robinson, C., Wild, K., and Sinning, I. (2008) Structural basis for specific substrate recognition by the chloroplast signal recognition particle protein cpSRP43. Science 321: 253–256.
Stenmark, H. (2009) Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10: 513–525.
Trotta, A., Bajwa, A. A., Mancini, I., Paakkarinen, V., Pribil, M., and Aro, E. M. (2019) The role of phosphorylation dynamics of CURVATURE THYLAKOID 1B in plant thylakoid membranes. Plant Physiol. 181: 1615–1631.
Tu, C. J., Peterson, E.C., Henry, R., and Hoffman, N. E. (2000) The L18 domain of light-harvesting chlorophyll proteins binds to chloroplast signal recognition particle 43. J. Biol. Chem. 275: 13187–13190.
Vener, A. V., Harms, A., Sussman, M. R., and Vierstra, R. D. (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J. Biol. Chem. 276: 6959–6966.
Vothknecht, U. C., Otters, S., Hennig, R., and Schneider, D. (2012) Vipp1: a very important protein in plastids?! J. Exp. Bot. 63: 1699–1712.
Walter, B., Hristou, A., Nowaczyk, M. M., and Schünemann, D. (2015) In vitro reconstitution of co-translational D1 insertion reveals a role of the cpSec–Alb3 translocase and Vipp1 in photosystem II biogenesis. Biochem. J. 468: 315–324.
Xing, S., Wallmeroth, N., Berendzen, K.W., and Grefen, C. (2016) Techniques for the analysis of protein–protein interactions in vivo. Plant Physiol. 171: 727–758.
Yuan, J., Henry, R., McCaffery, M., and Cline, K. (1994) SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting. Science 266: 796–798.
Zhang, L., and Sakamoto, W. (2015) Possible function of VIPP1 in maintaining chloroplast membranes. Biochim. Biophys. Acta Bioenerg. 1847: 831–837.
Zhang, X. P., and Glaser, E. (2002) Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci. 7: 14–21.
Ziehe, D., Dünschede, B., and Schünemann, D. (2018) Molecular mechanism of SRP-dependent light-harvesting protein transport to the thylakoid membrane in plants. Photosyn. Res. 138: 303–313.