The pigment binding behaviour of water-soluble chlorophyll protein (WSCP).
Journal
Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology
ISSN: 1474-9092
Titre abrégé: Photochem Photobiol Sci
Pays: England
ID NLM: 101124451
Informations de publication
Date de publication:
20 May 2020
20 May 2020
Historique:
pubmed:
28
4
2020
medline:
2
1
2021
entrez:
28
4
2020
Statut:
ppublish
Résumé
Water-soluble chlorophyll proteins (WSCPs) are homotetrameric proteins that bind four chlorophyll (Chl) molecules in identical binding sites, which makes WSCPs a good model to study protein-pigment interactions. In a previous study, we described preferential binding of Chl a or Chl b in various WSCP versions. Chl b binding is preferred when a hydrogen bond can be formed between the C7 formyl of the chlorin macrocycle and the protein, whereas Chl a is preferred when Chl b binding is sterically unfavorable. Here, we determined the binding affinities and kinetics of various WSCP versions not only for Chl a/b, but also for chlorophyllide (Chlide) a/b and pheophytin (Pheo) a/b. Altered KD values are responsible for the Chl a/b selectivity in WSCP whereas differences in the reaction kinetics are neglectable in explaining different Chl a/b preferences. WSCP binds both Chlide and Pheo with a lower affinity than Chl, which indicates the importance of the phytol chain and the central Mg2+ ion as interaction sites between WSCP and pigment. Pheophorbide (Pheoide), lacking both the phytol chain and the central Mg2+ ion, can only be bound as Pheoide b to a WSCP that has a higher affinity for Chl b than Chl a, which underlines the impact of the C7 formyl-protein interaction. Moreover, WSCP was able to bind protochlorophyllide and Mg-protoporphyrin IX, which suggests that neither the size of the π electron system of the macrocycle nor the presence of a fifth ring at the macrocycle notably affect the binding to WSCP. WSCP also binds heme to form a tetrameric complex, suggesting that heme is bound in the Chl-binding site.
Identifiants
pubmed: 32338263
doi: 10.1039/d0pp00043d
pii: 10.1039/d0pp00043d
doi:
Substances chimiques
Light-Harvesting Protein Complexes
0
Plant Proteins
0
Water
059QF0KO0R
Chlorophyll
1406-65-1
chlorophyll a'
22309-13-3
chlorophyll b
5712ZB110R
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
695-712Références
A. R. Battersby, Tetrapyrroles: the pigments of life, Nat. Prod. Rep., 2000, 17(6), 507–526.
pubmed: 11152419
N. Mochizuki, R. Tanaka, B. Grimm, T. Masuda, M. Moulin, A. G. Smith, A. Tanaka and M. J. Terry, The cell biology of tetrapyrroles: a life and death struggle, Trends Plant Sci., 2010, 15(9), 488–498.
pubmed: 20598625
R. Tanaka, K. Kobayashi and T. Masuda, Tetrapyrrole Metabolism in Arabidopsis thaliana, The arabidopsis book, 2011, vol. 9, p. e0145.
P. Brzezowski, A. S. Richter and B. Grimm, Regulation and function of tetrapyrrole biosynthesis in plants and algae, Biochim. Biophys. Acta, Bioenerg., 2015, 1847(9), 968–985.
N. Frankenberg-Dinkel and M. J. Terry, Synthesis and Role of Bilins in Photosynthetic Organisms, in Tetrapyrroles. Birth, Life and Death, ed. M. J. Warren and A. G. Smith, Springer-Verlag New York, New York, NY, 2009, pp. 208–220.
M. O. Senge, S. A. MacGowan and J. M. O’Brien, Conformational control of cofactors in nature –the influence of protein-induced macrocycle distortion on the biological function of tetrapyrroles, Chem. Commun., 2015, 51(96), 17031–17063.
R. G. L. op den Camp, D. Przybyla, C. Ochsenbein, C. Laloi, C. Kim, A. Danon, D. Wagner, E. Hideg, C. Göbel, I. Feussner, M. Nater and K. Apel, Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis, Plant Cell, 2003, 15(10), 2320–2332.
pubmed: 14508004
pmcid: 197298
L. Fiedor, M. Zbyradowski and M. Pilch, Tetrapyrrole pigments of photosynthetic antennae and reaction centers of higher plants: Structures, biophysics, functions, biochemistry, mechanisms of regulation, applications, in Metabolism, structure and function of plant tetrapyrroles. Introduction, microbial and eukaryotic chlorophyll synthesis and catabolism, ed. B. Grimm, Elsevier, 2019, vol. 90, pp. 1–33.
H. Scheer, An Overview of Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications, in Chlorophylls and Bacteriochlorophylls. Biochemistry, Biophysics, Functions and Applications, ed. B. Grimm, R. J. Porra, W. Rüdiger and H. Scheer, Springer, Dordrecht, 2006, pp. 1–26.
T. Mirkovic, E. E. Ostroumov, J. M. Anna, R. van Grondelle, Govindjee and G. D. Scholes, Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms, Chem. Rev., 2017, 117(2), 249–293.
pubmed: 27428615
A. Krieger-Liszkay, C. Fufezan and A. Trebst, Singlet oxygen production in photosystem II and related protection mechanism, Photosynth. Res., 2008, 98(1), 551–564.
pubmed: 18780159
D. M. Palm, A. Agostini, V. Averesch, P. Girr, M. Werwie, S. Takahashi, H. Satoh, E. Jaenicke and H. Paulsen, Chlorophyll a/b binding-specificity in water-soluble chlorophyll protein, Nat. Plants, 2018, 4(11), 920.
pubmed: 30297830
D. R. Ort, S. S. Merchant, J. Alric, A. Barkan, R. E. Blankenship, R. Bock, R. Croce, M. R. Hanson, J. M. Hibberd, S. P. Long, T. A. Moore, J. Moroney, K. K. Niyogi, M. A. J. Parry, P. P. Peralta-Yahya, R. C. Prince, K. E. Redding, M. H. Spalding, K. J. van Wijk, W. F. J. Vermaas, S. v. Caemmerer, A. P. M. Weber, T. O. Yeates, J. S. Yuan and X. G. Zhu, Redesigning photosynthesis to sustainably meet global food and bioenergy demand, Proc. Natl. Acad. Sci. U. S. A., 2015, 112(28), 8529–8536.
pubmed: 26124102
pmcid: 4507207
K. Schmidt, C. Fufezan, A. Krieger-Liszkay, H. Satoh and H. Paulsen, Recombinant water-soluble chlorophyll protein from Brassica oleracea var. Botrys binds various chlorophyll derivatives, Biochemistry, 2003, 42(24), 7427–7433.
pubmed: 12809498
H. Satoh, A. Uchida, K. Nakayama and M. Okada, Water-soluble chlorophyll protein in Brassicaceae plants is a stress-induced chlorophyll-binding protein, Plant Cell Physiol., 2001, 42(9), 906–911.
pubmed: 11577184
Y. Kamimura, T. Mori, T. Yamasaki and S. Katoh, Isolation, properties and a possible function of a water-soluble chlorophyll a/b-protein from brussels sprouts, Plant Cell Physiol., 1997, 38(2), 133–138.
pubmed: 9097480
I. Bektas, C. Fellenberg and H. Paulsen, Water-soluble chlorophyll protein (WSCP) of Arabidopsis is expressed in the gynoecium and developing silique, Planta, 2012, 236(1), 251–259.
pubmed: 22350767
H. Satoh, K. Nakayama and M. Okada, Molecular cloning and functional expression of a water-soluble chlorophyll protein, a putative carrier of chlorophyll molecules in cauliflower, J. Biol. Chem., 1998, 273(46), 30568–30575.
pubmed: 9804827
S. Takahashi, H. Yanai, Y. Nakamaru, A. Uchida, K. Nakayama and H. Satoh, Molecular cloning, characterization and analysis of the intracellular localization of a water-soluble Chl-binding protein from Brussels sprouts (Brassica oleracea var. gemmifera), Plant Cell Physiol., 2012, 53(5), 879–891.
pubmed: 22419824
S. Takahashi, H. Yanai, Y. Oka-Takayama, A. Zanma-Sohtome, K. Fujiyama, A. Uchida, K. Nakayama and H. Satoh, Molecular cloning, characterization and analysis of the intracellular localization of a water-soluble chlorophyll-binding protein (WSCP) from Virginia pepperweed (Lepidium virginicum), a unique WSCP that preferentially binds chlorophyll b in vitro, Planta, 2013, 238(6), 1065–1080.
pubmed: 23995835
C. E. Halls, S. W. Rogers, M. Oufattole, O. Østergard, B. Svensson and J. C. Rogers, A Kunitz-type cysteine protease inhibitor from cauliflower and Arabidopsis, Plant Sci., 2006, 170(6), 1102–1110.
E. Boex-Fontvieille, S. Rustgi, D. von Wettstein, S. Reinbothe and C. Reinbothe, Water-soluble chlorophyll protein is involved in herbivore resistance activation during greening of Arabidopsis thaliana, Proc. Natl. Acad. Sci. U. S. A., 2015, 112(23), 7303–7308.
pubmed: 26016527
pmcid: 4466707
E. Boex-Fontvieille, S. Rustgi, S. Reinbothe and C. Reinbothe, A Kunitz-type protease inhibitor regulates programmed cell death during flower development in Arabidopsis thaliana, J. Exp. Bot., 2015, 66(20), 6119–6135.
pubmed: 26160583
E. Boex-Fontvieille, S. Rustgi, D. von Wettstein, S. Pollmann, S. Reinbothe and C. Reinbothe, An Ethylene-Protected Achilles’ Heel of Etiolated Seedlings for Arthropod Deterrence, Front. Plant Sci., 2016, 7, 1246.
pubmed: 27625656
pmcid: 5003848
E. Boex-Fontvieille, S. Rustgi, D. von Wettstein, S. Pollmann, S. Reinbothe and C. Reinbothe, Jasmonic acid protects etiolated seedlings of Arabidopsis thaliana against herbivorous arthropods, Plant Signaling Behav., 2016, 11(8), e1214349.
S. Rustgi, E. Boex-Fontvieille, C. Reinbothe, D. von Wettstein and S. Reinbothe, Serpin1 and WSCP differentially regulate the activity of the cysteine protease RD21 during plant development in Arabidopsis thaliana, Proc. Natl. Acad. Sci. U. S. A., 2017, 114(9), 2212–2217.
pubmed: 28179567
pmcid: 5338515
A. Agostini, D. M. Palm, F.-J. Schmitt, M. Albertini, M. Di Valentin, H. Paulsen and D. Carbonera, An unusual role for the phytyl chains in the photoprotection of the chlorophylls bound to Water-Soluble Chlorophyll-binding Proteins, Sci. Rep., 2017, 7(1), 7504.
pubmed: 28790428
pmcid: 5548782
S. Takahashi, M. Ono, A. Uchida, K. Nakayama and H. Satoh, Molecular cloning and functional expression of a water-soluble chlorophyll-binding protein from Japanese wild radish, J. Plant Physiol., 2013, 170(4), 406–412.
pubmed: 23266282
D. Horigome, H. Satoh, N. Itoh, K. Mitsunaga, I. Oonishi, A. Nakagawa and A. Uchida, Structural mechanism and photoprotective function of water-soluble chlorophyllbinding protein, J. Biol. Chem., 2007, 282(9), 6525–6531.
pubmed: 17170107
D. Bednarczyk, O. Dym, V. Prabahar, Y. Peleg, D. H. Pike and D. Noy, Fine Tuning of Chlorophyll Spectra by Protein-Induced Ring Deformation, Angew. Chem., Int. Ed., 2016, 55(24), 6901–6905.
V. Prabahar, L. Afriat-Jurnou, I. Paluy, Y. Peleg and D. Noy, New homologues of Brassicaceae water-soluble chlorophyll proteins shed light on chlorophyll binding, spectral tuning and molecular evolution, FEBS J., 2020, 287(5), 991–1004.
pubmed: 31549491
G. N. Ramachandran, A. V. Lakshminarayanan, R. Balasubramanian and G. Tegoni, Studies on the conformation of amino acids XII. Energy calculations on prolyl residue, Biochim. Biophys. Acta, Protein Struct., 1970, 221(2), 165–181.
J. L. Hughes, R. Razeghifard, M. Logue, A. Oakley, T. Wydrzynski and E. Krausz, Magneto-optic spectroscopy of a protein tetramer binding two exciton-coupled chlorophylls, J. Am. Chem. Soc., 2006, 128(11), 3649–3658.
pubmed: 16536537
A. Agostini, D. M. Palm, H. Paulsen and D. Carbonera, Optically Detected Magnetic Resonance of Chlorophyll Triplet States in Water-Soluble Chlorophyll Proteins from Lepidium virginicum: Evidence for Excitonic Interaction among the Four Pigments, J. Phys. Chem. B, 2018, 122(23), 6156–6163.
pubmed: 29781619
D. M. Palm, A. Agostini, A.-C. Pohland, M. Werwie, E. Jaenicke and H. Paulsen, Stability of Water-Soluble Chlorophyll Protein (WSCP) Depends on Phytyl Conformation, ACS Omega, 2019, 4(5), 7971–7979.
pubmed: 31459885
pmcid: 6648419
A. Agostini, E. Meneghin, L. Gewehr, D. Pedron, D. M. Palm, D. Carbonera, H. Paulsen, E. Jaenicke and E. Collini, How water-mediated hydrogen bonds affect chlorophyll a/b selectivity in Water-Soluble Chlorophyll Protein, Sci. Rep., 2019, 9(1), 18255.
pubmed: 31796824
pmcid: 6890793
P. J. Booth and H. Paulsen, Assembly of light-harvesting chlorophyll a/b complex in vitro. Time-resolved fluorescence measurements, Biochemistry, 1996, 35(16), 5103–5108.
pubmed: 8611494
P. H. Hyninnen, Chemistry of chlorophylls: Modifications, in Chlorophylls, ed. H. Scheer, CRC Press, Boca Raton, Fla., 1991, pp. 145–209.
J. Kruk and B. Myśliwa-Kurdziel, Separation of Monovinyl and Divinyl Protochlorophyllides Using C30 Reverse Phase High Performance Liquid Chromatography Column: Analytical and Preparative Applications, Chromatographia, 2004, 60(1), 117–123.
D. M. Palm, A. Agostini, S. Tenzer, B. M. Gloeckle, M. Werwie, D. Carbonera and H. Paulsen, Water-Soluble Chlorophyll Protein (WSCP) Stably Binds Two or Four Chlorophylls, Biochemistry, 2017, 56(12), 1726–1736.
pubmed: 28252285
G. S. Collier, J. M. Pratt, C. R. de Wet and C. F. Tshabalala, Studies on haemin in dimethyl sulphoxide/water mixtures, Biochem. J., 1979, 179(2), 281–289.
pubmed: 486081
pmcid: 1186625
F. Zsila, Z. Bikádi and M. Simonyi, Probing the binding of the flavonoid, quercetin to human serum albumin by circular dichroism, electronic absorption spectroscopy and molecular modelling methods, Biochem. Pharmacol., 2003, 65(3), 447–456.
pubmed: 12527338
T. Murata, F. Toda, K. Uchino and E. Yakushiji, Water-soluble chlorophyll protein of Brassica oleracea var. Botrys (cauliflower), Biochim. Biophys. Acta, Bioenerg., 1971, 245(1), 208–215.
T. Murata and N. Murata, Water-soluble chlorophyll-proteins from Brassica nigra and Lepidium virginicum L, Carnegie Institution Year Book, 1971, 70, 504–507.
M. Helfrich and W. Rüdiger, Various Metallopheophorbides as Substrates for Chlorophyll Synthetase, Z. Naturforsch., C: J. Biosci., 1992, 47(3–4), 231–238.
C. J. Reedy, M. M. Elvekrog and B. R. Gibney, Development of a heme protein structure-electrochemical function database, Nucleic Acids Res., 2008, 36(Database issue), D307–D313.
M. C. Hsu and R. W. Woody, The origin of the heme Cotton effects in myoglobin and hemoglobin, J. Am. Chem. Soc., 1971, 93(14), 3515–3525.
pubmed: 5560471
M.-C. Hsu and R. W. Woody, Origin of the rotational strength of heme transitions of myoglobin, J. Am. Chem. Soc., 1969, 91(13), 3679–3681.
M. Nagai, Y. Nagai, Y. Aki, K. Imai, Y. Wada, S. Nagatomo and Y. Yamamoto, Effect of reversed heme orientation on circular dichroism and cooperative oxygen binding of human adult hemoglobin, Biochemistry, 2008, 47(2), 517–525.
pubmed: 18085800
R. W. Woody and G. Pescitelli, The Role of Heme Chirality in the Circular Dichroism of Heme Proteins, Z. Naturforsch., A: Phys. Sci., 2014, 69(7), 313–325.
M. Nagai, N. Mizusawa, T. Kitagawa and S. Nagatomo, A role of heme side-chains of human hemoglobin in its function revealed by circular dichroism and resonance Raman spectroscopy, Biophys. Rev., 2018, 10(2), 271–284.
pubmed: 29260461
A. Brigé, D. Leys, T. E. Meyer, M. A. Cusanovich and J. J. van Beeumen, The 1.25 A resolution structure of the diheme NapB subunit of soluble nitrate reductase reveals a novel cytochrome c fold with a stacked heme arrangement, Biochemistry, 2002, 41(15), 4827–4836.
pubmed: 11939777
A. C. K. Chan, B. Lelj-Garolla, F. I. Rosell, K. A. Pedersen, A. G. Mauk and M. E. P. Murphy, Cofacial Heme Binding is Linked to Dimerization by a Bacterial Heme Transport Protein, J. Mol. Biol., 2006, 362(5), 1108–1119.
pubmed: 16950397
N. Chim, A. Iniguez, T. Q. Nguyen and C. W. Goulding, Unusual Diheme Conformation of the Heme-Degrading Protein from Mycobacterium tuberculosis, J. Mol. Biol., 2010, 395(3), 595–608.
pubmed: 19917297
N. Shipulina, A. Smith and W. T. Morgan, Heme Binding by Hemopexin: Evidence for Multiple Modes of Binding and Functional Implications, J. Protein Chem., 2000, 19(3), 239–248.
pubmed: 10981817
Y. Sugita, M. Nagai and Y. Yoneyama, Circular Dichroism of Hemoglobin in Relation to the Structure Surrounding the Heme, J. Biol. Chem., 1971, 246(2), 383–388.
pubmed: 5542007
C. Fufezan, J. Zhang and M. R. Gunner, Ligand preference and orientation in b- and c-type heme-binding proteins, Proteins, 2008, 73(3), 690–704.
pubmed: 18491383
pmcid: 2727070
S. Takahashi, K. Aizawa, K. Nakayama and H. Satoh, Water-soluble chlorophyll-binding proteins from Arabidopsis thaliana and Raphanus sativus target the endoplasmic reticulum body, BMC Res. Notes, 2015, 8, 365.
pubmed: 26289422
pmcid: 4546050
R. T. Nakano, K. Yamada, P. Bednarek, M. Nishimura and I. Hara-Nishimura, ER bodies in plants of the Brassicales order: biogenesis and association with innate immunity, Front. Plant Sci., 2014, 5, 73.
pubmed: 24653729
pmcid: 3947992
J. Thomas and J. D. Weinstein, Measurement of heme efflux and heme content in isolated developing chloroplasts, Plant Physiol., 1990, 94(3), 1414–1423.
pubmed: 16667847
pmcid: 1077392
R. van Lis, A. Atteia, L. A. Nogaj and S. I. Beale, Subcellular localization and light-regulated expression of protoporphyrinogen IX oxidase and ferrochelatase in Chlamydomonas reinhardtii, Plant Physiol., 2005, 139(4), 1946–1958.
pubmed: 16306143
pmcid: 1310572
A. Grossman, E. Sanz-Luque, H. Yi and W. Yang, Building the GreenCut2 suite of proteins to unmask photosynthetic function and regulation, Microbiology, 2019, 165(7), 697–718.
pubmed: 31063126
S. Takahashi, T. Ogawa, K. Inoue and T. Masuda, Characterization of cytosolic tetrapyrrole -binding proteins in Arabidopsis thaliana, Photochem. Photobiol., 2008, 7(10), 1216–1224.
R. Mittler, S. Vanderauwera, N. Suzuki, G. Miller, V. B. Tognetti, K. Vandepoele, M. Gollery, V. Shulaev and F. van Breusegem, ROS signaling: the new wave?, Trends Plant Sci., 2011, 16(6), 300–309.
pubmed: 21482172
A. Baxter, R. Mittler and N. Suzuki, ROS as key players in plant stress signalling, J. Exp. Bot., 2014, 65(5), 1229–1240.
pubmed: 24253197
H. Vogel, J. Kroymann and T. Mitchell-Olds, Different transcript patterns in response to specialist and generalist herbivores in the wild Arabidopsis relative Boechera divaricarpa, PLoS One, 2007, 2(10), e1081.
W. L. Downing, F. Mauxion, M. O. Fauvarque, M. P. Reviron, D. de Vienne, N. Vartanian and J. Giraudat, A Brassica napus transcript encoding a protein related to the Künitz protease inhibitor family accumulates upon water stress in leaves, not in seeds, Plant J., 1992, 2(5), 685–693.
pubmed: 1302628
M. P. Reviron, N. Vartanian, M. Sallantin, J. C. Huet, J. C. Pernollet and D. de Vienne, Characterization of a Novel Protein Induced by Progressive or Rapid Drought and Salinity in Brassica napus Leaves, Plant Physiol., 1992, 100(3), 1486–1493.
pubmed: 16653148
pmcid: 1075810
F. Lopez, G. Vansuyt, P. Fourcroy and F. Casse-Delbart, Accumulation of a 22 kDa protein and its mRNA in the leaves of Raphanus sativus in response to salt stress or water deficit, Physiol. Plant., 1994, 91(4), 605–614.
N. Nishio and H. Satoh, A water-soluble chlorophyll protein in cauliflower may be identical to BnD22, a drought-induced, 22-kilodalton protein in rapeseed, Plant Physiol., 1997, 115(2), 841–846.
pubmed: 9342880
pmcid: 158544
G. Ilami, C. Nespoulous, J.-C. Huet, N. Vartanian and J.-C. Pernollet, Characterization of BnD22, a drought-induced protein expressed in Brassica napus leaves, Phytochemistry, 1997, 45(1), 1–8.
D. S. K. Nagahatenna, P. Langridge and R. Whitford, Tetrapyrrole-based drought stress signalling, Plant Biotechnol. J., 2015, 13(4), 447–459.
pubmed: 25756609
pmcid: 5054908
R. M. Larkin, Tetrapyrrole Signaling in Plants, Front. Plant Sci., 2016, 7, 1586.
pubmed: 27807442
pmcid: 5069423
J. E. Cornah, M. J. Terry and A. G. Smith, Green or red: what stops the traffic in the tetrapyrrole pathway?, Trends Plant Sci., 2003, 8(5), 224–230.
pubmed: 12758040
M. J. Terry and J. Bampton, The role of tetrapyrroles in chloroplast-to-nucleus retrograde signaling, in Metabolism, Structure and Function of Plant Tetrapyrroles: Control Mechanisms of Chlorophyll Biosynthesis and Analysis of Chlorophyll-Binding Proteins, Elsevier, 2019, vol. 91, pp. 225–246.
K. P. Lee, C. Kim, F. Landgraf and K. Apel, EXECUTER1-and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana, Proc. Natl. Acad. Sci. U. S. A., 2007, 104(24), 10270–10275.
pubmed: 17540731
pmcid: 1891253
F. Ramel, S. Birtic, C. Ginies, L. Soubigou-Taconnat, C. Triantaphylides and M. Havaux, Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants, Proc. Natl. Acad. Sci. U. S. A., 2012, 109(14), 5535–5540.
pubmed: 22431637
pmcid: 3325660
L. Shumbe, R. Bott and M. Havaux, Dihydroactinidiolide, a High Light-Induced β-Carotene Derivative that Can Regulate Gene Expression and Photoacclimation in Arabidopsis, Mol. Plant, 2014, 7(7), 1248–1251.
pubmed: 24646629
A. Villarejo, S. Buren, S. Larsson, A. Dejardin, M. Monne, C. Rudhe, J. Karlsson, S. Jansson, P. Lerouge, N. Rolland, G. von Heijne, M. Grebe, L. Bako and G. Samuelsson, Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast, Nat. Cell Biol., 2005, 7(12), 1224–1231.
pubmed: 16284624
R. N. Radhamony and S. M. Theg, Evidence for an ER to Golgi to chloroplast protein transport pathway, Trends Cell Biol., 2006, 16(8), 385–387.
pubmed: 16815014
P. Mehrshahi, G. Stefano, J. M. Andaloro, F. Brandizzi, J. E. Froehlich and D. DellaPenna, Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts, Proc. Natl. Acad. Sci. U. S. A., 2013, 110(29), 12126–12131.
pubmed: 23818635
pmcid: 3718160
J. Pérez-Sancho, J. Tilsner, A. L. Samuels, M. A. Botella, E. M. Bayer and A. Rosado, Stitching Organelles: Organization and Function of Specialized Membrane Contact Sites in Plants, Trends Cell Biol., 2016, 26(9), 705–717.
pubmed: 27318776
M. Laskowski and I. Kato, Protein inhibitors of proteinases, Annu. Rev. Biochem., 1980, 49, 593–626.
pubmed: 6996568