Plastoglobuli (PGs) are plastid lipoprotein particles surrounded by a membrane lipid monolayer. PGs contain small specialized proteomes and metabolomes. They are present in different plastid types (e.g., chloroplasts, chromoplasts, and elaioplasts) and are dynamic in size and shape in response to abiotic stress or developmental transitions. PGs in chromoplasts are highly enriched in carotenoid esters and enzymes involved in carotenoid metabolism. PGs in chloroplasts are associated with thylakoids and contain ∼30 core proteins (including six ABC1 kinases) as well as additional proteins recruited under specific conditions. Systems analysis has suggested that chloroplast PGs function in metabolism of prenyl lipids (e.g., tocopherols, plastoquinone, and phylloquinone); redox and photosynthetic regulation; plastid biogenesis; and senescence, including recycling of phytol, remobilization of thylakoid lipids, and metabolism of jasmonate. These functionalities contribute to chloroplast PGs’ role in responses to stresses such as high light and nitrogen starvation. PGs are thus lipid microcompartments with multiple functions integrated into plastid metabolism, developmental transitions, and environmental adaptation. This review provides an in-depth overview of PG experimental observations, summarizes the present understanding of PG features and functions, and provides a conceptual framework for PG research and the realization of opportunities for crop improvement.


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Literature Cited

  1. Ahrazem O, Rubio-Moraga A, Nebauer SG, Molina RV, Gómez-Gómez L. 1.  2015. Saffron: its phytochemistry, developmental processes, and biotechnological prospects. J. Agric. Food Chem. 63:8751–64 [Google Scholar]
  2. Ariizumi T, Kishimoto S, Kakami R, Maoka T, Hirakawa H. 2.  et al. 2014. Identification of the carotenoid modifying gene PALE YELLOW PETAL 1 as an essential factor in xanthophyll esterification and yellow flower pigmentation in tomato (Solanum lycopersicum). Plant J. 79:453–65 [Google Scholar]
  3. Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D. 3.  2009. A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21:2036–44 [Google Scholar]
  4. Austin JR II, Frost E, Vidi PA, Kessler F, Staehelin LA. 4.  2006. Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–703 [Google Scholar]
  5. Avendaño-Vázquez AO, Cordoba E, Llamas E, San Román C, Nisar N. 5.  et al. 2014. An uncharacterized apocarotenoid-derived signal generated in ζ-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis. Plant Cell 26:2524–37 [Google Scholar]
  6. Avila-Ospina L, Moison M, Yoshimoto K, Masclaux-Daubresse C. 6.  2014. Autophagy, plant senescence, and nutrient recycling. J. Exp. Bot. 65:3799–811 [Google Scholar]
  7. Babiychuk E, Bouvier-Nave P, Compagnon V, Suzuki M, Muranaka T. 7.  et al. 2008. Allelic mutant series reveal distinct functions for Arabidopsis cycloartenol synthase 1 in cell viability and plastid biogenesis. PNAS 105:3163–68 [Google Scholar]
  8. Bailey JL, Whyborn AG. 8.  1963. The osmophilic globules of chloroplasts. II. Globules of the spinach-beet chloroplast. Biochem. Biophys. Acta 78:163–74 [Google Scholar]
  9. Bayer RG, Stael S, Rocha AG, Mair A, Vothknecht UC, Teige M. 9.  2012. Chloroplast-localized protein kinases: a step forward towards a complete inventory. J. Exp. Bot. 63:1713–23 [Google Scholar]
  10. Besagni C, Kessler F. 10.  2013. A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation. Planta 237:463–70 [Google Scholar]
  11. Bhuiyan NH, Friso G, Rowland E, Majsec K, van Wijk KJ. 11.  2016. The plastoglobule-localized metallopeptidase PGM48 is a positive regulator of senescence in Arabidopsis thaliana. Plant Cell 283020–37 [Google Scholar]
  12. Blomqvist LA, Ryberg M, Sundqvist C. 12.  2008. Proteomic analysis of highly purified prolamellar bodies reveals their significance in chloroplast development. Photosynth. Res. 96:37–50 [Google Scholar]
  13. Boca S, Koestler F, Ksas B, Chevalier A, Leymarie J. 13.  et al. 2014. Arabidopsis lipocalins AtCHL and AtTIL have distinct but overlapping functions essential for lipid protection and seed longevity. Plant Cell Environ 37:368–81 [Google Scholar]
  14. Boyd JS, Mittelmeier TM, Lamb MR, Dieckmann CL. 14.  2011. Thioredoxin-family protein EYE2 and Ser/Thr kinase EYE3 play interdependent roles in eyespot assembly. Mol. Biol. Cell 22:1421–29 [Google Scholar]
  15. Bréhélin C, Kessler F, van Wijk KJ. 15.  2007. Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–66 [Google Scholar]
  16. Bugos RC, Hieber AD, Yamamoto HY. 16.  1998. Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. J. Biol. Chem. 273:15321–24 [Google Scholar]
  17. Camara B, Hugueney P, Bouvier F, Kuntz M, Moneger R. 17.  1995. Biochemistry and molecular biology of chromoplast development. Int. Rev. Cytol. 163:175–247 [Google Scholar]
  18. Cardazzo B, Hamel P, Sakamoto W, Wintz H, Dujardin G. 18.  1998. Isolation of an Arabidopsis thaliana cDNA by complementation of a yeast abc1 deletion mutant deficient in complex III respiratory activity. Gene 221:117–25 [Google Scholar]
  19. Carrie C, Murcha MW, Kuehn K, Duncan O, Barthet M. 19.  et al. 2008. Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett 582:3073–79 [Google Scholar]
  20. Charron JB, Ouellet F, Pelletier M, Danyluk J, Chauve C, Sarhan F. 20.  2005. Identification, expression, and evolutionary analyses of plant lipocalins. Plant Physiol 139:2017–28 [Google Scholar]
  21. Collins MD, Jones D. 21.  1981. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol. Rev. 45:316–54 [Google Scholar]
  22. Cunningham FX Jr., Tice AB, Pham C, Gantt E. 22.  2010. Inactivation of genes encoding plastoglobulin-like proteins in Synechocystis sp. PCC 6803 leads to a light-sensitive phenotype. J. Bacteriol. 192:1700–9 [Google Scholar]
  23. Davidi L, Levin Y, Ben-Dor S, Pick U. 23.  2015. Proteome analysis of cytoplasmatic and plastidic β-carotene lipid droplets in Dunaliella bardawil. Plant Physiol 167:60–79 [Google Scholar]
  24. Davidi L, Shimoni E, Khozin-Goldberg I, Zamir A, Pick U. 24.  2014. Origin of β-carotene-rich plastoglobuli in Dunaliella bardawil. Plant Physiol 164:2139–56 [Google Scholar]
  25. Deruere J, Bouvier F, Steppuhn J, Klein A, Camara B, Kuntz M. 25.  1994. Structure and expression of two plant genes encoding chromoplast-specific proteins: occurrence of partially spliced transcripts. Biochem. Biophys. Res. Commun. 199:1144–50 erratum Biochem. Biophys. Res. Commun. 201:486 [Google Scholar]
  26. Deruere J, Römer S, d'Harlingue A, Backhaus RA, Kuntz M, Camara B. 26.  1994. Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell 6:119–33 [Google Scholar]
  27. Do TQ, Hsu AY, Jonassen T, Lee PT, Clarke CF. 27.  2001. A defect in coenzyme Q biosynthesis is responsible for the respiratory deficiency in Saccharomyces cerevisiae abc1 mutants. J. Biol. Chem. 276:18161–68 [Google Scholar]
  28. Du ZY, Benning C. 28.  2016. Triacylglycerol accumulation in photosynthetic cells in plants and algae. Subcell. Biochem. 86:179–205 [Google Scholar]
  29. Egea I, Barsan C, Bian W, Purgatto E, Latche A. 29.  et al. 2010. Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51:1601–11 [Google Scholar]
  30. Eitzinger N, Wagner V, Weisheit W, Geimer S, Boness D. 30.  et al. 2015. Proteomic analysis of a fraction with intact eyespots of Chlamydomonas reinhardtii and assignment of protein methylation. Front. Plant Sci. 6:1085 [Google Scholar]
  31. Elhafez D, Murcha MW, Clifton R, Soole KL, Day DA, Whelan J. 31.  2006. Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant Cell Physiol 47:43–54 [Google Scholar]
  32. Engel BD, Schaffer M, Kuhn Cuellar L, Villa E, Plitzko JM, Baumeister W. 32.  2015. Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. eLife 4:e04889 [Google Scholar]
  33. Eugeni-Piller L, Besagni C, Ksas B, Rumeau D, Bréhélin C. 33.  et al. 2011. Chloroplast lipid droplet type II NAD(P)H quinone oxidoreductase is essential for prenylquinone metabolism and vitamin K1 accumulation. PNAS 108:14354–59 [Google Scholar]
  34. Eymery F, Rey P. 34.  1999. Immunocytolocalization of CDSP32 and CDSP34, two chloroplastic drought-induced stress proteins in Solanum tuberosum plants. Plant Physiol. Biochem. 37:305–12 [Google Scholar]
  35. Fatihi A, Latimer S, Schmollinger S, Block A, Dussault PH. 35.  et al. 2015. A dedicated type II NADPH dehydrogenase performs the penultimate step in the biosynthesis of vitamin K1 in Synechocystis and Arabidopsis. Plant Cell 27:1730–41 [Google Scholar]
  36. Frusciante S, Diretto G, Bruno M, Ferrante P, Pietrella M. 36.  et al. 2014. Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. PNAS 111:12246–51 [Google Scholar]
  37. Gámez-Arjona FM, de la Concepcíon JC, Raynaud S, Mérida A. 37.  2014. Arabidopsis thaliana plastoglobule-associated fibrillin 1a interacts with fibrillin 1b in vivo. FEBS Lett 588:2800–4 [Google Scholar]
  38. Gámez-Arjona FM, Raynaud S, Ragel P, Mérida A. 38.  2014. Starch synthase 4 is located in the thylakoid membrane and interacts with plastoglobule-associated proteins in Arabidopsis. Plant J. 80:305–16 [Google Scholar]
  39. Gaude N, Bréhélin C, Tischendorf G, Kessler F, Dörmann P. 39.  2007. Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. Plant J. 49:729–39 [Google Scholar]
  40. Ghosh S, Hudak KA, Dumbroff EB, Thompson JE. 40.  1994. Release of photosynthetic protein catabolites by blebbing from thylakoids. Plant Physiol 106:1547–53 [Google Scholar]
  41. 41.  Deleted in proof
  42. Gonzalez-Jorge S, Ha SH, Magallanes-Lundback M, Gilliland LU, Zhou A. 42.  et al. 2013. CAROTENOID CLEAVAGE DIOXYGENASE4 is a negative regulator of β-carotene content in Arabidopsis seeds. Plant Cell 25:4812–26 [Google Scholar]
  43. González-Mariscal I, García-Testón E, Padilla S, Martín-Montalvo A, Pomares-Viciana T. 43.  et al. 2014. Regulation of coenzyme Q biosynthesis in yeast: a new complex in the block. IUBMB Life 66:63–70 [Google Scholar]
  44. Greenwood AD, Leech RM, Williams JP. 44.  1963. The osmiophilic globules of chloroplasts: I. Osmiophilic globules as a normal component of chloroplasts and their isolation and composition in Vicia faba L. Biochim. Biophys. Acta 78:148–62 [Google Scholar]
  45. Guiamet JJ, Pichersky E, Nooden LD. 45.  1999. Mass exodus from senescing soybean chloroplasts. Plant Cell Physiol 40:986–92 [Google Scholar]
  46. Hadjeb N, Gounaris I, Price CA. 46.  1988. Chromoplast-specific proteins in Capsicum annuum. Plant Physiol 88:42–45 [Google Scholar]
  47. Hallin EI, Hasan M, Guo K, Akerlund HE. 47.  2016. Molecular studies on structural changes and oligomerisation of violaxanthin de-epoxidase associated with the pH-dependent activation. Photosynth. Res. 129:29–41 [Google Scholar]
  48. Hansmann P, Stitte P. 48.  1982. Composition and molecular structure of chromoplast globules of Viola tricolor. Plant Cell Rep 1:111–14 [Google Scholar]
  49. He CH, Xie LX, Allan CM, Tran UC, Clarke CF. 49.  2014. Coenzyme Q supplementation or over-expression of the yeast Coq8 putative kinase stabilizes multi-subunit Coq polypeptide complexes in yeast coq null mutants. Biochim. Biophys. Acta 1841:630–44 [Google Scholar]
  50. Hernández-Pinzón I, Ross JH, Barnes KA, Damant AP, Murphy DJ. 50.  1999. Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus. Planta 208:588–98 [Google Scholar]
  51. Hortensteiner S.51.  2009. Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–62 [Google Scholar]
  52. Hortensteiner S.52.  2013. Update on the biochemistry of chlorophyll breakdown. Plant Mol. Biol. 82:505–17 [Google Scholar]
  53. Hortensteiner S, Krautler B. 53.  2011. Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 1807:977–88 [Google Scholar]
  54. Huang FC, Molnár P, Schwab W. 54.  2009. Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J. Exp. Bot. 60:3011–22 [Google Scholar]
  55. Huang H, Yang M, Su Y, Qu L, Deng XW. 55.  2015. Arabidopsis atypical kinases ABC1K1 and ABC1K3 act oppositely to cope with photodamage under red light. Mol. Plant 8:1122–24 [Google Scholar]
  56. Huang M, Friso G, Nishimura K, Qu X, Olinares PD. 56.  et al. 2013. Construction of plastid reference proteomes for maize and Arabidopsis and evaluation of their orthologous relationships; the concept of orthoproteomics. J. Proteome Res. 12:491–504 [Google Scholar]
  57. Ishida H, Izumi M, Wada S, Makino A. 57.  2014. Roles of autophagy in chloroplast recycling. Biochim. Biophys. Acta 1837:512–21 [Google Scholar]
  58. Izumi M, Hidema J, Ishida H. 58.  2015. From Arabidopsis to cereal crops: conservation of chloroplast protein degradation by autophagy indicates its fundamental role in plant productivity. Plant Signal. Behav. 10:e1101199 [Google Scholar]
  59. Jasinski M, Sudre D, Schansker G, Schellenberg M, Constant S. 59.  et al. 2008. AtOSA1, a member of the Abc1-like family, as a new factor in cadmium and oxidative stress response. Plant Physiol 147:719–31 [Google Scholar]
  60. Kahlau S, Bock R. 60.  2008. Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20:856–74 [Google Scholar]
  61. Karpowicz SJ, Prochnik SE, Grossman AR, Merchant SS. 61.  2011. The GreenCut2 resource, a phylogenomically derived inventory of proteins specific to the plant lineage. J. Biol. Chem. 286:21427–39 [Google Scholar]
  62. Katz A, Jimenez C, Pick U. 62.  1995. Isolation and characterization of a protein associated with carotene globules in the alga Dunaliella bardawil. Plant Physiol 108:1657–64 [Google Scholar]
  63. Kaup MT, Froese CD, Thompson J. 63.  2002. A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol. 129:1616–26 [Google Scholar]
  64. Kelly AA, Feussner I. 64.  2016. Oil is on the agenda: lipid turnover in higher plants. Biochim. Biophys. Acta 1861:1253–68 [Google Scholar]
  65. Kessler F, Schnell D, Blobel G. 65.  1999. Identification of proteins associated with plastoglobules isolated from pea (Pisum sativum L.) chloroplasts. Planta 208:107–13 [Google Scholar]
  66. Kim EH, Lee Y, Kim HU. 66.  2015. Fibrillin 5 is essential for plastoquinone-9 biosynthesis by binding to solanesyl diphosphate synthases in Arabidopsis. Plant Cell 27:2956–71 [Google Scholar]
  67. Kim HU, Wu SS, Ratnayake C, Huang AH. 67.  2001. Brassica rapa has three genes that encode proteins associated with different neutral lipids in plastids of specific tissues. Plant Physiol 126:330–41 [Google Scholar]
  68. Kobayashi N, DellaPenna D. 68.  2008. Tocopherol metabolism, oxidation and recycling under high light stress in Arabidopsis. Plant J. 55:607–18 [Google Scholar]
  69. Kreimer G.69.  2009. The green algal eyespot apparatus: a primordial visual system and more?. Curr. Genet. 55:19–43 [Google Scholar]
  70. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S. 70.  et al. 2001. VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. PNAS 98:4238–42 [Google Scholar]
  71. Kruk J, Jemiola-Rzeminska M, Burda K, Schmid GH, Strzalka K. 71.  2003. Scavenging of superoxide generated in photosystem I by plastoquinol and other prenyllipids in thylakoid membranes. Biochemistry 42:8501–5 [Google Scholar]
  72. Kruk J, Szymańska R, Nowicka B, Dluzewska J. 72.  2016. Function of isoprenoid quinones and chromanols during oxidative stress in plants. New Biotechnol 33:636–43 [Google Scholar]
  73. Ksas B, Becuwe N, Chevalier A, Havaux M. 73.  2015. Plant tolerance to excess light energy and photooxidative damage relies on plastoquinone biosynthesis. Sci. Rep. 5:10919 [Google Scholar]
  74. Kusaba M, Tanaka A, Tanaka R. 74.  2013. Stay-green plants: What do they tell us about the molecular mechanism of leaf senescence?. Photosynth. Res. 117:221–34 [Google Scholar]
  75. Laizet Y, Pontier D, March R, Kuntz M. 75.  2004. Subfamily organization and phylogenetic origin of genes encoding plastid-lipid-associated proteins of the fibrillin type. J. Genome Sci. Technol. 3:19–28 [Google Scholar]
  76. Langenkämper G, Manac'h N, Broin M, Cuiné S, Becuwe N. 76.  et al. 2001. Accumulation of plastid lipid-associated proteins (fibrillin/CDSP34) upon oxidative stress, ageing and biotic stress in Solanaceae and in response to drought in other species. J. Exp. Bot. 52:1545–54 [Google Scholar]
  77. Leitner-Dagan Y, Ovadis M, Shklarman E, Elad Y, Rav David D, Vainstein A. 77.  2006. Expression and functional analyses of the plastid lipid-associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol 142:233–44 [Google Scholar]
  78. Levesque-Tremblay G, Havaux M, Ouellet F. 78.  2009. The chloroplastic lipocalin AtCHL prevents lipid peroxidation and protects Arabidopsis against oxidative stress. Plant J. 60:691–702 [Google Scholar]
  79. Li T, Jiang J, Zhang S, Shu H, Wang Y. 79.  et al. 2015. OsAGSW1, an ABC1-like kinase gene, is involved in the regulation of grain size and weight in rice. J. Exp. Bot. 66:5691–701 [Google Scholar]
  80. Lichtenthaler HK.80.  1968. Plastoglobuli and the fine structure of plastids. Endeavor 27:144–49 [Google Scholar]
  81. Lichtenthaler HK.81.  1970. Die Lokalisation der Plastidenchinone und Carotinoide in den Chromoplasten der Petalen von Sarothamnus scoparius (L.) Wimm ex Koch [The localization of plastid quinones and carotenoids in the chromoplasts of petals from Sarothamnus scoparius (L.) Wimm ex Koch]. Planta 90:142–52 [Google Scholar]
  82. Lichtenthaler LK.82.  2012. Plastoglobuli, thylakoids, chloroplast structure and development of plastids. Plastid Development in Leaves During Growth and Senescence KKB Biswal, UC Biswal 337–61 Adv. Photosynth. Respir. 36 Berlin: Springer [Google Scholar]
  83. Lippold F, vom Dorp K, Abraham M, Hölzl G, Wewer V. 83.  et al. 2012. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell 24:2001–14 [Google Scholar]
  84. Liu L.84.  2013. Ultrastructural study on dynamics of lipid bodies and plastids during ripening of chili pepper fruits. Micron 46:43–50 [Google Scholar]
  85. Liu L.85.  2016. Ultramicroscopy reveals that senescence induces in-situ and vacuolar degradation of plastoglobules in aging watermelon leaves. Micron 80:135–44 [Google Scholar]
  86. Liu L, Shao Z, Zhang M, Wang Q. 86.  2015. Regulation of carotenoid metabolism in tomato. Mol. Plant 8:28–39 [Google Scholar]
  87. Lohmann A, Schottler MA, Bréhélin C, Kessler F, Bock R. 87.  et al. 2006. Deficiency in phylloquinone (vitamin K1) methylation affects prenyl quinone distribution, photosystem I abundance, and anthocyanin accumulation in the Arabidopsis AtmenG mutant. J. Biol. Chem. 281:40461–72 [Google Scholar]
  88. Lohscheider JN, Friso G, van Wijk KJ. 88.  2016. Phosphorylation of plastoglobular proteins in Arabidopsis thaliana. J. Exp. Bot. 67:3975–84 [Google Scholar]
  89. Lundquist PK, Davis JI, van Wijk KJ. 89.  2012. ABC1K atypical kinases in plants: filling the organellar kinase void. Trends Plant Sci 17:546–55 [Google Scholar]
  90. Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ. 90.  2012. The functional network of the Arabidopsis thaliana plastoglobule proteome based on quantitative proteomics and genome-wide co-expression analysis. Plant Physiol 58:1172–92 [Google Scholar]
  91. Lundquist PK, Poliakov A, Giacomelli L, Friso G, Appel M. 91.  et al. 2013. Loss of plastoglobule-localized kinases ABC1K1 and ABC1K3 leads to a conditional degreening phenotype, a modified prenyl-lipid composition and recruitment of JA biosynthesis. Plant Cell 25:1818–39 [Google Scholar]
  92. Manara A, Dalcorso G, Furini A. 92.  2016. The role of the atypical kinases ABC1K7 and ABC1K8 in abscisic acid responses. Front. Plant Sci. 7:366 [Google Scholar]
  93. Manara A, Dalcorso G, Leister D, Jahns P, Baldan B, Furini A. 93.  2014. AtSIA1 and AtOSA1: two Abc1 proteins involved in oxidative stress responses and iron distribution within chloroplasts. New Phytol 201:452–65 [Google Scholar]
  94. Martín-Montalvo A, González-Mariscal I, Pomares-Viciana T, Padilla-López S, Ballesteros M. 94.  et al. 2013. The phosphatase Ptc7 induces coenzyme Q biosynthesis by activating the hydroxylase Coq7 in yeast. J. Biol. Chem. 288:28126–37 [Google Scholar]
  95. Martinis J, Glauser G, Valimareanu S, Kessler F. 95.  2013. A chloroplast ABC1-like kinase regulates vitamin E metabolism in Arabidopsis. Plant Physiol 162:652–62 [Google Scholar]
  96. Martinis J, Glauser G, Valimareanu S, Stettler M, Zeeman SC. 96.  et al. 2013. ABC1K1/PGR6 kinase: a regulatory link between photosynthetic activity and chloroplast metabolism. Plant J. 77:269–83 [Google Scholar]
  97. Martinis J, Kessler F, Glauser G. 97.  2011. A novel method for prenylquinone profiling in plant tissues by ultra-high pressure liquid chromatography-mass spectrometry. Plant Methods 7:23 [Google Scholar]
  98. Mehrshahi P, Stefano G, Andaloro JM, Brandizzi F, Froehlich JE, DellaPenna D. 98.  2013. Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts. PNAS 110:12126–31 [Google Scholar]
  99. Mene-Saffrane L, Jones AD, DellaPenna D. 99.  2010. Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. PNAS 107:17815–20 [Google Scholar]
  100. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ. 100.  et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–50 [Google Scholar]
  101. Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson U. 101.  et al. 2003. Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol 133:642–52 [Google Scholar]
  102. Motohashi R, Nagata N, Ito T, Takahashi S, Hobo T. 102.  et al. 2001. An essential role of a TatC homologue of a ΔpH-dependent protein transporter in thylakoid membrane formation during chloroplast development in Arabidopsis thaliana. PNAS 98:10499–504 [Google Scholar]

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