Экспрессия хлоропластного генома: современные представления и экспериментальные пути изучения

Уникальным свойством растений является наличие, кроме генома ядра, двух внеядерных геномов в хлоропластах и митохондриях. Геном хлоропластов относительно невелик – 100–120 генов, которые кодируют менее 5 % всех необходимых для функционирования пластид белков. Экспрессия генома пластид сохраняет черты прокариот: котранскрипцию генов в составе оперона, сходные c бактериями РНК-полимеразы и промоторы, присутствие 70S рибосом, однако появляются и новые свойства: транскрипция, не сопряженная c трансляцией, фагоподобные РНК-полимеразы, РНК эдитинг и сплайсинг транскриптов. Взаимодействие ядра (генома ядра) и цитоплазмы (генома пластид, митохондрий) в процессе развития растительного организма абсолютно необходимо для полноценного развития растения, адаптации (пластичности) к факторам окружающей среды. В обзоре обобщены современные представления об особенностях экспрессии генома пластид в клетке. Последовательно показано, что происходит при реализации генетической информации генома пластид в хлоропластах (транскрипции, эдитинге, сплайсинге, полиаденилировании, трансляции) и как отсутствие каких-либо компонентов отражается на функционировании растительной клетки и растения в целом. Описаны современные подходы к изучению пула транскриптов, выявлены критические точки ядерно-цитоплазматического взаимодействия при реали­зации функции хлоропластов в онтогенезе, воздействии факто­ров окружающей среды и др. Подробно представлена информация о важнейших факторах ядерно-цитоплазматического сигналинга у высших растений – сигма-факторах и PPR-белках, кодируемых ядром. Таким образом, показаны многоуровневость и целесообразность регуляции процессов экспрессии генома пластид в растительной клетке и взаимозависимость происходящих в разных компартментах клетки процессов. Составлена также сводка последних работ по изучению экспрессии генома пластид с помощью генетических чипов (микро- и макроэррей). Приводятся результаты собственных исследований.

хлоропласт, пластиды, экспрессия, транскрипция, РНК-полимеразы, эдитинг, сплайсинг, трансляция, микроэррей, макроэррей

1. Алейникова А.Ю. Неравномерность транскрипции генов в составе хлоропластных оперонов ячменя: Автореф. дис. … канд. биол. наук. М., 2012.

2. Алейникова А.Ю., Зубо Я.О., Кузнецов В.В. Интенсивность транскрипции генов atpB оперона хлоропластов листьев ячменя в зависимости от действия разных факторов. Вестн. Томского гос. ун-та. Биология. 2011;3(15):139-142.

3. Даниленко Н.Г., Давыденко О.Г. Миры геномов органелл. Минск: Тэхналогия, 2003.

4. Синявская М.Г., Сивицкая Л.Н., Давыденко О.Г. Создание макроэррей для изучения экспрессии геномов органелл у злаков. Генетика и биотехнология XXI в.: проблемы, достижения, перспективы (к 100-летию со дня рождения акад. Н.В. Турбина). Матер. междунар. науч. конф. Минск, 8-11 октября 2012 г. Минск, Ин-т генетики и цитологии НАН Беларуси, 2012.

5. Шимкевич А.М., Макаров В.Н., Голоенко И.М., Давыденко О.Г. Функциональное состояние фотосинтетического аппарата у аллоплазматических линий ячменя. Экол. генетика. 2006;4(3): 37-42.

6. Albrecht V., Ingenfeld A., Apel K. Characterization of the snowy cotyledon 1 mutant of Arabidopsis thaliana: the impact of chloroplast elongation factor G on chloroplast development and plant vitality. Plant Mol. Biol. 2006;60(4):507-518. https://doi.org/10.1007/s11103-005-4921-0

7. Allison L. The role of sigma factors in chloroplast transcription. Biochimie. 2000;82(6-7):537-548. https://doi.org/10.1016/S0300-9084(00)00611-8

8. Allison L., Simon L., Maliga P. Deletion of rpoBm reveals a second distinct transcription system in plastids of higher plants. EMBO J.1996;15(11):2802-2809.

9. Allorent G., Courtois F., Chevalier F., Lerbs-Mache S. Plastid gene expression during chloroplast differentiation and dedifferentiation into non-photosynthetic plastids during seed formation. Plant Mol. Biol. 2013;82(1):59-70. https://doi.org/10.1007/s11103-013-0037-0

10. Barkan A. Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J. 1988;7(9):2637-2644.

11. Barkan A., Walker M., Nolasco M., Johnson D. A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 1994;13(13):3170-3181.

12. Barkan A. Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol. 2011;155(4):1520-1532. https://doi.org/10.1104/pp.110.171231

13. Baumgartner B.J., Rapp J.C., Mullet J.E. Plastid genes encoding the transcription/translation apparatus are differentially transcribed early in barley (Hordeum vulgare) chloroplast development evidence for selective stabilization of psbA mRNA. Plant Physiol. 1993; 101(3):781-791.

14. Beligni M.V., Yamaguchi K., Mayfield S.P. The translational apparatus of Chlamydomonas reinhardtii chloroplast. Photosynth. Res. 2004;82(3):315-325.

15. Bentolila S., Oh J., Hanson M.R., Bukowski R. Comprehensive highresolution analysis of the role of an Arabidopsis gene family in RNA editing. PLoS Genet. 2013;9(6):e1003584. https://doi.org/10.1371/journal.pgen.1003584

16. Bock R. Structure, function, and inheritance of plastid genomes. Topics in Current Genetics. V. 19. Cell and Molecular Biology of Plastids. Ed. R. Bock. Berlin. Heidelberg: Springer-Verlag, 2007:29-63. https://doi.org/10.1007/978-3-540-75376-6

17. Bock R., Hermann M., Kцssel H. In vivo dissection of cis-acting determinants for plastid RNA editing. EMBO J. 1996;15(18):5052-5059.

18. Bock R., Koop H.U. Extraplastidic site-specific factors mediate RNA editing in chloroplasts. EMBO J. 1997;16(11): 3282-3288.

19. Börner T., Aleynikova A.Y., Zubo Y.O., Kusnetsov V.V. Chloroplast RNA polymerases: role in chloroplast biogenesis. Biochim. Biophys. Acta. 2015;1847(9):761-769. https://doi.org/10.1016/j.bbabio.2015.02.004

20. Cahoon A.B., Harris F.M., Stern D.B. Analysis of developing maize plastids reveals two mRNA stability classes correlating with RNA polymerase type. EMBO Rep. 2004;5(8):801-806. https://doi.org/10.1038/sj.embor.7400202

21. Cahoon B., Takacs E., Sharpe R., Stern D. Nuclear, chloroplast, and mitochondrial transcript abundance along a maize leaf developmental gradient. Plant Mol. Biol. 2008;66(1-2):33-46. https://doi.org/10.1007/s11103-007-9250-z

22. Cardi T., Giegé P., Kahlau S., Scotti N. Expression profiling of organellar genes. Advances in Photosynthesis and respiration. Genomics of Chloroplasts and Mitochondria. Ed. R. Bock, V. Knoop. Springer, 2012,35:323-355. https://doi.org/10.1007/978-94-007-2920-9

23. Chateigner-Boutin A., Hanson L, Maureen R. Developmental co-variation of RNA editing extent of plastid editing sites exhibiting similar cis-elements. Nucl. Acids Res. 2003;31(10):2586-2594. https://doi.org/10.1093/nar/gkg354

24. Cho W.K., Geimer S., Meurer J. Cluster analysis and comparison of various chloroplast transcriptomes and genes in Arabidopsis thaliana. DNA Res. 2009;16(1):31-44. https://doi.org/10.1093/dnares/dsn031

25. Courtois F., Merendino L., Demarsy E., Mache R., Lerbs-Mache S. Phage-type RNA polymerase RPOTmp transcribes the rrn operon from the PC promoter at early developmental stages in Arabidopsis. Plant Physiol. 2007;145(3):712-721. https://doi.org/10.1104/pp.107.103846

26. Covello P.S., Gray M.W. RNA editing in plant mitochondria. Nature. 1989;341(6243):662-666. https://doi.org/10.1038/341662a0

27. de Longevialle A.F., Small I.D., Lurin C. Nuclearly encoded splicing factors implicated in RNA splicing in higher plant organelles. Mol. Plant. 2010;3(4):691-705. https://doi.org/10.1093/mp/ssq025

28. Del Campo E.M. Post-transcriptional control of chloroplast gene expression. Gene Regul. Syst. Biol. 2009;3:31-47.

29. Demarsy E., Courtois F., Azevedo J., Buhot L., Lerbs-Mache S. Building up of the plastid transcriptional machinery during germination and early plant development. Plant Physiol. 2006;142(3): 993-1003. https://doi.org/10. 1104/pp. 106. 085043

30. Demarsy E., Buhr F., Lambert E., Lerbs-Mache S. Characterization of the plastid-specific germination and seedling establishment transcriptional programme. J. Exp. Bot. 2012;63(2):925-939. https://doi.org/10.1093/jxb/err322

31. Erikson B., Stern D., Higgs D. Microarray analysis confirms the specificity of a Chlamydomonas reinhadtrii chloroplast RNA stability mutant. Plant Physiol. 2005;137(2):534-544. https://doi.org/10.1104/pp.104.053256

32. Fargo D.C., Boynton J.E., Gillham N.W. Mutations altering the predicted secondary structure of a chloroplast 5’ untranslated region affect its physical and biochemical properties as well as its ability to promote translation of reporter mRNAs both in the Chlamydomonas reinhardtii chloroplast and in Escherichia coli. Mol. Cell Biol. 1999;19(10):6980-6990.

33. Freyer R., Hoch B., Neckermann K., Maier R.M., Kössel H. RNA editing in maize chloroplasts is a processing step independent of splicing and cleavage to monocistronic mRNAs. Plant J. 1993;4(4):621-629. https://doi.org/10.1046/j.1365-313X.1993.04040621

34. Geimer S., Belicová A., Legen J. Transcriptome analysis of the Euglena gracilis plastid chromosome. Curr. Genet. 2009;55(4):425-438. https://doi.org/10.1007/s00294-009-0256-8

35. Germain A., Hotto A.M., Barkan A., Stern D.B. RNA processing and decay in plastids. RNA (WIREs RNA). 2013;4(3):295-316. https://doi.org/10.1002/wrna.1161

36. Ghulam M.M., Zghidi-Abouzid O., Lambert E., Lerbs-Mache S., Merendino L. Transcriptional organization of the large and the small ATP synthase operons, atpI/H/F/A and atpB/E, in Arabidopsis thaliana chloroplasts. Plant Mol. Biol. 2012;79(3):259-272. https://doi.org/10.1007/s11103-012-9910-5

37. Giege P., Brennicke A. RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc. Natl Acad. Sci. USA. 1999; 96(26):15324-15329. https://doi.org/10.1073/pnas.96.26.15324

38. Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu. Rev. Biochem. 1988;57:199-233.

39. Gray J.C., Sullivan J.A., Wang J.H., Jerome C.A., MacLean D. Coordination of plastid and nuclear gene expression. Phil. Trans. R. Soc. Lond. 2003;358(1429):135-145. https://doi.org/10.1098/rstb.2002.1180

40. Gualberto J.M., Lamattina L., Bonnard G., Weil J.H., Grienenberger J.M. RNA editing in wheat mitochondria results in conservation of protein sequences. Nature. 1989;341(6243):660-662. https://doi.org/10.1038/341660a0

41. Hajdukiewicz P.T., Allison L.A., Maliga P. The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 1997;16(13):4041-4048.

42. Hattori M., Sugita M. A moss pentatricopeptide repeat protein binds to the 3’end of plastid clpP pre-mRNA and assists with mRNA maturation. FEBS J. 2009;276(20):5860-5869. https://doi.org/10.1111/j.1742-4658.2009.07267.x

43. Hess W.R., Börner T. Organellar RNA polymerases of higher plants. Int. Rev. Cytol. 1999;190:1-59.

44. Hiesel R., Wissinger B., Schuster W., Brennicke A. RNA editing in plant mitochondria. Science. 1989;246(4937):1632-1634. https://doi.org/10.1126/science.2480644

45. Hirose T., Sugiura M. Multiple elements required for translation of plastid atpB mRNA lacking the Shine-Dalgarno sequence. Nucl. Acids Res. 2004;32(11):3503-3510. https://doi.org/10.1093/nar/gkh682 Hoch B., Maier R.M., Appel K., Igloi G.L., Kössel H. Editing of a chloroplast mRNA by creation of an initiation codon. Nature. 1991;353(6340):178-180. https://doi.org/10.1038/353178a0

46. Hotto A.M., Schmitz R.J., Fei Z., Ecker J.R., Stern D.B. Unexpected diversity of chloroplast noncoding RNAs as revealed by deep sequencing of the Arabidopsis transcriptome. G3 (Bethesda). 2011;1(7):559-570. https://doi.org/10.1534/g3.111.000752

47. Kahlau S., Bock R. 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. 2008;20(4):856-874. https://doi.org/10.1105/tpc.107.055202

48. Kanesaki Y., Imamura S., Minoda A., Tanaka K. External light conditions and internal cell cycle phases coordinate accumulation of chloroplast and mitochondrial transcripts in the red alga Cyanidioschyzon merolae. DNA Res. 2012;19(3):289-303. https://doi.org/10.1093/dnares/dss013

49. Kapoor S., Sugira M. Expression and regulation of plastid genes. Photosynthesis: A Comprehensive Treatise. Camridge, UK: Cambr. Univ. Press, 1998.

50. Kehoe D., Villand P., Somerville S. DNA microarrays for studies of higher plants and other photosynthetic organisms. Trends Plant Sci. 1999;4(1):38-41. https://doi.org/10.1016/S1360-1385(98)01354-5

51. Khanam S.M., Naydenov N.G., Kadowaki K., Nakamura C. Mitochondrial biogenesis as revealed by mitochondrial transcript profiles during germination and early seedling growth in wheat. Genes Genet. Syst. 2007;82(5):409-420. https://doi.org/10.1266/ggs.82.409

52. Kozak M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene. 2005;361:13-37. https://doi.org/10.1016/j.gene.2005.06.037

53. Kudla J., Hayes R., Gruissem W. Polyadenylation accelerates degradation of chloroplast mRNA. EMBO J. 1996;15(24):7137-7146.

54. Legen J., Kemp S., Krause K., Profanter B., Herrmann R.G., Maier R. M. Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J. 2002;31(2):171-188. https://doi.org/10.1046/j.1365-313X.2002.01349.x

55. Legen J., Wanner G., Herrmann R.G., Small I., Schmitz-Linneweber C. Plastid tRNA genes trnC-GCA and trnN-GUU are essential for plant cell development. Plant J. 2007;51(5):751-762. https://doi.org/10.1111/j.1365-313X.2007.03177.x

56. Leister D. Chloroplast research in the genomic age. Trends Genet. 2003;19(1):47-56. https://doi.org/10.1016/S0168-9525(02)00003-3

57. Lerbs-Mache S. Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription? Plant Mol. Biol. 2011;76(3-5):235-249. https://doi.org/10.1007/s11103-010-9714-4

58. Liere K., Börner T. Transcription and transcriptional regulation in plastids. Topics in Current Genetics. Cell and Molecular Biology of Plastids. Ed. R. Bock. Berlin: Heidelberg: Springer-Verlag, 2007;19: 121-174. https://doi.org/10.1007/978-3-540-75376-6

59. Liere K., Maliga P. Plastid RNA polymerases in higher plants. Regulation of photosynthesis. Eds B. Andersson, E.-M. Aro. Netherlands, Dordrecht: Kluwer Acad. Publ., 2001.

60. Lin Q., Yu N.-J., Spremulli L.L. Expression and functional analysis of Euglena gracilis chloroplast initiation factor 3. Plant Mol. Biol. 1996;32(5):937-945.

61. Li-Pook-Than, J., Bonen L. Multiple physical forms of excised group II intron RNAs in wheat mitochondria. Nucl. Acids Res. 2006;34(9): 2782-2790. https://doi.org/10.1093/nar/gkl328

62. Loiselay C., Gumpel N.J., Girard-Bascou J., Watson A.T., Purton S., Wollman F.-A., Choquet Y. Molecular identification and function of cis- and trans-acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts. Mol. Cell Biol. 2008; 28(17):5529-5542. https://doi.org/10.1128/MCB.02056-07

63. Lurin C., Andres C., Aubourg S., Bellaoui M., Bitton F. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell. 2004;16(8):2089-2103. https://doi.org/10.1105/tpc.104.022236

64. Luro S., Germain A., Sharwood R., Stern D.B. RNase J participates in a pentatricopeptide repeat protein-mediated 5’ end maturation of chloroplast mRNAs. Nucl. Acids Res. 2013;41(19):9141-9151. https://doi.org/10.1093/nar/gkt640

65. Lyska D., Meierhoff K., Westhoff P. How to build functional thylakoid membranes: from plastid transcription to protein complex assembly? Planta. 2013;237(2):413-428. https://doi.org/10.1007/s00425-012-1752-5

66. Maier U.G., Bozarth A., Funk H.T., Zauner S., Rensing S.A., SchmitzLinneweber C., Börner T., Tillich M. Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biology. 2008;6(36):1-9. https://doi.org/10.1186/1741-7007-6-36

67. Manna S. An overview of pentatricopeptide repeat proteins and their applications. Biochimie. 2015;113:93-99. https://doi.org/10.1016/j.biochi.2015.04.004

68. Meierhoff K., Felder S., Nakamura T., Bechtold N., Schuster G. HCF152 an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-psbT-psbHpetB-petD RNAs. Plant Cell. 2003;15(6):1480-1495. https://doi.org/10.1105/tpc.010397

69. Melonek J., Mulisch M., Schmitz-Linneweber C., Grabowski E., Hensel G., Krupinska K. Whirly1 in chloroplasts associates with intron containing RNAs and rarely co-localizes with nucleoids. Planta. 2010;232(2):471-481. https://doi.org/10.1007/s00425-010-1183-0

70. Minoda A., Nagasawa K., Hanaoka M., Horiuchi M., Takahashi H., Tanaka K. Microarray profiling of plastid gene expression in a unicellular red alga, Cyanidioschyzon merola. Plant Mol. Biol. 2005;59(3):375-385. https://doi.org/10.1007/s11103-005-0182-1

71. Miyamoto T., Obokata J., Sugiura M. A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts. Proc. Natl Acad. Sci. 2004;101(1):48-52. https://doi.org/10.1073/pnas.0307163101

72. Nagashima A., Hanaoka M., Motohashi R., Seki M., Shinozaki K., Kanamaru K., Takahashi H., Tanaka K. DNA microarray analysis of plastid gene expression in an Arabidopsis mutant deficient in a plastid transcription factor sigma, SIG2. Bioscience Biotechnology and Biochemistry. 2004;68(3):694-704. https://doi.org/10.1271/bbb.68.694

73. Nakamura T., Furuhashi Y., Hasegawa K., Hashimoto H., Watanabe K., Obokata J., Sugita M., Sugiura M. Array-based analysis on tobacco plastid transcripts:preparation of a genomic microarray containing all genes and all intergeneric regions. Plant Cell Physiol. 2003a; 44(8):861-867. https://doi.org/10.1093/pcp/pcg101

74. Nakamura T., Meierhoff K., Westhoff P., Schuster G. RNA-binding properties of HCF152, an arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur. J. Biochem. 2003b;270(20): 4070-4081. https://doi.org/10.1046/j.1432-1033.2003.03796.x

75. Nakamura T., Sugiura C., Kobayashi Y., Sugita M. Transcript profiling in plastid arginine tRNA-CCG gene knockout moss: construction of Physcomitrella patens plastid DNA microarray. Plant Biol. (Stuttg). 2005;7(3):258-265. https://doi.org/10.1055/s-2005-865620

76. Noordally Z.B., Ishii K., Atkins K.A., Wetherill S.J., Kusakina J., Walton E.J., Kato M., Azuma M., Tanaka K., Hanaoka M., Dodd A.N. Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science. 2013;339(6125):1316-1319. https://doi.org/10.1126/science.1230397

77. Notsu Y., Masood S., Nishikawa T., Kubo N., Akiduki G., Nakazono M., Hirai A., Kadowaki K. The complete sequence of the rice (Oryza sativa L.) mitochondrial genome. Mol. Genet. Genomics. 2002;268(4):434-445. https://doi.org/10.1007/s00438-002-0767-1

78. Ogihara Y, Endo A., Kojima T., Isono K., Hanaoka M., ShiinaT., Terachi T., Utsugi S., Murata M., Mori N., Murai K., Matsuoka Y., Ohnishi Y., Tajiri H., Tsunewaki K Chinese Spring wheat (Triticum aestivum L.) chloroplast genome: complete sequence and contig clones. Plant Mol Biol Rep. 2000;18:243-253. https://doi.org/10.1007/BF02823995

79. Ogihara Y., Isono K., Kojima T., Endo A., Hanaoka M., Shiina T., Terachi T., Utsugi S., Murata M., Mori N., Takumi S., Ikeo K., Gojobori T., Murai R., Murai K., Matsuoka Y., Ohnishi Y., Tajiri H., Tsunewaki K. Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA. Mol. Genet. Genomics. 2002;266(5):740-746. https://doi.org/10.1007/s00438-001-0606-9

80. Ohyama K. Chloroplast and mitochondrial genomes from a liverwort, Marchantia polymorpha - gene organization and molecular evolution. Biosci. Biotech. Biochem. 1996;60:16-24.

81. Okuda K., Hammani K., Tanz S.K., Peng L., Fukao Y., Myouga F., Motohashi R., Shinozaki K., Small I., Shikanai T. The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts. Plant J. 2010;61(2):339-349. https://doi.org/10.1111/j.1365-313X.2009.04059.x

82. Okuda K., Nakamura T., Sugita M., Shimizu T., Shikanai T. A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J. Biol. Chem. 2006;281(49):37661-37667.

83. Opdyke J.A., Kang J.G., Storz G. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J. Bacteriol. 2004;186(20):6698-705. https://doi.org/10.1128/JB.186.20.6698-6705.2004

84. Peled-Zehavi H., Danon A. Translation and translational regulation in Chloroplasts. Topics in Current Genetics. Cell and Molecular Biology of Plastids. Ed. R. Bock. Berlin: Springer-Verlag, 2007;19:249-281. https://doi.org/10.1007/978-3-540-75376-6

85. Pfalz J., Bayraktar O.A., Prikryl J., Barkan A. Site-specific binding of a PPR protein defines and stabilizes 5’ and 3’ mRNA termini in chloroplasts. EMBO J. 2009;28 (14):2042-2052. https://doi.org/10.1038/emboj.2009.121

86. Plader W., Sugiura M. The Shine-Dalgarno-like sequence is a negative regulatory element for translation of tobacco chloroplast rps2 mRNA: an additional mechanism for translational control in chloroplasts. Plant J. 2003;34(3):377-382. https://doi.org/10.1046/j.1365-313X.2003.01732.x

87. Pogoryelov D., Reichen C., Klyszejko A.L., Brunisholz R., Muller D. J., Dimroth P., Meier T. The oligomeric state of c rings from cyanobacterial F-ATP synthases varies from 13 to 15. J. Bacteriol. 2007;189(16):5895-5902. https://doi.org/10.1128/JB.00581-07

88. Pogoryelov D., Yu J., Meier T., Vonck J., Dimroth P., Muller D.J. The c15 ring of the Spirulina platensis F-ATP synthase: F1/F0 symmetry mismatch is not obligatory. EMBO Rep. 2005;6(11):1040-1044. https://doi.org/10.1038/sj.embor.7400517

89. Prikryl J., Rojas M., Schuster G., Barkan A. Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl Acad. Sci. USA. 2011;108(1):415-420. https://doi.org/10.1073/pnas.1012076108

90. Rogalski M., Ruf S., Bock R. Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucl. Acids Res. 2006;34(16):4537-4545. https://doi.org/10.1093/nar/gkl634

91. Rüdinger M., Polsakiewicz M., Knoop V. Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat proteins in junger manniid but not in marchantiid liverworts. Mol. Biol. Evol. 2008;25(7):1405-1414. https://doi.org/0.1093/molbev/msn084

92. Ruwe H., Castandet B., Schmitz-Linneweber C., Stern D.B. Arabidopsis chloroplast quantitative editotype. FEBS Lett. 2013;587(9):1429-1433. https://doi.org/10.1016/j.febslet.2013.03.022

93. Salone V., Rudinger M., Polsakiewicz M., Hoffmann B., Groth-Malonek M., Szurek B., Small I., Knoop V., Lurin C. A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett. 2007;581(22):4132-4138. https://doi.org/10.1016/j.febslet.2007.07.075

94. Schena M., Shalon D., Davis R.W., Brown P.O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science. 1995;270(5235):467-470. https://doi.org/10.1126/science.270.5235.467

95. Schmitz-Linneweber C., Regel R., Du T.G., Hupfer H., Herrmann R.G., Maier R.M. The plastid chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: The role of RNA editing in generating divergence in the process of plant speciation. Mol. Biol. Evol. 2002;19(9):1602-1612. https://doi.org/10.1093/oxfordjournals. molbev.a004222

96. Schmitz-Linneweber C., Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 2008;13(12):663-670. https://doi.org/10.1016/j.tplants.2008.10.001

97. Schmitz-Linneweber C., Williams-Carrier R., Barkan A. RNA immunoprecipitation and microarray analysis show a chloroplast PPR protein to be associated with the 5′-region of mRNAs whose translation it activates. Plant Cell. 2005;17:2791-2804. https://doi.org/10.1105/tpc.105.034454

98. Schweer J., Türkeri H., Kolpack A., Link G. Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription - recent lessons from Arabidopsis thaliana. Eur. J. Cell Biol. 2010;89(12):940-946. https://doi.org/10.1016/j.ejcb.2010.06.016

99. Sharma M.R., Wilson D.N., Datta P.P., Barat C., Schluenzen F., Fucini P., Agrawal R.K. Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc. Natl Acad. Sci. USA. 2007;104(49):19315-19320. https://doi.org/10.1073/pnas.0709856104

100. Shen Y., Li C., McCarty d.R., Meeley R., Tan B.-C. Embryo defective12 encodes the plastid initiation factor 3 and is essential for embryogenesis in maize. Plant J. 2013;74(5):792-804. https://doi.org/10.1111/tpj.12161

101. Shiina T., Yuichi T., Yoichi N., Khan M.S. Plastid RNA polymerases, promoters, and transcription regulators in higher plants. Intern. Rev. Cytology. 2005;244:1-68. https://doi.org/10.1016/S0074-7696(05)44001-2

102. Shikanai T. RNA editing in plants: Machinery and flexibility of site recognition. Biochim. Biophys Acta. 2015;1847(9):779-785. https://doi.org/10.1016/j.bbabio.2014.12.010

103. Shikanai T., Fujii S. Function of PPR proteins in plastid gene expression. RNA Biology. 2013;10(9):1446-1456. https://doi.org/10.4161/rna.25207

104. Siniauskaya M., Naydenov N., Davydenko O., Nakamura C. Macroarray for studying chloroplast gene expression profiles associated with the initial development of wheat. Proc. of the 11th Intern. Wheat Genet. Symp. Ed. R. Appels et al. 2008.

105. Small I.D., Peeters N. The PPR motif: a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 2000;25(2):46-47. https://doi.org/10.1016/S0968-0004(99)01520-0

106. Staub J.M., Maliga P. Accumulation of D1 polypeptide in tobacco plastids is regulated via the untranslated region of the psbA mRNA. EMBO J. 1993;12(2):601-606.

107. Stern D.B., Goldschmidt-Clermont M., Hanson M.R. Chloroplast RNA metabolism. Annu. Rev. Plant Biol. 2010;61:125-155. https://doi.org/10.1146/annurev-arplant-042809-112242

108. Stock D., Leslie A.G.W., Walker J.E. Molecular architecture of the rotary motor in ATP synthase. Science. 1999;86(5445):1700-1705. https://doi.org/10.1126/science.286.5445.1700

109. Stoppel R., Meurer J. Complex RNA metabolism in the chloroplast: an update on the psbB operon. Planta. 2013;237(2):441-449. https://doi.org/10.1007/s00425-012-1782-z

110. Stoughton R.B. Applications of DNA microarrays in biology. Annu. Rev. Biochem. 2005;74:53-82. https://doi.org/10.1146/annurev.biochem. 74.082803.133212

111. Sugita M., Miyata Y., Maruyama K., Sugiura C., Arikawa T., Higuchi M. Extensive RNA editing in transcripts from the PsbB operon and RpoA gene of plastids from the enigmatic moss Takakia lepidozioides. Biosci. Biotechnol. Biochem. 2006;70(9):2268-2274. https://doi.org/10.1271/bbb.60204

112. Sugiura M. Plastid mRNA translation Chloroplast Biotechnology. Methods and Protocols. Methods in Molecular Biology. Ed. P. Maliga. Humana Press. 2014;1132:73-90. https://doi.org/10.1007/978-1-62703-995-6

113. Sugiura M., Hirose T., Sugita M. Evolution and mechanism of translation in chloroplasts. Annu. Rev. Genet. 1998;32:437-459. https://doi.org/10.1146/annurev.genet.32.1.437

114. Swiatecka-Hagenbruch M., Emanuel C., Hedtke B., Liere K., Börner T. Impaired function of the phage-type RNA polymerase RpoTp in transcription of chloroplast genes is compensated by a second phage-type RNA polymerase. Nucl. Acids Res. 2008;36(3):785-792. https://doi.org/10.1093/nar/gkm1111

115. Takenaka M., Zehrmann A., Hartel B., Kugelmann M., Verbitskiy D., Brennicke A. Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proc. Natl Acad. Sci. USA. 2012;109(13):5104-5109. https://doi.org/10.1073/pnas.1202452109

116. Takenaka M., Zehrmann A., Verbitskiy D., Härtel B., Brennicke A. RNA editing in plants and its evolution. Annu. Rev. Genet. 2013; 47(13):335-352. https://doi.org/10.1146/annurev-genet-111212-133519

117. Tiller N., Bock R. The translational apparatus of plastids and its role in plant development. Mol. Plant. 2014;7(7):1105-1120. https://doi.org/10.1093/mp/ssu022

118. Tiller N., Weingartner M., Thiele W., Maximova E., Schöttler M.A., Bock R. The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins. Plant J. 2012;69(2):302-316. https://doi.org/10.1111/j.1365-313X.2011.04791.x

119. Toyoshima Y., Onda Y., Shiina T., Nakahira Y. Plastid transcription in higher plants. CRC Crit Rev. Plant Sci. 2005;24(1):59-81. https://doi.org/10.1080/07352680590910438

120. Tozawa Y., Teraishi M., Sasaki T., Sonoike K., Nishiyama Y., Itaya M., Miyao A., Hirochika H. The plastid sigma factor SIG1 maintains photosystem I activity via regulated expression of the psaA operon in rice chloroplasts. Plant J. 2007;52(1):124-132. https://doi.org/10.1111/j.1365-313X.2007.03216.x

121. Valkov V.T., Scotti N., Kahlau S. Maclean D., Grillo S., Gray J.C., Bock R., Cardi T. Genome-wide analysis of plastid gene expression in potato leaf chloroplasts and tuber amyloplasts: transcriptional and posttranscriptional control. Plant Physiol. 2009;150(4):2030-2044. https://doi.org/10.1104/pp.109.140483

122. Verbitskiy D., van der Merwe J.A., Zehrmann A., Brennicke A., Takenaka M. Multiple specificity recognition motifs enhance plant mitochondrial RNA editing in vitro. J. Biol. Chem. 2008:283(36):24374-24381. https://doi.org/10.1074/jbc.M803292200

123. Wakasugi T., Tsudzuki J., Ito S., Nakashima K., Tsudzuki T., Sugiura M. Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the Black Pine Pinus thunbergii. Proc. Natl Acad. Sci. USA. 1994;91(21):9794-9798. https://doi.org/10.1073/pnas.91.21.9794

124. Walter M., Kilian J., Kudla J. PNPase activity determines the efficiency of mRNA 3′-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. EMBO J. 2002;21(24):6905-6914. https://doi.org/10.1093/emboj/cdf686

125. Westhoff P., Hermann R.G. Complex RNA maturation in chloroplasts: the psbB operon from spinach. Eur. J. Biochem. 1988;171(3):551-564. https://doi.org/10.1111/j.1432-1033.1988.tb13824.x

126. Wicke S., Schneeweiss G.M., dePamphilis C.W., Müller K.F., Quandt D. Thе evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol. Biol. 2011;76(3/5):273-297. https://doi.org/10.1007/s11103-011-9762-4

127. Williams-Carrier R., Kroeger T., Barkan A. Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA. 2008;14(9):1930-1941. https://doi.org/10.1261/rna.1077708

128. Wostrikoff K., Stern D. Rubisco large-subunit translation is autoregulatedin response to its assembly state in tobacco chloroplasts. Proc. Natl Acad. Sci. USA. 2007;104(15):6466-6471. https://doi.org/10.1073/pnas.0610586104

129. Xu T., Lee K., Gu L., Kim J.I., Kang H. Functional characterization of a plastid-specific ribosomal protein PSRP2 in Arabidopsis thaliana under abiotic stress conditions. Plant Physiol. Biochem. 2013;73:405-411. https://doi.org/10.1016/j.plaphy.2013.10.027

130. Yagi Y., Shiina T. Recent advances in the study of chloroplast gene expression and its evolution. Front. Plant Sci. 2014;5(61):1-7. https://doi.org/10.3389/fpls.2014.00061

131. Yamaguchi K., Beligni M.V., Prieto S., Haynes P.A., McDonald W.H., Yates J.R. 3rd Mayfield S.P. Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome. Identification of proteins unique to the 70 S ribosome. J. Biol. Chem. 2003;278(36):33774-33785. https://doi.org/10.1074/jbc.M301934200

132. Yamaguchi K., Prieto S., Beligni M.V., Haynes P.A., McDonald W.H., Yates J.R. 3rd, Mayfield S.P. Proteomic characterization of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: identification of a novel S1 domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. Plant Cell. 2002;14(11):2957-2974. https://doi.org/10.1105/tpc.004341

133. Yehudai-Resheff S., Hirsh M., Schuster G. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol. Cell Biol. 2001;21(16):5408-5416. https://doi.org/10.1128/MCB.21.16.5408-5416.2001

134. Zerges W., Auchincloss A.H., Rochaix J.D. Multiple translational control sequences in the 5’ leader of the chloroplast psbC mRNA interact with nuclear gene products in Chlamydomonas reinhardtii. Genetics. 2003;163(3):895-904.

135. Zerges W., Girard-Bascou J., Rochaix J.D. Translation of the chloroplast psbC mRNA is controlled by interactions between its 5’ leader and the nuclear loci TBC1 and TBC3 in Chlamydomonas reinhardtii. Mol. Cell Biol. 1997;17(6):3440-3448.

136. Zghidi W., Merendino L., Cottet A., Mache R., Lerbs-Mache S. Nucleus-encoded plastid sigma factor SIG3 transcribes specifically the psbN gene in plastids. Nucl. Acids Res. 2007;35(2):455-464. https://doi.org/10.1093/nar/gkl1067

137. Zghidi-Abouzid O., Merendino L., Buhr F., M. Ghulam M., Lerbs-Mache S. Characterization of plastid psbT sense and antisense RNAs. Nucl. Acids Res. 2011;39(13):5379-5387. https://doi.org/10.1093/nar/gkr143

138. Zhelyazkova P. The transcriptome of barley chloroplasts revealed by deep sequencing. Dissertation. Berlin, 2012

139. Zhelyazkova P., Hammani K., Rojas M., Voelker R., Vargas-Suárez M., Börner T., Barkan A. Protein-mediated protection as the predominant mechanism for defining processed mRNA termini in land plant chloroplasts. Nucl. Acids Res. 2012;40(7):3092-3105. https://doi.org/10.1093/nar/gkr1137

140. Zhelyazkova P., Sharma C.M., Förstner K.U., Liere K., Vogel J., Börner T. The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell. 2012;4(1):123-136. https://doi.org/10.1105/tpc.111.089441

141. Zmienko A., Guzowska-Nowowiejska M., Urbaniak R., Plаder W., Formanowicz P., Figlerowicz M. A tiling microarray for global analysis of chloroplast genome expression in cucumber and other plants. Plant Methods. 2011;7:29. https://doi.org/10.1186/1746-4811-7-29

142. Zoschke R., Nakamura M., Liere K., Sugiura M., Börner T., SchmitzLinneweber C. An organellar maturase associates with multiple group II Introns. Proc. Natl. Acad. Sci. USA. 2010;107(7):3245-3250. https://doi.org/10.1073/pnas.0909400107