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Biochemistry (Moscow)

, Volume 82, Issue 6, pp 678–691 | Cite as

Structure of plastid genomes of photosynthetic eukaryotes

  • N. P. YurinaEmail author
  • L. S. Sharapova
  • M. S. Odintsova
Review

Abstract

This review presents current views on the plastid genomes of higher plants and summarizes data on the size, structural organization, gene content, and other features of plastid DNAs. Special emphasis is placed on the properties of organization of land plant plastid genomes (nucleoids) that distinguish them from bacterial genomes. The prospects of genetic engineering of chloroplast genomes are discussed.

Keywords

plastids photosynthetic eukaryotes chloroplast genome 

Abbreviations

IR

inverted repeat

kb

thousand base pairs

LSC

large single copy region

nupDNA

nuclear-localized plastid DNA

SSC

small single copy region

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References

  1. 1.
    Xu, J. H., Liu, Q., Hu, W., Wang, T., Xue, Q., and Messing, J. (2015) Dynamics of chloroplast genomes in green plants, Genomics, 106, 221–231.CrossRefPubMedGoogle Scholar
  2. 2.
    Jensen, P. E., and Leister, D. (2014) Chloroplast evolution, structure and functions, F1000Prime Rep., 6, 40.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Howe, C. J., Barbrook, A. C., Nisbet, R. E., Lockhart, P. J., and Larkum, A. W. (2008) The origin of plastids, Phil. Trans. R. Soc. B, 363, 2675–2685.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Green, B. R. (2011) Chloroplast genomes of photosynthetic eukaryotes, Plant J., 66, 34–44.CrossRefPubMedGoogle Scholar
  5. 5.
    Ruck, E. C., Nakov, T., Jansen, R. K., Theriot, E. C., and Alverson, A. J. (2014) Serial gene losses and foreign DNA underlie size and sequence variation in the plastid genomes of diatoms, Gen. Biol. Evol., 6, 644–654.CrossRefGoogle Scholar
  6. 6.
    Barbrook, A. C., Howe, C. J., Kurniawan, D. P., and Tarr, S. J. (2010) Organization and expression of organellar genomes, Phil. Trans. R. Soc. B, 365, 785–797.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Curtis, B. A., Tanifuji, G., Burki, F., Gruber, A., Irimia, M., Maruyama, S., Arias, M. C., Ball, S. G., Gile, G. H., Hirakawa, Y., Hopkins, J. F., Kuo, A., Rensing, S. A., Schmutz, J., Symeonidi, A., Elias, M., Eveleigh, R. J., Herman, E. K., Klute, M. J., Nakayama, T., Obornik, M., Reyes-Prieto, A., Armbrust, E. V., Aves, S. J., Beiko, R. G., Coutinho, P., Dacks, J. B., Durnford, D. G., Fast, N. M., Green, B. R., Grisdale, C. J., Hempel, F., Henrissat, B., Höppner, M. P., Ishida, K., Kim, E., Koreny, L., Kroth, P. G., Liu, Y., Malik, S. B., Maier, U. G., McRose, D., Mock, T., Neilson, J. A., Onodera, N. T., Poole, A. M., Pritham, E. J., Richards, T. A., Rocap, G., Roy, S. W., Sarai, C., Schaack, S., Shirato, S., Slamovits, C. H., Spencer, D. F., Suzuki, S., Worden, A. Z., Zauner, S., Barry, K., Bell, C., Bharti, A. K., Crow, J. A., Grimwood, J., Kramer, R., Lindquist, E., Lucas, S., Salamov, A., McFadden, G. I., Lane, C. E., Keeling, P. J., Gray, M. W., Grigoriev, I. V., and Archibald, J. M. (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs, Nature, 492, 59–65.CrossRefPubMedGoogle Scholar
  8. 8.
    Lloyd, A. H., and Timmis, J. N. (2011) The origin and characterization of new nuclear genes originating from a cytoplasmic organellar genome, Mol. Biol. Evol., 28, 2019–2028.CrossRefPubMedGoogle Scholar
  9. 9.
    Raman, G., and Park, S. (2015) Analysis of the complete chloroplast genome of a medicinal plant, Dianthus superbus var. longicalyncinus, from a comparative genomics perspective, PLoS One, 10, e0141329.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Rochaix, J.-D., and Ramundo, S. (2015) Conditional repression of essential chloroplast genes: evidence for new plastid signaling pathways, Biochim. Biophys. Acta, 1847, 986–992.CrossRefPubMedGoogle Scholar
  11. 11.
    Yagi, Y., and Shiina, T. (2014) Recent advances in the study of chloroplast gene expression and its evolution, Front. Plant Sci., 5, 61.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Leister, D. (2003) Chloroplast research in the genomic age, Trends Genet., 19, 47–57.CrossRefPubMedGoogle Scholar
  13. 13.
    Woodson, J. D., and Chory, J. (2012) Organelle signaling: how stressed chloroplasts communicate with the nucleus, Curr. Biol., 22, R690–692.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Ortelt, J., and Link, G. (2014) Plastid gene transcription: promoters and RNA polymerases, Methods Mol. Biol., 1132, 47–72.CrossRefPubMedGoogle Scholar
  15. 15.
    Golczyk, H., Greiner, S., Wanner, G., Weihe, A., Bock, R., Borner, T., and Herrmann, R. G. (2014) Chloroplast DNA in mature and senescing leaves: a reappraisal, Plant Cell, 26, 847–854.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Chen, H., Yu, Y., Chen, X., Zhang, Z., Gong, C., Li, J., and Wang, A. (2015) Plastid DNA insertions in plant nuclear genomes: the sites, abundance and ages, and a predicted promoter analysis, Funct. Integr. Genomics, 15, 131–139.CrossRefPubMedGoogle Scholar
  17. 17.
    Cullis, C. A., Vorster, B. J., Van Der Vyver, C., and Kunert, K. J. (2009) Transfer of genetic material between the chloroplast and nucleus: how is it related to stress in plants? Ann. Bot., 103, 625–633.CrossRefPubMedGoogle Scholar
  18. 18.
    Hsu, C. Y., Wu, C. S., and Chaw, S. M. (2014) Ancient nuclear plastid DNA in the yew family (Taxaceae), Genome Biol. Evol., 6, 2111–2121.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Wang, D., Qu, Z., Adelson, D. L., Zhu, J. K., and Timmis, J. N. (2014) Transcription of nuclear organellar DNA in a model plant system, Genome Biol. Evol., 6, 1327–1334.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Krupinska, K., Melonek, J., and Krause, K. (2013) New insights into plastid nucleoid structure and functionality, Planta, 237, 653–664.CrossRefPubMedGoogle Scholar
  21. 21.
    Pfalz, J., and Pfannschmidt, T. (2015) Plastid nucleoids: evolutionary reconstruction of a DNA/protein structure with prokaryotic ancestry, Front. Plant Sci., 6, 220.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Yagi, Y., and Shiina, T. (2012) Evolutionary aspects of plastid proteins involved in transcription: the transcription of a tiny genome is mediated by a complicated machinery, Transcription, 3, 290–294.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Melonek, J., Mulisch, M., Schmitz-Linneweber, C., Grabowski, E., Hensel, G., and Krupinska, K. (2010) Whirly1 in chloroplasts associates with intron containing RNAs and rarely co-localizes with nucleoids, Planta, 232, 471–481.CrossRefPubMedGoogle Scholar
  24. 24.
    Powikrowska, M., Oetke, S., Jensen, P. E., and Krupinska, K. (2014) Dynamic composition, shaping and organization of plastid nucleoids, Front. Plant Sci., 5, 424.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Bohne, A. V. (2014) The nucleoid as a site of rRNA processing and ribosome assembly, Front. Plant Sci., 5, 257.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Moriyama, T., and Sato, N. (2014) Enzymes involved in organellar DNA replication in photosynthetic eukaryotes, Front. Plant Sci., 5, 480.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Ruhlman, T. A., and Jansen, R. K. (2014) The plastid genomes of flowering plants, Methods Mol. Biol., 1132, 3–38.CrossRefPubMedGoogle Scholar
  28. 28.
    Pfalz, J., and Pfannschmidt, T. (2013) Essential nucleoid proteins in early chloroplast development, Trends Plant Sci., 18, 186–194.CrossRefPubMedGoogle Scholar
  29. 29.
    Powikrowska, M., Khrouchtchova, A., Martens, H. J., Zygadlo-Nielsen, A., Melonek, J., Schulz, A., Krupinska, K., Rodermel, S., and Jensen, P. E. (2014) SVR4 (suppressor of variegation 4) and SVR4-like: two proteins with a role in proper organization of the chloroplast genetic machinery, Physiol. Plant., 150, 477–492.CrossRefPubMedGoogle Scholar
  30. 30.
    Majeran, W., Friso, G., Asakura, Y., Qu, X., Huang, M., Ponnala, L., Watkins, K. P., Barkan, A., and Van Wijk, K. J. (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions, Plant Physiol., 158, 156–189.CrossRefPubMedGoogle Scholar
  31. 31.
    Kodama, Y. (2007) Plastidic proteins containing motifs of nuclear transcription factors, Plant Biotechnol., 24, 165–170.CrossRefGoogle Scholar
  32. 32.
    Melonek, J., Matros, A., Trosch, M., Mock, H. P., and Krupinska, K. (2012) The core of chloroplast nucleoids contains architectural SWIB domain proteins, Plant Cell, 24, 3060–3073.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Grabowski, E., Miao, Y., Mulisch, M., and Krupinska, K. (2008) Single-stranded DNA-binding protein Whirly1 in barley leaves is located in plastids and the nucleus of the same cell, Plant Physiol., 147, 1800–1804.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Yu, Q. B., Huang, C., and Yang, Z. N. (2014) Nuclearencoded factors associated with the chloroplast transcription machinery of higher plants, Front. Plant Sci., 5, 316.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K. J., and Oelmuller, R. (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression, Plant Cell, 18, 176–197.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Xu, Y. Z., Arrieta-Montiel, M. P., Virdi, K. S., De Paula, W. B., Widhalm, J. R., Basset, G. J., Davila, J. I., Elthon, T. E., Elowsky, C. G., Sato, S. J., Clemente, T. E., and Mackenzie, S. A. (2011) MutS homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light, Plant Cell, 23, 3428–3441.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Odintsova, M. S., and Yurina, N. P. (2003) Plastidic genome of higher plants and algae: structure and function, Mol. Biol. (Moscow), 37, 1–16.CrossRefGoogle Scholar
  38. 38.
    Odintsova, M. S., and Yurina, N. P. (2005) Genomics and evolution of cell organelles, Genetika, 41, 1–12.Google Scholar
  39. 39.
    Wicke, S., Schneeweiss, G. M., De Pamphilis, C. W., Muller, K. F., and Quandt, D. (2011) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function, Plant Mol. Biol., 76, 273–297.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    McCoy, S. R., Kuehl, J. V., Boore, J. L., and Raubeson, L. A. (2008) The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates, BMC Evol. Biol., 8, 130.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Wicke, S., Muller, K. F., De Pamphilis, C. W., Quandt, D., Wickett, N. J., Zhang, Y., Renner, S. S., and Schneeweiss, G. M. (2013) Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family, Plant Cell, 25, 3711–3725.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Nazareno, A. G., Carlsen, M., and Lohmann, L. G. (2015) Complete chloroplast genome of Tanaecium tetragonolobum: the first Bignoniaceae plastome, PLoS One, 10, 129930.CrossRefGoogle Scholar
  43. 43.
    Oldenburg, D. J., and Bendich, A. J. (2015) DNA maintenance in plastids and mitochondria of plants, Front. Plant Sci., 6, 883.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Zhu, A., Guo, W., Gupta, S., Fan, W., and Mower, J. P. (2016) Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates, New Phytol., 209, 1747–1756.CrossRefPubMedGoogle Scholar
  45. 45.
    Wu, C. S., and Chaw, S. M. (2015) Evolutionary stasis in cycad plastomes and the first case of plastome GC-biased gene conversion, Genome Biol. Evol., 7, 2000–2009.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Guo, W., Grewe, F., Cobo-Clark, A., Fan, W., Duan. Z., Adams, R. P., Schwarzbach, A. E., and Mower, J. P. (2014) Predominant and substoichiometric isomers of the plastid genome coexist within Juniperus plants and have shifted multiple times during cupressophyte evolution, Genome Biol. Evol., 6, 580–590.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Jeong, H., Lim, J. M., Park, J., Sim, Y. M., Choi, H. G., Lee, J., and Jeong, W. J. (2014) Plastid and mitochondrion genomic sequences from Arctic Chlorella sp. ArM0029B, BMC Genomics, 15, 286–300.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Tiller, N., and Bock, R. (2014) The translational apparatus of plastids and its role in plant development, Mol. Plant, 7, 1105–1120.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Barbrook, A. C., Howe, C. J., and Purton, S. (2006) Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci., 11, 101–108.CrossRefPubMedGoogle Scholar
  50. 50.
    Borner, T., Aleynikova, A. Y., Zubo, Y. O., and Kusnetsov, V. V. (2015) Chloroplast RNA polymerases: role in chloroplast biogenesis, Biochim. Biophys. Acta, 1847, 761–769.CrossRefPubMedGoogle Scholar
  51. 51.
    Knox, E. B. (2014) The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms, Proc. Natl. Acad. Sci. USA, 111, 11097–11102.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Gockel, G., and Hachtel, W. (2000) Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa, Protist, 151, 347–351.CrossRefPubMedGoogle Scholar
  53. 53.
    Wolfe, K. H., Morden, C. W., and Palmer, J. D. (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant, Proc. Natl. Acad. Sci. USA, 89, 10648–10652.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Smith, D. R., and Lee, R. W. (2014) A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella, Plant Physiol., 164, 1812–1819.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Braukmann, T., Kuzmina, M., and Stefanovic, S. (2013) Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus Grammica exhibit extensive gene loss, J. Exp. Bot., 64, 977–989.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Molina, J., Hazzouri, K. M., Nickrent, D., Geisler, M., Meyer, R. S., Pentony, M. M., Flowers, J. M., Pelser, P., Barselona, J., Inovejas, S. A., Uy, I., Yuan, W., Wilkins, O., Michel, C. I., Locklear, S., and Purugganan, M. D., Concepcion, G. P., and Purugganan, M. D. (2014) Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae), Mol. Biol. Evol., 31, 793–803.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Wolf, P. G., Der, J. P., Duffy, A. M., Davidson, J. B., Grusz, A. L., and Pryer, K. M. (2011) The evolution of chloroplast genes and genomes in ferns, Plant Mol. Biol., 76, 251–261.CrossRefPubMedGoogle Scholar
  58. 58.
    Sessa, E. B., Banks, J. A., Barker, M. S., Der, J. P., Duffy, A. M., Graham, S. W., Hasebe, M., Langdale, J., Li, F. W., Marchant, D. B., Pryer, K. M., Rothfels, C. J., Roux, S. J., Salmi, M. L., Sigel, E. M., Soltis, D. E., Soltis, P. S., Stevenson, D. W., and Wolf, P. G. (2014) Between two fern genomes, Giga Sci., 3, 15.CrossRefGoogle Scholar
  59. 59.
    Odintsova, M. S., and Yurina, N. P. (2000) RNA editing in plant chloroplasts and mitochondria, Fiziol. Rast., 47, 307–320.Google Scholar
  60. 60.
    Yurina, N. P., and Odintsova, M. S. (2016) Mitochondrial genome structure of photosynthetic eukaryotes, Biochemistry (Moscow), 81, 101–113.CrossRefGoogle Scholar
  61. 61.
    Wolf, P. G., Rowe, C. A., and Hasebe, M. (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillusveneris, Gene, 339, 89–97.CrossRefPubMedGoogle Scholar
  62. 62.
    Kugita, M., Yamamoto, Y., Fujikawa, T., Matsumoto, T., and Yoshinaga, K. (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional, Nucleic Acids Res., 31, 2417–2423.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Chateigner-Boutin, A. L., and Small, I. (2007) A rapid high-throughput method for the detection and quantification of RNA editing based on high-resolution melting of amplicons, Nucleic Acids Res., 35, 114.CrossRefGoogle Scholar
  64. 64.
    Bell, N. E., Boore, J. L., Mishler, B. D., and Hyvonen, J. (2014) Organellar genomes of the four-toothed moss, Tetraphis pellucida, BMC Genomics, 15, 383–394.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Wickett, N. J., Forrest, L. L., Budke, J. M., Shaw, B., and Goffinet, B. (2011) Frequent pseudogenization and loss of the plastid-encoded sulfate-transport gene cysA throughout the evolution of liverworts, Am. J. Bot., 98, 1263–1275.CrossRefPubMedGoogle Scholar
  66. 66.
    Kugita, M., Kaneko, A., Yamamoto, Y., Takeya, Y., Matsumoto, T., and Yoshinaga, K. (2003) The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants, Nucleic Acids Res., 31, 716–721.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Villarreal, J. C., Forrest, L. L., Wickett, N., and Goffinet, B. (2013) The plastid genome of the hornwort Nothoceros aenigmaticus (Dendrocerotaceae): phylogenetic signal in inverted repeat expansion, pseudogenization, and intron gain, Am. J. Bot., 100, 467–477.CrossRefPubMedGoogle Scholar
  68. 68.
    Maliga, P. (2004) Plastid transformation in higher plants, Annu. Rev. Plant Biol., 55, 289–313.CrossRefPubMedGoogle Scholar
  69. 69.
    Lutz, K. A., Azhagiri, A., Tungsuchat-Huang, T., and Maliga, P. (2007) A guide to choosing vectors for transformation of the plastid genome of higher plants, Plant Physiol., 145, 1201–1210.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Lutz, K. A., and Maliga, P. (2007) Construction of marker-free transplastomic plants, Curr. Opin. Biotechnol., 18, 107–114.CrossRefPubMedGoogle Scholar
  71. 71.
    Maliga, P., and Bock, R. (2011) Plastid biotechnology: food, fuel and medicine for the 21st century, Plant Physiol., 155, 1501–1510.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Shchelkunov, S. N., Konstantinov, Yu. M., and Deineko, E. V. (2011) Transplastomic plants, Vavilov. Zh. Genet. Selekt., 15, 808–817.Google Scholar
  73. 73.
    Maliga, P. (2012) Plastid transformation in flowering plants, in Genomics of Chloroplasts and Mitochondria (Bock, R., and Knoop, V., eds.) Springer, pp. 393–414.CrossRefGoogle Scholar
  74. 74.
    Hanson, M. R., Gray, B. N., and Ahner, B. A. (2013) Chloroplast transformation for engineering of photosynthesis, J. Exp. Bot., 64, 731–742.CrossRefPubMedGoogle Scholar
  75. 75.
    Daniell, H., Chan, H.-T., and Pasoreck, E. K. (2016) Vaccination via chloroplast genetics: affordable protein drugs for the prevention and treatment of inherited or infectious human diseases, Annu. Rev. Genet., 50, 595–618.CrossRefPubMedGoogle Scholar
  76. 76.
    Bock, R. (2015) Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology, Annu. Rev. Plant Biol., 66, 211–241.CrossRefPubMedGoogle Scholar
  77. 77.
    Jin, S., and Daniell, H. (2015) The engineered chloroplast genome just got smarter, Trends Plant Sci., 20, 622–640.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Bock, R. (2014) Genetic engineering of the chloroplast: novel tools and new applications, Curr. Opin. Biotechnol., 26, 7–13.CrossRefPubMedGoogle Scholar
  79. 79.
    Waheed, M. T., Ismail, H., Gottschamel, J., Mirza, B., and Lossl, A. G. (2015) Plastids: the green frontiers for vaccine production, Front. Plant Sci., 6, 1005.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Bock, R. (2014) Engineering chloroplasts for high-level foreign protein expression, Methods Mol. Biol., 1132, 93–106.CrossRefPubMedGoogle Scholar
  81. 81.
    Gisby, M. F., Mudd, E. A., and Day, A. (2012) Growth of transplastomics cells expressing D-amino acid oxidase in chloroplasts is tolerant to D-alanine and inhibited by D-valine, Plant Physiol., 160, 2219–2226.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • N. P. Yurina
    • 1
    Email author
  • L. S. Sharapova
    • 1
  • M. S. Odintsova
    • 1
  1. 1.Bach Institute of Biochemistry, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia

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