Endosymbiotic Origin of Chloroplasts in Plant Cells’ Evolution

Abstract

The theory of endosymbiotic origin of chloroplasts has become basal in present-day biology. In this regard, the emergence of eukaryotic photosynthesis has been established as a result of phagocytal capture of cyanobacteria by some ancestral eukaryotic cell. The phenomenon of endosymbiosis is an indispensable element of cell evolution theory. The process of endosymbiogenesis belongs to the crucial factors of biological progress that gave rise to astonishing diversity and complexity of the eukaryotic organisms. The modern theory of evolution is built on the joint base of the phenomena of endosymbiosis, parallel gene transfer, the theory of natural selection, and the data of phylogenomics. Ultimately, eukaryogenesis has integrated different supramolecular complexes in the cells, created the diversity of organelles, and has led to biosphere oxygenation and modern diversity of living forms.

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REFERENCES

  1. 1

    Mereschkowsky, C., Über Natur und Ursprung der Chromatophoren im Pflanzenreiche, Biol. Centralbl., 1905, vol. 25, p. 593.

    Google Scholar 

  2. 2

    Merezhkovskii, K.S., Teoriya dvukh plazm, kak osnova simbiogeneza, novogo ucheniya o proizkhozhdenii organizmov (Theory of Two Plasmas as the Basis of Symbiogenesis—A New Concept on Origin of Organisms), Kazan: Tipogr. Imper. Univ., 1909.

  3. 3

    Khakhina, L.N., Problema simbiogeneza (A Problem of Symbiogenesis), Leningrad: Nauka, 1979.

  4. 4

    Kolchinskii, E.I., Edinstvo evolyutsionnoi teorii v razdelennom mire XX veka (The Integration of Evolutionary Theory in the Divided World of the 20th Century), St. Petersburg: Nestor-Istoriya, 2015.

  5. 5

    Gibbs S.P., The evolution of algal chloroplasts, in Origins of Plastids: Symbiogenesis, Prochlorophytes and the Origins of Chloroplasts, Lewin, R.A., Ed., New York: Springer-Verlag, 1993, p. 107.

    Google Scholar 

  6. 6

    Archibald, J.M., Endosymbiosis and eukaryotic cell evolution, Curr. Biol., 2015, vol. 25, p. 911.

    Article  CAS  Google Scholar 

  7. 7

    Martin, W. and Kowallik, K.W., Annotated english translation of Mereschkowsky’s 1905 paper “Über Natur und Ursprung der Chromatophoren im Pflanzenreiche”, Eur. J. Phycol., 1999, vol. 34, p. 287.

    Google Scholar 

  8. 8

    Strel’nikova, N.I., Merezhkovskii K.S. and his research works on diatoms (to the 150th anniversary). http:// www.ksu.ru/conf/botan200/s183.rtf.

  9. 9

    Zakharov, I.A., The 100 anniversary of the theory of symbiogenesis, Vestn. Vavilovsk. O-va Genet. Sel., 2009, vol. 13, p. 355.

    Google Scholar 

  10. 10

    Provorov, N.A., Merezhkovskii K.S. and origin of eukaryotic cell: 111 years of the theory of symbiogenesis, S-kh. Biol., 2016, vol. 51, p. 746.

    Google Scholar 

  11. 11

    Fedonkin, M.A., Geochemical impoverishment and eukaryotization of the biosphere: a causal link, Paleontol. J., 2003, vol. 37, no. 6, p. 592.

    Google Scholar 

  12. 12

    Rozanov, A.Yu., Bacterial paleontology, sedimentogenesis, and early evolution of biosphere, Tr. Geol. Inst., Ross. Akad. Nauk, 2004, no. 565, p. 448.

  13. 13

    Woese, C.R., Kandler, O., and Wheelis, M.L., Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya, Proc. Natl. Acad. Sci. U.S.A., 1990, vol. 87, p. 4576.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  14. 14

    MacLeod, F., Gareth, S., Kindler, G.S., Wong, H.L., Chen, R., and Burns, B.P., Asgard archaea: diversity, function, and evolutionary implications in a range of microbiomes, AIMS Microbiol., 2019, vol. 5, p. 48. https://doi.org/10.3934/microbiol.2019.1.48

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15

    Yutin, N., Wolf, M.Y., Wolf, Y.I., and Koonin, E.V., The origins of phagocytosis and eukaryogenesis, Biol. Direct., 2009, vol. 4, p. 9. https://doi.org/10.1186/1745-6150-4-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16

    Shestakov, S.V., The role of archaea in the origin of eukaryotes, Ekol. Genet., 2017, vol. 15, p. 52. https://doi.org/10.17816/ecogen15452-59

    Article  Google Scholar 

  17. 17

    Martijn, J., Vosseberg, J., Guy, L., Offre, P., and Ettema, T.J.G., Deep mitochondrial origin outside the sampled alphaproteobacteria, Nature., 2018, vol. 557, p. 101.

    CAS  PubMed  Article  Google Scholar 

  18. 18

    López-García, P. and Móreira, D., The syntrophy hypothesis for the origin of eukaryotes revisited, Nat. Microbiol., 2020, vol. 5, p. 655.

    PubMed  Article  CAS  Google Scholar 

  19. 19

    Gorlenko, V.M., Anoxygenic phototrophic bacteria, Tr. Inst. Mikrobiol. im. S.N. Vinogradskogo, 2010, no. 15, p. 133.

  20. 20

    Wachterschauser, G., From volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya, Philos. Trans. R. Soc. B., 2006, vol. 361, p. 1787.

    Article  CAS  Google Scholar 

  21. 21

    Schopf, J.W., Kudrjavtsev, A.B., Agresti, D.G., Wdowiak, T., and Czaja, F.D., Laser-Raman imagery of Earth’s earliest fossils, Nature, 2003, vol. 416, p. 73.

    Article  Google Scholar 

  22. 22

    Schirrmeister, B.E., Gugger, M., and Donoghue, P.C.J., Cyanobacteria and the great oxidation event: evidence from genes and fossils, Palaeontology, 2015, vol. 58, p. 769.

    PubMed  PubMed Central  Article  Google Scholar 

  23. 23

    Nelson, N. and Junge, W., Structure and energy transfer in photosystems of oxygenic photosynthesis, Annu. Rev. Biochem., 2015, vol. 84, p. 659.

    CAS  PubMed  Article  Google Scholar 

  24. 24

    Stadnichuk, I.N., Krasilnikov, P.M., and Zlenko, D.V., Cyanobacterial phycobilisomes and phycobiliproteins, Microbiology (Moscow), 2015, vol. 84, p. 101.

    CAS  Article  Google Scholar 

  25. 25

    Stadnichuk, I.N. and Tropin, I.V., Antenna replacement in the evolutionary origin of chloroplasts, Microbiology (Moscow), 2014, vol. 83, p. 299.

    CAS  Article  Google Scholar 

  26. 26

    Keely, B.G., Geochemistry of chlorophylls, in Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications, Grimm, B., Porra, R.J., Rüdiger, W., and Scheer, H., Eds., Dordrecht: Springer-Verlag, 2006, p. 535.

    Google Scholar 

  27. 27

    Granick, S., Speculations on the origins and evolution of photosynthesis, Ann. N.Y. Acad. Sci., 1957, vol. 69, p. 292.

    CAS  PubMed  Article  Google Scholar 

  28. 28

    Beale, S.I., Enzymes of chlorophyll biosynthesis, Photosynth. Res., 1999, vol. 60, p. 43.

    CAS  Article  Google Scholar 

  29. 29

    Oster, U., Tanaka, R., Tanaka, A., and Rüdiger, W., Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana, Plant J., 2000, vol. 21, p. 305.

    CAS  PubMed  Article  Google Scholar 

  30. 30

    South, G.R. and Whittick, A., An Introduction to Phycology, Chichester: Wiley, 1987.

    Google Scholar 

  31. 31

    Kusakin, O.G. and Drozdov, A.L., Filema organicheskogo mira. Chast’ 2. Prokaryota, Eukaryota (Fileme of the Organic World, Part 2: Prokaryota, Eukaryota), St. Petersburg: Nauka, 1987.

  32. 32

    Hausmann, K., Hülsmann, N., and Radek, R., Protistology, Stuttgart: Schweizerbart, 2003.

    Google Scholar 

  33. 33

    Cavalier-Smith, T., Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences, Protoplasma, 2017, vol. 255, p. 297. https://doi.org/10.1007/s00709-017-1147-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34

    Burki, F., Okamoto, N., Pombert, J.F., and Keeling, P.J., The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins, Proc. R. Soc. B, 2012, vol. 279, p. 2246. https://doi.org/10.1098/rspb.2011.2301

    Article  PubMed  Google Scholar 

  35. 35

    Keeling, P.J., The endosymbiotic origin diversification and fate of plastids, Philos. Trans. R. Soc. B, 2010, vol. 365, p. 792.

    Article  CAS  Google Scholar 

  36. 36

    Sánchez-Baracaldo, P., Raven, J.A., Pisani, D., and Knoll, A.H., Early photosynthetic eukaryotes inhabited low-salinity habitats, Proc. Natl. Acad. Sci. U.S.A., 2017, vol. 114, p. e7737.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  37. 37

    Donoghue, P. and Paps, J., Plant evolution: assembling land plants, Curr. Biol., 2020, vol. 30, p. R81. https://doi.org/10.1016/j.cub.2019.11.084

    CAS  Article  PubMed  Google Scholar 

  38. 38

    Lhee, D., Ha, J.-S. Kim, S., Park, M.G., Bhattacharya, D., and Yoon, H.S., Evolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species, Sci. Rep., 2019, vol. 9. 1https://doi.org/10.1038/s41598-019-38621-8

    CAS  Article  Google Scholar 

  39. 39

    Gibbs, S.P., The chloroplast of some algal groups may evolved from endosymbiotic eukaryotic algae, Ann. N.Y. Acad. Sci., 1981, vol. 361, p. 193.

    CAS  PubMed  Article  Google Scholar 

  40. 40

    Archibald, J.M., The puzzle of plastid evolution, Curr. Biol., 2009, vol. 19, p. R81.

    CAS  PubMed  Article  Google Scholar 

  41. 41

    Ludwig, M. and Gibbs, S.P., Evidence that the nucleomorphs of Chlororachnion reptans (Chlororachniophyceae) are vestigal nuclei: morphologi, division and DNA-DAPI fluorescence, J. Phycol., 1989, vol. 25, p. 385.

    Article  Google Scholar 

  42. 42

    Luo, Z., Hu, Z., Tang, Y., Mertens, K.N., Leaw, C.P., Lim, P.T., Teng, S.T., Wang, L., and Gu, H., Morphology, ultrastructure, and molecular phylogeny of Wangodinium sinense Gen. et sp. nov. (Gymnodiniales, Dinophyceae) and revisiting of Gymnodinium dorsalisulcum and Gymnodinium impudicum, J. Phycol., 2018, vol. 54, p. 744. https://doi.org/10.1111/jpy.12780

    Article  PubMed  Google Scholar 

  43. 43

    Sheiner, L., Vaidya, A.B., and McFadden, G.I., The metabolic roles of the endosymbiotic organelles of Toxoplasma and Plasmodium spp., Curr. Opin. Microbiol., 2013, vol. 16, p. 452.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. 44

    Striepen, B., The apicoplast: a red alga in human parasites, Essays Biochem., 2011, vol. 51, p. 111. https://doi.org/10.1042/BSE0510111

    CAS  Article  PubMed  Google Scholar 

  45. 45

    Smith, D.R. and Lee, R.W., A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella, Plant Physiol., 2014, vol. 164, p. 1812.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. 46

    Larkum, A.W.D., Light-harvesting systems in algae, in Photosynthesis of Algae, Larkum, A.W.D., Douglas, S.E., and Raven, J.A., Eds., Dordrecht: Springer-Verlag, 2003, p. 277.

    Google Scholar 

  47. 47

    Tomo, T. and Allakhverdiev S.I., The divergence of chlorophyll and photosynthetic reactions in chlorophyll d-containing algae, in Sovremennye problemy fotosineza (Contemporary Problems of Photosynthesis), Allakhverdiev, S.I., Rubin, A.B., and Shuvalov, V.A., Eds., Moscow, 2014, vol. 2, p. 115.

  48. 48

    Averina, S.G., Velichko, N.V., Pinevich, A.A., Senatskaya, E.V., and Pinevich, A.V., Non-a chlorophylls in cyanobacteria, Photosynthetica, 2019, vol. 57, p. 1109.

    CAS  Article  Google Scholar 

  49. 49

    Raven, J.A., Photosynthesis in watercolours, Nature, 2007, vol. 448, p. 418.

    CAS  PubMed  Article  Google Scholar 

  50. 50

    Glazer, A.N., Light guides. Directional energy transfer in a photosynthetic antenna, J. Biol. Chem., 1989, vol. 264, p. 1.

    CAS  PubMed  Article  Google Scholar 

  51. 51

    Raven, J.A., A cost-benefit analysis of photon absorption by photosynthetic unicells, New Phytol., 1984, vol. 98, p. 274.

    Google Scholar 

  52. 52

    Gorshkova, T.A., Rastitel’naya kletochnaya stenka kak dinamichnaya sistema (The Plant Cell Wall as the Dynamics System), Moscow: Nauka, 2007.

  53. 53

    Sarkar, P., Bosneaga, E., and Auer, M., Plant cell walls throughout evolution: towards a molecular understanding of their design principles, J. Exp. Bot., 2009, vol. 60, p. 3615.

    CAS  PubMed  Article  Google Scholar 

  54. 54

    Yong, W., O’Malley, R., and Link, B., Plant cell wall genomics, Planta., 2005, vol. 221, p. 745.

    Article  CAS  Google Scholar 

  55. 55

    Kuznetsov, V.V., The structure and expression of chloroplast genome, Fiziol. Rast., 2018, vol. 65, p. 243.

    Google Scholar 

  56. 56

    Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., Leister, D., Stoebe, B., Hasegawa, M., and Penny, D., Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus, Proc. Natl. Acad. Sci. U.S.A., 2002, vol. 99, p. 12246.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. 57

    Nakayama, T., Archibald, J.M., Evolving a photosynthetic organelle, BMC Biol., 2012. https://doi.org/10.1186/1741-7007-10-35

  58. 58

    Ponce-Toledo, R.I., López-Garcıa, P., and Moreira, D., Horizontal and endosymbiotic gene transfer in early plastid evolution, New Phytol., 2019, vol. 224, p. 618. https://doi.org/10.1111/nph.15965

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59

    Matsuo, M., Ito, Y., Yamauchi, R., and Obokata, J., The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplast–nuclear DNA flux, Plant Cell, 2005, vol. 17, p. 665.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. 60

    Allen, J.F., The CoRR hypothesis for genes in organelles, J. Theor. Biol., 2017, vol. 434, p. 50. https://doi.org/10.1016/j.jtbi.2017.04.008

    CAS  Article  PubMed  Google Scholar 

  61. 61

    Tripathi, D., Oldenburg, D.J., Nam, A., and Bendich, A.J., Reactive oxygen species, antioxidant agents, and DNA damage in developing maize mitochondria and plastids, Front. Plant Sci., 2020, vol. 11, p. 596. https://doi.org/10.3389/fpls.2020.00596

    Article  PubMed  PubMed Central  Google Scholar 

  62. 62

    Bendich, A.J., Why do chloroplasts and mitochondria contain so many copies of their genome? BioEssays, 1987, vol. 6, p. 279. https://doi.org/10.1002/bies.950060608

    CAS  Article  PubMed  Google Scholar 

  63. 63

    Danilenko, N.G. and Davydenko, O.G., Miry genomov organell (The World of Organelle Genomes), Minsk: Tekhnologiya, 2003.

  64. 64

    Ling, Q. and Jarvis, P., Regulation of chloroplast protein import by the ubiquitin E3 ligase SP1 is important for stress tolerance in plants, Curr. Biol., 2015, vol. 25, p. 1.

    Article  CAS  Google Scholar 

  65. 65

    Yurina, N.P. and Odintsova, M.S., Chloroplast retrograde signaling system, Russ. J. Plant Physiol., 2019, vol. 66, p. 509.

    CAS  Article  Google Scholar 

  66. 66

    Pfannschmidt, T., Terry, M.J., van Aken, O., and Quiros, P.M., Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells, Philos. Trans. R. Soc. B, 2020, vol. 375, art. ID 20190396. https://doi.org/10.1098/rstb.2019.0396

    CAS  Article  Google Scholar 

  67. 67

    Krupinska, K., Blanco, N.E., Oetke, S., and Zottini, M., Genome communication in plants mediated by organelle–nucleus-located proteins, Philos. Trans. R. Soc. B, 2020, vol. 375, art. ID e 20190397. https://doi.org/10.1098/rstb., 2019.0397

  68. 68

    Sinetova, M.A. and Los, D.A., Lessons from cyanobacterial transcriptomics: universal genes and triggers of stress responses, Mol. Biol. (Moscow), 2016, vol. 50, p. 606.

    CAS  Article  Google Scholar 

  69. 69

    Konstantinov, Yu.M., Dietrich, A., Weber-Lotfi, F., Ibrahim, N., Klimenko, E.S., Tarasenko, V.I., Bolotova, T.A., and Koulintchenko, M.V., DNA import into mitochondria, Biochemistry (Moscow), 2016, vol. 81, no. 10, p. 1044.

    CAS  PubMed  Google Scholar 

  70. 70

    Zilberg-Rosenberg, J. and Rosenberg, E., Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution, FEMS Microbiol. Rev., 2008, vol. 32, p. 723.

    Article  CAS  Google Scholar 

  71. 71

    Murakami, A., Miyashita, H., Iseki, M., Adachi, K., and Mimuro, M., Chlorophyll d in an epiphytic cyanobacterium of red algae, Science, 2004, vol. 303, p. 1633.

    CAS  PubMed  Article  Google Scholar 

  72. 72

    Nakayama, T., Kamikawa, R., Tanifuji, G., Kashiyama, Y., Ohkouchi, N., Archibald, J.M., and Inagaki, Y., Complete genome of a nonphotosynthetic cyanobacterium in a diatom reveals recent adaptations to an intracellular lifestyle, Proc. Natl. Acad. Sci. U.S.A., 2014, vol. 111, p. 11407.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. 73

    Adams, D.G., Bergman, B., Nierzwicki-Bauer, S.A., Duggan, P.S., Rai, A.N., and Schüßler, A., Cyanobacterial-plant symbioses, in The Prokaryotes: Prokaryotic Biology and Symbiotic Associations, Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F., Eds., New York: Springer-Verlag, 2002, p. 359.

    Google Scholar 

  74. 74

    Pinevich, A.V., Averina, S.G., and Velichko, N.V., Ocherki biologii prokhlorofitov (Biology of Prochlorophytes), St. Petersburg: S.-Peterb. Gos. Univ., 2010.

  75. 75

    Tuovinen, V., Ekman, S., Thor, G., Vanderpool, D., Spribille, T., and Johannesson, H., Two basidiomycete fungi in the cortex of wolf lichens, Curr. Biol., 2019, vol. 29, p. 476.

    CAS  PubMed  Article  Google Scholar 

  76. 76

    Spribille, T., Lichen symbionts outside of symbiosis: how do they find their match? A commentary on: ‘A case study on the re-establishment of the cyanolichen symbiosis: where do the compatible photobionts come from?’ Ann. Bot., 2019, vol. 124, p. 379.

    Article  Google Scholar 

  77. 77

    Johnson, M.D., The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles, Photosynth. Res., 2011, vol. 107, p. 117. https://doi.org/10.1007/s11120-010-9546-8

    CAS  Article  PubMed  Google Scholar 

  78. 78

    Stoecker, D.K., Hansen, P.J., Caron, D.A., and Mitra, A., Mixotrophy in the marine plankton, Ann. Rev. Mar. Sci., 2017, vol. 9, p. 311.

    PubMed  Article  Google Scholar 

  79. 79

    Klochkova, T.A., A review of the phenomenon of kleptoplasty in the marine posteriorbranch molluscs, Vestn. Kamchat. Gos. Tekh. Univ., 2016, no. 37, p. 57. https://doi.org/10.17217/2079-0333-2016-37-57-69

  80. 80

    Sage, R.F. and Stata, M., Photosynthetic diversity meets biodiversity: the C4 plant example, Plant Physiol., 2015, vol. 172, p. 104.

    CAS  Article  Google Scholar 

  81. 81

    Ivanishchev, V.V., Evolutionary aspects of C4 photosynthesis, Izv. Tul’sk. Gos. Univ., Estestv. Nauki, 2017, no. 3, p. 64.

  82. 82

    Folk, R.A., Soltis, P.S., Soltis, D.E., and Guralnick, R., New prospects in the detection and comparative analysis of hybridization in the tree of life, Am. J. Bot., 2018, vol. 105, p. 364.

    PubMed  Article  Google Scholar 

  83. 83

    Kiu, L.-X., Du, Y.-X., Folk, R.A., Wang, S.-Y., Soltis, D.E., Shang, F.-D., and Li, P., Plastome evolution in Saxifragaceae and multiple plastid capture events involving Heuchera and Tiarella, Front. Plant Sci., 2020, vol. 11, p. 361. https://doi.org/10.3389/fpls.2020.0036183

    Article  Google Scholar 

  84. 84

    Brillouet, J.M., Romieu, C., Schoefs, B., Solymosi, K., Cheynier, V., Fulcrand, H., Verdeil, J.L., and Conéjéro, G., The tannosome is an organelle forming condensed tannins in the chlorophyllous organs of Tracheophyta, Ann. Bot., 2013, vol. 112, p. 1003.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. 85

    Sineshchekov, V.A. and Belyaeva, O.B., Regulation of chlorophyll biogenesis by phytochrome A, Biochemistry (Moscow), 2019, vol. 84, no. 5, p. 491.

    CAS  PubMed  Google Scholar 

  86. 86

    Kuznetsov, V.V., doroshenko, A.S., Kudryakova, N.V., and Danilova, M.N., Role of phytohormones and light in de-etiolation, Russ. J. Plant Physiol., 2020, vol. 67, no. 6, p. 971.

    Article  Google Scholar 

  87. 87

    Jarvis, P. and López-Juez, E., Biogenesis and homeostasis of chloroplasts and other plastids, Nat. Rev. Mol. Cell Biol., 2014, vol. 27, p. 787.

    Google Scholar 

  88. 88

    Westwood, J.H., Yoder, J.I., Timko, M.P., and de Pamphilis, C.W., Evolution of parasitism in plants, Trends Plant Sci., 2010, vol. 15, p. 227.

    CAS  Article  Google Scholar 

  89. 89

    Filyushin, M.A., Kochieva, E.Z., Shchennikova, A.V., Beletsky, A.V., Mardanov, A.V., Ravin, N.V., and Skryabin, K.G., SWEET uniporter gene family expression profile in the pitcher development in the carnivorous plant Nepenthes sp., Russ. J. Genet., 2019, vol. 55, p. 692.

    CAS  Article  Google Scholar 

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This work was supported by the Russian Foundation for Basic Research, project no. 19-14-50366.

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Translated by A. Aver’yanov

Abbreviations: Chl—chlorophyll.

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Stadnichuk, I.N., Kusnetsov, V.V. Endosymbiotic Origin of Chloroplasts in Plant Cells’ Evolution. Russ J Plant Physiol 68, 1–16 (2021). https://doi.org/10.1134/S1021443721010179

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Keywords:

  • plastids
  • chloroplasts
  • cyanobacteria
  • evolution
  • endosymbiosis