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Regulation systems for stress responses in cyanobacteria

  • A. A. Zorina
  • K. S. Mironov
  • N. S. Stepanchenko
  • M. A. Sinetova
  • N. V. Koroban
  • V. V. Zinchenko
  • E. V. Kupriyanova
  • S. I. Allakhverdiev
  • D. A. Los
Reviews

Abstract

The article reviews the main systems that regulate gene expression in cyanobacteria in response to various treatments: low and high temperatures, salt, hyperosmotic and oxidative stresses. The systems for perception of light are also reviewed. Functional characteristics are presented for known two-component regulatory systems, eukaryotic-type serine-threonine protein kinases, σ-subunits of RNA-polymerase, DNA-binding transcription factors. Different mechanisms of perception of stress signals are analyzed, including changes in DNA supercoiling under different stress conditions.

Keywords

cyanobacteria gene expression histidine kinases sensors serine-threonine protein kinases stress transcription factors 

Abbreviations

HSP

heat shock protein

STPK

serine-threonine protein kinase

TF

transcription factors

Hik

histidine kinase

Rre

response regulator

References

  1. 1.
    Zavarzin, G.A., Formation of Biosphere, Vestn. Ross. Akad. Nauk, 2001, vol. 71, pp. 988–1001.Google Scholar
  2. 2.
    Carr, N.G. and Whitton, B.A., The Biology of Cyanobacteria, Berkely, Los Angeles: Univ. California Press; Blackwell, 1982.Google Scholar
  3. 3.
    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. USA, 2002, vol. 99, pp. 12 246–12 251.Google Scholar
  4. 4.
    Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M., and Tabata, S., Sequence Analysis of the Genome of the Unicellular Cyanobacterium Synechocystis sp. Strain PCC 6803: 2. Sequence Determination of the Entire Genome and Assignment of Potential Protein-Coding Regions (Supplement), DNA Res., 1996, vol. 3, pp. 185–209.PubMedCrossRefGoogle Scholar
  5. 5.
    Kaneko, T., Nakamura, Y., Wolk, C.P., Kuritz, T., Sasamoto, S., Watanabe, A., Iriguchi, M., Ishikawa, A., Kawashima, K., Kimura, T., Kishida, Y., Kohara, M., Matsumoto, M., Matsuno, A., Muraki, A., Nakazaki, N., Shimpo, S., Sugimoto, M., Takazawa, M., Yamada, M., Yasuda, M., and Tabata, S., Complete Genomic Sequence of the Filamentous Nitrogen-Fixing Cyanobacterium Anabaena sp. Strain PCC 7120, DNA Res., 2001, vol. 8, pp. 205–213.PubMedCrossRefGoogle Scholar
  6. 6.
    Nakamura, Y., Kaneko, T., Sato, S., Ikeuchi, M., Katoh, H., Sasamoto, S., Watanabe, A., Iriguchi, M., Kawashima, K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeuchi, C., Yamada, M., and Tabata, S., Complete Genome Structure of the Thermophilic Cyanobacterium Thermosynechococcus elongatus BP-1 (Supplement), DNA Res., 2002, vol. 9, pp. 135–148.PubMedCrossRefGoogle Scholar
  7. 7.
    Nakamura, Y., Kaneko, T., Sato, S., Mimuro, M., Miyashita, H., Tsuchiya, T., Sasamoto, S., Watanabe, A., Kawashima, K., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Nakazaki, N., Shimpo, S., Takeuchi, C., Yamada, M., and Tabata, S., Complete Genome Structure of Gloeobacter violaceus PCC 7421, a Cyanobacterium That Lacks Thylakoids (Supplement), DNA Res., 2003, vol. 10, pp. 181–201.PubMedCrossRefGoogle Scholar
  8. 8.
    Palenik, B., Brahamsha, B., Larimer, F.W., Land, M., Hauser, L., Chain, P., Lamerdin, J., Regala, W., Allen, E.E., McCarren, J., Paulsen, I., Dufresne, A., Partensky, F., Webb, E.A., and Waterbury, J., The Genome of a Motile Marine Synechococcus, Nature, 2003, vol. 424, pp. 1037–1042.PubMedCrossRefGoogle Scholar
  9. 9.
    Kaneko, T., Nakajima, N., Okamoto, S., Suzuki, I., Tanabe, Y., Tamaoki, M., Nakamura, Y., Kasai, F., Watanabe, A., Kawashima, K., Kishida, Y., Ono, A., Shimizu, Y., Takahashi, C., Minami, C., Fujishiro, T., Kohara, M., Katoh, M., Nakazaki, N., Nakayama, S., Yamada, M., Tabata, S., and Watanabe, M.M., Complete Genomic Structure of the Bloom-Forming Toxic Cyanobacterium Microcystis aeruginosa NIES-843, DNA Res., 2007, vol. 14, pp. 247–256.PubMedCrossRefGoogle Scholar
  10. 10.
    Swingley, W.D., Chen, M., Cheung, P.C., Conrad, A.L., Dejesa, L.C., Hao, J., Honchak, B.M., Karbach, L.E., Kurdoglu, A., Lahiri, S., Mastrian, S.D., Miyashita, H., Page, L., Ramakrishna, P., Satoh, S., Sattley, W.M., Shimada, Y., Taylor, H.L., Tomo, T., Tsuchiya, T., Wang, Z.T., Raymond, J., Mimuro, M., Blankenship, R.E., and Touchman, J.W., Niche Adaptation and Genome Expansion in the Chlorophyll d-Producing Cyanobacterium Acaryochloris marina, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 2005–2010.PubMedCrossRefGoogle Scholar
  11. 11.
    Fujisawa, T., Narikawa, R., Okamoto, S., Ehira, S., Yoshimura, H., Suzuki, I., Masuda, T., Mochimaru, M., Takaichi, S., Awai, K., Sekine, M., Horikawa, H., Yashiro, I., Omata, S., Takarada, H., Katano, Y., Kosugi, H., Tanikawa, S., Ohmori, K., Sato, N., Ikeuchi, M., Fujita, N., and Ohmori, M., Genomic Structure of an Economically Important Cyanobacterium, Arthrospira (Spirulina) platensis NIES-39, DNA Res., 2010, vol. 17, pp. 85–103.PubMedCrossRefGoogle Scholar
  12. 12.
    Kaneko, T., Nakamura, Y., Sasamoto, S., Watanabe, A., Kohara, M., Matsumoto, M., Shimpo, S., Yamada, M., and Tabata, S., Structural Analysis of Four Large Plasmids Harboring in a Unicellular Cyanobacterium, Synechocystis sp. PCC 6803, DNA Res., 2003, vol. 10, pp. 221–228.PubMedCrossRefGoogle Scholar
  13. 13.
    Sato, N., Ohmori, M., Ikeuchi, M., Tashiro, K., Wolk, C.P., Kaneko, T., Okada, K., Tsuzuki, M., Ehira, S., Katoh, H., Okamoto, S., Yoshimura, H., Fujisawa, T., Kamei, A., Yoshihara, S., Narikawa, R., Hamano, T., Tabata, S., and Kuhara, S., Use of Segment-Based Microarray in the Analysis of Global Gene Expression in Response to Various Environmental Stresses in the Cyanobacterium Anabaena sp. PCC 7120, J. Gen. Appl. Microbiol., 2004, vol. 50, pp. 1–8.PubMedCrossRefGoogle Scholar
  14. 14.
    Ehira, S., Ohmori, M., and Sato, N., Genome-Wide Expression Analysis of the Responses to Nitrogen Deprivation in the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120, DNA Res., 2003, vol. 10, pp. 97–113.PubMedCrossRefGoogle Scholar
  15. 15.
    Suzuki, I., Kanesaki, Y., Mikami, K., Kanehisa, M., and Murata, N., Cold-Regulated Genes under Control of the Cold Sensor Hik33 in Synechocystis, Mol. Microbiol., 2001, vol. 40, pp. 235–244.PubMedCrossRefGoogle Scholar
  16. 16.
    Mikami, K., Kanesaki, Y., Suzuki, I., and Murata, N., The Histidine Kinase Hik33 Perceives Osmotic Stress and Cold Stress in Synechocystis sp. PCC 6803, Mol. Microbiol., 2002, vol. 46, pp. 905–915.PubMedCrossRefGoogle Scholar
  17. 17.
    Los, D.A. and Murata, N., Responses to Cold Shock in Cyanobacteria, J. Mol. Microbiol. Biotechnol., 1999, vol. 1, pp. 221–230.PubMedGoogle Scholar
  18. 18.
    Los, D.A. and Murata, N., Sensing and Response to Low Temperature in Cyanobacteria, Cell and Molecular Responses to Stress, Sensing, Signaling and Cell Adaptation, vol. 3, Storey, K.B. and Storey, J.V., Eds, Amsterdam: Elsevier, 2002, pp. 139–153.CrossRefGoogle Scholar
  19. 19.
    Los, D.A., Suzuki, I., Zinchenko, V.V., and Murata, N., Stress Responses in Synechocystis: Regulated Genes and Regulatory Systems, The Cyanobacteria: Molecular Biology, Genomics and Evolution, Herrero, A. and Flores, E., Eds, Norfolk: Caister Academic, 2008, pp. 117–157.Google Scholar
  20. 20.
    Los, D.A., Ray, M.K., and Murata, N., Differences in the Control of the Temperature-Dependent Expression of Four Genes for Desaturases in Synechocystis sp. PCC 6803, Mol. Microbiol., 1997, vol. 25, pp. 1167–1175.PubMedCrossRefGoogle Scholar
  21. 21.
    Inaba, M., Suzuki, I., Szalontai, B., Kanesaki, Y., Los, D.A., Hayashi, H., and Murata, N., Gene-Engineered Rigidification of Membrane Lipids Enhances the Cold Inducibility of Gene Expression in Synechocystis, J. Biol. Chem., 2003, vol. 278, pp. 12 191–12 198.Google Scholar
  22. 22.
    Los, D.A. and Zinchenko, V.V., Regulatory Role of Membrane Fluidity in Gene expression, Lipids in Photosynthesis. Essential and Regulatory Functions, Wada, H. and Murata, N., Eds, Dordrecht: Springer Science + Business Media B.V., 2009, pp. 329–348.Google Scholar
  23. 23.
    Los, D.A., Zorina, A., Sinetova, M., Kryazhov, S., Mironov, K., and Zinchenko, V.V., Stress Sensors and Signal Transducers in Cyanobacteria, Sensors, 2010, vol. 10, pp. 2386–2415.CrossRefGoogle Scholar
  24. 24.
    Allakhverdiev, S.I., Sakamoto, A., Nishiyama, Y., Inaba, M., and Murata, N., Ionic and Osmotic Effects of NaCl-Induced Inactivation of Photosystems I and II in Synechococcus sp., Plant Physiol., 2000, vol. 123, pp. 1047–1056.PubMedCrossRefGoogle Scholar
  25. 25.
    Allakhverdiev, S.I., Sakamoto, A., Nishiyama, Y., and Murata, N., Inactivation of Photosystems I and II in Response to Osmotic Stress in Synechococcus. Contribution of Water Channels, Plant Physiol., 2000, vol. 122, pp. 1201–1208.PubMedCrossRefGoogle Scholar
  26. 26.
    Allakhverdiev, S.I., Nishiyama, Y., Miyairi, S., Yamamoto, H., Inagaki, N., Kanesaki, Y., and Murata, N., Salt Stress Inhibits the Repair of Photo-damaged Photosystem II by Suppressing the Transcription and Translation of psbA2 Genes in Synechocystis, Plant Physiol., 2002, vol. 130, pp. 1443–1453.PubMedCrossRefGoogle Scholar
  27. 27.
    Allakhverdiev, S.I. and Murata, N., Salt Stress Inhibits Photosystems II and I in Cyanobacteria, Photosynth. Res., 2008, vol. 98, pp. 529–539.PubMedCrossRefGoogle Scholar
  28. 28.
    Kanesaki, Y., Suzuki, I., Allakhverdiev, S.I., Mikami, K., and Murata, N., Salt Stress and Hyperosmotic Stress Regulate the Expression of Different Sets of Genes in Synechocystis sp. PCC 6803, Biochem. Biophys. Res. Commun., 2002, vol. 290, pp. 339–348.PubMedCrossRefGoogle Scholar
  29. 29.
    Paithoonrangsarid, K., Shoumskaya, M.A., Kanesaki, Y., Satoh, S., Tabata, S., Los, D.A., Zinchenko, V.V., Hayashi, H., Tanticharoen, M., Suzuki, I., and Murata, N., Five Histidine Kinases Perceive Osmotic Stress and Regulate Distinct Sets of Genes in Synechocystis, J. Biol. Chem., 2004, vol. 279, pp. 53078–53086.PubMedCrossRefGoogle Scholar
  30. 30.
    Shoumskaya, M.A., Paithoonrangsarid, K., Kanesaki, Y., Los, D.A., Zinchenko, V.V., Tanticharoen, M., Suzuki, I., and Murata, N., Identical Hik-Rre Systems Are Involved in Perception and Transduction of Salt Signals and Hyperosmotic Signals But Regulate the Expression of Individual Genes to Different Extents in Synechocystis, J. Biol. Chem., 2005, vol. 280, pp. 21531–21538.PubMedCrossRefGoogle Scholar
  31. 31.
    Shapiguzov, A., Lyukevich, A.A., Allakhverdiev, S.I., Sergeyenko, T.V., Suzuki, I., Murata, N., and Los, D.A., Osmotic Shrinkage of Cells of Synechocystis sp. PCC 6803 by Water Efflux via Aquaporins Regulates Osmostress-Inducible Gene Expression, Microbiology, 2005, vol. 151, pp. 447–455.PubMedCrossRefGoogle Scholar
  32. 32.
    Suzuki, I., Kanesaki, Y., Hayashi, H., Hall, J.J., Simon, W.J., Slabas, A.R., and Murata, N., The Histidine Kinase Hik34 Is Involved in Thermotolerance by Regulating the Expression of Heat Shock Genes in Synechocystis, Plant Physiol., 2005, vol. 138, pp. 1409–1421.PubMedCrossRefGoogle Scholar
  33. 33.
    Suzuki, I., Simon, W.J., and Slabas, A.R., The Heat Shock Response of Synechocystis sp. PCC 6803 Analyzed by Transcriptomics and Proteomics, J. Exp. Bot., 2006, vol. 57, pp. 1573–1578.PubMedCrossRefGoogle Scholar
  34. 34.
    Kanesaki, Y., Yamamoto, H., Paithoonrangsarid, K., Shoumskaya, M., Suzuki, I., Hayashi, H., and Murata, N., Histidine Kinases Play Important Roles in the Perception and Signal Transduction of Hydrogen Peroxide in the Cyanobacterium, Synechocystis sp. PCC 6803, Plant J., 2007, vol. 49, pp. 313–324.PubMedCrossRefGoogle Scholar
  35. 35.
    Hihara, Y., Kamei, A., Kanehisa, M., Kaplan, A., and Ikeuchi, M., DNA Microarray Analysis of Cyanobacterial Gene Expression during Acclimation to High Light, Plant Cell, 2001, vol. 13, pp. 793–806.PubMedCrossRefGoogle Scholar
  36. 36.
    Huang, L., McCluskey, M.P., Ni, H., and La Rossa, R.A., Global Gene Expression Profiles of the Cyanobacterium Synechocystis sp. Strain PCC 6803 in Response to Irradiation with UV-B and White Light, J. Bacteriol., 2002, vol. 184, pp. 6845–6858.PubMedCrossRefGoogle Scholar
  37. 37.
    Suzuki, I., Los, D.A., Kanesaki, Y., Mikami, K., and Murata, N., The Pathway for Perception and Transduction of Low-Temperature Signals in Synechocystis, EMBO J., 2000, vol. 19, pp. 1327–1334.PubMedCrossRefGoogle Scholar
  38. 38.
    Kappell, A.D. and van Waasbergen, L.G., The Response Regulator RpaB Binds the High Light Regulatory 1 Sequence Upstream of the High-Light-Inducible hliB Gene from the Cyanobacterium Synechocystis PCC 6803, Arch. Microbiol., 2007, vol. 187, pp. 337–342.PubMedCrossRefGoogle Scholar
  39. 39.
    Sakayori, T., Shiraiwa, Y., and Suzuki, I., A Synechocystis Homolog of SipA Protein, Ssl3451, Enhances the Activity of the Histidine Kinase Hik33, Plant Cell Physiol., 2009, vol. 50, pp. 1439–1448.PubMedCrossRefGoogle Scholar
  40. 40.
    Yamaguchi, K., Suzuki, I., Yamamoto, H., Lyukevich, A., Bodrova, I., Los, D.A., Piven, I., Zinchenko, V., Kanehisa, M., and Murata, N., A Two-Component Mn2+-Sensing System Negatively Regulates Expression of the mntCAB Operon in Synechocystis, Plant Cell, 2002, vol. 14, pp. 2901–2913.PubMedCrossRefGoogle Scholar
  41. 41.
    Kehoe, D.M. and Grossman, A.R., Similarity of a Chromatic Adaptation Sensor to Phytochrome and Ethylene Receptors, Science, 1996, vol. 273, pp. 1409–1412.PubMedCrossRefGoogle Scholar
  42. 42.
    Kehoe, D.M. and Gutu, A., Responding to Color: The Regulation of Complementary Chromatic Adaptation, Annu. Rev. Plant Biol., 2006, vol. 57, pp. 127–150.PubMedCrossRefGoogle Scholar
  43. 43.
    Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gartner, W., Wilde, A., and Borner, T., A Prokaryotic Phytochrome, Nature, 1997, vol. 386, p. 663.PubMedCrossRefGoogle Scholar
  44. 44.
    Hubschmann, T., Yamamoto, H., Gieler, T., Murata, N., and Borner, T., Red and Far-Red Light Alter the Transcript Profile in the Cyanobacterium Synechocystis sp. PCC 6803: Impact of Cyanobacterial Phytochromes, FEBS Lett., 2005, vol. 579, pp. 1613–1618.PubMedCrossRefGoogle Scholar
  45. 45.
    Ulijasz, A.T., Cornilescu, G., von S.D., Cornilescu, C., Velazquez, E.F., Zhang, J., Stankey, R.J., Rivera, M., Hildebrandt, P., and Vierstra, R.D., Cyanochromes Are Blue/Green Light Photoreversible Photoreceptors Defined by a Stable Double Cysteine Linkage to a Phycoviolobilin-Type Chromophore, J. Biol. Chem., 2009, vol. 284, pp. 29 757–29 772.CrossRefGoogle Scholar
  46. 46.
    Ikeuchi, M. and Ishizuka, T., Cyanobacteriochromes: A New Superfamily of Tetrapyrrole-Binding Photoreceptors in Cyanobacteria, Photochem. Photobiol. Sci., 2008, vol. 7, pp. 1159–1167.PubMedCrossRefGoogle Scholar
  47. 47.
    Takai, N., Nakajima, M., Oyama, T., Kito, R., Sugita, C., Sugita, M., Kondo, T., and Iwasaki, H., A KaiC-Associating SasA-RpaA Two-Component Regulatory System as a Major Circadian Timing Mediator in Cyanobacteria, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 12 109–12 114.CrossRefGoogle Scholar
  48. 48.
    Vogeley, L., Sineshchekov, O.A., Trivedi, V.D., Sasaki, J., Spudich, J.L., and Luecke, H., Anabaena Sensory Rhodopsin: A Photochromic Color Sensor at 2.0 A, Science, 2004, vol. 306, pp. 1390–1393.PubMedCrossRefGoogle Scholar
  49. 49.
    Nazarenko, L.V., Andreev, I.M., Lyukevich, A.A., Pisareva, T.V., and Los, D.A., Calcium Release from Synechocystis Cells Induced by Depolarization of the Plasma Membrane: MscL as an Outward Ca2+ Channel, Microbiology, 2003, vol. 149, pp. 1147–1153.PubMedCrossRefGoogle Scholar
  50. 50.
    Panichkin, V.B., Rakawa-Kobayashi, S., Kanaseki, T., Suzuki, I., Los, D.A., Shestakov, S.V., and Murata, N., Serine/Threonine Protein Kinase SpkA in Synechocystis sp. Strain PCC 6803 Is a Regulator of Expression of Three Putative pilA Operons, Formation of Thick Pili, and Cell Motility, J. Bacteriol., 2006, vol. 188, pp. 7696–7699.PubMedCrossRefGoogle Scholar
  51. 51.
    Zorina, A., Stepanchenko, N., Sinetova, M., Panichkin, V.B., Novikova, G.V., Moshkov, I.E., Zinchenko, V.V., Shestakov, S.V., Suzuki, I., Murata, N., and Los, D.A., Eukaryotic-Like Ser/Thr Protein Kinases SpkC/F/K Are Involved in Phosphorylation of GroES in the Cyanobacterium Synechocystis, DNA Res., 2011, vol. 18, pp. 137–151.PubMedCrossRefGoogle Scholar
  52. 52.
    Osanai, T., Kanesaki, Y., Nakano, T., Takahashi, H., Asayama, M., Shirai, M., Kanehisa, M., Suzuki, I., Murata, N., and Tanaka, K., Positive Regulation of Sugar Catabolic Pathways in the Cyanobacterium Synechocystis sp. PCC 6803 by the Group 2 Sigma Factor SigE, J. Biol. Chem., 2005, vol. 280, pp. 30653–30659.PubMedCrossRefGoogle Scholar
  53. 53.
    Osanai, T., Imamura, S., Asayama, M., Shirai, M., Suzuki, I., Murata, N., and Tanaka, K., Nitrogen Induction of Sugar Catabolic Gene Expression in Synechocystis sp. PCC 6803, DNA Res., 2006, vol. 13, pp. 185–195.PubMedCrossRefGoogle Scholar
  54. 54.
    Osanai, T., Imashimizu, M., Seki, A., Sato, S., Tabata, S., Imamura, S., Asayama, M., Ikeuchi, M., and Tanaka, K., ChlH, the H Subunit of the Mg-Chelatase, Is an Anti-Sigma Factor for SigE in Synechocystis sp. PCC 6803, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 6860–6865.PubMedCrossRefGoogle Scholar
  55. 55.
    Prakash, J.S., Sinetova, M., Zorina, A., Kupriyanova, E., Suzuki, I., Murata, N., and Los, D.A., DNA Supercoiling Regulates the Stress-Inducible Expression of Genes in the Cyanobacterium Synechocystis, Mol. Biosyst., 2009, vol. 5, pp. 1904–1912.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • A. A. Zorina
    • 1
  • K. S. Mironov
    • 1
  • N. S. Stepanchenko
    • 1
  • M. A. Sinetova
    • 1
  • N. V. Koroban
    • 2
  • V. V. Zinchenko
    • 2
  • E. V. Kupriyanova
    • 1
  • S. I. Allakhverdiev
    • 1
    • 3
  • D. A. Los
    • 1
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Biological FacultyMoscow State UniversityMoscowRussia
  3. 3.Institute for Basic Biological ProblemsPuschino, Moscow oblastRussia

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