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Peptides of the Innate Immune System of Plants. Part I. Structure, Biological Activity, and Mechanisms of Action

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Abstract

A plant immune system is able to rapidly react in response to changes in environmental conditions and provides protection against stress, pathogens, and insects. In the case of infection, plants synthesize many pathogenesis-associated compounds, including various peptides. These peptides not only have the antimicrobial activity and enhance each other’s action but participate in a complex of defense strategies as well. Peptide factors of the plant’s innate immune system have a diverse structural organization and exhibit a wide spectrum of biological activities, including antimicrobial, antiviral, antitumor, insecticidal, antiinflammatory, antiproliferative, mitogenic, and analgesic. Some of them take part in binding and transfer of lipids, whereas the others exhibit the properties of ion-channel blockers or inhibitors of proteases and α-amylases but have no toxic effect on their own and mammalian cells. Some parts of plant peptides are clinically significant food or pollen allergens. All the abovementioned facts make them attractive objects for a detailed investigation and possible practical application to various aspects of human life. This review summarizes data on a diversity of structures, biological activity, and mechanisms of the antimicrobial action of the peptides of the plant’s innate immune system.

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Abbreviations

AMPs:

antimicrobial peptides

BBI:

Bowman-Birk Inhibitors

ChBD:

Chitin-Binding Domain

DAMP:

Damage-Associated Molecular Pattern

LTP:

Lipid-Transfer Proteins

MAPK:

Mitogen-Activated Protein Kinase)

PAMP:

Pathogen-Associated Molecular Pattern

PR-:

Pathogenesis-Related Protein

ROS:

Reactive Oxygen Species

SAR:

Systemic Acquired Resistance

References

  1. Nürnberger, T., Brunner, F., Kemmerling, B., and Piater, L., Immunol. Rev., 2004, vol. 198, pp. 249–266.

    Article  PubMed  Google Scholar 

  2. Ranf, S., Curr. Opin. Plant Biol., 2017, vol. 38, pp. 68–77.

    Article  CAS  PubMed  Google Scholar 

  3. He, Y., Zhou, J., Shan, L., and Meng, X., J. Cell Sci., 2018, vol. 131. pii jcs209353. doi 10.1242/jcs.209353

    Google Scholar 

  4. Zhang, X., Dodds, P.N., and Bernoux, M., Annu. Rev. Phytopathol., 2017, vol. 55, pp. 205–229.

    Article  CAS  PubMed  Google Scholar 

  5. Kachroo, A., Vincelli, P., and Kachroo, P., Phytopathology, 2017, vol. 107, pp. 1452–1461.

    Article  CAS  PubMed  Google Scholar 

  6. Birkenbihl, R.P., Liu, S., and Somssich, I.E., Curr. Opin. Plant Biol., 2017, vol. 38, pp. 1–9.

    Article  CAS  PubMed  Google Scholar 

  7. Golshani, F., Fakheri, B.A., Behshad, E., and Vashvaei, R.M., Biol. Forum Int. J., 2015, vol. 7, pp. 477–495.

    CAS  Google Scholar 

  8. Wong, J.H., Ng, T.B., Cheung, R.C., Ye, X.J., Wang, H.X., Lam, S.K., Lin, P., Chan, Y.S., Fang, E.F., Ngai, P.H., Xia, L.X., Ye, X.Y., Jiang, Y., and Liu, F., Appl. Microbiol. Biotechnol., 2010, vol. 87, pp. 1221–1235.

    Article  CAS  PubMed  Google Scholar 

  9. Tam, J.P., Wang, S., Wong, K.H., and Tan, W.L., Pharmaceut. (Basel), 2015, vol. 8, pp. 711–757.

    Article  CAS  Google Scholar 

  10. Bolouri Moghaddam, M.R., Vilcinskas, A., and Rahnamaeian, M., Mol. Plant Pathol., 2016, vol. 17, pp. 464–471.

    Article  CAS  PubMed  Google Scholar 

  11. Broekaert, W., Terras, F.R., Cammue, B.P., and Osborn, R.W., Plant Physiol., 1995, vol. 108, pp. 1353–1358.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Finkina, E.I., Shramova, E.I., Tagaev, A.A., and Ovchinnikova, T.V., Biochem. Biophys. Res. Commun., 2008, vol. 371, pp. 860–865.

    Article  CAS  PubMed  Google Scholar 

  13. Janssen, B.J., Schirra, H.J., Lay, F.T., Anderson, M.A., and Craik, D.J., Biochemistry, 2003, vol. 42, pp. 8214–8222.

    Article  CAS  PubMed  Google Scholar 

  14. Shenkarev, Z.O., Gizatullina, A.K., Finkina, E.I., Alekseeva, E.A., Balandin, S.V., Mineev, K.S., Arseniev, A.S., and Ovchinnikova, T.V., Biochem. Biophys. Res. Commun., 2014, vol. 451, pp. 252–257.

    Article  CAS  PubMed  Google Scholar 

  15. Léonard, R., Wopfner, N., Pabst, M., Stadlmann, J., Petersen, B.O., Duus, J.O., Himly, M., Radauer, C., Gadermaier, G., Razzazi-Fazeli, E., et al., J. Biol. Chem., 2010, vol. 285, pp. 27192–27200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Vriens, K., Cools, T.L., Harvey, P.J., Craik, D.J., Braem, A., Vleugels, J., De Coninck, B., Cammue, B.P., and Thevissen, K., Peptides, 2016, vol. 75, pp. 71–79.

    Article  CAS  PubMed  Google Scholar 

  17. Vriens, K., Peigneur, S., De Coninck, B., Tytgat, J., Cammue, B.P., and Thevissen, K., Sci. Rep., 2016. doi 10.1038/srep32121

    Google Scholar 

  18. Chen, G.H., Hsu, M.P., Tan, C.H., Sung, H.Y., Kuo, C.G., Fan, M.J., Chen, H.M., Chen, S., and Chen, C.S., J. Agric. Food Chem., 2005, vol. 53, pp. 982–988.

    Article  CAS  PubMed  Google Scholar 

  19. Anaya-López, J.L., López-Meza, J.E., Baizabal-Aguirre, V.M., Cano-Camacho, H., and Ochoa-Zarzosa, A., Biotechnol. Lett., 2006, vol. 28, pp. 1101–1108.

    Article  CAS  PubMed  Google Scholar 

  20. Wong, J.H., Zhang, X.Q., Wang, H.X., and Ng, T.B., Peptides, 2006, vol. 27, pp. 2075–2081.

    Article  CAS  PubMed  Google Scholar 

  21. Díaz-Murillo, V., Medina-Estrada, I., López-Meza, J.E., and Ochoa-Zarzosa, A., Peptides, 2016, vol. 78, pp. 109–118.

    Article  CAS  PubMed  Google Scholar 

  22. Sarkar, P., Jana, J., Chatterjee, S., and Sikdar, S.R., Springerplus, 2016. doi 10.1186/s40064-016-2144-2142

    Google Scholar 

  23. Stec, B., Cell Mol. Life Sci., 2006, vol. 63, pp. 1370–1385.

    Article  CAS  PubMed  Google Scholar 

  24. Bohlmann, H. and Apel, K., Mol. Gen. Genet., 1987, vol. 207, pp. 446–454.

    Article  CAS  Google Scholar 

  25. Sauviat, M.P., Toxicon, 1990, vol. 28, pp. 83–89.

    Article  CAS  PubMed  Google Scholar 

  26. Stein, G.M., Bussing, A., Schaller, G., Pfuller, U., and Schietzel, M., Ann. Oncol., 1998, vol. 9, p. 87.

    Article  Google Scholar 

  27. Schmidt, A., Teeter, M., Weckert, E., and Lamzin, V.S., Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun., 2011, vol. 67, pp. 424–428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Castagnaro, A., Segura, A., and Garciaolmedo, F., Plant Physiol., 1995, vol. 107, pp. 1475–1476.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Florack, D.E.A. and Stiekema, W.J., Plant. Mol. Biol., 1994, vol. 26, pp. 25–37.

    Article  CAS  PubMed  Google Scholar 

  30. Bohlmann, H., Clausen, S., and Behnke, S., EMBO J., 1988, vol. 7, pp. 1559–1565.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Broekaert, W.F., Cammue, B.P.A., De Bolle, M.F.C., Thevissen, K., De Samblanx, G.W., and Osborn, R.W., Crit. Rev. Plant Sci., 1997, vol. 16, pp. 297–323.

    Article  CAS  Google Scholar 

  32. Báez-Magaña, M., Díaz-Murillo, V., López-Meza, J.E., and Ochoa-Zarzosa, A., Int. Immunopharmacol., 2018, vol. 57, pp. 47–54.

    Article  CAS  PubMed  Google Scholar 

  33. Edstam, M.M., Viitanen, L., Salminen, T.A., and Edqvist, J., Mol. Plant, 2011, vol. 4, pp. 947–964.

    Article  CAS  PubMed  Google Scholar 

  34. Palacin, A., Varela, J., Quirce, S., del Pozo, V., Tordesillas, L., Barranco, P., Fernandez-Nieto, M., Sastre, J., Diaz-Perales, A., and Salcedo, G., Clin. Exp. Allergy, 2009, vol. 39, pp. 1267–1276.

    Article  CAS  PubMed  Google Scholar 

  35. Bogdanov, I.V., Shenkarev, Z.O., Finkina, E.I., Melnikova, D.N., Rumynskiy, E.I., Arseniev, A.S., and Ovchinnikova, T.V., BMC Plant Biol., 2016, vol. 16, p. 107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Samuel, D., Liu, Y.J., Cheng, C.S., and Lyu, P.C., J. Biol. Chem., 2002, vol. 277, pp. 35267–35273.

    Article  CAS  PubMed  Google Scholar 

  37. Finkina, E.I., Melnikova, D.N., Bogdanov, I.V., and Ovchinnikova, T.V., Acta Naturae, 2016, vol. 8, pp. 47–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Finkina, E.I., Melnikova, D.N., Bogdanov, I.V., and Ovchinnikova, T.V., Curr. Med. Chem., 2017, vol. 24, pp. 1772–1787.

    Article  CAS  PubMed  Google Scholar 

  39. Diz, M.S., Carvalho, A.O., Ribeiro, S.F., Da Cunha M., Beltramini, L., Rodrigues, R., Nascimento, V.V., Machado, O.L., and Gomes, V.M., Physiol. Plant., 2011, vol. 142, pp. 233–246.

    Article  CAS  PubMed  Google Scholar 

  40. Zottich, U., Da Cunha, M., Carvalho, A.O., Dias, G.B., Silva, N.C., Santos, I.S., do Nacimento, V.V., Miguel, E.C., Machado, O.L., and Gomes, V.M., Biochim. Biophys. Acta, 2011, vol. 1810, pp. 375–383.

    Article  CAS  PubMed  Google Scholar 

  41. Ooi, L.S., Tian, L., Su, M., Ho, W.S., Sun, S.S., Chung, H.Y., Wong, H.N., and Ooi, V.E., Peptides, 2008, vol. 29, pp. 2101–2109.

    Article  CAS  PubMed  Google Scholar 

  42. Lin, P., Xia, L., Wong, J.H., Ng, T.B., Ye, X., Wang, S., and Shi, X., J. Pept. Sci., 2007, vol. 13, pp. 642–648.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Sawano, Y., Hatano, K., Miyakawa, T., Komagata, H., Miyauchi, Y., Yamazaki, H., and Tanokura, M., Plant Physiol., 2008, vol. 146, pp. 1909–1919.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Crimi, M., Astegno, A., Zoccatelli, G., and Esposti, M.D., Arch. Biochem. Biophys., 2006, vol. 445, pp. 65–71.

    Article  CAS  PubMed  Google Scholar 

  45. Campos, D.C., Costa, A.S., Lima, A.D., Silva, F.D., Lobo, M.D., Monteiro-Moreira, A.C., Moreira, R.A., Leal, L.K., Miron, D., Vasconcelos, I.M., et al., Int. J. Biol. Macromol., 2016, vol. 86, pp. 71–79.

    Article  CAS  PubMed  Google Scholar 

  46. Postic, G., Gracy, J., Perin, Ch., Chiche, L., and Gelly, J.-Ch., Nucleic Acids Res., 2018, vol. 46, pp. D454–D458. doi 10.1093/nar/gkx1084

    Google Scholar 

  47. Molesini, B., Treggiari, D., Dalbeni, A., Minuz, P., and Pandolfini, T., Br. J. Clin. Pharmacol., 2017, vol. 83, pp. 63–70.

    Article  CAS  PubMed  Google Scholar 

  48. Kolmar, H., Curr. Opin. Pharmacol., 2009, vol. 9, pp. 608–614.

    Article  CAS  PubMed  Google Scholar 

  49. Cammue, B.P.A., De Bolle, M.F., Terras, F.R.G., Van Damme, P.P.J., Rees, S.B., Vanderleyden, J., and Broekaert, W.F., J. Biol. Chem., 1992, vol. 267, pp. 2228–2233.

    CAS  PubMed  Google Scholar 

  50. Shao, F., Hu, Z., Xiong, Y.M., Huang, Q.Z., Wang, C.G., Zhu, R.H., and Wang, D.C., Biochim. Biophys. Acta, 1999, vol. 1430, pp. 262–268.

    Article  CAS  PubMed  Google Scholar 

  51. Gao, G.H., Liu, W., Dai, J.X., Wang, J.F., Hu, Z., Zhang, Y., and Wang, D.C., Biochemistry, 2001, vol. 40, pp. 10973–10978.

    Article  CAS  PubMed  Google Scholar 

  52. Kaas, Q. and Craik, D.J., Biopolymers, 2010, vol. 94, pp. 584–591.

    Article  CAS  PubMed  Google Scholar 

  53. Gould, A. and Camarero, J.A., Chembiochem, 2017, vol. 18, pp. 1350–1363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Craik, D.J., Daly, N.L., Bond, T., and Waine, C., J. Mol. Biol., 1999, vol. 294, pp. 1327–1336.

    Article  CAS  PubMed  Google Scholar 

  55. Chiche, L., Heitz, A., Gelly, J.C., Gracy, J., Chau, P.T., Ha, P.T., Hernandez, J.F., and Le-Nguyen, D., Curr. Protein Pept. Sci., 2004, vol. 5, pp. 341–349.

    Article  CAS  PubMed  Google Scholar 

  56. Tam, J.P., Lu, Y.A., Yang, J.L., and Chiu, K.W., Proc. Natl. Acad. Sci. U. S. A., 1999, vol. 96, pp. 8913–8918.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Nguyen, G.K., Zhang, S., Nguyen, N.T., Nguyen, P.Q., Chiu, M.S., Hardjojo, A., and Tam, J.P., J. Biol. Chem., 2011, vol. 286, pp. 24275–24287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Henriques, S.T. and Craik, D.J., Biochemistry, 2017, vol. 56, pp. 669–682.

    Article  CAS  Google Scholar 

  59. Pinto, M.F.S., Fensterseifer, I.C.M., Migliolo, L., Sousa, D.A., de Capdville, G., Arboleda-Valencia, J.W., Colgrave, M.L., Craik, D.J., Magalhães, B.S., Dias, S.C., et al., J. Biol. Chem., 2012, vol. 287, pp. 134–147.

    Article  CAS  PubMed  Google Scholar 

  60. Plan, M.R.R., Saska, I., Cagauan, A.G., and Craik, D.J., J. Agric. Food Chem., 2008, vol. 56, pp. 5237–5241.

    Article  CAS  PubMed  Google Scholar 

  61. Colgrave, M.L., Kotze, A.C., Kopp, S., McCarthy, J.S., Coleman, G.T., and Craik, D.J., Acta Trop., 2009, vol. 109, pp. 163–166.

    Article  CAS  PubMed  Google Scholar 

  62. Chen, B., Colgrave, M.L., Daly, N.L., Rosengren, K.J., Gustafson, K.R., and Craik, D.J., J. Biol. Chem., 2005, vol. 280, pp. 22395–22405.

    Article  CAS  PubMed  Google Scholar 

  63. Hu, E., Wang, D., Chen, J., and Tao, X., Int. J. Clin. Exp. Med., 2015, vol. 8, pp. 4059–4065.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Subroto, T., de Vries, H., Schuringa, J.J., Soedjanaatmadja, U.M.S., Hofsteenge, J., Jekel, P.A., and Beintema, J.J., Plant Physiol. Biochem., 2001, vol. 39, pp. 1047–1055.

    Article  CAS  Google Scholar 

  65. Wong, K.H., Tan, W.L., Kini, S.G., Xiao, T., Serra, A., Sze, S.K., and Tam, J.P., Front. Plant Sci., 2017, vol. 8, p. 1100. doi 10.3389/fpls.2017.01100

    Article  PubMed  PubMed Central  Google Scholar 

  66. Broekaert, W.F., Marien, W., Terras, F.R., De Bolle, M.F., Proost, P., Van Damme, J., Dillen, L., Claeys, M., Rees, S.B., Vanderleyden, J., et al., Biochemistry, 1992, vol. 31, pp. 4308–4314.

    Article  CAS  PubMed  Google Scholar 

  67. Rogozhin, E.A., Slezina, M.P., Slavokhotova, A.A., Istomina, E.A., Korostyleva, T.V., Smirnov, A.N., Grishin, E.V., Egorov, T.A., and Odintsova, T.I., Biochimie, 2015, vol. 116, pp. 125–132.

    Article  CAS  PubMed  Google Scholar 

  68. Loo, S., Kam, A., Xiao, T., and Tam, J.P., Front. Plant Sci., 2017, vol. 8, p. 2162. doi 10.3389/fpls.2017.02162

    Article  PubMed  PubMed Central  Google Scholar 

  69. Fujimura, M., Minami, Y., Watanabe, K., and Tadera, K., Biosci. Biotechnol. Biochem., 2003, vol. 67, pp. 1636–1642.

    Article  CAS  PubMed  Google Scholar 

  70. Li, S.S. and Claeson, P., Phytochemistry, 2003, vol. 63, pp. 249–255.

    Article  CAS  PubMed  Google Scholar 

  71. Odintsova, T.I., Vassilevski, A.A., Slavokhotova, A.A., Musolyamov, A.K., Finkina, E.I., Khadeeva, N.V., Rogozhin, E.A., Korostyleva, T.V., Pukhalsky, V.A., and Grishin, E., V, et al, FEBS J., 2009, vol. 276, pp. 4266–4275.

    Article  CAS  PubMed  Google Scholar 

  72. Bergh, K.P.B., Rouge, P., Proost, P., Coosemans, J., Krouglova, T., Engelborghs, Y., Peumans, W.J., and Van Damme, E.J.M., Planta, 2004, vol. 219, pp. 221–232.

    Article  CAS  PubMed  Google Scholar 

  73. Wong, K.H., Tan, W.L., Serra, A., Xiao, T., Sze, S.K., Yang, D., and Tam, J.P., Front. Plant Sci., 2016, vol. 7, p. 1639. doi 10.3389/fpls.2016.01639

    Article  PubMed  PubMed Central  Google Scholar 

  74. Gomes, V.M., Okorokov, L.A., Rose, T.L., Fernandes, K.V., and Xavier-Filho, J., Biochim. Biophys. Acta, 1998, vol. 1379, pp. 207–216.

    Article  CAS  PubMed  Google Scholar 

  75. Wang, X., Bunkers, G.J., Walters, M.R., and Thoma, R.S., Biochem. Biophys. Res. Commun., 2001, vol. 282, pp. 1224–1228.

    Article  CAS  PubMed  Google Scholar 

  76. Vieira Bard, G.C., Nascimento, V.V., Oliveira, A.E., Rodrigues, R., Da Cunha, M., Dias, G.B., Vasconcelos, I.M., Carvalho, A.O., and Gomes, V.M., Biopolymers, 2014, vol. 102, pp. 335–343.

    Article  CAS  PubMed  Google Scholar 

  77. Chung, R.P.-T., Neumann, G.M., and Polya, G.M., Plant Sci., 1997, vol. 127, pp. 1–16.

    Article  CAS  Google Scholar 

  78. Oparin, P.B., Mineev, K.S., Dunaevsky, Y.E., Arseniev, A.S., Belozersky, M.A., Grishin, E.V., Egorov, T.A., and Vassilevski, A.A., Biochem. J., 2012, vol. 446, pp. 69–77.

    Article  CAS  PubMed  Google Scholar 

  79. Berkut, A.A., Usmanova, D.R., Peigneur, S., Oparin, P.B., Mineev, K.S., Odintsova, T.I., Tytgat, J., Arseniev, A.S., Grishin, E.V., and Vassilevski, A.A., J. Biol. Chem., 2014, vol. 289, pp. 14331–14340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Nolde, S.B., Vassilevski, A.A., Rogozhin, E.A., Barinov, N.A., Balashova, T.A., Samsonova, O.V., Baranov, Y.V., Feofanov, A.V., Egorov, T.A., Arseniev, A.S., and Grishin, E.V., J. Biol. Chem., 2011, vol. 286, pp. 25145–25153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Slavokhotova, A.A., Rogozhin, E.A., Musolyamov, A.K., Andreev, Y.A., Oparin, P.B., Berkut, A.A., Vassilevski, A.A., Egorov, T.A., Grishin, E.V., and Odintsova, T.I., Plant. Mol. Biol., 2014, vol. 84, pp. 189–202.

    Article  CAS  PubMed  Google Scholar 

  82. Sousa, D.A., Porto, W.F., Silva, M.Z., Silva, T.R., and Franco, O.L., Molecules, 2016, vol. 21. pii E1062. doi 10.3390/molecules21081062

    Google Scholar 

  83. Ng, Y.M., Yang, Y., Sze, K.H., Zhang, X., Zheng, Y.T., and Shaw, P.C., J. Struct. Biol., 2011, vol. 174, pp. 164–172.

    Article  CAS  PubMed  Google Scholar 

  84. Conners, R., Konarev, A.V., Forsyth, J., Lovegrove, A., Marsh, J., Joseph-Horne, T., Shewry, P., and Brady, R.L., J. Biol. Chem., 2007, vol. 282, pp. 27760–27768.

    Article  CAS  PubMed  Google Scholar 

  85. Cui, X., Du, J., Li, J., and Wang, Z., Acta Biochim. Biophys. Sin. (Shanghai), 2018. doi 10.1093/abbs/gmy015

    Google Scholar 

  86. Marcus, J.P., Green, J.L., Goulter, K.C., and Manners, J.M., Plant J., 1999, vol. 19, pp. 699–710.

    Article  CAS  PubMed  Google Scholar 

  87. Tailor, R.H., Acland, D.P., Attenborough, S., Cammue, B.P., Evans, I.J., Osborn, R.W., Ray, J.A., Rees, S.B., and Broekaert, W.F., J. Biol. Chem., 1997, vol. 272, pp. 24480–24487.

    Article  CAS  PubMed  Google Scholar 

  88. Lee, D.G., Shin, S.Y., Kim, D.-H., Seo, M.Y., Kang, J.H., Lee, Y., Kim, K.L., and Hahm, K.-S., Biotech. Lett., 1999, vol. 21, pp. 1047–1050.

    Article  CAS  Google Scholar 

  89. Wang, P., Bang, J.K., Kim, H.J., Kim, J.K., Kim, Y., and Shin, S.Y., Peptides, 2009, vol. 30, pp. 2144–2149.

    Article  CAS  PubMed  Google Scholar 

  90. Qi, R.F., Song, Z.W., and Chi, C.W., Acta Biochim. Biophys. Sin. (Shanghai), 2005, vol. 37, pp. 283–292.

    Article  CAS  Google Scholar 

  91. Ye, X.Y., Ng, T.B., and Rao, P.F., Biochem. Biophys. Res. Commun., 2001, vol. 289, pp. 91–96.

    Article  CAS  PubMed  Google Scholar 

  92. James, A.M., Jayasena, A.S., Zhang, J., Berkowitz, O., Secco, D., Knott, G.J., Whelan, J., Bond, C.S., and Mylne, J.S., Plant Cell, 2017, vol. 29, pp. 461–473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. VieiraBard G.C., Nascimento, V.V., Ribeiro, S.F., Rodrigues, R., Perales, J., Teixeira-Ferreira, A., Carvalho, A.O., Fernandes, K.V., and Gomes, V.M., Protein J., 2015, vol. 34, pp. 122–129.

    Article  CAS  Google Scholar 

  94. Arulpandi, I. and Sangeetha, R., ISRN Pharm., 2012. 584073. doi 10.5402/2012/584073

    Google Scholar 

  95. Wang, S., Lin, J., Ye, M., Ng, T.B., Rao, P., and Ye, X., Peptides, 2006, vol. 27, pp. 3129–3136.

    Article  CAS  PubMed  Google Scholar 

  96. Kim, J.Y., Gopal, R., Kim, S.Y., Seo, C.H., Lee, H.B., Cheong, H., and Park, Y., Cell. Int. J. Mol. Sci., 2013, vol. 14, pp. 4349–4360.

    Article  CAS  PubMed  Google Scholar 

  97. Bendre, A.D., Ramasamy, S., and Suresh, C.G., Int. J. Biol. Macromol., 2018. pii S0141-8130(18)30322-2. doi 10.1016/j.ijbiomac.2018.02.148

    Google Scholar 

  98. Kim, M.H., Park, S.C., Kim, J.Y., Lee, S.Y., Lim, H.T., Cheong, H., Hahm, K.S., and Park, Y., Biochem. Biophys. Res. Commun., 2006, vol. 346, pp. 681–686.

    Article  CAS  PubMed  Google Scholar 

  99. Oliveira-Lima, M., Benko-Iseppon, A.M., Neto, J.R.C.F., Rodriguez-Decuadro, S., Kido, E.A., Crovella, S., and Pandolfi, V., Curr. Protein Pept. Sci., 2017, vol. 18, pp. 368–374.

    Article  CAS  PubMed  Google Scholar 

  100. Segura, A., Moreno, M., Madueno, F., Molina, A., and Garcia-Olmedo, F., Mol. Plant Microb. Inter., 1999, vol. 12, pp. 16–23.

    Article  CAS  Google Scholar 

  101. Berrocal-Lobo, M., Segura, A., Moreno, M., Lopez, G., Garcia-Olmedo, F., and Molina, A., Plant Physiol., 2002, vol. 128, pp. 951–961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Yeung, H., Squire, C.J., Yosaatmadja, Y., Panjikar, S., López, G., Molina, A., Baker, E.N., Harris, P.W., and Brimble, M.A., Angew Chem. Int. Ed. Engl., 2016, vol. 55, pp. 7930–7933.

    Article  CAS  PubMed  Google Scholar 

  103. Herbel, V., Schäfer, H., and Wink, M., Molecules, 2015, vol. 20, pp. 14889–14901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. García, A.N., Ayub, N.D., Fox, A.R., Gómez, M.C., Diéguez, M.J., Pagano, E.M., Berini, C.A., Muschietti, J.P., and Soto, G., BMC Plant Biol., 2014, vol. 14, pii 248. doi 10.1186/s12870–014–0248–9

    Google Scholar 

  105. Park, C.J., Park, C.B., Hong, S.S., Lee, H.S., Lee, S.Y., and Kim, S.C., Plant. Mol. Biol., 2000, vol. 44, pp. 187–197.

    Article  CAS  PubMed  Google Scholar 

  106. Remuzgo, C., Oewel, T.S., Daffre, S., Lopes, T.R., Dyszy, F.H., Schreier, S., Machado-Santelli, G.M., and Machini, T.M., Amino Acids, 2014, vol. 46, pp. 2573–2586.

    Article  CAS  PubMed  Google Scholar 

  107. Brown, L., Wolf, J.M., Prados-Rosales, R., and Casadevall, A., Nat. Rev. Microbiol., 2015, vol. 13, pp. 620–630.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Theis, T. and Stahl, U., Cell. Mol. Life Sci., 2004, vol. 61, pp. 437–455.

    Article  CAS  PubMed  Google Scholar 

  109. Teixeira, V., Feio, M.J., and Bastos, M., Prog. Lipid Res., 2012, vol. 51, pp. 149–177.

    Article  CAS  PubMed  Google Scholar 

  110. Fontaine, T., Biochimie, 2017, vol. 141, pp. 9–15.

    Article  CAS  PubMed  Google Scholar 

  111. Stec, B., Markman, O., Rao, U., Heffron, G., Henderson, S., Vernon, L.P., Brumfeld, V., and Teeter, M.M., J. Pept. Res., 2004, vol. 64, pp. 210–224.

    Article  CAS  PubMed  Google Scholar 

  112. Regente, M.C., Giudici, A.M., Villalain, J., and de la Canal, L., Lett. Appl. Microbiol., 2005, vol. 40, pp. 183–189.

    Article  CAS  PubMed  Google Scholar 

  113. Herbel, V. and Wink, M., Peer J., 2016, vol. 4. e1987. doi 10.7717/peerj.1987

    Google Scholar 

  114. Cools, T.L., Struyfs, C., Cammue, B.P., and Thevissen, K., Future Microbiol., 2017, vol. 12, pp. 441–454.

    Article  CAS  PubMed  Google Scholar 

  115. El-Mounadi, K., Islam, K.T., Hernandez-Ortiz, P., Read, N.D., and Shah, D.M., Mol. Microbiol., 2016, vol. 100, pp. 542–559.

    Article  CAS  PubMed  Google Scholar 

  116. Finkina, E.I. and Ovchinnikova, T.V., Russ. J. Bioorg. Chem., 2018, vol. 44, pp. 261–278.

    Article  CAS  Google Scholar 

  117. Henriques, S., Huang, Y.H., Chaousis, S., Wang, C.K., and Craik, D.J., Chembiochem, 2014, vol. 15, pp. 1956–1965.

    Article  CAS  Google Scholar 

  118. Henriques, S.T., Huang, Y.H., Rosengren, K.J., Franquelim, H.G., Carvalho, F.A., Johnson, A., Sonza, S., Tachedjian, G., Castanho, M.A., Daly, N.L., and Craik, D.J., J. Biol. Chem., 2011, vol. 286, pp. 24231–24241.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Lobo, D.S., Pereira, I.B., Fragel-Madeira, L., Medeiros, L.N., Cabral, L.M., Faria, J., Bellio, M., Campos, R.C., Linden, R., and Kurtenbach, E., Biochemistry, 2007, vol. 46, pp. 987–996.

    Article  CAS  PubMed  Google Scholar 

  120. Li, S.S., Gullbo, J., Lindholm, P., Larsson, R., Thunberg, E., Samuelsson, G., Bohlin, L., and Claeson, P., Biochem. J., 2002, vol. 366, pp. 405–413.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Diaz, I., Carmona, M.J., and Garcia-Olmedo, F., FEBS Lett., 1992, vol. 296, pp. 279–282.

    Article  CAS  PubMed  Google Scholar 

  122. Ja, C.K., Lee, B., Young, M.E., Sung, C.K., Cooper, J.A., Baek, D., Chae, O.L., Sang, Y.L., Yun, D.J., and Moo, J.C., Plant Cell Physiol., 2004, vol. 45, pp. 1669–1680.

    Article  Google Scholar 

  123. Jashni, M.K., Mehrabi, R., Collemare, J., Mesarich, C.H., and de Wit, P.J., Front. Plant Sci., 2015, vol. 6, p. 584.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Pogány, M., Dankó, T., Kámán-Tóth, E., Schwarczinger, I., and Bozsó, Z., Int. J. Mol. Sci., 2015, vol. 16, pp. 23177–23194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Jashni, M.K., Dols, I.H., Iida, Y., Boeren, S., Beenen, H.G., Mehrabi, R., Collemare, J., and de Wit, P.J., Mol. Plant Microbe Interact., 2015, vol. 28, pp. 996–1008.

    Article  CAS  PubMed  Google Scholar 

  126. Olivieri, F., Zanetti, M.E., Oliva, C.R., Covarrubias, A.A., and Casalongue, C.A., Eur. J. Plant Pathol., 2002, vol. 108, pp. 63–72.

    Article  CAS  Google Scholar 

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  1. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Moscow, 117997, Russia

    E. I. Finkina, D. N. Melnikova, I. V. Bogdanov & T. V. Ovchinnikova

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Finkina, E.I., Melnikova, D.N., Bogdanov, I.V. et al. Peptides of the Innate Immune System of Plants. Part I. Structure, Biological Activity, and Mechanisms of Action. Russ J Bioorg Chem 44, 573–585 (2018). https://doi.org/10.1134/S1068162019010060

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