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Phytopathogens and Molecular Mimicry

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Abstract

The co-evolution of plants and their pathogens is an example of an “arms race” between the virulence factors of pathogens and the immune system of the host plant. In this case, pathogens use a variety of strategies, including those based on molecular mimicry. In the genomes of phytopathogenic organisms of different groups, genes have been identified whose products are similar to certain groups of plant proteins—enzymes for cell walls destabilization, precursors of peptide phytohormones, etc. In particular, the ability to produce effectors that are used to alter the growth of the host plant and suppress its defense reactions has become widespread among phytopathogens from different kingdoms of the living world—bacteria, fungi, and animals (namely, nematodes). In our review, we will consider the main examples of molecular mimicry found in plant pathogens.

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REFERENCES

  1. Rojas, M., Restrepo-Jiménez, P., Monsalve, D.M., et al., Molecular mimicry and autoimmunity, J. Autoimmun., 2018, vol. 95, pp. 100—123. https://doi.org/10.1016/j.jaut.2018.10.012

    Article  CAS  PubMed  Google Scholar 

  2. Nobori, T., Mine, A., and Tsuda, K., Molecular networks in plant—pathogen holobiont, FEBS Lett., 2018, vol. 592, no. 12, pp. 1937—1953. https://doi.org/10.1002/1873-3468.13071

    Article  CAS  PubMed  Google Scholar 

  3. Bohlmann, H. and Sobczak, M., The plant cell wall in the feeding sites of cyst nematodes, Front. Plant Sci., 2014, vol. 5, p. 89. https://doi.org/10.3389/fpls.2014.00089

    Article  PubMed  PubMed Central  Google Scholar 

  4. Dodueva, I., Lebedeva, M., and Lutova, L., Dialog between kingdoms: enemies, allies and peptide phytohormones, Plants (Basel), 2021, vol. 10, no. 11, p. 2243. https://doi.org/10.3390/plants10112243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ludwig-Müller, J., Bacteria and fungi controlling plant growth by manipulating auxin: balance between development and defense, J. Plant Physiol., 2015, vol. 172, pp. 4—12.

    Article  Google Scholar 

  6. Spallek, T., Gan, P., Kadota, Y., and Shirasu, K., Same tune, different song-cytokinins as virulence factors in plant—pathogen interactions?, Curr. Opin. Plant Biol., 2018, vol. 44, pp. 82—87. https://doi.org/10.1016/j.pbi.2018.03.002

    Article  CAS  PubMed  Google Scholar 

  7. Jiang, S., Yao, J., Ma, K.W., et al., Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors, PLoS Pathog., 2013, vol. 9, no. 10. e1003715. https://doi.org/10.1371/journal.ppat.1003715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Geng, X., Jin, L., Shimada, M., et al., The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae, Planta, 2014, vol. 240, no. 6, pp. 1149—1165. https://doi.org/10.1007/s00425-014-2151-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bird, D.M., Jones, J.T., Opperman, C.H., et al., Signatures of adaptation to plant parasitism in nematode genomes, Parasitology, 2015, vol. 142, suppl. 1, pp. S71—S84. https://doi.org/10.1017/S0031182013002163

    Article  CAS  PubMed  Google Scholar 

  10. Danchin, E.G.J., What nematode genomes tell us about the importance of horizontal gene transfers in the evolutionary history of animals, Mob. Genet. Elem., 2011, vol. 1, no. 4, pp. 269—273. https://doi.org/10.4161/mge.18776

    Article  Google Scholar 

  11. Danchin, E.G.J., Rosso, M.N., Vieira, P., et al., Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 41, pp. 17651—17656. https://doi.org/10.1073/pnas.1008486107

    Article  PubMed  PubMed Central  Google Scholar 

  12. Paganini, J.¸ Campan-Fournier, A., Da Rocha, M., et al., Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes, PLoS One, 2012, vol. 7, no. 11. e50875. https://doi.org/10.1371/journal.pone.0050875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Frébortová, J. and Frébort, I., Biochemical and structural aspects of cytokinin biosynthesis and degradation in bacteria, Microorganisms, 2021, vol. 9, no. 6, p. 1314. https://doi.org/10.3390/microorganisms9061

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ali, M.A., Azeem, F., Li, H., and Bohlmann, H., Smart parasitic nematodes use multifaceted strategies to parasitize plants, Front. Plant Sci., 2017, vol. 8, p. 1699. https://doi.org/10.3389/fpls.2017.01699

    Article  PubMed  PubMed Central  Google Scholar 

  15. Siddique, S., Radakovic, Z.S., De La Torre, C.M., et al., A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants, Proc. Natl. Acad. Sci. U.S.A., 2015, vol. 112, no. 41, pp. 12669—12674. https://doi.org/10.1073/pnas.15036571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lee, C., Chronis, D., Kenning, C., et al., The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development, Plant Physiol., 2011, vol. 155, no. 2, pp. 866—880. https://doi.org/10.1104/pp.110.16719

    Article  CAS  PubMed  Google Scholar 

  17. Hewezi, T., Juvale, P.S., Piya, S., et al., The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis, Plant Cell, 2015, vol. 27, no. 3, pp. 891—907. https://doi.org/10.1105/tpc.114.135327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Gheysen, G. and Mitchum, M.G., Phytoparasitic nematode control of plant hormone pathways, Plant Physiol. 2019, vol. 179, no. 4, pp. 1212—1226. https://doi.org/10.1104/pp.18.01067

    Article  CAS  PubMed  Google Scholar 

  19. Haegeman, A., Mantelin, S., Jones, J.T., and Gheysen, G., Functional roles of effectors of plant-parasitic nematodes, Gene, 2012, vol. 492, no. 1, pp. 19—31. https://doi.org/10.1016/j.gene.2011.10.040

    Article  CAS  PubMed  Google Scholar 

  20. Bobay, B.G., DiGennaro, P., Scholl, E., et al., Solution NMR studies of the plant peptide hormone CEP inform function, FEBS Lett., 2013, vol. 587, no. 24, pp. 3979—3985. https://doi.org/10.1016/j.febslet.2013.10.033

    Article  CAS  PubMed  Google Scholar 

  21. de Almeida Engler, J., Kyndt, T., Vieira, P., et al., CCS52 and DEL1 genes are key components of the endocycle in nematode-induced feeding sites, Plant J., 2012, vol. 72, no. 2, pp. 185—198. https://doi.org/10.1111/j.1365-313X.2012.05054.x

    Article  CAS  PubMed  Google Scholar 

  22. Dodueva, I.E., Lebedeva, M.A., Kuznetsova, K.A., et al., Plant tumors: a hundred years of study, Planta, 2020, vol. 251, no. 4, p. 82. https://doi.org/10.1007/s00425-020-03375-5

    Article  CAS  PubMed  Google Scholar 

  23. Chen, Z., Agnew, J.L., Cohen, J.D., et al., Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, no. 50, pp. 20131—20136. https://doi.org/10.1073/pnas.0704901104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Choi, J., Huh, S.U., Kojima, M., et al., The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis, Dev. Cell, 2010, vol. 19, no. 2, pp. 284—295. https://doi.org/10.1016/j.devcel.2010.07.011

    Article  CAS  PubMed  Google Scholar 

  25. Taya, Y., Tanaka, Y., Nishimura, S., 5'-AMP is a direct precursor of cytokinin in Dictyostelium discoideum, Nature, 1978, vol. 271, no. 5645, pp. 545—547. https://doi.org/10.1038/271545a0

    Article  CAS  PubMed  Google Scholar 

  26. Barry, G.F., Rogers, S.G., Fraley, R.T., and Brand, L., Identification of a cloned cytokinin biosynthetic gene, Proc. Natl. Acad. Sci. U.S.A., 1984, vol. 81, no. 15, pp. 4776—4780. https://doi.org/10.1073/pnas.81.15.4776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kemper, E., Wafenschmidt, S., Weiler, E.W., et al., T‑DNA-encoded auxin formation in crown-gall cells, Planta, 1985, vol. 163, no. 2, pp. 257—262. https://doi.org/10.1007/BF00393516

    Article  CAS  PubMed  Google Scholar 

  28. Fu, S.-F., Wie, J.Y., Chen, H.W., et al., Indole-3-acetic acid: a widespread physiological code in interactions of fungi with other organisms, Plant Signal. Behav., 2015, vol. 10, no. 8. e1048052. https://doi.org/10.1080/15592324.2015.1048052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Spíchal, L., Cytokinins—recent news and views of evolutionally old molecule, Funct. Plant Biol., 2012, vol. 39, no. 4, pp. 267—284. https://doi.org/10.1071/FP11276

    Article  CAS  Google Scholar 

  30. Takei, K., Sakakibara, H., and Sugiyama, T., Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana, J. Biol. Chem., 2001, vol. 276, no. 28, pp. 26405—26410. https://doi.org/10.1074/jbc.M102130200

    Article  CAS  PubMed  Google Scholar 

  31. Persson, B.C., Esberg, B., Olafsson, O., and Björk, G.R., Synthesis and function of isopentenyl adenosine derivatives in tRNA, Biochimie, 1994, vol. 76, no. 12, pp. 1152—1160. https://doi.org/10.1016/0300-9084(94)90044-2

    Article  CAS  PubMed  Google Scholar 

  32. Frébort, I., Kowalska, M., Hluska, T., et al., Evolution of cytokinin biosynthesis and degradation, J. Exp. Bot., 2011, vol. 62, no. 8, pp. 2431—2452. https://doi.org/10.1093/jxb/err004

    Article  CAS  PubMed  Google Scholar 

  33. Yue, J., Hu, X., and Huang, J., Origin of plant auxin biosynthesis, Trends Plant Sci., 2014, vol. 19, no. 12, pp. 764—770. https://doi.org/10.1016/j.tplants.2014.07.004

    Article  CAS  PubMed  Google Scholar 

  34. Hinsch, J., Galuszka, P., and Tudzynski, P., Functional characterization of the first filamentous fungal tRNA-isopentenyltransferase and its role in the virulence of Claviceps purpurea, New Phytol., 2016, vol. 211, no. 3, pp. 980—992. https://doi.org/10.1111/nph.13960

    Article  CAS  PubMed  Google Scholar 

  35. Chapman, E.J. and Estelle, M., Mechanism of auxin-regulated gene expression in plants, Annu. Rev. Genet., 2009, vol. 43, pp. 265—285. https://doi.org/10.1242/dev.131870

    Article  CAS  PubMed  Google Scholar 

  36. Cui, F., Wu, S., Sun, W., et al., The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover, Plant Physiol., 2013, vol. 162, no. 2, pp. 1018—1029. https://doi.org/10.1104/pp.113.219659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Pieterse, C.M.J., Van der Does, D., Zamioudis, C., et al., Hormonal modulation of plant immunity, Annu. Rev. Cell. Dev. Biol., 2012, vol. 28, pp. 489—521. https://doi.org/10.1146/annurev-cellbio-092910-154055

    Article  CAS  PubMed  Google Scholar 

  38. Lambert, K.N., Allen, K.D., and Sussex, I.M., Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica, Mol. Plant—Microbe Interact., 1999, vol. 12, no. 4, pp. 328—336. https://doi.org/10.1094/MPMI.1999.12.4.328

    Article  CAS  PubMed  Google Scholar 

  39. Doyle, E.A. and Lambert, K.N., Meloidogyne javanica chorismate mutase 1 alters plant cell development, Mol. Plant Microbe Interact., 2003, vol. 16, no. 2, pp. 123—131. https://doi.org/10.1094/MPMI.2003.16.2.123

    Article  CAS  PubMed  Google Scholar 

  40. Huang, G., Dong, R., Allen, R., et al., Two chorismate mutase genes from the root-knot nematode Meloidogyne incognita, Mol. Plant Pathol., 2005, vol. 6, no. 1, pp. 23—30. https://doi.org/10.1111/j.1364-3703.2004.00257.x

    Article  CAS  PubMed  Google Scholar 

  41. Vanholme, B., Kast, P., and Haegeman, A., et al., Structural and functional investigation of a secreted chorismate mutase from the plant-parasitic nematode Heterodera schachtii in the context of related enzymes from diverse origins, Mol. Plant Pathol., 2009, vol. 10, no. 2, pp. 189—200. https://doi.org/10.1111/j.1364-3703.2008.00521.x

    Article  CAS  PubMed  Google Scholar 

  42. Wang, X., Xue, B., Dai, J., and Qin, X., A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism, Plant Pathol., 2018, vol. 67, no. 6, pp. 1436—1448. https://doi.org/10.1111/ppa/12841

    Article  CAS  Google Scholar 

  43. Parkinson, J., Whitton, C., Guiliano, D., et al., 200 000 nematode expressed sequence tags on the net, Trends Parasitol., 2001, vol. 17, no. 8, pp. 394—396. https://doi.org/10.1016/s1471-4922(01)01954-7

    Article  CAS  PubMed  Google Scholar 

  44. Djamei, A., Schipper, K., Rabe, F., et al., Metabolic priming by a secreted fungal effector, Nature, 2011, vol. 478, no. 7369, pp. 395—398. https://doi.org/10.1038/nature10454

    Article  CAS  PubMed  Google Scholar 

  45. Degrassi, G., Devescovi, G., Bigirimana, J., and Venturi, V., Xanthomonas oryzae pv. oryzae XKK.12 contains an AroQgamma chorismate mutase that is involved in rice virulence, Phytopathology, 2010, vol. 100, no. 3, pp. 262—270. https://doi.org/10.1094/PHYTO-100-3-0262

    Article  CAS  PubMed  Google Scholar 

  46. de Assis, R.A.B., Sagawa, C.H.D., Zaini, P.A., et al., A secreted chorismate mutase from Xanthomonas arboricola pv. juglandis attenuates virulence and walnut blight symptoms, Int. J. Mol. Sci., 2021, vol. 22, no. 19, p. 10374. https://doi.org/10.3390/ijms221910374

  47. Noon, J.B. and Baum, T.J., Horizontal gene transfer of acetyltransferases, invertases and chorismate mutases from different bacteria to diverse recipients, BMC Evol. Biol., 2016, vol. 16, p. 74. https://doi.org/10.1186/s12862-016-0651-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Liu, T., Song, T., Zhang, X., et al., Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis, Nat. Commun., 2014, vol. 5, p. 4686. https://doi.org/10.1038/ncomms5686

    Article  CAS  PubMed  Google Scholar 

  49. Brooks, D.M., Bender, C.L., and Kunkel, B.N., The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defenses in Arabidopsis thaliana, Mol. Plant Pathol., 2005, vol. 6, no. 6, pp. 629—639. https://doi.org/10.1111/j.1364-3703.2005.00311.x

    Article  CAS  PubMed  Google Scholar 

  50. Thines, B., Katsir, L., Melotto, M., et al., JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling, Nature, 2007, vol. 448, no. 7154, pp. 661—665. https://doi.org/10.1038/nature05960

    Article  CAS  PubMed  Google Scholar 

  51. Ejaz, U., Sohail, M., and Ghanemi, A., Cellulases: from bioactivity to a variety of industrial applications, Biomimetics (Basel), 2021, vol. 6, no. 3, p. 44. https://doi.org/10.3390/biomimetics6030044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cosgrove, D.J., Microbial expansins, Annu. Rev. Microbiol., 2017, vol. 71, pp. 479—497. https://doi.org/10.1146/annurev-micro-090816-093315

    Article  CAS  PubMed  Google Scholar 

  53. Jahr, H., Dreier, J., Meletzus, D., et al., The endo-beta-1,4-glucanase CelA of Clavibacter michiganensis subsp. michiganensis is a pathogenicity determinant required for induction of bacterial wilt of tomato, Mol. Plant—Microbe Interact., 2000, vol. 13, no. 7, pp. 703—714. https://doi.org/10.1094/MPMI.2000.13.7.703

    Article  CAS  PubMed  Google Scholar 

  54. Quarantin, A., Castiglioni, C., Schäfer, W., et al., The Fusarium graminearum cerato-platanins loosen cellulose substrates enhancing fungal cellulase activity as expansin-like proteins, Plant Physiol. Biochem., 2019, vol. 139, pp. 229—238. https://doi.org/10.1016/j.plaphy.2019.03.025

    Article  CAS  PubMed  Google Scholar 

  55. Smant, G., Stokkermans, J.P., Yan, Y., et al., Endogenous cellulases in animals: isolation of beta-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes, Proc. Natl. Acad. Sci. U.S.A., 1998, vol. 95, no. 9, pp. 4906—4911. https://doi.org/10.1073/pnas.95.9.4906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ali, S., Magne, M., Chen, S., et al., Analysis of putative apoplastic effectors from the nematode, Globodera rostochiensis, and identification of an expansin-like protein that can induce and suppress host defenses, PLoS One, 2015, vol. 10, no. 1. e0115042. https://doi.org/10.1371/journal.pone.0115042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Chen, Q., Rehman, S., Smant, G., Jones, J.T., Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi, Mol. Plant—Microbe Interact., 2005, vol. 18, no. 7, pp. 621—625. https://doi.org/10.1094/MPMI-18-0621

    Article  CAS  PubMed  Google Scholar 

  58. Hewezi, T., Howe, P., Maier, T.R., et al., Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism, Plant Cell, 2008, vol. 20, no. 11, pp. 3080—3093. https://doi.org/10.1105/tpc.108.063065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Gancheva, M.S., Malovichko, Y.V., Poliushkevich, L.O., et al., Plant peptide hormones, Russ. J. Plant Physiol., 2019, vol. 66, no. 2, pp. 171—189. https://doi.org/10.1134/S1021443719010072

    Article  CAS  Google Scholar 

  60. Stührwohldt, N. and Schaller, A., Regulation of plant peptide hormones and growth factors by post-translational modification, Plant Biol. (Stuttgart), 2019, vol. 21, suppl. 1, pp. 49—63. https://doi.org/10.1111/plb.12881

    Article  CAS  PubMed  Google Scholar 

  61. Poliushkevich, L.O., Gancheva, M.S., Dodueva, I.E., et al., Receptors of CLE peptides in plants, Russ. J. Plant Physiol., 2020, vol. 67, no. 1, pp. 1—16. https://doi.org/10.1134/S1021443720010288C

    Article  CAS  Google Scholar 

  62. Chakraborty, S., Nguyen, B., Wasti, S.D., and Xu, G., Plant leucine-rich repeat receptor kinase (LRR-RK): structure, ligand perception, and activation mechanism, Molecules, 2019, vol. 24, no. 17. E3081. https://doi.org/10.3390/molecules24173081

    Article  CAS  PubMed  Google Scholar 

  63. Yuan, N., Furumizu, C., Zhang, B., and Sawa, S., Database mining of plant peptide homologues, Plant Biotechnol. (Tokyo), 2021, vol. 38, no. 1, pp. 137—143. https://doi.org/10.5511/plantbiotechnology.20.0720a

    Article  CAS  Google Scholar 

  64. Willoughby, A.C. and Nimchuk, Z.L., WOX going on: CLE peptides in plant development, Curr. Opin. Plant Biol., 2021, vol. 63, p. 102056. https://doi.org/10.1016/j.pbi.2021.1020

    Article  CAS  PubMed  Google Scholar 

  65. Taleski, M., Imin, N., and Djordjevic, M.A., CEP peptide hormones: key players in orchestrating nitrogen-demand signalling, root nodulation, and lateral root development, J. Exp. Bot., 2018, vol. 69, no. 8, pp. 1829—1836. https://doi.org/10.1093/jxb/ery037

    Article  CAS  PubMed  Google Scholar 

  66. Aalen, R.B., Wildhagen, M., Stø, I.M., and Butenko, M.A., IDA: a peptide ligand regulating cell separation processes in Arabidopsis, J. Exp. Bot., 2013, vol. 64, no. 17, pp. 5253–5261 https://doi.org/10.1093/jxb/ert338

    Article  CAS  PubMed  Google Scholar 

  67. Wang, J., Joshi, S., Korkin, D., and Mitchum, M.G., Variable domain I of nematode CLEs directs post-translational targeting of CLE peptides to the extracellular space, Plant Signal. Behav., 2010, vol. 5, no. 12, pp. 1633—1635. https://doi.org/10.4161/psb.5.12.13774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wubben, M.J., Gavilano, L., Baum, T.J., and Davis, E.L., Sequence and spatiotemporal expression analysis of CLE-motif containing genes from the reniform nematode (Rotylenchulus reniformis Linford and Oliveira), J. Nematol., 2015, vol. 47, no. 2, pp. 159—165.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Lu, S.-W., Chen, S., Wang, J., et al., Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis, Mol. Plant—Microbe Interact., 2009, vol. 22, no. 9, pp. 1128—1142. https://doi.org/10.1094/MPMI-22-9-112

    Article  CAS  PubMed  Google Scholar 

  70. Rutter, W.B., Hewezi, T., Maier, T.R., et al., Members of the Meloidogyne avirulence protein family contain multiple plant ligand-like motifs, Phytopathology, 2014, vol. 104, no. 8, pp. 879—885. https://doi.org/10.1094/PHYTO-11-13-0326-R

    Article  CAS  PubMed  Google Scholar 

  71. Eves-Van Den Akker, S., Lilley, C.J., Yusup, H.B., et al., Functional C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis, Mol. Plant Pathol., 2016, vol. 17, no. 8, pp. 1265—1275. https://doi.org/10.1111/mpp.12402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Wang, X., Allen, R., Ding, X., et al., Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines, Mol. Plant—Microbe Interact., 2001, vol. 14, no. 4, pp. 536—544. https://doi.org/10.1094/MPMI.2001.14.4.53

    Article  CAS  PubMed  Google Scholar 

  73. Tucker, M.L. and Yang, R., A gene encoding a peptide with similarity to the plant IDA signaling peptide (AtIDA) is expressed most abundantly in the root-knot nematode (Meloidogyne incognita) soon after root infection, Exp. Parasitol., 2013, vol. 134, no. 2, pp. 165—170. https://doi.org/10.1016/j.exppara.2013.03.019

    Article  CAS  PubMed  Google Scholar 

  74. Guo, Y., Ni, J., Denver, R., et al., Mechanisms of molecular mimicry of plant CLE peptide ligands by the parasitic nematode Globodera rostochiensis, Plant Physiol., 2011, vol. 157, no. 1, pp. 476—484. https://doi.org/10.1104/pp.111.180554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Guo, X., Wang, J., Gardner, M., et al., Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation, PLoS Pathog., 2017, vol. 13, no. 2. e1006142. https://doi.org/10.1371/journal.ppat.1006142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Replogle, A., Wang, J., Bleckmann, A., et al., Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE, Plant J., 2011, vol. 65, no. 3, pp. 430—440. https://doi.org/10.1111/j.1365-313X.2010.04433.x

    Article  CAS  PubMed  Google Scholar 

  77. Replogle, A., Wang, J., Paolillo, V., et al., Synergistic interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE 2 in cyst nematode parasitism of Arabidopsis, Mol. Plant—Microbe Interact., 2013, vol. 26, no. 1, pp. 87—96. https://doi.org/10.1094/MPMI-05-12-0118-F

    Article  CAS  PubMed  Google Scholar 

  78. Wang, J., Replogle, A., Hussey, R., et al., Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii, Mol. Plant Pathol., 2011, vol. 12, no. 2, pp. 177—186. https://doi.org/10.1111/j.1364-3703.2010.00660.x

    Article  CAS  PubMed  Google Scholar 

  79. Chen, S., Lang, P., Chronis, D., et al., In planta processing and glycosylation of a nematode CLAVATA3/ ENDOSPERM SURROUNDING REGION-like effector and its interaction with a host CLAVATA2-like receptor to promote parasitism, Plant Physiol., 2015, vol. 167, no. 1, pp. 262—272. https://doi.org/10.1104/pp.114.251637

    Article  CAS  PubMed  Google Scholar 

  80. Guo, X., Chronis, D., De La Torre, C.M., et al., Enhanced resistance to soybean cyst nematode Heterodera glycines in transgenic soybean by silencing putative CLE receptors, Plant Biotechnol. J., 2015, vol. 13, no. 6, pp. 801—810. https://doi.org/10.1111/pbi.12313

    Article  CAS  PubMed  Google Scholar 

  81. Kim, J., Yang, R., Chang, C., et al., The root-knot nematode Meloidogyne incognita produces a functional mimic of the Arabidopsis INFLORESCENCE DEFICIENT IN ABSCISSION signaling peptide, J. Exp. Bot., 2018, vol. 69, no. 12, pp. 3009—3021. https://doi.org/10.1093/jxb/ery135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Huang, G., Dong, R., Allen, R., et al., A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor, Mol. Plant—Microbe Interact., 2006, vol. 19, no. 5, pp. 463—470. https://doi.org/10.1094/MPMI-19-046

    Article  CAS  PubMed  Google Scholar 

  83. Zhou, Y., Liu, X., Engstrom, E.M., et al., Control of plant stem cell function by conserved interacting transcriptional regulators, Nature, 2015, vol. 517, no. 7534, pp. 377—380. https://doi.org/10.1038/nature13853

    Article  CAS  PubMed  Google Scholar 

  84. Gao, B., Allen, R., Maier, T., et al., The parasitome of the phytonematode Heterodera glycines, Mol. Plant—Microbe Interact., 2003, vol. 16, no. 8, pp. 720—726. https://doi.org/10.1094/MPMI.2003.16.8.720

    Article  CAS  PubMed  Google Scholar 

  85. Dinh, P.T.Y., Zhang, L., Mojtahedi, H., et al., Broad Meloidogyne resistance in potato based on RNA interference of effector gene 16D10, J. Nematol., 2015, vol. 47, no. 1, pp. 71—78.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Pruitt, R.N., Joe, A., Zhang, W., et al., A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone, New Phytol., 2017, vol. 215, no. 2, pp. 725—736. https://doi.org/10.1111/nph.14609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pruitt, R.N., Schwessinger, B., Joe, A., et al., The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium, Sci. Adv., 2015, vol. 1, no. 6. e1500245. https://doi.org/10.1126/sciadv.1500245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Oehlenschlæger, C.B., Gersby, L.B.A., Ahsan, N., et al., Activation of the LRR receptor-like kinase PSY1R requires transphosphorylation of residues in the activation loop, Front. Plant Sci., 2017, vol. 8, p. 2005. https://doi.org/10.3389/fpls.2017.02005

    Article  PubMed  PubMed Central  Google Scholar 

  89. Wang, G.L., Song, W.Y., Ruan, D.L., et al., The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants, Mol. Plant—Microbe Interact., 1996, vol. 9, no. 9, pp. 850—855. https://doi.org/10.1094/mpmi-9-085

    Article  CAS  PubMed  Google Scholar 

  90. Luu, D.D., Joe, A., Chen, Y., et al., Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor, Proc. Natl. Acad. Sci. U.S.A., 2019, vol. 116, no. 17, pp. 8525—8534. https://doi.org/10.1073/pnas.181827511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Masachis, S., Segorbe, D., Turrà, D., et al., A fungal pathogen secretes plant alkalinizing peptides to increase infection, Nat. Microbiol., 2016, vol. 1, no. 6, p. 16043. https://doi.org/10.1038/nmicrobiol.2016.43

    Article  CAS  PubMed  Google Scholar 

  92. Cui, H., Tsuda, K., and Parker, J.E., Effector-triggered immunity: from pathogen perception to robust defense, Annu. Rev. Plant Biol., 2015, vol. 66, pp. 487—511. https://doi.org/10.1146/annurev-arplant-050213-040012

    Article  CAS  PubMed  Google Scholar 

  93. Thynne, E., Saur, I.M.L., Simbaqueba, J., et al., Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides, Mol. Plant Pathol., 2017, vol. 18, no. 6, pp. 811—824. https://doi.org/10.1111/mpp.12444

    Article  CAS  PubMed  Google Scholar 

  94. Gordon, T.R., Fusarium oxysporum and the Fusarium wilt syndrome, Annu. Rev. Phytopathol., 2017, vol. 55, pp. 23—39. https://doi.org/10.1146/annurev-phyto-080615-095919

    Article  CAS  PubMed  Google Scholar 

  95. Blackburn, M.R., Haruta, M., and Moura, D.S., Twenty years of progress in physiological and biochemical investigation of RALF peptides, Plant Physiol., 2020, vol. 182, no. 4, pp. 1657—1666. https://doi.org/10.1104/pp.19.0131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Wood, A.K.M., Walker, C., Lee, W.S., et al., Functional evaluation of a homologue of plant rapid alkalinisation factor (RALF) peptides in Fusarium graminearum, Fungal Biol., 2020, vol. 124, no. 9, pp. 753—765. https://doi.org/10.1016/j.funbio.2020.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Sauter, M., Phytosulfokine peptide signalling, J. Exp. Bot., 2015, vol. 66, no. 17, pp. 5161—5169. https://doi.org/10.1093/jxb/erv071

    Article  CAS  PubMed  Google Scholar 

  98. Patel, N., Hamamouch, N., Li, C., et al., A nematode effector protein similar to annexins in host plants, J. Exp. Bot., 2010, vol. 61, no. 1, pp. 235—248. https://doi.org/10.1093/jxb/erp293

    Article  CAS  PubMed  Google Scholar 

  99. Chen, C., Liu, S., Liu, Q., et al., An ANNEXIN-like protein from the cereal cyst nematode Heterodera avenae suppresses plant defense, PLoS One, 2015, vol. 10, no. 4. e0122256. https://doi.org/10.1371/journal.pone.0122256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Chronis, D., Chen, S., Lu, S., et al., A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism, Plant J., 2013, vol. 74, no. 2, pp. 185—196. https://doi.org/10.1111/tpj.12125

    Article  CAS  PubMed  Google Scholar 

  101. Zhang, L., Davies, L.J., and Elling, A.A., A Meloidogyne incognita effector is imported into the nucleus and exhibits transcriptional activation activity in planta, Mol. Plant Pathol., 2015, vol. 16, no. 1, pp. 48—60. https://doi.org/10.1111/mpp.12160

    Article  CAS  PubMed  Google Scholar 

  102. Kloppholz, S., Kuhn, H., and Requena, N., A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy, Curr. Biol., 2011, vol. 21, no. 14, pp. 1204—1209. https://doi.org/10.1016/j.cub.2011.06.044

    Article  CAS  PubMed  Google Scholar 

  103. Shaharoona, B., Arshad, M., and Zahir, Z.A., Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.), Lett. Appl. Microbiol., 2006, vol. 42, no. 2, pp. 155—159. https://doi.org/10.1111/j.1472-765X.2005.01827.x

    Article  CAS  PubMed  Google Scholar 

  104. Frugier, F., Kosuta, S., Murray, J.D., et al., Cytokinin: secret agent of symbiosis, Trend. Plant Sci., 2008, vol. 13, no. 3, pp. 115—120. https://doi.org/10.1016/j.tplants.2008.01.003

    Article  CAS  Google Scholar 

  105. Kisiala, A., Laffont, C., Emery, R.J., and Frugier, F., Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains, Mol. Plant—Microbe Interact., 2013, vol. 26, no. 10, pp. 1225—1231. https://doi.org/10.1094/MPMI-02-13-0054-R

    Article  CAS  PubMed  Google Scholar 

  106. Crafts, C.B. and Miller, C.O., Detection and identification of cytokinins produced by mycorrhizal fungi, Plant Physiol., 1974, vol. 54, no. 4, pp. 586—588. https://doi.org/10.1104/pp.54.4.586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Fu, S.-F., Wie, J.Y., Chen, H.W., et al., Indole-3-acetic acid: a widespread physiological code in interactions of fungi with other organisms, Plant Signal. Behav., 2015, vol. 10, no. 8. e1048052. https://doi.org/10.1080/15592324.2015.1048052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Duca, D.R. and Glick, B.R., Indole-3-acetic acid biosynthesis and its regulation in plant-associated bacteria, Appl. Microbiol. Biotechnol., 2020, vol. 104, no. 20, pp. 8607—8619. https://doi.org/10.1007/s00253-020-10869-5

    Article  CAS  PubMed  Google Scholar 

  109. Pons, S., Fournier, S., Chervin, C., et al., Phytohormone production by the arbuscular mycorrhizal fungus Rhizophagus irregularis, PLoS One, 2020, vol. 15, no. 10. e0240886. https://doi.org/10.1371/journal.pone.0240886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Marquer, M.L., Bécard, G., and Frey, N.F., Arbuscular mycorrhizal fungi possess a CLAVATA3/embryo surrounding region-related gene that positively regulates symbiosis, New Phytol., 2019, vol. 222, no. 2, pp. 1030—1042. https://doi.org/10.1111/nph.1564

    Article  PubMed  Google Scholar 

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Funding

The present study was supported by the Russian Science Foundation (project no. 21-66-00012).

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  1. Saint Petersburg State University, 199034, St. Petersburg, Russia

    I. E. Dodueva, M. A. Lebedeva & L. A. Lutova

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  1. I. E. Dodueva
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  2. M. A. Lebedeva
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Dodueva, I.E., Lebedeva, M.A. & Lutova, L.A. Phytopathogens and Molecular Mimicry. Russ J Genet 58, 638–654 (2022). https://doi.org/10.1134/S1022795422060035

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