The review highlights the current state and prospects of research on the interaction in the pathosystem between plants and pathogens of various taxonomic groups (bacteria, phytoplasmas, and viruses) at the cellular, physiological-biochemical, and molecular-genetic levels. Attention is paid to the features and mechanisms of action of the most common virulence factors of these pathogens, namely: secretion systems and effector proteins secreted by them (in phytopathogenic bacteria and phytoplasmas), phytotoxins (in phytopathogenic bacteria). It is shown that unlike bacteria and phytoplasmas, different viruses do not have the same strategy for transporting nucleic acids and effector proteins into the chloroplast. In general, targeting and damaging the chloroplast is believed to be one of the key steps in successful both bacterial and viral infection. This is evidenced by the effector proteins found in bacteria, viruses, and other pathogens with N-terminal chloroplast localization domains, thanks to which these proteins are transported into the middle of the organelle, causing structural and functional changes. An unsolved question in this direction remains: whether the chloroplast is a target for effector proteins of phytoplasma or they are damaged due to plant metabolism reprogramming through the translocation of their effectors to the nucleus. Disturbances of plant metabolism at different levels of the organization due to the infectious effect of these pathogens are considered. The peculiarities of the plant defense mechanisms of the induced immune response, which are activated in the case of pathogen penetration, are briefly considered. In this regard, the regulatory function of phytohormones and other signaling molecules (H2O2, NO, Ca2+ ions) in the initiation of protective mechanisms is briefly considered. Attention is paid to the strategies of pathogens to interfere with the metabolism of the host plant and inhibit immunity, one of which is molecular mimicry (for example, functional analogs of signaling molecules). These and further studies in this direction are relevant for the development of new approaches to plant protection against a wide range of phytopathogens, in particular with the aim of creating strategies to protect chloroplasts from penetration and subsequent inhibition of the immune response by effector proteins. In this regard, the study of the regulatory mechanisms of the secretion system III (T3SS), the most widespread in bacteria, and the discovery of a group of compounds of different nature that are inhibitors of this system are described. A model is considered that involves the use of the T3SS system as a target for inhibiting bacterial pathogenesis. An in-depth study of regulatory systems, localization, transport mechanisms and molecular targets of virulence factors of phytopathogens of different taxonomic groups is also important in this sense. However, the creation of a new generation of protective models based on the results of these studies is an open question, since their verification and approval in field conditions is necessary to evaluate their effectiveness. Such studies are becoming increasingly relevant due to the lack of effective means to combat phytopathogens of various taxonomic groups, and in contrast to chemical protection means, which can cause mutational variability of phytopathogenic microorganisms.
Keywords: bacteria, phytoplasmas, viruses, host plant, chloroplast, phytoimmunity, phytohormones, secretion systems, virulence
Full text and supplemented materials
Free full text: PDFReferences
1. Hvozdiak, R.I., Pasichnyk, L.A., Yakovleva, L.M., Moroz, S.M., Lytvynchuk, O.A., Zhytkevych, N.V., Khodos, S.F., Butsenko, L.M., Dankevych, L.A., Hrynyk, I.V. & Patyka, V.P. (2011). Fitopatohenni bakterii. Bakterialni khvoroby roslyn: monohrafiia. T. 1. Patyka, V.P. (Ed.). Kyiv: TOV NVP Interservis [in Ukrainian].
2. Carezzano, M.E., Paletti Rovey, M.F., Cappellari, Ld.R., Gallarato, L.A., Bogino, P., Oliva, Mdl.M. & Giordano, W. (2023). Biofilm-forming ability of phytopathogenic bacteria: a review of its involvement in plant stress. Plants. 12 (11), 2207. https://doi.org/10.3390/plants12112207
3. Zhang, Y., Zhang, A., Li, X. & Lu, C. (2020). The role of chloroplast gene expression in plant responses to environmental stress. Int. J. Mol. Sci., 21(17), 6082. https://doi.org/10.3390/ijms21176082
4. Singh, K., Wegulo, S.N., Skoracka, A. & Kundu, J.K. (2018). Wheat streak mosaic virus: a century old virus with rising importance worldwide. Mol. Plant Pathol., 19 (9), pp. 2193-2206. https://doi.org/10.1111/mpp.12683
5. Namba, S. (2019). Molecular and biological properties of phytoplasmas. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci., 95 (7), pp. 401-418. https://doi.org/10.2183/pjab.95.028
6. Meena, K.K., Sorty, A.M., Bitla, U.M., Choudhary, K., Gupta, P., Pareek, A., Singh, D.P., Prabha, R., Sahu, P.K., Gupta, V.K., Singh, H.B. & Krishanani, K.K. (2017). Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front. Plant Sci., 8, 172. https://doi.org/10.3389/fpls.2017.00172
7. Park, E., Nedo, A., Caplan, J.L. & Dinesh-Kumar, S.P. (2018). Plant-microbe interactions: organelles and the cytoskeleton in action. New Phytol., 217, pp. 1012-1028. https://doi.org/10.1111/nph.14959
8. Janik, K., Mittelberger, C. & Moser, M. (2020). Lights out: the chloroplast under attack during Phytoplasma infection? In: Ann. Plant Rev. Roberts, J. (Ed.). pp. 399-426. https://doi.org/10.1002/9781119312994.apr0747
9. Bhattacharyya, D. & Chakraborty, S. (2018). Chloroplast: the Trojan horse in plant-virus interaction. Mol. Plant Pathol., 19 (2), pp.504-518. https://doi.org/10.1111/mpp.12533
10. Lu, Y. & Yao, J. (2018). Chloroplasts at the crossroad of photosynthesis, pathogen infection and plant defense. Int. J. Mol. Sci., 19 (12), 3900. https://doi.org/10.3390/ijms19123900
11. Medina-Puche, L., Tan, H., Dogra, V., Wu, M., Rosas-Diaz, T., Wang, L., Ding, X., Zhang, D., Fu, X., Kim, C. & Lozano-Duran, R.A. (2020). Defense pathway linking plasma membrane and chloroplasts and Co-opted by pathogens. Cell, 182 (5), pp. 1109-1124. e25. https://doi.org/10.1016/j.cell.2020.07.020
12. Littlejohn, G.R., Breen, S., Smirnoff, N. & Grant, M. (2020). Chloroplast immunity illuminated. New Phytol., 229 (6), pp. 3088-3107. https://doi.org/10.1111/nph.17076
13. Xu, Q., Tang, C., Wang, X., Sun, S., Zhao, J., Kang, Z. & Wang, X. (2019). An effector protein of the wheat stripe rust fungus targets chloroplasts and suppresses chloroplast function Nat. Commun., 10, 5571. https://doi.org/10.1038/s41467-019-13487-6
14. Rosas-Diaz, T., Zhang, D., Fan, P., Wang, L., Ding, X., Jiang, Y., Jimenez-Gongora, T., Medina-Puche, L., Zhao, X., Feng, Z., Zhang, G., Liu, X., Bejarano, E.R., Tan, L., Zhang, H., Zhu, J.-K., Xing, W., Faulkner, C., Nagawa, S. & Lozano-Duranet, R. (2018). A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of RNAi Proc. Natl. Acad. Sci. USA, 115, pp. 1388-1393. https://doi.org/10.1073/pnas.1715556115
15. Gao, C., Xu, H., Huang, J., Sun, B., Zhang, F., Savage, Z., Duggan, C., Yan, T., Wu, C.H., Wang, Y., Vleeshouwers, V.G.A.A., Kamoun, S., Bozkurt, T.O. & Dong, S. (2020). Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition. Proc. Natl. Acad. Sci. USA, 117. https://doi.org/10.1073/pnas.2002759117
16. Lee, D.W., Lee, S., Oh, Y.J. & Hwang, I. (2009). Multiple sequence motifs in the rubisco small subunit transit peptide independently contribute to Toc 159-dependent import of proteins into chloroplasts. Plant Physiol., 151 (1), pp. 129-141. https://doi.org/10.1104/pp.109.140673
17. Nellaepalli, S., Lau, A.S. & Jarvis, R.P. (2023). Chloroplast protein translocation pathways and ubiquitin-dependent regulation at a glance. J. Cell Sci. 136, jcs241125. https://doi.org/10.1242/jcs.241125
18. Chen, K., Khatabi, B. & Fondong, V.N. (2019). The AC4 protein of a cassava geminivirus is required for virus infection. Mol. Plant Microb. Int. 32 (7), pp. 865-875. https://doi.org/10.1094/MPMI-12-18-0354-R
19. Fondong, V.N., Reddy, R.V., Lu, C., Hankoua, B., Felton, C., Czymmek, K. & Achenjang, F. (2007). The consensus N-myristoylation motif of a geminivirus AC4 protein is required for membrane binding and pathogenicity. Mol. Plant Microb. Int. 20 (4), pp. 380-391. https://doi.org/10.1094/MPMI-20-4-0380
20. Traverso, J.A., Meinnel, T. & Giglione, C. (2008). Expanded impact of protein N-myristoylation in plants. Plant Signal Behav. 3 (7), pp. 501-502. https://doi.org/10.4161/psb.3.7.6039
21. Adriotis, V.M.E. & Rathjen, J.P. (2006). The Pto kinase of tomato, which regulates plant immunity, is repressed by its myristoylated N terminus. J. Biol. Chem. 281, pp. 26578-26586. https://doi.org/10.1074/jbc.M603197200
22. Gohre, V. (2015). Photosynthetic defence. Nature Plants, 1, 15079. https://doi.org/10.1038/nplants.2015.79
23. Kangasj¬rvi, S., Neukermans, J., Li, S., Aro, E.M. & Noctor, G. (2012). Photosynthesis, photorespiration, and light signalling in defence responses. J. Exp. Bot. 63 (4), pp. 1619-1636. https://doi.org/10.1093/jxb/err402
24. Li, P., Lu, Y.J., Chen, H. & Day, B. (2020). The lifecycle of the plant immune system. CRC Crit. Rev. Plant Sci., 39, pp. 72-100. https://doi.org/10.1080/07352689.2020.1757829
25. Henry, E., ToruФo, T.Y., Jauneau, A., Deslandes, L. & Coaker, G. (2017). Direct and indirect visualization of bacterial effector delivery into diverse plant cell types during infection. The Plant Cell, 29 (7), pp. 1555-1570. https://doi.org/10.1105/tpc.17.00027
26. Xin, X.F. & He, S.Y. (2013). Pseudomonas syringae pv. tomato DC3000: A model pathogen for probing disease susceptibility and hormone signaling in plants. Annu. Rev. Phytop., 51, pp. 473-498. https://doi.org/10.1146/annurev-phyto-082712-102321
27. ToruФo, T.Y., Stergiopoulos, I. & Coaker, G. (2016). Plant-pathogen effectors: Cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol., 54, pp. 419-441. https://doi.org/10.1146/annurev-phyto-080615-100204
28. Galan, J.E. & Wolf-Watz, H. (2006). Protein delivery into eukaryotic cells by type III secretion machines. Nature, 444, pp. 567-573. https://doi.org/10.1038/nature05272
29. Wagner, S., Grin, I., Malmsheimer, S., Singh, N., Torres-Vargas, C.E. & Westerhausen, S. (2018). Bacterial type III secretion systems: a complex device for the delivery of bacterial effector proteins into eukaryotic host cells, FEMS Microbiol. Lett., 365 (19), fny201. https://doi.org/10.1093/femsle/fny201
30. Xiaochen, Y., Yu, M. & Yang, C.-H. (2020). Innovation and application of the type III secretion system inhibitors in plant pathogenic bacteria. Microorgan., 8 (12), 1956. https://doi.org/10.3390/microorganisms8121956
31. Green, E.R. & Mecsas, J. (2016). Bacterial secretion systems: an overview. Microbiol. Spectr., 4, pp. 213-239. https://doi.org/10.1128/microbiolspec.VMBF-0012-2015
32. Durbin, R.D. (1991). Bacterial phytotoxins: mechanisms of action. Experientia, 47, pp. 776-783. https://doi.org/10.1007/BF01922457
33. Strange, R.N. (2007). Phytotoxins produced by microbial plant pathogens. Nat. Prod. Rep., 24, pp. 127-144. https://doi.org/10.1039/B513232K
34. Duke, S.O. & Dayan, F.E. (2011). Modes of action of microbially-produced phytotoxins. Toxins (Basel), 3 (8), pp. 1038-1064. https://doi.org/10.3390/toxins3081038
35. Uppalapati, S.R., Ayoubi, P., Weng, H., Palmer, D.A., Mitchell, R.E., Jones, W. & Bender, C.L. (2005). The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J., 42, pp. 201-217. https://doi.org/10.1111/j.1365-313X.2005.02366.x
36. Kang, Y., Jelenska, J., Cecchini, N.M., Li, Y., Lee, M.W., Kovar, D.R. & Greenberg, J.T. (2014). HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog., 10, e1004232. https://doi.org/10.1371/journal.ppat.1004232
37. Shimono, M., Lu, Y.J., Porter, K., Kvitko, B.H., Henty-Ridilla, J., Creason, A., He, S.Y., Chang, J.H., Staiger, C.J. & Day, B. (2016). The Pseudomonas syringae type III effector HopG1 induces actin remodeling to promote symptom development and susceptibility during infection. Plant Physiol., 171 (3), pp. 2239-2255. https://doi.org/10.1104/pp.16.01593
38. Katsir, L., Schilmiller, A.L., Staswick, P.E., He, S.Y. & Howe, G.A. (2008). COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Nat. Acad. Sci. USA, 105, pp. 7100-7105. https://doi.org/10.1073/pnas.0802332105
39. Geng, X., Jin, L., Shimada, M., Kim, M.G. & Mackey, D. (2014). The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae. Planta, 240, pp. 1149-1165. https://doi.org/10.1007/s00425-014-2151-x
40. de Torres Zabala, M., Littlejohn, G., Jayaraman, S., Studholme, D., Bailey, T., Lawson, T., Tillich, M., Licht, D., Bolter, B., Delfino, L., Truman, W., Mansfield, J., Smirnoff, N. & Grant, M. (2015). Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nature Plants, 1, 15074. https://doi.org/10.1038/nplants.2015.74
41. Li, G., Froehlich, J.E., Elowsky, C., Msanne, J., Ostosh, A.C., Zhang, C., Awada, T. & Alfano, J.R. (2014). Distinct pseudomonas type-III effectors use a cleavable transit peptide to target chloroplasts. Plant J., 77, pp. 310-321. https://doi.org/10.1111/tpj.12396
42. Petre, B., Lorrain, C., Saunders, D.G.O., Win, J., Sklenar, J., Duplessis, S. & Kamoun, S. (2016). Rust fungal effectors mimic host transit peptides to translocate into chloroplasts. Cell. Microbiol., 18, pp. 453-465. https://doi.org/10.1111/cmi.12530
43. Sohn, K.H., Zhang, Y. & Jones, J.D. (2009). The Pseudomonas syringae effector protein, AvrRPS4, requires in planta processing and the KRVY domain to function. Plant J., 57, pp. 1079-1091. https://doi.org/10.1111/j.1365-313X.2008.03751.x
44. Soto, S.M. (2013). Role of efflux pumps in the antibiotic resistance of bacteria embedded in a biofilm. Virulence., 4, pp. 223-229. https://doi.org/10.4161/viru.23724
45. Singh, S., Singh, S.K., Chowdhury, I. & Singh, R. (2017). Understanding the mechanism of bacterial biofilms resistance to antimicrobial agents. Open Microbiol. J., 11, pp. 53-62. https://doi.org/10.2174/1874285801711010053
46. Hardham, A.R., Jones, D.A. & Takemoto, D. (2007). Cytoskeleton and cell wall function in penetration resistance. Curr. Opin. Plant Biol., 10, pp. 342-348. https://doi.org/10.1016/j.pbi.2007.05.001
47. Boevink, P.C., Birch, P.R., Turnbull, D. & Whisson, S.C. (2020). Devastating intimacy: the cell biology of plant-Phytophthora interactions. New Phytologist., 228, pp. 445-458. https://doi.org/10.1111/nph.16650
48. Rojas, C.M., Senthil-Kumar, M., Tzin, V. & Mysore, K.S. (2014). Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front. Plant Sci., 5, 17. https://doi.org/10.3389/fpls.2014.00017
49. Gohre, V., Jones, A.M., Sklenar, J., Robatzek, S. & Weber, A.P. (2012). Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol. Plant Microbe Interact., 25, pp. 1083-1092. https://doi.org/10.1094/MPMI-11-11-0301
50. Jones, J.D. & Dangl, J.L.(2006). The plant immune system. Nature., 444, pp. 323-329. https://doi.org/10.1038/nature05286
51. van der Burgh, A.M. & Joosten, M. (2019). Plant immunity: thinking outside and insidethe box. Trends Plant Sci., 24, pp. 587-601. https://doi.org/10.1016/j.tplants.2019.04.009
52. Havaux, M. (2014). Carotenoid oxidation products as stress signals in plants. Plant J., 79, pp. 597-606. https://doi.org/10.1111/tpj.12386
53. Zoeller, M., Stingl, N., Krischke, M., Fekete, A., Waller, F., Berger, S. & Mueller, M.J. (2012). Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol., 160, pp. 365-378. https://doi.org/10.1104/pp.112.202846
54. Durrant, W.E. & Dong, X. (2004). Systemic acquired resistance. Annu. Rev. Phytopathol., 42, pp. 185-209. https://doi.org/10.1146/annurev.phyto.42.040803.140421
55. Zehra, A., Raytekar, N.A., Meena, M. & Swapnil, P. (2021). Efficiency of microbial bio-agents as elicitors in plant defense mechanism under biotic stress: A review. Curr. Res. Microb. Sci., 2, 100054. https://doi.org/10.1016/j.crmicr.2021.100054
56. Moustafa-Farag, M., Almoneafy, A., Mahmoud, A., Elkelish, A., Arnao, M.B., Li, L. & Ai, S. (2020). Melatonin and its protective role against biotic stress impacts on plants. Biomol., 10, 54. https://doi.org/10.3390/biom10010054
57. Orozco-Mosqueda, M.C., Fadiji, A.E., Babalola, O.O. & Santoyo, G. (2023). Bacterial elicitors of the plant immune system: an overview and the way forward. Plant Stress, 7, 100138. https://doi.org/10.1016/j.stress.2023.100138
58. Chiang, Yi-H. & Coaker, G. (2015). Effector triggered immunity: NLR immune perception and downstream defense responses. Arabidopsis Book, 13. https://doi.org/10.1199/tab.0183
59. Coll, N.S., Epple, P. & Dangl, J.L. (2011). Programmed cell death in the plant immune system. Cell. Death Differ., 18, pp. 1247-1256. https://doi.org/10.1038/cdd.2011.37
60. Van Loon, L.C., Rep, M. & Pieterse, C.M. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol., 44, pp. 135-162. https://doi.org/10.1146/annurev.phyto.44.070505.143425
61. Lim, C.W., Baek, W., Jung, J., Kim, J.-H. & Lee, S.C. (2015). Function of ABA in stomatal defense against biotic and drought stresses. Int. J. Mol. Sci., 16, pp. 15251-15270. https://doi.org/10.3390/ijms160715251
62. Hsu, P.K., Dubeaux, G., Takahashi, Y. & Schroeder, J.I. (2021). Signaling mechanisms in abscisic acid-mediated stomatal closure. Plant J., 105 (2), pp. 307-321. https://doi.org/10.1111/tpj.15067
63. Webb, A.A., Larman, M.G., Montgomery, L.T., Taylor, J.E. & Hetherington, A.M. (2001). The role of calcium in ABA-induced gene expression and stomatal movements. Plant J., 26, pp. 351-362. https://doi.org/10.1046/j.1365-313X.2001.01032.x
64. de Torres Zabala, M., Bennett, M.H., Truman, W.H. & Grant, M.R. (2009). Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J., 59, pp. 375-386. https://doi.org/10.1111/j.1365-313X.2009.03875.x
65. de Torres-Zabala, M., Truman, W., Bennett, M.H., Lafforgue, G., Mansfield, J.W., Rodriguez Egea, P., Bogre, L. & Grant, M. (2007). Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J., 26, pp. 1434-1443. https://doi.org/10.1038/sj.emboj.7601575
66. Adie, B.A.T., Pѕrez-Pѕrez, J., Pѕrez-Pѕrez, M.M., Godoy, M., S«nchez-Serrano, J.-J., Schmelz, E.A. & Solano, R. (2007). ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell, 19, pp. 1665-1681. https://doi.org/10.1105/tpc.106.048041
67. Wang, K.L.-C., Li, H. & Ecker, J.R. (2002). Ethylene biosynthesis and signaling networks. Plant Cell, 14, 1311. https://doi.org/10.1105/tpc.001768
68. Ceusters, J. & Van de Poel, B. (2018). Ethylene exerts species-specific and age-dependent control of photosynthesis. Plant Physiol., 176 (4), pp. 2601-2612. https://doi.org/10.1104/pp.17.01706
69. ZieliXska, M. & Michniewicz, M. (2001). The effect of calcium on the production of ethylene and abscisic acid by fungus Fusarium culmorum and by wheat seedlings infected with that pathogen. Acta Physiol. Plant., 23, pp. 79-85. https://doi.org/10.1007/s11738-001-0026-9
70. Cao, F.Y., Yoshioka, K. & Desveaux, D. (2011). The roles of ABA in plant-pathogen interactions. J. Plant Res., 124, pp. 489-499. https://doi.org/10.1007/s10265-011-0409-y
71. Melotto, M., Underwood, W. & He, S.Y. (2008). Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Phytopathol., 46, pp. 101-122. https://doi.org/10.1146/annurev.phyto.121107.104959
72. Goritschnig, S., Weihmann, T., Zhang, Y., Fobert, P., McCourt, P. & Li, X. (2008). A novel role for protein farnesylation in plant innate immunity. Plant Physiol., 148, pp. 348-357. https://doi.org/10.1104/pp.108.117663
73. Hoffman, T., Schmidt, J.S., Zheng, X. & Bent, A.F. (1999). Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiol., 119, pp. 935-950. https://doi.org/10.1104/pp.119.3.935
74. Wasternack, C. & Hause, B. (2013). Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot., 111, pp. 1021-1058. https://doi.org/10.1093/aob/mct067
75. Andersson, M.X., Hamberg, M., Kourtchenko, O., Brunnstrom, A., McPhail, K.L., Gerwick, W.H, Gobel, C., Feussner, I. & Ellerstrom, M. (2006). Oxylipin profiling of the hypersensitive response in Arabidopsis thaliana: Formation of a novel oxo-phytodienoic acid-containing galactolipid, arabidopside. J. Biol. Chem., 281, pp. 31528-31537. https://doi.org/10.1074/jbc.M604820200
76. Truman, W., Bennett, M.H., Kubigsteltig, I., Turnbull, C. & Grant, M. (2007). Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proceed. Nat. Acad. Sci. USA., 104, pp. 1075-1080. https://doi.org/10.1073/pnas.0605423104
77. Matsuura, H., Takeishi, S., Kiatoka, N., Sato, C., Sueda, K., Masuta, C. & Nabeta, K. (2012). Transportation of de novo synthesized jasmonoyl isoleucine in tomato, Phytochem., 83, pp. 25-33. https://doi.org/10.1016/j.phytochem.2012.06.009
78. Zoeller, M., Stingl, N., Krischke, M., Fekete, A., Waller, F., Berger, S. & Mueller M.J. (2012). Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol., 2, 160, pp. 365-378. https://doi.org/10.1104/pp.112.202846
79. Ding, Y., Sun, T., Ao, K., Peng, Y., Zhang, Y., Li, X. & Zhang, Y. (2018). Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell, 173, pp. 1454-1467. https://doi.org/10.1016/j.cell.2018.03.044
80. Zhang, Z.S., Xu, Y.Y., Xie, Z.W., Li, X.Y., He, Z.H. & Peng, X.X. (2016). Association-dissociation of glycolate oxidase with catalase in rice: a potential switch to modulate intracellular H2O2 levels. Mol. Plant, 9, pp. 737-748. https://doi.org/10.1016/j.molp.2016.02.002
81. Petroutsos, D., Busch, A., Janssen, I., Trompelt, K., Bergner, S.V., Weinl, S., Holtkamp, M., Karst, U., Kudla, J. & Hippler, M. (2011). The chloroplast calcium sensor CAS is required for photoacclimation in Chlamydomonas reinhardtii. Plant Cell, 23, pp. 2950-2963. https://doi.org/10.1105/tpc.111.087973
82. Nomura, H., Komori, T., Uemura, S., Kanda, Y., Shimotani, K., Nakai, K., Furuichi, T., Takebayashi, K., Sugimoto, T., Sano, S., Suwastika, I.N., Fukusaki, E., Yoshioka, H., Nakahira, Y. & Shiina, T. (2012). Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat. Comm., 3, 926. https://doi.org/10.1038/ncomms1926
83. Shapiguzov, A., Vainonen, J.P., Wrzaczek, M. & Kangasj¬rvi, J. (2012). ROS-talk-how the apoplast, the chloroplast, and the nucleus get the message through. Front. Plant Sci., 3, 292. https://doi.org/10.3389/fpls.2012.00292
84. Delledonne, M., Xia, Y., Dixon, R.A. & Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature, 394, pp. 585-588. https://doi.org/10.1038/29087
85. Yang, J., Liao, Y.J., Ning, J. ., Wang, J.Z., Wang, H. & Ren, Z.G. (2020). Identification of a phytoplasma associated with Syringa reticulata witches' broom disease in China. Forest Pathol., 50, e12592. https://doi.org/10.1111/efp.12592
86. Xiao-Yan, W., Rong-Yue, Z., Jie, L., Yin-Hu, L., Hong-Li, S., Wen-Feng, L. & Ying-Kun, H. (2022). The diversity, distribution and status of phytoplasma diseases in China. Front. Sust. Food Syst., 6. https://doi.org/10.3389/fsufs.2022.943080
87. Wang, N., Li, Y., Chen, W., Yang, H.Z., Zhang, P.H. & Wu, Y.F. (2018). Identification of wheat blue dwarf phytoplasma effectors targeting plant proliferation and defence responses. Plant Pathol., 67, 3. https://doi.org/10.1111/ppa.12786
88. Jurga, M. & ZwoliXska, A. (2020). Phytoplasmas in Poaceae species: a threat to the most important cereal crops in Europe. J. Plant Pathol., 102 (2), pp. 287-297. https://www.jstor.org/stable/48741408 https://doi.org/10.1007/s42161-019-00481-6
89. Hogenhout, S.A., Oshima, K., Ammar, El-D., Kakizawa, S., Kingdom, H.N. & Namba, S. (2008). Phytoplasmas: bacteria that manipulate plants and insects. Mol. Plant Pathol., 9, pp. 403-423. https://doi.org/10.1111/j.1364-3703.2008.00472.x
90. Perilla-Henao, L.M. & Casteel, C.L. (2016). Vector-borne bacterial plant pathogens: interactions with hemipteran insects and plants. Front. Plant Sci., 7, 1163. https://doi.org/10.3389/fpls.2016.01163
91. Kube, M., Mitrovic, J., Duduk, B., Rabus, R. & Seemuller, E. (2012). Current view on phytoplasma genomes and encoded metabolism. Sci. World J., 185942. https://doi.org/10.1100/2012/185942
92. Bai, X., Zhang, J., Ewing, A., Miller, S.A., Jancso Radek, A., Shevchenko, D.V., Tsukerman, K., Walunas, T., Lapidus, A., Campbell, J.W. & Hogenhout, S.A. (2006). Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. J. Bacteriol., 188, pp. 3682-3696. https://doi.org/10.1128/JB.188.10.3682-3696.2006
93. Minato, N., Himeno, M., Hoshi, A., Maejima, K., Komatsu, K., Takebayashi, Y., Kasahara, H., Yusa, A., Yamaji, Y., Oshima, K., Kamiya, Y. & Namba, S. (2014). The phytoplasma virulence factor TENGU causes plant sterility by downregulating of the jasmonic acid and auxin pathways. Sci. Rep., 4, 7399. https://doi.org/10.1038/srep07399
94. Kakizawa, S., Oshima, K., Ishii, Y., Hoshi, A., Maejima, K., Jung, H.-Y., Yamaji, Y. & Namba, S. (2009). Cloning of immunodominant membrane protein genes of phytoplasmas and their in planta expression. FEMS Microbiol. Lett., 293, pp. 92-101. https://doi.org/10.1111/j.1574-6968.2009.01509.x
95. Bertaccini, A. (2022). Plants and phytoplasmas: when bacteria modify plants. Plants., 11 (11), 1425. https://doi.org/10.3390/plants11111425
96. Dermastia, M., Tomaz, S., Strah, R., Lukan, T., Coll, A., Dusak, B., Anzic, B., Cepin, T., Wienkoop, S., Kladnik, A., Zagorscak, M., Riedle-Bauer, M., Schonhuber, C., Weckwerth, W., Gruden, K., Roitsch, T., Pompe Novak, M. & Brader, G. (2023). Candidate pathogenicity factor/effector proteins of 'Candidatus Phytoplasma solani' modulate plant carbohydrate metabolism, accelerate the ascorbate-glutathione cycle, and induce autophagosomes. Front. Plant Sci., 14. https://doi.org/10.3389/fpls.2023.1232367
97. Huang, W., MacLean, A.M., Sugio, A., Maqbool, A., Busscher, M., Cho, S.T., Kamoun, S., Kuo, C.H., Immink, R.G.H. & Hogenhout, S.A. (2021). Parasitic modulation of host development by ubiquitin-independent protein degradation. Cell., 184 (20), pp. 5201-5214. e12. https://doi.org/10.1016/j.cell.2021.08.029
98. Kenro, O., Kensaku, M. & Shigetou, N. (2013). Genomic and evolutionary aspects of phytoplasmas. Front. Microbiol., 4. https://doi.org/10.3389/fmicb.2013.00230
99. Buoso, S., Pagliari, L., Musetti, R., Martini, M., Marroni, F., Schmidt, W. & Santi, S. (2019). 'Candidatus phytoplasma solani' interferes with the distribution and uptake of iron in tomato. BMC Genom., 20, 703. https://doi.org/10.1186/s12864-019-6062-x
100. Xue, C., Liu, Z., Dai, L., Bu, J., Liu, M., Zhao, Z., Jiang, Z., Gao, W. & Zhao, J. (2018). Changing host photosynthetic, carbohydrate, and energy metabolisms play important roles in phytoplasma infection. Phytopathology, 108. https://doi.org/10.1094/PHYTO-02-18-0058-R
101. Dermastia, M., Kube, M. & Seruga Music, M. (2019). Transcriptomic and proteomic studies of phytoplasma-infected plants. In: Phytoplasmas: Plant Pathogenic Bacteria - III: Genomics, Host Pathogen Interactions and Diagnosis. Bertaccini, A., Oshima, K., Kube, M. & Rao, G.-P. (Eds.). Singapore: Springer Nature. https://doi.org/10.1007/978-981-13-9632-8_3
102. Zhao, Y., Liu, Q.Z. & Davis, R.E. (2004). Transgene expression in strawberries driven by a heterologous phloem-specific promoter. Plant Cell Rep., 23, pp. 224-230. https://doi.org/10.1007/s00299-004-0812-0
103. Lemoine, R., La Camera, S., Atanassova, R., Dѕdaldѕchamp, F., Allario, T., Pourtau, N., Bonnemain, J.L., Laloi, M., Coutos-Thѕvenot, P., Maurousset, L., Faucher, M., Girousse, C., Lemonnier, P., Parrilla, J. & Durand, M. (2013). Source-to-sink transport of sugar and regulation by environmental factors. Front. Plant Sci., 4, 272. https://doi.org/10.3389/fpls.2013.00272
104. Reveles-Torres, L.R., Vel«squez-Valle, R., Salas-MuФoz, S., Mauricio-Castillo, J.A., Esqueda-D«vila, K.C.J. & Herrera, M.D. (2018). Candidatus Phytoplasma trifolii (16SrVI) infection modifies the polyphenols concentration in pepper (Capsicum annuum) plant tissues. J. Phytopathol., 166(7/8), pp. 555-564. Retrieved from: https://onlinelibrary.wiley.com/journal/14390434 https://doi.org/10.1111/jph.12717
105. Vel«squez-Valle, R., Villa-Ruanob, N., Hidalgo-MartHnez, D., Zepeda-Vallejod, L.G., Pѕrez-Hern«ndez, N., Reyes-LЩpez, C.A., Reyes-Cervantes, E., Medina-Melchor, D.L. & Becerra-MartHnez, E. (2020). Revealing the 1H NMR metabolome of mirasol chili peppers (Capsicum annuum) infected by Candidatus Phytoplasma trifolii. Food Res. Int., 131108863. https://doi.org/10.1016/j.foodres.2019.108863
106. Ding, Y., Wu, W., Wei, W., Davis, R. E., Lee, I. M., Hammond, R. W., Sheng, J. P., Shen, L., Jiang, Y. & Zhao, Y. (2013). Potato purple top phytoplasma-induced disruption of gibberellin homeostasis in tomato plants. Ann. Appl. Biol., 162 (1), pp. 131-139. https://doi.org/10.1111/aab.12008
107. Ding, Y., Wei, W., Wu, W., Davis, R.E., Jiang, Y., Lee, I.M., Hammond, R.W., Shen, L., Sheng, J.P. & Zhao, Y. (2013). Role of gibberellic acid in tomato defence against potato purple top phytoplasma infection. Ann. Appl. Biol., 162 (2), pp. 191-199. https://doi.org/10.1111/aab.12011
108. Wei, W., Inaba, J., Zhao, Y., Mowery, J.D. & Hammond, R. (2022). Phytoplasma infection blocks starch breakdown and triggers chloroplast degradation, leading to premature leaf senescence, sucrose reallocation, and spatiotemporal redistribution of phytohormones. Int. J. Mol. Sci., 23 (3), 1810. https://doi.org/10.3390/ijms23031810
109. Wang, Q., Guo, Y., Wang, N., Li, Y., Chen, W., Chen, W. & Wu, Y. (2014). Identification of a conserved core genome with group-specific genes from comparative genomics of ten different Candidatus Phytoplasma strains. J. Phytopathol., 162, pp. 650-659. https://doi.org/10.1111/jph.12239
110. Bai, X., Correa, V.R., Toruno, T.Y., Ammar, El-D., Kamoun, S. & Hogenhout, S.A. (2009). AY-WB phytoplasma secretes a protein that targets plant cell nuclei. Mol. Plant Microb. Interact., 22, pp. 18-30. https://doi.org/10.1104/pp.111.181586
111. Mittelberger, C., Stellmach, H., Hause, B., Kerschbamer, C., Schlink, K., Letschka, T. & Janik, K. (2019). A novel effector protein of apple proliferation phytoplasma disrupts cell integrity of Nicotiana spp. protoplasts. Int. J. Mol. Sci., 18, 20 (18), 4613. https://doi.org/10.3390/ijms20184613
112. Wang, R., Bai, B., Li, D., Wang, J., Huang, W., Wu, Y. & Zhao, L. (2024). Phytoplasma: a plant pathogen that cannot be ignored in agricultural production - research progress and outlook. Mol. Plant Pathol., 25 (2), e13437. https://doi.org/10.1111/mpp.13437
113. Strohmayer, A., Moser, M., Si-Ammour, A., Krczal, G. & Boonrod, K. (2019).'Candidatus Phytoplasma mali' genome encodes a protein that functions as a E3 Ubiquitin Ligase and could inhibit plant basal defense. Mol. Plant-Microbe Interac., 32, pp. 1487-1495. https://doi.org/10.1094/MPMI-04-19-0107-R
114. Bai, B., Zhang, G., Li, Y., Wang, Y., Sujata, S., Zhang, X., Wang, L., Zhao, L. & Wu, Y. (2022). The 'Candidatus Phytoplasma tritici' effector SWP12 degrades the transcription factor TaWRKY74 to suppress wheat resistance. Plant J., 112 (6), pp. 1473-1488. https://doi.org/10.1111/tpj.16029
115. Yadav, S. & Chhibbar, A.K. (2018). Plant-virus interactions. In: Singh, A., Singh, I. (Eds.). Mol. Aspect. Plant-Pathogen Int. Springer, Singapore. https://doi.org/10.1007/978-981-10-7371-7_3
116. Paudel, D.B. & Sanfaзon, H. (2018). Exploring the diversity of mechanisms associated with plant tolerance to virus infection. Front. Plant Sci., 9, 1575. https://doi.org/10.3389/fpls.2018.01575
117. Gnanasekaran, P., Ponnusamy, K. & Chakraborty, S. (2019). A geminivirus betasatellite encoded bC1 protein interacts with PsbP and subverts PsbP-mediated antiviral defence in plants. Mol. Plant Pathol. 20, pp. 943-960. https://doi.org/10.1111/mpp.12804
118. Bhattacharyya, D., Gnanasekaran, P., Kumar, R.K., Kushwaha, N.K., Sharma, V.K., Yusuf, M.A. & Chakraborty, S.A. (2015). Geminivirus betasatellite damages the structural and functional integrity of chloroplasts leading to sympto m formation and inhibition of photosynthesis. J. Exp. Bot., 66 (19), pp. 5881-5895. https://doi.org/10.1093/jxb/erv299
119. Seo, E.Y., Nam, J., Kim, H.S., Park, Y.H., Hong, S.M., Lakshman, D., Bae, H., Hammond, J. & Lim, H.S. (2014) Selective interaction between chloroplast b-ATPase and TGB1L88 retards Server symptoms caused by Alternanthera mosaic virus infection. Plant Pathol. J., 30, pp. 58-67. https://doi.org/10.5423/PPJ.OA.09.2013.0097
120. Karjee, S., Islam, M.N. & Mukherjee, S.K. (2008). Screening and identification of virus-encoded RNA silencing suppressors. Method. Mol. Biol., 442, pp. 187-203. https://doi.org/10.1007/978-1-59745-191-8_14