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The Ralstonia pseudosolanacearum Type III Effector RipL Delays Flowering and Promotes Susceptibility to Pseudomonas syringae in Arabidopsis thaliana

  • Wanhui Kim (Plant Immunity Research Center, Seoul National University) ;
  • Hyelim Jeon (Plant Immunity Research Center, Seoul National University) ;
  • Hyeonjung Lee (School of Interdisciplinary Bioscience and Bioengineering, Pohang University of Science and Technology) ;
  • Kee Hoon Sohn (Plant Immunity Research Center, Seoul National University) ;
  • Cecile Segonzac (Plant Immunity Research Center, Seoul National University)
  • 투고 : 2023.08.02
  • 심사 : 2023.09.24
  • 발행 : 2023.11.30

초록

The plant defense responses to microbial infection are tightly regulated and integrated with the developmental program for optimal resources allocation. Notably, the defense-associated hormone salicylic acid (SA) acts as a promoter of flowering while several plant pathogens actively target the flowering signaling pathway to promote their virulence or dissemination. Ralstonia pseudosolanacearum inject tens of effectors in the host cells that collectively promote bacterial proliferation in plant tissues. Here, we characterized the function of the broadly conserved R. pseudosolanacearum effector RipL, through heterologous expression in Arabidopsis thaliana. RipL-expressing transgenic lines presented a delayed flowering, which correlated with a low expression of flowering regulator genes. Delayed flowering was also observed in Nicotiana benthamiana plants transiently expressing RipL. In parallel, RipL promoted plant susceptibility to virulent strains of Pseudomonas syringae in the effector-expressing lines or when delivered by the type III secretion system. Unexpectedly, SA accumulation and SA-dependent immune signaling were not significantly affected by RipL expression. Rather, the RNA-seq analysis of infected RipL-expressing lines revealed that the overall amplitude of the transcriptional response was dampened, suggesting that RipL could promote plant susceptibility in an SA-independent manner. Further elucidation of the molecular mechanisms underpinning RipL effect on flowering and immunity may reveal novel effector functions in host cells.

키워드

과제정보

This work was carried out with the support of the National Research Foundation of Korea (NRF) projects No. 2022R1I1A1A01066399, No. 2019R1I1A1A01060721, and No. 2018R1A5A1023599.

참고문헌

  1. Banday, Z.Z. and Nandi, A.K. (2015). Interconnection between flowering time control and activation of systemic acquired resistance. Front. Plant Sci. 6, 174.
  2. Bauters, L., Stojilkovic, B., and Gheysen, G. (2021). Pathogens pulling the strings: effectors manipulating salicylic acid and phenylpropanoid biosynthesis in plants. Mol. Plant Pathol. 22, 1436-1448. https://doi.org/10.1111/mpp.13123
  3. Berens, M.L., Berry, H.M., Mine, A., Argueso, C.T., and Tsuda, K. (2017). Evolution of hormone signaling networks in plant defense. Annu. Rev. Phytopathol. 55, 401-425. https://doi.org/10.1146/annurev-phyto-080516-035544
  4. Bouche, F., Lobet, G., Tocquin, P., and Perilleux, C. (2016). FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res. 44(D1), D1167-D1171. https://doi.org/10.1093/nar/gkv1054
  5. Buttner, D. and He, S.Y. (2009). Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150, 1656-1664. https://doi.org/10.1104/pp.109.139089
  6. Campos, M.L., de Souza, C.M., de Oliveira, K.B.S., Dias, S.C., and Franco, O.L. (2018). The role of antimicrobial peptides in plant immunity. J. Exp. Bot. 69, 4997-5011. https://doi.org/10.1093/jxb/ery294
  7. Cho, H.J., Kim, J.J., Lee, J.H., Kim, W., Jung, J.H., Park, C.M., and Ahn, J.H. (2012). SHORT VEGETATIVE PHASE (SVP) protein negatively regulates miR172 transcription via direct binding to the pri-miR172a promoter in Arabidopsis. FEBS Lett. 586, 2332-2337. https://doi.org/10.1016/j.febslet.2012.05.035
  8. Coll, N.S. and Valls, M. (2013). Current knowledge on the Ralstonia solanacearum type III secretion system. Microb. Biotechnol. 6, 614-620. https://doi.org/10.1111/1751-7915.12056
  9. Cook, D.E., Mesarich, C.H., and Thomma, B.P.H.J. (2015). Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53, 541-563. https://doi.org/10.1146/annurev-phyto-080614-120114
  10. Dillon, M.M., Almeida, R.N.D., Laflamme, B., Martel, A., Weir, B.S., Desveaux, D., and Guttman, D.S. (2019). Molecular evolution of Pseudomonas syringae type III secreted effector proteins. Front. Plant Sci. 10, 418.
  11. Engler, C., Kandzia, R., and Marillonnet, S. (2008). A one pot, one step, precision cloning method with high throughput capability. PLoS One 3, e3647.
  12. Fernandez-Santos, R., Izquierdo, Y., Lopez, A., Muniz, L., Martinez, M., Cascon, T., Hamberg, M., and Castresana, C. (2020). Protein profiles of lipid droplets during the hypersensitive defense response of Arabidopsis against Pseudomonas infection. Plant Cell Physiol. 61, 1144-1157. https://doi.org/10.1093/pcp/pcaa041
  13. Fornara, F., Panigrahi, K.C.S., Gissot, L., Sauerbrunn, N., Ruhl, M., Jarillo, J.A., and Coupland, G. (2009). Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 17, 75-86. https://doi.org/10.1016/j.devcel.2009.06.015
  14. Genin, S. and Denny, T.P. (2012). Pathogenomics of the Ralstonia solanacearum species complex. Annu. Rev. Phytopathol. 50, 67-89. https://doi.org/10.1146/annurev-phyto-081211-173000
  15. Gimenez-Ibanez, S., Hann, D.R., Ntoukakis, V., Petutschnig, E., Lipka, V., and Rathjen, J.P. (2009b). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423-429. https://doi.org/10.1016/j.cub.2009.01.054
  16. Gimenez-Ibanez, S., Ntoukakis, V., and Rathjen, J.P. (2009a). The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Signal. Behav. 4, 539-541. https://doi.org/10.4161/psb.4.6.8697
  17. Gupta, S., Malviya, N., Kushwaha, H., Nasim, J., Bisht, N.C., Singh, V.K., and Yadav, D. (2015). Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta 241, 549-562. https://doi.org/10.1007/s00425-014-2239-3
  18. Howard, B.E., Hu, Q., Babaoglu, A.C., Chandra, M., Borghi, M., Tan, X., He, L., Winter-Sederoff, H., Gassmann, W., Veronese, P., et al. (2013). Highthroughput RNA sequencing of Pseudomonas-infected Arabidopsis reveals hidden transcriptome complexity and novel splice variants. PLoS One 8, e74183.
  19. Hulsmans, S., Rodriguez, M., De Coninck, B., and Rolland, F. (2016). The SnRK1 energy sensor in plant biotic interactions. Trends Plant Sci. 21, 648-661. https://doi.org/10.1016/j.tplants.2016.04.008
  20. Huot, B., Yao, J., Montgomery, B.L., and He, S.Y. (2014). Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7, 1267-1287. https://doi.org/10.1093/mp/ssu049
  21. Jelenska, J., Yao, N., Vinatzer, B.A., Wright, C.M., Brodsky, J.L., and Greenberg, J.T. (2007). A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 17, 499-508. https://doi.org/10.1016/j.cub.2007.02.028
  22. Jeon, H., Kim, W., Kim, B., Lee, S., Jayaraman, J., Jung, G., Choi, S., Sohn, K.H., and Segonzac, C. (2020). Ralstonia solanacearum type III effectors with predicted nuclear localization signal localize to various cell compartments and modulate immune responses in Nicotiana spp. Plant Pathol. J. 36, 43-53.
  23. Kazan, K. and Lyons, R. (2016). The link between flowering time and stress tolerance. J. Exp. Bot. 67, 47-60. https://doi.org/10.1093/jxb/erv441
  24. Kim, E.H., Kim, S.H., Chung, J.I., Chi, H.Y., Kim, J.A., and Chung, I.M. (2006). Analysis of phenolic compounds and isoflavones in soybean seeds (Glycine max (L.) Merill) and sprouts grown under different conditions. Eur. Food Res. Technol. 222, 201-208. https://doi.org/10.1007/s00217-005-0153-4
  25. Kim, J.J., Lee, J.H., Kim, W., Jung, H.S., Huijser, P., and Ahn, J.H. (2012). The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol. 159, 461-478. https://doi.org/10.1104/pp.111.192369
  26. Koseoglou, E., van der Wolf, J.M., Visser, R.G.F., and Bai, Y. (2022). Susceptibility reversed: modified plant susceptibility genes for resistance to bacteria. Trends Plant Sci. 27, 69-79. https://doi.org/10.1016/j.tplants.2021.07.018
  27. Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop, R.M., 2nd, and Peterson, K.M. (1995). Four new derivatives of the broad-hostrange cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166, 175-176. https://doi.org/10.1016/0378-1119(95)00584-1
  28. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. (2004). The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16, 3496-3507. https://doi.org/10.1105/tpc.104.026765
  29. Landry, D., Gonzalez-Fuente, M., Deslandes, L., and Peeters, N. (2020). The large, diverse, and robust arsenal of Ralstonia solanacearum type III effectors and their in planta functions. Mol. Plant Pathol. 21, 1377-1388. https://doi.org/10.1111/mpp.12977
  30. Lee, H., Suh, S.S., Park, E., Cho, E., Ahn, J.H., Kim, S.G., Lee, J.S., Kwon, Y.M., and Lee, I. (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366-2376. https://doi.org/10.1101/gad.813600
  31. Lee, J.H., Yoo, S.J., Park, S.H., Hwang, I., Lee, J.S., and Ahn, J.H. (2007). Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev. 21, 397-402. https://doi.org/10.1101/gad.1518407
  32. Lefevere, H., Bauters, L., and Gheysen, G. (2020). Salicylic acid biosynthesis in plants. Front. Plant Sci. 11, 338.
  33. Li, L.S., Ying, J., Li, E., Ma, T., Li, M., Gong, L.M., Wei, G., Zhang, Y., and Li, S. (2021). Arabidopsis CBP60b is a central transcriptional activator of immunity. Plant Physiol. 186, 1645-1659. https://doi.org/10.1093/plphys/kiab164
  34. Lijavetzky, D., Carbonero, P., and Vicente-Carbajosa, J. (2003). Genomewide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol. Biol. 3, 17.
  35. Lin, N.C. and Martin, G.B. (2005). An avrPto/avrPtoB mutant of Pseudomonas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Mol. Plant Microbe Interact. 18, 43-51. https://doi.org/10.1094/MPMI-18-0043
  36. Lowe-Power, T.M., Khokhani, D., and Allen, C. (2018). How Ralstonia solanacearum exploits and thrives in the flowing plant xylem environment. Trends Microbiol. 26, 929-942. https://doi.org/10.1016/j.tim.2018.06.002
  37. Lurin, C., Andres, C., Aubourg, S., Bellaoui, M., Bitton, F., Bruyere, C., Caboche, M., Debast, C., Gualberto, J., Hoffmann, B., et al. (2004). Genomewide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089-2103. https://doi.org/10.1105/tpc.104.022236
  38. MacFarlane, S.A. and Popovich, A.H. (2000). Efficient expression of foreign proteins in roots from Tobravirus vectors. Virology 267, 29-35. https://doi.org/10.1006/viro.1999.0098
  39. Macho, A.P. (2016). Subversion of plant cellular functions by bacterial type-III effectors: beyond suppression of immunity. New Phytol. 210, 51-57. https://doi.org/10.1111/nph.13605
  40. MacLean, A.M., Orlovskis, Z., Kowitwanich, K., Zdziarska, A.M., Angenent, G.C., Immink, R.G., and Hogenhout, S.A. (2014). Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLoS Biol. 12, e1001835.
  41. MacLean, A.M., Sugio, A., Makarova, O.V., Findlay, K.C., Grieve, V.M., Toth, R., Nicolaisen, M., and Hogenhout, S.A. (2011). Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiol. 157, 831-841. https://doi.org/10.1104/pp.111.181586
  42. Manna, S. (2015). An overview of pentatricopeptide repeat proteins and their applications. Biochimie 113, 93-99. https://doi.org/10.1016/j.biochi.2015.04.004
  43. Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S.V., Machado, M.A., et al. (2012). Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13, 614-629. https://doi.org/10.1111/j.1364-3703.2012.00804.x
  44. March-Diaz, R., Garcia-Dominguez, M., Florencio, F.J., and Reyes, J.C. (2007). SEF, a new protein required for flowering repression in Arabidopsis, interacts with PIE1 and ARP6. Plant Physiol. 143, 893-901. https://doi.org/10.1104/pp.106.092270
  45. March-Diaz, R., Garcia-Dominguez, M., Lozano-Juste, J., Leon, J., Florencio, F.J., and Reyes, J.C. (2008). Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J. 53, 475-487. https://doi.org/10.1111/j.1365-313X.2007.03361.x
  46. Mukaihara, T., Tamura, N., and Iwabuchi, M. (2010). Genome-wide identification of a large repertoire of Ralstonia solanacearum type III effector proteins by a new functional screen. Mol. Plant Microbe Interact. 23, 251-262. https://doi.org/10.1094/MPMI-23-3-0251
  47. Nafisi, M., Goregaoker, S., Botanga, C.J., Glawischnig, E., Olsen, C.E., Halkier, B.A., and Glazebrook, J. (2007). Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell 19, 2039-2052. https://doi.org/10.1105/tpc.107.051383
  48. Nakamura, Y., Andres, F., Kanehara, K., Liu, Y.C., Dormann, P., and Coupland, G. (2014). Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering. Nat. Commun. 5, 3553.
  49. Nakano, M. and Mukaihara, T. (2018). Ralstonia solanacearum type III effector RipAL targets chloroplasts and induces jasmonic acid production to suppress salicylic acid-mediated defense responses in plants. Plant Cell Physiol. 59, 2576-2589. https://doi.org/10.1093/pcp/pcy177
  50. Ngou, B.P.M., Ding, P., and Jones, J.D.G. (2022). Thirty years of resistance: zig-zag through the plant immune system. Plant Cell 34, 1447-1478. https://doi.org/10.1093/plcell/koac041
  51. Peeters, N., Carrere, S., Anisimova, M., Plener, L., Cazale, A.C., and Genin, S. (2013). Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex. BMC Genomics 14, 859.
  52. Perez-Quintero, A.L. and Szurek, B. (2019). A decade decoded: spies and hackers in the history of TAL effectors research. Annu. Rev. Phytopathol. 57, 459-481. https://doi.org/10.1146/annurev-phyto-082718-100026
  53. Pieterse, C.M., Van der Does, D., Zamioudis, C., Leon-Reyes, A., and Van Wees, S.C. (2012). Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489-521. https://doi.org/10.1146/annurev-cellbio-092910-154055
  54. Prior, P., Ailloud, F., Dalsing, B.L., Remenant, B., Sanchez, B., and Allen, C. (2016). Genomic and proteomic evidence supporting the division of the plant pathogen Ralstonia solanacearum into three species. BMC Genomics 17, 90.
  55. Prokchorchik, M., Pandey, A., Moon, H., Kim, W., Jeon, H., Jung, G., Jayaraman, J., Poole, S., Segonzac, C., Sohn, K.H., et al. (2020). Host adaptation and microbial competition drive Ralstonia solanacearum phylotype I evolution in the Republic of Korea. Microb. Genom. 6, mgen000461.
  56. Pyc, M., Cai, Y., Gidda, S.K., Yurchenko, O., Park, S., Kretzschmar, F.K., Ischebeck, T., Valerius, O., Braus, G.H., Chapman, K.D., et al. (2017). Arabidopsis lipid droplet-associated protein (LDAP) - interacting protein (LDIP) influences lipid droplet size and neutral lipid homeostasis in both leaves and seeds. Plant J. 92, 1182-1201. https://doi.org/10.1111/tpj.13754
  57. Qi, P., Huang, M., Hu, X., Zhang, Y., Wang, Y., Li, P., Chen, S., Zhang, D., Cao, S., Zhu, W., et al. (2022). A Ralstonia solanacearum effector targets TGA transcription factors to subvert salicylic acid signaling. Plant Cell 34, 1666-1683. https://doi.org/10.1093/plcell/koac015
  58. Qin, J., Wang, K., Sun, L., Xing, H., Wang, S., Li, L., Chen, S., Guo, H.S., and Zhang, J. (2018). The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. Elife 7, e34902.
  59. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., Billault, A., Brottier, P., Camus, J.C., Cattolico, L., et al. (2002). Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415, 497-502. https://doi.org/10.1038/415497a
  60. Schwartz, A.R., Potnis, N., Timilsina, S., Wilson, M., Patane, J., Martins, J., Jr., Minsavage, G.V., Dahlbeck, D., Akhunova, A., Almeida, N., et al. (2015). Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front. Microbiol. 6, 535.
  61. Singh V., Roy S., Giri M.K., Chaturvedi, R., Chowdhury, Z., Shah, J., and Nandi, A.K. (2013). Arabidopsis thaliana FLOWERING LOCUS D is required for systemic acquired resistance. Mol. Plant Microbe Interact. 26, 1079-1088. https://doi.org/10.1094/MPMI-04-13-0096-R
  62. Sohn, K.H., Lei, R., Nemri, A., and Jones, J.D.G. (2007). The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19, 4077-4090. https://doi.org/10.1105/tpc.107.054262
  63. Sun, Y., Li, P., Shen, D., Wei, Q., He, J., and Lu, Y. (2019). The Ralstonia solanacearum effector RipN suppresses plant PAMP-triggered immunity, localizes to the endoplasmic reticulum and nucleus, and alters the NADH/NAD(+) ratio in Arabidopsis. Mol. Plant Pathol. 20, 533-546. https://doi.org/10.1111/mpp.12773
  64. Sun, Z., Guo, T., Liu, Y., Liu, Q., and Fang, Y. (2015). The roles of Arabidopsis CDF2 in transcriptional and posttranscriptional regulation of primary microRNAs. PLoS Genet. 11, e1005598.
  65. Susila, H., Juric, S., Liu, L., Gawarecka, K., Chung, K.S., Jin, S., Kim, S.J., Nasim, Z., Youn, G., Suh, M.C., et al. (2021). Florigen sequestration in cellular membranes modulates temperature-responsive flowering. Science 373, 1137-1142. https://doi.org/10.1126/science.abh4054
  66. Villajuana-Bonequi, M., Elrouby, N., Nordstrom, K., Griebel, T., Bachmair, A., and Coupland, G. (2014). Elevated salicylic acid levels conferred by increased expression of ISOCHORISMATE SYNTHASE 1 contribute to hyperaccumulation of SUMO1 conjugates in the Arabidopsis mutant early in short days. Plant J. 79, 206-219. https://doi.org/10.1111/tpj.12549
  67. Wang, L., Mitra, R.M., Hasselmann, K.D., Sato, M., Lenarz-Wyatt, L., Cohen, J.D., Katagiri, F., and Glazebrook, J. (2008). The genetic network controlling the Arabidopsis transcriptional response to Pseudomonas syringae pv. maculicola: roles of major regulators and the phytotoxin coronatine. Mol. Plant Microbe Interact. 21, 1408-1420. https://doi.org/10.1094/MPMI-21-11-1408
  68. Wilson, D.C., Kempthorne, C.J., Carella, P., Liscombe, D.K., and Cameron, R.K. (2017). Age-related resistance in Arabidopsis thaliana involves the MADS-Domain transcription factor SHORT VEGETATIVE PHASE and direct action of salicylic acid on Pseudomonas syringae. Mol. Plant Microbe Interact. 30, 919-929. https://doi.org/10.1094/MPMI-07-17-0172-R
  69. Winter, C.M., Austin, R.S., Blanvillain-Baufume, S., Reback, M.A., Monniaux, M., Wu, M.F., Sang, Y., Yamaguchi, A., Yamaguchi, N., Parker, J.E., et al. (2011). LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev. Cell 20, 430-443. https://doi.org/10.1016/j.devcel.2011.03.019
  70. Wirthmueller, L., Asai, S., Rallapalli, G., Sklenar, J., Fabro, G., Kim, D.S., Lintermann, R., Jaspers, P., Wrzaczek, M., Kangasjarvi, J., et al. (2018). Arabidopsis downy mildew effector HaRxL106 suppresses plant immunity by binding to RADICAL-INDUCED CELL DEATH1. New Phytol. 220, 232-248. https://doi.org/10.1111/nph.15277
  71. Woo, H.R., Dittmer, T.A., and Richards, E.J. (2008). Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis. PLoS Genet. 4, e1000156.
  72. Wroblewski, T., Caldwell, K.S., Piskurewicz, U., Cavanaugh, K.A., Xu, H., Kozik, A., Ochoa, O., McHale, L.K., Lahre, K., Jelenska, J., et al. (2009). Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol. 150, 1733-1749. https://doi.org/10.1104/pp.109.140251
  73. Xin, X.F., Kvitko, B., and He, S.Y. (2018). Pseudomonas syringae: what it takes to be a pathogen. Nat. Rev. Microbiol. 16, 316-328. https://doi.org/10.1038/nrmicro.2018.17
  74. Xue, B., Hamamouch, N., Li, C., Huang, G., Hussey, R.S., Baum, T.J., and Davis, E.L. (2013). The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots. Phytopathology 103, 175-181. https://doi.org/10.1094/PHYTO-07-12-0173-R
  75. Yang, Y. and Benning, C. (2018). Functions of triacylglycerols during plant development and stress. Curr. Opin. Biotechnol. 49, 191-198. https://doi.org/10.1016/j.copbio.2017.09.003
  76. Zhang, Y. and Li, X. (2019). Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50, 29-36. https://doi.org/10.1016/j.pbi.2019.02.004
  77. Zhang, Y., Xu, S., Ding, P., Wang, D., Cheng, Y.T., He, J., Gao, M., Xu, F., Li, Y., Zhu, Z., et al. (2010). Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc. Natl. Acad. Sci. U. S. A. 107, 18220-18225. https://doi.org/10.1073/pnas.1005225107
  78. Zheng, X., Li, X., Wang, B., Cheng, D., Li, Y., Li, W., Huang, M., Tan, X., Zhao, G., Song, B., et al. (2019). A systematic screen of conserved Ralstonia solanacearum effectors reveals the role of RipAB, a nuclear-localized effector that suppresses immune responses in potato. Mol. Plant Pathol. 20, 547-561. https://doi.org/10.1111/mpp.12774
  79. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J.D.G., Boller, T., and Felix, G. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749-760. https://doi.org/10.1016/j.cell.2006.03.037
  80. Zipfel, C. and Rathjen, J.P. (2008). Plant immunity: AvrPto targets the frontline. Curr. Biol. 18, R218-R220. https://doi.org/10.1016/j.cub.2008.01.016