Abstract
Main conclusion
This review highlights the most relevant and recent updated information available on the defense responses of selected hosts against Xanthomonas spp.
Abstract
Xanthomonas is one of the most important genera of Gram-negative phytopathogenic bacteria, severely affecting the productivity of economically important crops worldwide, colonizing either the vascular system or the mesophyll tissue of the host. Due to its rapid propagation, Xanthomonas poses an enormous challenge to farmers, because it is usually controlled using huge quantities of copper-based chemicals, adversely impacting the environment. Thus, developing new ways of preventing colonization by these bacteria has become essential. Advances in genomic and transcriptomic technologies have significantly elucidated at molecular level interactions between various crops and Xanthomonas species. Understanding how these hosts respond to the infection is crucial if we are to exploit potential approaches for improving crop breeding and cutting productivity losses. This review focuses on our current knowledge of the defense response mechanisms in agricultural crops after Xanthomonas infection. We describe the molecular basis of host–bacterium interactions over a broad spectrum with the aim of improving our fundamental understanding of which genes are involved and how they work in this interaction, providing information that can help to speed up plant breeding programs, namely using gene editing approaches.
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No datasets were generated or analyzed during the current study.
References
Aerts N, Pereira Mendes M, Van Wees SCM (2020) Multiple levels of crosstalk in hormone networks regulating plant defense. Plant J 105:489–504. https://doi.org/10.1111/tpj.15124
Afrin KS, Rahim MA, Park JI, Natarajan S, Kim HT, Nou IS (2018) Identification of NBS-encoding genes linked to black rot resistance in cabbage (Brassica oleracea var. Capitata). Mol Biol Rep 45:773–785. https://doi.org/10.1007/s11033-018-4217-5
Ali A, Chu N, Ma P, Javed T, Zaheer U, Huang MT, Fu HY, Gao SJ (2021a) Genome-wide analysis of mitogen-activated protein (MAP) kinase gene family expression in response to biotic and abiotic stresses in sugarcane. Physiol Plant 171:86–107. https://doi.org/10.1111/ppl.13208
Ali A, Javed T, Zaheer U, Zhou JR, Huang MT, Fu HY, Gao SJ (2021b) Genome-wide identification and expression profiling of the bHLH transcription factor gene family in Saccharum spontaneum under bacterial pathogen stimuli. Trop Plant Biol 14:283–294. https://doi.org/10.1007/s12042-021-09290-7
Alizadeh M, Askari H, Najafabadi MS (2017) Temporal expression of three conserved putative microRNAs in response of Citrus × Limon to Xanthomonas citri subsp. citri and Xanthomonas fuscans subsp. aurantifolii. Biotechnologia 98:257–264. https://doi.org/10.5114/bta.2017.70803
Alvarez-Martinez CE, Sgro GG, Araujo GG, Paiva MRN, Matsuyama BY, Guzzo CR, Andrade MO, Farah CS (2020) Secrete or perish: The role of secretion systems in Xanthomonas biology. Comput Struct Biotechnol J 19:279–302. https://doi.org/10.1016/j.csbj.2020.12.020
An S, Potnis N, Dow M, Vorhölter FJ, He Y, Becker A, Teper D, Li Yi, Wang N, Bleris L, Tang J (2020) Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol Rev 44:1–32. https://doi.org/10.1093/femsre/fuz024
Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–3876. https://doi.org/10.1105/tpc.110.078964
Bai W, Chern M, Ruan D, Canlas PE, Sze-To WH, Ronald PC (2011) Enhanced disease resistance and hypersensitivity to BTH by introduction of an NH1/OsNPR1 paralog. Plant Biotechnol J 9:205–215. https://doi.org/10.1111/j.1467-7652.2010.00544
Baltenneck J, Reverchon S, Hommais F (2021) Quorum sensing regulation in phytopathogenic bacteria. Microorganisms 9:239. https://doi.org/10.3390/microorganisms9020239
Behlau F, Gochez AM, Jones JB (2020) Diversity and copper resistance of Xanthomonas affecting citrus. Trop Plant Pathol 45:200–212. https://doi.org/10.1007/s40858-020-00340-1
Belkhadir Y, Yang L, Hetzel J, Dangl JL, Chory J (2014) The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem Sci 39:447–456. https://doi.org/10.1016/j.tibs.2014.06.006
Bernal I, Börnicke J, Heidemann J, Svergun D, Horstmann JA, Erhardt M, Tuukkanen A, Uetrecht C, Kolbe M (2019) Molecular organization of soluble type III secretion system sorting platform complexes. J Mol Biol 431:3787–3803. https://doi.org/10.1016/j.jmb.2019.07.004
Boch J, Bonas U, Lahaye T (2014) TAL effectors-pathogen strategies and plant resistance engineering. New Phytol 204:823–832. https://doi.org/10.1111/nph.13015
Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16:727–741. https://doi.org/10.1038/nrm4085
Boutrot F, Zipfel C (2017) Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu Rev Phytopathol 55:257–286. https://doi.org/10.1146/annurev-phyto-080614-120106
Buendia L, Girardin A, Wang T, Cottret L, Lefebvre B (2018) LysM receptor-like kinase and LysM receptor-like protein families: An update on phylogeny and functional characterization. Front Plant Sci 9:1531. https://doi.org/10.3389/fpls.2018.01531
Buist G, Steen A, Kok J, Kuipers OP (2008) LysM, a widely distributed protein motif for binding to (peptido) glycans. Mol Microbiol 68:838–847. https://doi.org/10.1111/j.1365-2958.2008.06211
Buscaill P, Chandrasekar B, Sanguankiattichai N, Kourelis J, Kaschani F, Thomas EL, Morimoto K, Kaiser M, Preston GM, Ichinose Y, van der Hoorn RAL (2019) Glycosidase and glycan polymorphism control hydrolytic release of immunogenic flagellin peptides. Science 364(6436):aav0748. https://doi.org/10.1126/science.aav0748
Cai Z, Yuan ZH, Zhang H, Pan Y, Wu Y, Tian XQ, Wang FF, Wang L, Qian W (2017) Fatty acid DSF binds and allosterically activates histidine kinase RpfC of phytopathogenic bacterium Xanthomonas campestris pv. campestris to regulate quorum-sensing and virulence. PLoS Pathog 13:e1006304. https://doi.org/10.1371/journal.ppat.1006304
Caicedo JC, Villamizar S, Ferro JA (2017) Quorum sensing, its role in virulence and symptomatology in bacterial citrus canker. In: Gill H, Garg H (eds) Citrus pathology. InTechOpen, London. https://doi.org/10.5772/66721
Cao J, Zhang M, Zhu M, He L, Xiao J, Li X, Yuan M (2019) Autophagy-like cell death regulates hydrogen peroxide and calcium ion distribution in Xa3/Xa26-mediated resistance to Xanthomonas oryzae pv. oryzae. Int J Mol Sci 21:194. https://doi.org/10.3390/ijms21010194
Cernadas RA, Camillo LR, Benedetti CE (2008) Transcriptional analysis of the sweet orange interaction with the citrus canker pathogens Xanthomonas axonopodis pv. citri and Xanthomonas axonopodis pv. aurantifolii. Mol Plant Pathol 9:609–631. https://doi.org/10.1111/j.1364-3703.2008.00486
Chatterjee S, Samal B, Singh P, Pradhan BB, Verma RK (2020) Transition of a solitary to a biofilm community life style in bacteria: a survival strategy with division of labour. Int J Dev Biol 64:259–265. https://doi.org/10.1387/ijdb.190176sc
Chen LQ (2013) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155. https://doi.org/10.1111/nph.12445
Chen LL, Yang L (2015) Regulation of circRNA biogenesis. RNA Biol 12:381–388. https://doi.org/10.1080/15476286.2015.1020271
Chen X, Liu P, Mei L, He X, Chen L, Liu H, Shen S, Ji Z, Zheng X, Zhang Y, Gao Z, Zeng D, Qian Q, Ma B (2021) Xa7, a new executor R gene that confers durable and broad-spectrum resistance to bacteria-blight disease in rice. Plant Commun 2:100143. https://doi.org/10.1016/j.xplc.2021.100143
Cheng X, Wu Y, Guo J, Du B, Chen R, Zhu L, He G (2013) A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J 76:687–698. https://doi.org/10.1111/tpj.12328
Chernyatina AA, Low HH (2019) Core architecture of a bacterial type II secretion system. Nat Commun 10:5437. https://doi.org/10.1038/s41467-019-13301-3
Choi DS, Hong JK, Hwang BK (2013a) Pepper osmotin-like protein 1 (CaOSM1) is an essential component for defense response, cell death, and oxidative burst in plants. Planta 238:1113–1124. https://doi.org/10.1007/s00425-013-1956-3
Choi HW, Kim NH, Lee YK, Hwang BK (2013b) The pepper extracellular xyloglucan-specific endo-β-1,4-glucanase inhibitor protein gene, CaXEGIP1, is required for plant cell death and defense responses. Plant Physiol 161:384–396. https://doi.org/10.1104/pp.112.203828
Choi DS, Kim NH, Hwang BK (2014) Pepper mitochondrial FORMATE DEHYDROGENASE1 regulates cell death and defense responses against bacterial pathogens. Plant Physiol 166:1298–1311. https://doi.org/10.1104/pp.114.246736
Choi N, Im JH, Lee E, Lee J, Choi C, Park SR, Hwang DJ (2020) WRKY10 transcriptional regulatory cascades in rice are involved in basal defense and Xa1-mediated resistance. J Exp Bot 71:3735–3748. https://doi.org/10.1093/jxb/eraa135
Cohn M, Bart RS, Shybut M, Dahlbeck D, Gomez M, Morbitzer R, Hou BH, Frommer WB, Lahaye T, Staskawicz BJ (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Mol Plant Microbe Interact 27:1186–1198. https://doi.org/10.1094/MPMI-06-14-0161-R
Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G (2015) Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13:343–359. https://doi.org/10.1038/nrmicro3456
Coulthurst S (2019) The type VI secretion system: a versatile bacterial weapon. Microbiology (reading) 165:503–515. https://doi.org/10.1099/mic.0.000789
Couto D, Zipfel C (2016) Regulation of pattern recognition receptor signaling in plants. Nat Rev Immunol 16:537–552. https://doi.org/10.1038/nri.2016.77
Cox KL, Meng F, Wilkins KE, Li F, Wang P, Booher NJ, Carpenter SCD, Chen LQ, Zheng H, Gao X, Zheng Y, Fei Z, Yu JZ, Isakeit T, Wheeler T, Frommer WB, Ping He W, Bogdanove AJ, Shan L (2017) TAL effector driven induction of a SWEET gene confers susceptibility to bacterial blight of cotton. Nat Commun 8:15588. https://doi.org/10.1038/ncomms15588
Delplace F, Huard-Chauveau C, Berthomé R, Roby D (2021) Network organization of the plant immune system: from pathogen perception to robust defense induction. Plant J 109:447–470. https://doi.org/10.1111/tpj.15462
Denny TP (1995) Involvement of bacterial polysaccharides in plant pathogenesis. Annu Rev Phytopathol 33:173–197. https://doi.org/10.1146/annurev.py.33.090195.001133
Di Lorenzo F, Silipo A, Andersen Gersby LB, Palmigiano A, Lanzetta R, Garozzo D, Boyer C, Pruvost O, Newman MA, Molinaro A (2017) Xanthomonas citri pv. citri pathotypes: LPS structure and function as microbe-associated molecular patterns. ChemBioChem 18:772–781. https://doi.org/10.1002/cbic.201600671
Díaz Tatis PA, Herrera Corzo M, Ochoa Cabezas JC, Medina Cipagauta A, Prías MA, Verdier V, Chavarriaga Aguirre P, López Carrascal CE (2018a) The overexpression of RXam1, a cassava gene coding for an RLK, confers disease resistance to Xanthomonas axonopodis pv. manihotis. Planta 247(4):1031–1042. https://doi.org/10.1007/s00425-018-2863-4
Díaz Tatis PA, Herrera Corzo M, Ochoa Cabezas JC, Medina Cipagauta A, Prías MA, Verdier V, Aguirre PC, López Carrascal CE (2018b) The overexpression of RXam1, a cassava gene coding for an RLK, confers disease resistance to Xanthomonas axonopodis pv. manihotis. Planta 247:1031–1042. https://doi.org/10.1007/s00425-018-2863-4
Díaz-Tatis PA, Ochoa JC, Rico EM, Rodríguez C, Medina A, Szurek B, Chavarriaga P, López CE (2022) RXam2, a NLR from cassava (Manihot esculenta) contributes partially to the quantitative resistance to Xanthomonas phaseoli pv. manihotis. Plant Mol Biol 109(3):313–324. https://doi.org/10.1007/s11103-021-01211-2
Ding L, Xu X, Kong W, Xia X, Zhang S, Liu LW, Liu A, Zou L (2020) Genome-wide identification and expression analysis of rice NLR genes responsive to the infections of Xanthomonas oryzae pv. oryzae and Magnaporthe oryzae. Physiol Mol Plant Pathol 111:101488. https://doi.org/10.1016/j.pmpp.2020.101488
Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357. https://doi.org/10.1016/0048-4059(83)90019-X
Du H, Wang Y, Yang J, Yang W (2015) Comparative transcriptome analysis of resistant and susceptible tomato lines in response to infection by Xanthomonas perforans race T3. Front Plant Sci 6:1173. https://doi.org/10.3389/fpls.2015.01173
Dubey N, Singh K (2018) Role of NBS-LRR proteins in plant defense. Molecular aspects of plant-pathogen interaction. In: Singh A, Singh I (eds) Molecular aspects of plant-pathogen interaction. Springer, Singapore, pp 115–138. https://doi.org/10.1007/978-981-10-7371-7_5
Dutta B, Langston DB, Luo X, Carlson S, Kichler J, Gitaitis R (2017) A risk assessment model for bacterial leaf spot of pepper (Capsicum annuum), caused by Xanthomonas euvesicatoria, based on concentrations of macronutrients, micronutrients, and micronutrient ratios. Phytopathology 107:1331–1338. https://doi.org/10.1094/PHYTO-05-17-0187-R
Engelhardt S, Stam R, Hückelhoven R (2018) Good riddance? Breaking disease susceptibility in the era of new breeding technologies. Agronomy 8:114. https://doi.org/10.3390/agronomy8070114
Fan E, Chauhan N, Udatha DBRKG, Leo JC, Linke D (2016) Type V secretion systems in bacteria. Microbiol Spectr. https://doi.org/10.1128/microbiolspec
Fan S, Chang Y, Liu G, Shang S, Tian L, Shi H (2020) Molecular functional analysis of auxin/indole-3-acetic acid proteins (Aux/IAAs) in plant disease resistance in cassava. Physiol Plant 168:88–97. https://doi.org/10.1111/ppl.12970
Feller A, Machemer K, Braun EL, Grotewold E (2021) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116. https://doi.org/10.1111/j.1365-313X.2010.04459.x
Fleming MB, Miller T, Fu W, Li Z, Gasic K, Saski C (2022) Ppe.XapF: high throughput KASP assays to identify fruit response to Xanthomonas arboricola pv. pruni (Xap) in peach. PLoS ONE 17(2):e0264543. https://doi.org/10.1371/journal.pone.0264543
Foucher J, Ruh M, Préveaux A, Carrère S, Pelletier S, Briand M, Chen NWG (2020) Common bean resistance to Xanthomonas is associated with upregulation of the salicylic acid pathway and downregulation of photosynthesis. BMC Genomics. https://doi.org/10.1186/s12864-020-06972-6
Fu H, Zhao M, Xu J, Tan L, Han J, Li D, Wang M, Xiao S, Ma X, Deng Z (2020) Citron C-05 inhibits both the penetration and colonization of Xanthomonas citri subsp. citri to achieve resistance to citrus canker disease. Hortic Res 7:58. https://doi.org/10.1038/s41438-020-0278-4
Gao S, Wang F, Niran J, Li N, Yin Y, Yu C, Jiao C, Yao M (2021) Transcriptome analysis reveals defense-related genes and pathways against Xanthomonas campestris pv. vesicatoria in pepper (Capsicum annuum L.). PLoS ONE 16:e0240279. https://doi.org/10.1371/journal.pone.0240279
Garita-Cambronero J, Palacio-Bielsa A, López MM, Cubero J (2016) Comparative genomic and phenotypic characterization of pathogenic and non-pathogenic strains of Xanthomonas arboricola reveals insights into the infection process of bacterial spot disease of stone fruits. PLoS ONE 11:e0161977. https://doi.org/10.1371/journal.pone.0161977
Gasic K, Reighard G, Okie W, Clark J, Gradziel T, Byrne D, Peace C, Stegmeir T, Rosyara U, Iezzoni A (2015) Bacterial spot resistance in peach: functional allele distribution in breeding germplasm. Acta Hortic 1084:69–74. https://doi.org/10.17660/ActaHortic.2015.1084.7
Gervasi F, Ferrante P, Dettori MT, Scortichini M, Verde I (2018) Transcriptome reprogramming of resistant and susceptible peach genotypes during Xanthomonas arboricola pv. pruni early leaf infection. PLoS ONE 13:e0196590. https://doi.org/10.1371/journal.pone.0196590
Giraldo-González JJ, de Souza Carvalho FM, Ferro JA, Herai RH, Bedoya GC, Mendoza EFR (2021) Transcriptional changes involved in kumquat (Fortunella spp) defense response to Xanthomonas citri subsp. citri in early stages of infection. Physiol Mol Plant Pathol. https://doi.org/10.1016/j.pmpp.2021.101729
Gu K, Tian D, Yang F, Wu L, Sreekala C, Wang D, Wang GL, Yin Z (2004) High-resolution genetic mapping of Xa27(t), a new bacterial blight resistance gene in rice, Oryza sativa L. Theor Appl Genet 108:800–807. https://doi.org/10.1007/s00122-003-1491-x
Gupta PK (2020) SWEET Genes for disease resistance in plants. Trends Genet 36:901–904. https://doi.org/10.1016/j.tig.2020.08.007
Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Götz F, Glawischnig E, Lee J, Felix G, Nürnberger T (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282:32338–32348. https://doi.org/10.1074/jbc.M704886200
He YW, Wu J, Cha JS, Zhang LH (2010) Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiol 10:187. https://doi.org/10.1186/1471-2180-10-187
He YW, Cao XQ, Poplawsky AR (2020) Chemical structure, biological roles, biosynthesis and regulation of the yellow xanthomonadin pigments in the phytopathogenic genus Xanthomonas. Mol Plant Microbe Interact 33:705–714. https://doi.org/10.1094/MPMI-11-19-0326-CR
Hu Y, Zhang J, Jia H, Sosso D, Li T, Frommer WB, Yang B, White FF, Wang N, Jones JB (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci 111:E521–E529. https://doi.org/10.1073/pnas.1313271111
Hu K, Cao J, Zhang J, Xia F, Ke Y, Zhang H, Xie W, Liu H, Cui Y, Cao Y, Sun X, Xiao J, Li X, Zhang Q, Wang S (2017) Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement. Nat Plants 3:17009. https://doi.org/10.1038/nplants.2017.9
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:800. https://doi.org/10.3389/fpls.2019.00800
Huang S, Tang Z, Zhao R, Hong Y, Zhu S, Fan R, Ding K, Cao M, Luo K, Geng M, Jiang L, Chen Y (2021) Genome-wide identification of cassava MeRboh genes and functional analysis in Arabidopsis. Plant Physiol and Biochem 167:296–308. https://doi.org/10.1016/j.plaphy.2021.07.039
Hutin M, Sabot F, Ghesquière A, Koebnik R, Szurek B (2015) A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. Plant J 84:694–703. https://doi.org/10.1111/tpj.13042
Hwang IS, Hwang BK (2010) Role of the pepper cytochrome P450 gene CaCYP450A in defense responses against microbial pathogens. Planta 232:1409–1421. https://doi.org/10.1007/s00425-010-1266-y
Hwang IS, Choi DS, Kim NH, Kim DS, Hwang BK (2014) The pepper cysteine/histidine-rich DC1 domain protein CaDC1 binds both RNA and DNA and is required for plant cell death and defense response. New Phytol 201:518–530. https://doi.org/10.1111/nph.12521
Hwang SH, Kwon SI, Jang JY, Fang IL, Lee H, Choi C, Park S, Ahn I, Bae SC, Hwang DJ (2016) OsWRKY51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas oryzae pv. oryzae. Plant Cell Rep 35:1975–1985. https://doi.org/10.1007/s00299-016-2012-0
Im JH, Lee SG, Lee E, Park SR, Ahn I, Hwang DJ (2019) OsbZIP75 positively regulates plant defense against the bacterial leaf blight pathogen Xanthomonas oryzae pv. oryzae. Plant Biotechnol Rep 13:645–651. https://doi.org/10.1007/s11816-019-00561-0
Ishida AKN, Halfeld-Vieira BA (2009) Mancha-bacteriana do maracujazeiro (Xanthomonas axonopodis pv passiflorae): Etiologia e estratégias de controle. Documentos Embrapa Amazonia Oriental 357:22
Islam MT, Lee BR, Park SH, La VH, Bae DW, Kim TH (2017) Cultivar variation in hormonal balance is a significant determinant of disease susceptibility to Xanthomonas campestris pv. campestris in Brassica napus. Front Plant Sci 8:2121. https://doi.org/10.3389/fpls.2017.02121
Itako AT, Tolentino Júnior JB, Silva Júnior TA, Soman JM, Maringoni AC (2015) Chemical products induce resistance to Xanthomonas perforans in tomato. Braz J Microbiol 46(3):701–706. https://doi.org/10.1590/S1517-838246320140177
Jacobs JM, Pesce C, Lefeuvre P, Koebnik R (2015) Comparative genomics of a cannabis pathogen reveals insight into the evolution of pathogenicity in Xanthomonas. Front Plant Sci 6:431. https://doi.org/10.3389/fpls.2015.00431
Jalmi S, Sinha A (2016) Functional involvement of a mitogen activated protein kinase module, OsMKK3-OsMPK7-OsWRK30 in mediating resistance against Xanthomonas oryzae in rice. Sci Rep 6:37974. https://doi.org/10.1038/srep37974
Jia H, Omar AA, Orbović V, Wang N (2022) Biallelic editing of the LOB1 promoter via CRISPR/Cas9 creates canker-resistant ‘Duncan’ grapefruit. Phytopathol 112(2):308–314. https://doi.org/10.1094/PHYTO-04-21-0144-R
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Jordan T, Römer P, Meyer A, Szczesny R, Pierre M, Piffanelli P, Bendahmane A, Bonas U, Lahaye T (2006) Physical delimitation of the pepper Bs3 resistance gene specifying recognition of the AvrBs3 protein from Xanthomonas campestris pv. vesicatoria. Theor Appl Genet 113:895–905. https://doi.org/10.1007/s00122-006-0349-4
Katzen F, Ferreiro DU, Oddo CG, Ielmini MV, Becker A, Pühler A, Ielpi L (1998) Xanthomonas campestris pv. campestris gum mutants: effects on xanthan biosynthesis and plant virulence. J Bacteriol 180:1607–1617. https://doi.org/10.1128/JB.180.7.1607-1617.1998
Kim JG, Mudgett MB (2019) Tomato bHLH132 transcription factor controls growth and defense and is activated by Xanthomonas euvesicatoria effector XopD during pathogenesis. Mol Plant Microbe Interact 32:1614–1622. https://doi.org/10.1094/MPMI-05-19-0122-R
Kim SY, Kim YC, Lee JH, Oh SK, Chung E, Lee S, Lee YH, Choi D, Park JM (2005) Identification of a CaRAV1 possessing an AP2/ERF and B3 DNA-binding domain from pepper leaves infected with Xanthomonas axonopodis pv. glycines 8ra by differential display. Biochim Biophys Acta 1729:141–146. https://doi.org/10.1016/j.bbaexp.2005.04.009
Kong Y, Wang G, Chen X, Li L, Zhang X, Chen S, He Y, Hong G (2021) OsPHR2 modulates phosphate starvation-induced OsMYC2 signalling and resistance to Xanthomonas oryzae pv. oryzae. Plant Cell Environ 44:3432–3444. https://doi.org/10.1111/pce.14078
Lee D, Lal NK, Lin ZJD, Ma S, Liu J, Castro B, Toruño T, Dinesh-Kumar SP, Coaker G (2020) Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD. Nat Commun 11:1838. https://doi.org/10.1038/s41467-020-15601-5
Lefevere H, Bauters L, Gheysen G (2020) Salicylic acid biosynthesis in plants. Front Plant Sci 11:338. https://doi.org/10.3389/fpls.2020.00338
Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, Chen S, Zhou JM (2014a) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–338. https://doi.org/10.1016/j.chom.2014.02.009
Li Z, Zou L, Ye G, Xiong L, Ji Z, Zakria M, Hong N, Wang G, Chen G (2014b) A potential disease susceptibility gene CsLOB of citrus is targeted by a major virulence effector PthA of Xanthomonas citri subsp. citri. Mol Plant 7:912–915. https://doi.org/10.1093/mp/sst176
Li X, Fan S, Hu W, Liu G, Wei Y, He C, Shi H (2017) Two cassava basic leucine zipper (bZIP) transcription factors (MebZIP3 and MebZIP5) confer disease resistance against cassava bacterial blight. Front Plant Sci 8:2110. https://doi.org/10.3389/fpls.2017.02110
Li L, Li J, Zhang Y, Wang N (2019) Diffusible signal factor (DSF)-mediated quorum sensing modulates expression of diverse traits in Xanthomonas citri and responses of citrus plants to promote disease. BMC Genomics 20:55. https://doi.org/10.1186/s12864-018-5384-4
Li Q, Qi J, Qin X, Hu A, Fu Y, Chen S, He Y (2021) Systematic identification of lysin-motif receptor-like kinases (LYKs) in Citrus sinensis, and analysis of their inducible involvements in citrus bacterial canker and phytohormone signaling. Sci Hortic 276:109755. https://doi.org/10.1016/j.scienta.2020.109755
Liang X, Zhou JM (2018) Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu Rev Plant Biol 69:267–299. https://doi.org/10.1146/annurev-arplant-042817-040540
Liao H, Xiao X, Li X, Chen Y, Fu X, Lin D, Niu X, Chen Y, He C (2016) OsBAK1 is involved in rice resistance to Xanthomonas oryzae pv. oryzae PXO99. Plant Biotechnol Rep 10:75–82. https://doi.org/10.1007/s11816-016-0387-6
Liebrand TW, Van den Burg HA, Joosten MH (2014) Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19:123–132. https://doi.org/10.1016/j.tplants.2013.10.003
Lima Silva CC, de Shimo HM, de Felício R, Mercaldi GF, Rocco SA, Benedetti CE (2019) Structure-function relationship of a citrus salicylate methylesterase and role of salicylic acid in citrus canker resistance. Sci Rep 9:3901. https://doi.org/10.1038/s41598-019-40552-3
Liu B, Li JF, Ao Y, Qu J, Li Z, Su J, Zhang Y, Liu J, Feng D, Qi K, He Y, Wang J, Wang HB (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–3419. https://doi.org/10.1105/tpc.112.102475
Liu Y, Sun T, Sun Y, Zhang Y, Radojičić A, Ding Y, Tian H, Huang X, Lan J, Chen S, Ar O, Zhang K, Jetter R, Li X, Zhang Y (2020a) Diverse roles of the salicylic acid receptors NPR1 and NPR3/NPR4 in plant immunity. Plant Cell 32:4002–4016. https://doi.org/10.1105/tpc.20.00499
Liu F, Zhang W, Schwessinger B, Wei T, Ruan D, Ronald P (2020b) The rice Xa3 gene confers resistance to Xanthomonas oryzae pv. oryzae in the model rice Kitaake genetic background. Front Plant Sci 11:49. https://doi.org/10.3389/fpls.2020b.00049
Liu X, Meng G, Wang M, Qian Z, Zhang Y, Yang W (2021) Tomato SlPUB24 enhances resistance to Xanthomonas euvesicatoria pv. perforans race T3. Hortic Res 8:30. https://doi.org/10.1038/s41438-021-00468-4
Long Q, Du M, Long J, Xie Y, Zhang J, Xu L, He Y, Li Q, Chen S, Zou X (2021) Transcription factor WRKY22 regulates canker susceptibility in sweet orange (Citrus sinensis Osbeck) by enhancing cell enlargement and CsLOB1 expression. Hortic Res. https://doi.org/10.1038/s41438-021-00486-2
Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci 107:496–501. https://doi.org/10.1073/pnas.0909705107
Lu J, Wang C, Zhang F, Zeng D, Zhou Y (2020) Comparative microRNA profiling reveals microRNAs involved in rice resistant response to bacterial blight. Crop J 9:834–842. https://doi.org/10.1016/j.cj.2020.08.009
Ma X, Xu G, He P, Shan L (2016) SERKing coreceptors for receptors. Trends Plant Sci 21:1017–1033. https://doi.org/10.1016/j.tplants.2016.08.014
Ma X, Claus LAN, Leslie ME, Tao K, Wu Z, Liu J, Yu X, Li B, Zhou J, Savatin DV, Peng J, Tyler BM, Heese A, Russinova E, He P, Shan L (2020) Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature 581:199–203. https://doi.org/10.1038/s41586-020-2210-3
Mamun MA, Islam MT, Lee BR, La VH, Bae DW, Kim TH (2020) Genotypic variation in resistance gene-mediated calcium signaling and hormonal signaling involved in effector-triggered immunity or disease susceptibility in the Xanthomonas campestris pv. campestris-Brassica napus pathosystem. Plants 9:303. https://doi.org/10.3390/plants9030303
Martins L, Fernandes C, Blom J, Dia NC, Pothier JF, Tavares F (2020) Xanthomonas euroxanthea sp. nov., a new xanthomonad species including pathogenic and non-pathogenic strains of walnut. Int J Syst Evol Microbiol 70:6024–6031. https://doi.org/10.1099/ijsem.0.004386
Mei P, Song Z, Li Z, Zhou C (2019) Functional study of Csrbohs in defence response against Xanthomonas citri ssp. citri. Funct Plant Biol 46:543–554. https://doi.org/10.1071/fp18243
Mei PY, Zhou Y, Li ZA, Zhou CY (2020) New insights into the resistance of four citrus genotypes to Xanthomonas citri subsp. citri. J Plant Pathol. https://doi.org/10.1007/s42161-020-00493-7
Melech-Bonfil S, Sessa G (2011) The SlMKK2 and SlMPK2 genes play a role in tomato disease resistance to Xanthomonas campestris pv. vesicatoria. Plant Signal Behav 6:154–156. https://doi.org/10.4161/psb.6.1.14311
Mitre LK, Teixeira-Silva NS, Rybak K, Magalhães DM, de Souza-Neto RR, Robatzek S, Zipfel C, de Souza AA (2021) The Arabidopsis immune receptor EFR increases resistance to the bacterial pathogens Xanthomonas and Xylella in transgenic sweet orange. Plant Biotechnol J 19:1294–1296. https://doi.org/10.1111/pbi.13629
Moeder W, Phan V, Yoshioka K (2019) Ca2+ to the rescue–Ca2+channels and signaling in plant immunity. Plant Sci 279:19–26. https://doi.org/10.1016/j.plantsci.2018.04.012
Munhoz CF, Weiss B, Hanai LR, Zucchi MI, Fungaro MHP, Oliveira ALM, Monteiro-Vitorello CB, Vieira MLC (2011) Genetic diversity and a PCR-based method for Xanthomonas axonopodis detection in passion fruit. Phytopathol 101:416–424. https://doi.org/10.1094/PHYTO-06-10-0169
Munhoz CF, Santos AA, Arenhart RA, Santini L, Monteiro-Vitorello CB, Vieira MLC (2015) Analysis of plant gene expression during passion fruit-Xanthomonas axonopodis interaction implicates lipoxygenase 2 in host defence. Ann Appl Biol 167:135–155. https://doi.org/10.1111/aab.12215
Muñoz-Bodnar A, Perez-Quintero AL, Gomez-Cano F, Gil J, Michelmore R, Bernal A, Szurek B, Lopez C (2014) RNAseq analysis of cassava reveals similar plant responses upon infection with pathogenic and non-pathogenic strains of Xanthomonas axonopodis pv. manihotis. Plant Cell Rep 33:1901–1912. https://doi.org/10.1007/s00299-014-1667-7
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439. https://doi.org/10.1126/science.1126088
Noman A, Aqeel M, Lou Y (2019) PRRs and NB-LRRs: from signal perception to activation of plant innate immunity. Int J Mol Sci 20:1882. https://doi.org/10.3390/ijms20081882
Ogawa T, Tabien RE, Busto GA, Khush GS, Mew TW (1986) The relationships between Xa-3, Xa-4, and Xa-4b for resistances to rice bacterial blight. Rice Genet Newslet 3:83–84
Oliveira ML, de Lima Silva CC, Abe VY, Costa MG, Cernadas RA, Benedetti CE (2013) Increased resistance against citrus canker mediated by a citrus mitogen-activated protein kinase. Mol Plant Microbe Interact 26:1190–1199. https://doi.org/10.1094/MPMI-04-13-0122-R
Onohata T, Gomi K (2020) Overexpression of jasmonate-responsive OsbHLH034 in rice results in the induction of bacterial blight resistance via an increase in lignin biosynthesis. Plant Cell Rep 39:1175–1184. https://doi.org/10.1007/s00299-020-02555-7
Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70:5607–5612. https://doi.org/10.1099/ijsem.0.004332
Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X (2017) Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J 15:1509–1519. https://doi.org/10.1111/pbi.12733
Pérez-Quintero ÁL, Quintero A, Urrego O, Vanegas P, López C (2012) Bioinformatic identification of cassava miRNAs differentially expressed in response to infection by Xanthomonas axonopodis pv. manihotis. BMC Plant Biol 12:29. https://doi.org/10.1186/1471-2229-12-29
Peyraud R, Dubiella U, Barbacci A, Genin S, Raffaele S, Roby D (2017) Advances on plant-pathogen interactions from molecular toward systems biology perspectives. Plant J 90:720–737. https://doi.org/10.1111/tpj
Picchi SC, Granato LM, Franzini MJF, Andrade MO, Takita MA, Machado MA, de Souza AA (2021) Modified monosaccharides content of xanthan gum impairs citrus canker disease by affecting the epiphytic lifestyle of Xanthomonas citri subsp. citri. Microorganisms 9:1176. https://doi.org/10.3390/microorganisms9061176
Pieretti I, Cociancich S, Bolot S, Carrère S, Morisset A, Rott P, Royer M (2015) Full genome sequence analysis of two isolates reveals a novel Xanthomonas species close to the sugarcane pathogen Xanthomonas albilineans. Genes 6:714–733. https://doi.org/10.3390/genes6030714
Pitsili E, Phukan UJ, Coll NS (2019) Cell death in plant immunity. Cold Spring Harb Perspect Biol 12:a036483. https://doi.org/10.1101/cshperspect.a036483
Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F, Albert M, Robinson MR, Chan LJ, Luu DD, Chen H, Bahar O, Daudi A, De Vleesschauwer D, Caddell D, Zhang W, Zhao X, Li X, Heazlewood JL, Ruan D, Majumder D, Chern M, Kalbacher H, Midha S, Patil PB, Sonti RV, Petzold CJ, Liu CC, Brodbelt JS, Felix G, Ronald PC (2015) The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a gram-negative bacterium. Sci Adv 24:e1500245. https://doi.org/10.1126/sciadv.1500245
Qi J, Wang J, Gong Z, Zhou JM (2017) Apoplastic ROS signaling in plant immunity. Curr Opin Plant Biol 38:92–100. https://doi.org/10.1016/j.pbi.2017.04.022
Raffeiner M, Üstün S, Guerra T, Spinti D, Fitzner M, Sonnewald S, Baldermann S, Börnke F (2022) The Xanthomonas type-III effector XopS stabilizes CaWRKY40a to regulate defense responses and stomatal immunity in pepper (Capsicum annuum). Plant Cell 34(5):1684–1708. https://doi.org/10.1093/plcell/koac032
Safaie-Farahani A, Taghavi SM (2017) Transcript analysis of some defense genes of tomato in response to host and non-host bacterial pathogens. Mol Biol Res Commun 6:177–183. https://doi.org/10.22099/mbrc.2017.25600.1273
Saijo Y, Loo EP, Yasuda S (2018) Pattern recognition receptors and signaling in plant-microbe interactions. Plant J 93:592–613. https://doi.org/10.1111/tpj.13808
Santos LS, Maximiano MR, Megias E, Pappas M, Ribeiro SG, Mehta A (2019) Quantitative expression of microRNAs in Brassica oleracea infected with Xanthomonas campestris pv. campestris. Mol Biol Rep 46:3523–3529. https://doi.org/10.1007/s11033-019-04779-7
Schornack S, Ballvora A, Gürlebeck D, Peart J, Ganal M, Baker B, Bonas U, Lahaye T (2004) The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37:46–60. https://doi.org/10.1046/j.1365-313x.2003.01937.x
Schornack S, Minsavage GV, Stall RE, Jones JB, Lahaye T (2008) Characterization of AvrHah1, a novel AvrBs3-like effector from Xanthomonas gardneri with virulence and avirulence activity. New Phytol 179:546–556. https://doi.org/10.1111/j.1469-8137.2008.02487.x
Schultink A, Qi T, Lee A, Steinbrenner AD, Staskawicz B (2017) Roq1 mediates recognition of the Xanthomonas and Pseudomonas effector proteins XopQ and HopQ1. Plant J 92(5):787–795. https://doi.org/10.1111/tpj.13715
Seo YS, Chern M, Bartley LE, Han M, Jung KH, Lee I, Walia H, Richter T, Xu X, Cao P, Bai W, Ramanan R, Amonpant F, Arul L, Canlas PE, Ruan R, Park CJ, Chen X, Hwang S, Jeon JS, Ronald PC (2011) Towards establishment of a rice stress response interactome. PLoS Genet 7:e1002020. https://doi.org/10.1371/journal.pgen.1002020
Seybold H, Trempel F, Ranf S, Scheel D, Romeis T, Lee J (2014) Ca2+ signalling in plant immune response: from pattern recognition receptors to Ca2+ decoding mechanisms. New Phytol 204:782–790. https://doi.org/10.1111/nph.13031
Sgro GG, Oka GU, Souza DP, Cenens W, Bayer-Santos E, Matsuyama BY, Bueno NF, Dos Santos TR, Alvarez-Martinez CE, Salinas RK, Farah CS (2019) Bacteria-killing type IV secretion systems. Front Microbiol 10:1078. https://doi.org/10.3389/fmicb.2019.01078
Shen X, Yuan B, Liu H, Li X, Xu C, Wang S (2010) Opposite functions of a rice mitogen-activated protein kinase during the process of resistance against Xanthomonas oryzae. Plant J 64:86–99. https://doi.org/10.1111/j.1365-313X.2010.04306.x
Shen X, Liu H, Yuan B, Li X, Xu C, Wang S (2011) OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant Cell Environ 34:179–191. https://doi.org/10.1111/j.1365-3040.2010.02219.x
Shigenaga AM, Berens ML, Tsuda K, Argueso CT (2017) Towards engineering of hormonal crosstalk in plant immunity. Curr Opin Plant Biol 38:164–172. https://doi.org/10.1016/j.pbi.2017.04.021
Socquet-Juglard D, Kamber T, Pothier JF, Christen D, Gessler C, Duffy B, Patochi A (2013) Comparative RNA-Seq analysis of early-infected peach leaves by the invasive phytopathogen Xanthomonas arboricola pv. pruni. PLoS ONE 8:e54196. https://doi.org/10.1371/journal.pone.0054196
Son S, An HK, Seol YJ, Park SR, Im JH (2020) Rice transcription factor WRKY114 directly regulates the expression of OsPR1a and chitinase to enhance resistance against Xanthomonas oryzae pv. oryzae. Biochem Biophys Res Commun 533:1262–1268. https://doi.org/10.1016/j.bbrc.2020.09.141
Son S, Moon SJ, Kim H, Lee KS, Park SR (2021) Identification of a novel NPR1 homolog gene, OsNH5N16, which contributes to broad-spectrum resistance in rice. Biochem Biophys Res Commun 549:200–206. https://doi.org/10.1016/j.bbrc.2021.02.108
Song L, Fang Y, Chen L, Wang J, Chen X (2021) Role of non-coding RNAs in plant immunity. Plant Commun 20:100180. https://doi.org/10.1016/j.xplc.2021.100180
Spitz O, Erenburg IN, Beer T, Kanonenberg K, Holland IB, Schmitt L (2019) Type I secretion systems-one mechanism for all? Microbiol Spectr. https://doi.org/10.1128/microbiolspec
Strauss T, van Poecke RM, Strauss A, Römer P, Minsavage GV, Singh S, Wolf C, Strauss A, Kim S, Lee HA, Yeom SI, Parniske M, Stall RE, Jones JB, Choi D, Prins M, Lahaye T (2012) RNA-seq pinpoints a Xanthomonas TAL-effector activated resistance gene in a large-crop genome. Proc Natl Acad 109:19480–19485. https://doi.org/10.1073/pnas.1212415109
Studholme DJ, Wasukira A, Paszkiewicz K, Aritua V, Thwaites R, Smith J, Grant M (2011) Draft Genome sequences of Xanthomonas sacchari and two banana-associated Xanthomonads reveal insights into the Xanthomonas group 1 clade. Genes 2:1050–1065. https://doi.org/10.3390/genes2041050
Sun W, Dunning M, Pfund C, Weingarten R, Bent AF (2006) Within-species flagellin polymorphism in Xanthomonas campestris pv. campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18:764–779. https://doi.org/10.1105/tpc.105.037648
Sun W, Cao Y, Jansen Labby K, Bittel P, Boller T, Bent AF (2012) Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function. Plant Cell 24:1096–1113. https://doi.org/10.1105/tpc.112.095919
Tabassum N, Blilou I (2021) Cell-to-cell communication during plant-pathogen interaction. Mol Plant Microbe Interact 35:98–108. https://doi.org/10.1094/MPMI-09-21-0221-CR
Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci 96(24):14153–14158. https://doi.org/10.1073/pnas.96.24.14153
Tang J, Wang Y, Yin W, Dong G, Sun K, Teng Z, Wu X, Wang S, Qian Y, Pan X, Qian Q, Chu C (2019) Mutation of a nucleotide-binding leucine-rich repeat immune receptor-type protein disrupts immunity to bacterial blight. Plant Physiol 181(3):1295–1313. https://doi.org/10.1104/pp.19.00686
Teper D, Wang N (2021) Consequences of adaptation of TAL effectors on host susceptibility to Xanthomonas. PLoS Genet 17:e1009310. https://doi.org/10.1371/journal.pgen.1009310
Teper D, Girija AM, Bosis E, Popov G, Savidor A, Sessa G (2018) The Xanthomonas euvesicatoria type III effector XopAU is an active protein kinase that manipulates plant MAP kinase signaling. PLoS Pathog 14:e1006880. https://doi.org/10.1371/journal.ppat.1006880
Thomas NC, Hendrich CG, Gill US, Allen C, Hutton SF, Schultink A (2020) The immune receptor Roq1 confers resistance to the bacterial pathogens Xanthomonas, Pseudomonas syringae, and Ralstonia in tomato. Front Plant Sci 11:463. https://doi.org/10.3389/fpls.2020.00463
Tian D, Wang J, Zeng X, Gu K, Qiu C, Yang X, Zhou Z, Goh M, Luo Y, Murata-Hori M, White FF, Yin Z (2014) The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell 26:497–515. https://doi.org/10.1105/tpc.113.119255
Timilsina S, Kara S, Jacques MA, Potnis N, Minsavage GV, Vallad GE, Jones JB, Fischer-Le Saux M et al (2019) Reclassification of Xanthomonas gardneri (ex Šutič 1957) Jones et al. 2006 as a later heterotypic synonym of Xanthomonas cynarae Trébaol, 2000 and description of X. cynarae pv. cynarae and X. cynarae pv. gardneri based on whole genome analyses. Int J Syst Evol Microbiol 69:343–349. https://doi.org/10.1099/ijsem.0.003104
Timilsina S, Potnis N, Newberry EA, Liyanapathiranage P, Iruegas-Bocardo F, White FF, Goss EM, Jones JB (2020) Xanthomonas diversity, virulence and plant-pathogen interactions. Nat Rev Microbiol 18:415–427. https://doi.org/10.1038/s41579-020-0361-8
Tortosa M, Cartea ME, Velasco P, Soengas P, Rodriguez VM (2019) Calcium-signaling proteins mediate the plant transcriptomic response during a well-established Xanthomonas campestris pv campestris infection. Hortic Res 6:103. https://doi.org/10.1038/s41438-019-0186-7
Tripathi L, Tripathi JN, Shah T, Muiruri KS, Katari M (2019) Molecular basis of disease resistance in banana progenitor Musa balbisiana against Xanthomonas campestris pv. musacearum. Sci Rep 9:7007. https://doi.org/10.1038/s41598-019-43421-1
Triplett LR, Verdier V, Campillo T, Van Malderghem C, Cleenwerck I, Maes M, Deblais L, Corral R, Koita O, Cottyn B, Leach JE (2015) Characterization of a novel clade of Xanthomonas isolated from rice leaves in Mali and proposal of Xanthomonas maliensis sp. nov. Antonie Van Leeuwenhoek 107:869–881. https://doi.org/10.1007/s10482-015-0379-5
Valea I, Motegi A, Kawamura N, Kawamoto K, Miyao A, Ozawa R, Takabayashi J, Gomi K, Nemoto K, Nozawa A, Sawasaki T, Shinya T, Galis I, Miyamoto K, Nojiri H, Okada K (2021) The rice wound-inducible transcription factor RERJ1 sharing same signal transduction pathway with OsMYC2 is necessary for defense response to herbivory and bacterial blight. Plant Mol Biol. https://doi.org/10.1007/s11103-021-01186-0
van Wersch S, Tian L, Hoy R, Li X (2019) Plant NLRs: The whistleblowers of plant immunity. Plant Commun 1:100016. https://doi.org/10.1016/j.xplc.2019.100016
Voloudakis AE, Reignier TM, Cooksey DA (2005) Regulation of resistance to copper in Xanthomonas axonopodis pv vesicatoria. Appl Environ Microbiol 71(2):782–789. https://doi.org/10.1128/AEM.71.2.782-789.2005
Wang L, Tsuda K, Truman W, Sato M, le Nguyen V, Katagiri F, Glazebrook J (2011) CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J 67:1029–1041. https://doi.org/10.1111/j.1365-313X.2011.04655.x
Wang X, Chen J, Yang Y, Zhou J, Qiu Y, Yu C, Ye C, Yan C, Chen J (2012) Characterization of a novel NBS-LRR gene involved in bacterial blight resistance in rice. Plant Mol Biol Rep 31:649–656. https://doi.org/10.1007/s11105-012-0537-0
Wang Y, Lin A, Loake GJ, Chu C (2013) H2O2-induced leaf cell death and the crosstalk of reactive nitric/oxygen species. J Integr Plant Biol 55:202–208. https://doi.org/10.1111/jipb.12032
Wang G, Roux B, Feng F, Guy E, Li L, Li N, Zhang X, Lautier M, Jardinaud MF, Chabannes M, Arlat M, Chen S, He C, Noël LD, Zhou JM (2015a) The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285–295. https://doi.org/10.1016/j.chom.2015.08.004
Wang C, Zhang X, Fan Y, Gao Y, Zhu Q, Zheng C, Qin T, Li Y, Che J, Zhang M, Yang B, Liu Y, Zhao K (2015b) XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. Mol Plant 8:290–302. https://doi.org/10.1016/j.molp.2014.10.010
Wang L, Chen S, Peng A, Xie Z, He Y, Zou X (2019a) CRISPR/Cas9-mediated editing of CsWRKY22 reduces susceptibility to Xanthomonas citri subsp. Citri in Wanjincheng orange (Citrus sinensis (L.) Osbeck). Plant Biotechnol Rep 13:501–510. https://doi.org/10.1007/s11816-019-00556-x
Wang J, Wang J, Hu M, Wu S, Qi J, Wang G, Han Z, Qi Y, Gao N, Wang HW, Zhou JM, Chai J (2019b) Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364:eaav5868. https://doi.org/10.1126/science.aav5868
Wang R, He F, Ning Y, Wang GL (2020) Fine-tuning of RBOH-mediated ROS signaling in plant immunity. Trend in Plant Sci 25:1060–1062. https://doi.org/10.1016/j.tplants.2020.08
Wang P, Wang S, Wu Y, Nie W, Yiming A, Huang J, Ahmad I, Zhu B, Chen G (2022) Identification and characterization of rice circular RNAs responding to Xanthomonas oryzae pv. oryzae invasion. Phytopathol 112(3):492–500. https://doi.org/10.1094/PHYTO-06-21-0235-R
Whiteley M, Diggle SP, Greenberg EP (2017) Progress in and promise of bacterial quorum sensing research. Nature 551:313–320. https://doi.org/10.1038/nature24624
Woo JY, Jeong KJ, Kim YJ, Paek KH (2016) CaLecRK-S.5, a pepper l-type lectin receptor kinase gene, confers broad-spectrum resistance by activating priming. J Exp Bot 67:5725–5741. https://doi.org/10.1093/jxb/erw336
Wu CH, Derevnina L, Kamoun S (2018) Receptor networks underpin plant immunity. Science 360:1300–1301. https://doi.org/10.1126/science.aat2623
Xu C, Luo F, Hochholdinger F (2016) LOB domain proteins: beyond lateral organ boundaries. Trend Plant Sci 21:159–167. https://doi.org/10.1016/j.tplants.2015.10
Yan Y, He X, Hu W, Liu G, Wang P, He C, Shi H (2018) Functional analysis of MeCIPK23 and MeCBL1/9 in cassava defense response against Xanthomonas axonopodis pv. manihotis. Plant Cell Rep 37:887–900. https://doi.org/10.1007/s00299-018-2276-7
Yan Y, Wang P, Wei Y, Bai Y, Lu Y, Zeng H, Liu G, Reiter RJ, He C, Shi H (2020) The dual interplay of RAV5 in activating nitrate reductases and repressing catalase activity to improve disease resistance in cassava. Plant Biotechnol J 19:785–800. https://doi.org/10.1111/pbi.13505
Yang N, Reighard G, Ritchie D, Okie W, Gasic K (2013) Mapping quantitative trait loci associated with resistance to bacterial spot (Xanthomonas arborícola pv. pruni) in peach. Tree Genet Genomes 9:573–586. https://doi.org/10.1007/s11295-012-0580-x
Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci 103:10503–10508. https://doi.org/10.1073/pnas.0604088103
Yang Z, Ma H, Hong H, Yao W, Xie W, Xiao J, Li X, Wang S (2015) Transcriptome-based analysis of mitogen-activated protein kinase cascades in the rice response to Xanthomonas oryzae infection. Rice 8:4. https://doi.org/10.1186/s12284-014-0038
Yang W, Zhang B, Qi G, Shang L, Liu H, Ding X, Chu Z (2019) Identification of the phytosulfokine receptor 1 (OsPSKR1) confers resistance to bacterial leaf streak in rice. Planta 250:1603–1612. https://doi.org/10.1007/s00425-019-03238-8
Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci 95:1663–1668. https://doi.org/10.1073/pnas.95.4.1663
Yu X, Feng B, He P, Shan L (2017) From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu Rev Phytopathol 55:109–137. https://doi.org/10.1146/annurev-phyto-080516-035649
Yu Y, Zhou YF, Feng YZ, He H, Lian JP, Yang YW, Lei MQ, Zhang YC, Chen YQ (2020) Transcriptional landscape of pathogen-responsive lncRNAs in rice unveils the role of ALEX1 in jasmonate pathway and disease resistance. Plant Biotechnol J 18:679–690. https://doi.org/10.1111/pbi.13234
Yun MH, Torres PS, El Oirdi M, Rigano LA, Gonzalez-Lamothe R, Marano MR, Castagnaro AP, Dankert MA, Bouarab K, Vojnov AA (2006) Xanthan induces plant susceptibility by suppressing callose deposition. Plant Physiol 141:178–187. https://doi.org/10.1104/pp.105.074542
Zaka A, Grande G, Coronejo T, Quibod IL, Chen CW, Chang SJ, Szurek B, Arif M, Cruz CV, Oliva R (2018) Natural variations in the promoter of OsSWEET13 and OsSWEET14 expand the range of resistance against Xanthomonas oryzae pv oryzae. PLoS ONE 13:e0203711. https://doi.org/10.1371/journal.pone.0203711
Zeng X, Luo Y, Vu NTQ, Shen S, Xia K, Zhang M (2020) CRISPR/Cas9-mediated mutation of OsSWEET14 in rice cv. Zhonghua11 confers resistance to Xanthomonas oryzae pv oryzae without yield penalty. BMC Plant Biol 20:313. https://doi.org/10.1186/s12870-020-02524-y
Zhang L, Du L, Poovaiah BW (2014) Calcium signaling and biotic defense responses in plants. Plant Signal Behav 9:11. https://doi.org/10.4161/15592324.2014.973818
Zhang S, Mei J, Wang T, Wang C, Zhang W, Yang L (2015a) Identification and expression analysis of OsmiR1861k in rice leaves in response to Xanthomonas oryzae pv. oryzae. J Gen Plant Pathol 81:108–117. https://doi.org/10.1007/s10327-015-0579-x
Zhang J, Yin Z, White F (2015b) TAL effectors and the executor R genes. Front Plant Sci 6:641. https://doi.org/10.3389/fpls.2015.00641
Zhang C, Lv M, Yin W, Dong T, Chang C, Miao Y, Jia Y, Deng Y (2019) Xanthomonas campestris promotes diffusible signal factor biosynthesis and pathogenicity by utilizing glucose and sucrose from host plants. Mol Plant Microbe Interact 32:157–166. https://doi.org/10.1094/MPMI-07-18-0187-R
Zhang Y, Li Z, Ma B, Hou Q, Wan X (2020a) Phylogeny and functions of LOB domain proteins in plants. Int J Mol Sci 21:2278. https://doi.org/10.3390/ijms21072278
Zhang X, Li N, Liu X, Wang J, Zhang Y, Liu D, Wang Y, Caol H, Zhao B, Yang W (2020b) Tomato protein Rx4 mediates the hypersensitive response to Xanthomonas euvesicatoria pv. perforans race T3. Plant J 105:1630–1644. https://doi.org/10.1111/tpj.15138
Zhang B, Zhang H, Li F, Ouyang Y, Yuan M, Li X, Xiao J, Wang S (2020c) Multiple alleles encoding atypical NLRs with unique central tandem repeats (CTRs) in rice confer resistance to Xanthomonas oryzae pv. oryzae. Plant Commun 1:100088. https://doi.org/10.1016/j.xplc.2020c.100088
Zhou P, Jia R, Chen S, Xu L (2017) Cloning and expression analysis of four citrus WRKY genes responding to Xanthomonas axonopodis pv. citri. Acta Horticult Sin 44:452–462. https://doi.org/10.16420/j.issn.0513-353x.2016-0577
Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351. https://doi.org/10.1016/j.it.2014.05.004
Zou X, Du M, Liu Y, Wu L, Xu L, Long Q, Peng A, He Y, Andrade M, Chen S (2021) CsLOB1 regulates susceptibility to citrus canker through promoting cell proliferation in citrus. Plant J 106:1039–1057. https://doi.org/10.1111/tpj.15217
Funding
The work of Jessica Luana Souza Cardoso was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico. Alessandra Alves de Souza was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico, Fundação de Amparo à Pesquisa do Estado de São Paulo, 2013/10957-0. Maria Lucia Carneiro Vieira was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo.
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Cardoso, J.L.S., Souza, A.A. & Vieira, M.L.C. Molecular basis for host responses to Xanthomonas infection. Planta 256, 84 (2022). https://doi.org/10.1007/s00425-022-03994-0
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DOI: https://doi.org/10.1007/s00425-022-03994-0