Abstract
Citrus is one of the most ancient fruit crops cultivated in the world. For many countries, citrus production is an important source of revenues. However, despite the richness of citrus production worldwide, fruit yields are constantly threatened by diseases that cause serious economic and social impacts to growers and consumers. One such example is citrus canker, a disease that affects all commercial citrus varieties and for which there is no cure. Currently, control measures for citrus canker are restricted to the application of copper-based compounds and the elimination of infected trees to prevent pathogen spreading in the field. However, new alternatives for the control of this disease are being developed, spanning through transgenic plants to innovative chemicals and biological control. New genome editing approaches and a repertoire of plant defense-related genes have been exploited to produce citrus lineages more tolerant to X. citri. In addition, a series of new molecules have been tested to not only inhibit X. citri growth but to also boost the plant immune system to suppress disease progression. In this review, we provide the state of art of all citrus canker control measures in use today, highlighting their utility and drawbacks and commenting on novel strategies to better control this important citrus disease.
Similar content being viewed by others
References
Abe VY, Benedetti CE (2016) Additive roles of PthAs in bacterial growth and pathogenicity associated with nucleotide polymorphisms in effector-binding elements of citrus canker susceptibility genes. Mol Plant Pathol 17:1223–1236
Adler C, Corbalán NS, Seyedsayamdost MR et al (2012) Catecholate Siderophores Protect Bacteria from Pyochelin Toxicity. PLoS ONE 7:e46754
Ahmad AA, Askora A, Kawasaki T et al (2014a) The filamentous phage XacF1 causes loss of virulence in Xanthomonas axonopodis pv. citri, the causative agent of citrus canker disease. Frontiers in Microbiology 5:321
Ahmad AA, Ogawa M, Kawasaki T et al (2014b) Characterization of bacteriophages cp1 and cp2, the strain-typing agents for Xanthomonas axonopodis pv. citri. Appl Environ Microbiol 80:77–85
Ahmad AA, Kawabe M, Askora A et al (2017) Dynamic integration and excision of filamentous phage XacF1 in Xanthomonas citri pv. citri, the causative agent of citrus canker disease. FEBS Open Bio 7:1715–1721
Akthar MS, Degaga B, Azam T (2014) Antimicrobial activity of essential oils extracted from medicinal plants against the pathogenic microorganisms: A review. Issues Bio Sci Pharma Res 2:001–007
Al-Saadi A, Reddy JD, Duan YP et al (2007) All five host-range variants of Xanthomonas citri carry one pthA homolog with 17.5 repeats that determines pathogenicity on citrus, but none determine host-range variation. Molecular plant-microbe interactions 20:934–943
Al-Saleh MA, Saleh AA, Ibrahim YE (2015) Integration of Pseudomonas fluorescens and salicylic acid improves citrus canker disease management caused by Xanthomonas citri subsp citri A*. Archives of Phytopathology Plant Protection 48:863–872
Aldini G, Altomare A, Baron G et al (2018) N-Acetylcysteine as an antioxidant and disulphide breaking agent: the reasons why. Free Radic Res 52:751–762
Alferez FM, Gerberich KM, Li J-L et al (2018) Exogenous nicotinamide adenine dinucleotide induces resistance to citrus canker in citrus. Frontiers in plant science 9:1472
Alpha CJ, Campos M, Jacobs-Wagner C, Strobel SA (2015) Mycofumigation by the volatile organic compound-producing fungus Muscodor albus induces bacterial cell death through DNA damage. Appl Environ Microbiol 81:1147–1156
Amiche M, Galanth C (2011) Dermaseptins as models for the elucidation of membrane-acting helical amphipathic antimicrobial peptides. Curr Pharm Biotechno 12:1184–1193
Amiche M, Seon AA, Pierre TN, Nicolas P (1999) The dermaseptin precursors: a protein family with a common preproregion and a variable C-terminal antimicrobial domain. FEBS Letters 456:352–356
Andrade MO, Alegria MC, Guzzo CR et al (2006) The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol Microbiol 62:537–551
Andrade MO, Farah CS, Wang N (2014) The post-transcriptional regulator rsmA/csrA activates T3SS by stabilizing the 5′ UTR of hrpG, the master regulator of hrp/hrc Genes, in xanthomonas. PLoS pathogens 10:e1003945
Backer R, Naidoo S, van den Berg N (2019) The nonexpressor of pathogenesis-related genes 1 (NPR1) and related family: Mechanistic insights in plant disease resistance. Frontiers in Plant Science 10:102
Bahar O, Pruitt R, Luu DD et al (2014) The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles. PeerJ 2:e242
Ballester A, Cervera M, Peña L (2008) Evaluation of selection strategies alternative to nptII in genetic transformation of citrus. Plant Cell Rep 27:1005–1015
Ballottin D, Fulaz S, Cabrini F et al (2017) Antimicrobial textiles: Biogenic silver nanoparticles against Candida and Xanthomonas. Mater Sci Eng C 75:582–589
Balogh B, Canteros BI, Stall RE, Jones JB (2008) Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dis 92:1048–1052
Balogh B, Nga NTT, Jones JB (2018) Relative level of bacteriophage multiplication in vitroor in phyllosphere may not predict in planta efficacy for controlling bacterial leaf spot on tomato caused by xanthomonas perforans. Front Microbiol 9:2176
Bao A, Burritt DJ, Chen H et al (2019) The CRISPR/Cas9 system and its applications in crop genome editing. Crit Rev Biotechnol 39:321–336
Barbosa-Mendes JM, Filho F, de Filho AAM et al (2009) Genetic transformation of Citrus sinensis cv. Hamlin with hrpN gene from Erwinia amylovora and evaluation of the transgenic lines for resistance to citrus canker. Scientia Horticulturae 122:109–115
Bártová V, Bárta J, Jarošová M (2019) Antifungal and antimicrobial proteins and peptides of potato (Solanum tuberosum L.) tubers and their applications. Appl Microbiol Biotechnol 103:5533–5547
Bastianel M, Pereira-Martin JA, Novelli VM et al (2018) Citrus leprosis resistance within the citrus group. Virus Disease 29:491–498
Bayer-Santos E, Lima L, dosde Ceseti P et al (2018) Xanthomonas citri T6SS mediates resistance to Dictyostelium predation and is regulated by an ECF σ factor and cognate Ser/Thr kinase. Environ Microbiol 20:1562–1575
Behlau F, Belasque J, Graham JH, Leite RP (2010) Effect of frequency of copper applications on control of citrus canker and the yield of young bearing sweet orange trees. Crop Prot 29:300–305
Behlau F, Jones JB, Myers ME, Graham JH (2012) Monitoring for resistant populations of Xanthomonas citri subsp. citri and epiphytic bacteria on citrus trees treated with copper or streptomycin using a new semi-selective medium. Eur J Plant Pathol 132:259–270
Behlau F, Hong JC, Jones JB, Graham JH (2013) Evidence for acquisition of copper resistance genes from different sources in citrus-associated xanthomonads. Phytopathology 103:409–418
Berlanga M, Guerrero R (2016) Living together in biofilms: The microbial cell factory and its biotechnological implications. Microb Cell Fact 15:165
Blasi F, Page C, Rossolini GM et al (2016) The effect of N-acetylcysteine on biofilms: Implications for the treatment of respiratory tract infections. Respir Med 117:190–197
Boscariol RM, Takahashi E, Chabregas S et al (2006) Attacin A Gene from Tricloplusia ni Reduces Susceptibility to Xanthomonas axonopodis pv. citri in Transgenic Citrus sinensis `Hamlin’. J Am Soc Hortic Sci 131:530–536
Boscariol-Camargo RL, Takita MA, Machado MA (2016) Bacterial resistance in AtNPR1 transgenic sweet orange is mediated by priming and involves EDS1 and PR2. Trop Plant Pathol 41:341–349
Breen S, Solomon PS, Bedon F, Vincent D (2015) Surveying the potential of secreted antimicrobial peptides to enhance plant disease resistance. Front Plant Sci 6:900
Brunings AM, Gabriel DW (2003) Xanthomonas citri: breaking the surface. Mol Plant Pathol 4:141–157
Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ (2014) Interactions in multispecies biofilms: Do they actually matter? Trends Microbiol 22:84–91
Caicedo JC, Villamizar S, Ferro MIT et al (2016) Bacteria from the citrus phylloplane can disrupt cell-cell signalling in Xanthomonas citri and reduce citrus canker disease severity. Plant Pathol 65:782–791
Campos BM, Sforça ML, Ambrosio ALB et al (2013) A Redox 2-cys mechanism regulates the catalytic activity of divergent cyclophilins. Plant Physiol 162:1311–1323
Campos ML, Lião LM, Alves ESF et al (2018) A structural perspective of plant antimicrobial peptides. Biochem J 475:3359–3375
Canteros BI, Gochez AM, Moschini RC (2017) Management of citrus canker in argentina, a success story. Plant Pathol J 33:441–449
Cardoso SC, Barbosa-Mendes JM, Boscariol-Camargo RL et al (2010) Transgenic sweet orange (Citrus sinensis L. Osbeck) expressing the attacin a gene for resistance to Xanthomonas citri subsp. citri. Plant Mol Biol Rep 28:185–192
Carlsson A, Nyström T, De Cock H, Bennich H (1998) Attacin - an insect immune protein - binds LPS and triggers the specific inhibition of bacterial outer-membrane protein synthesis. Microbiology 144:2179–2188
Casabuono A, Petrocelli S, Ottado J et al (2011) Structural analysis and involvement in plant innate immunity of Xanthomonas axonopodis pv. citri lipopolysaccharide. J Biol Chem 286:25628–25643
Caserta R, Picchi SC, Takita MA et al (2014) Expression of Xylella fastidiosa RpfF in Citrus Disrupts Signaling in Xanthomonas citri subsp. citri and Thereby Its Virulence. Mol Plant Microbe Interact 27:1241–1252
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
Cervera M, Juárez J, Navarro L, Peña L (2005) Genetic transformation of mature citrus plants. Methods Mol Biol (Clifton NJ) 286:177–188
Cervera M, Navarro A, Navarro L, Peña L (2008) Production of transgenic adult plants from clementine mandarin by enhancing cell competence for transformation and regeneration. Tree Physiol 28:55–66
Chen X, Barnaby JY, Sreedharan A et al (2013) Over-expression of the citrus gene CtNH1 confers resistance to bacterial canker disease. Physiol Mol Plant Pathol 84:115–122
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124:803–814
Choi J, Moon E (2009) Identification of novel bioactive hexapeptides against phytopathogenic bacteria through rapid screening of a synthetic combinatorial library. J Microbiol Biotechnol 19:792–802
Choi MS, Kim W, Lee C, Oh CS (2013) Harpins, multifunctional proteins secreted by gram-negative plant-pathogenic bacteria. Mol Plant Microbe Interact 26:1115–1122
Choi J, Park E, Lee SW et al (2017) Selection of small synthetic antimicrobial peptides inhibiting Xanthomonas citri subsp. citri causing citrus canker. Plant Pathol J 33:87–94
Constantin EC, Cleenwerck I, Maes M et al (2016) Genetic characterization of strains named as Xanthomonas axonopodis pv. dieffenbachiae leads to a taxonomic revision of the X. axonopodis species complex. Plant Pathol 65:792–806
Dalio RJD, Magalhaes DM, Rodrigues CM et al (2017) PAMPs, PRRs, effectors and R-genes associated with citrus-pathogen interactions. Ann Bot 119
Danna CH, Millet YA, Koller T et al (2011) The Arabidopsis flagellin receptor FLS2 mediates the perception of Xanthomonas Ax21 secreted peptides. Proc Natl Acad Sci U. S. A. 108:9286–9291
Das K, Datta K, Karmakar S, Datta SK (2019) Antimicrobial Peptides - Small but Mighty Weapons for Plants to Fight Phytopathogens. Protein Peptide Lett 26:720–742
Das RMB, Mondal P, Khatua D, Mukherjee3 N (2013) Biological management of citrus canker on acid lime through Bacillus subtilis (S-12) in West Bengal, India. J Biopestic 7:38–41
Daungfu O, Youpensuk S, Lumyong S (2019) Endophytic bacteria isolated from citrus plants for biological control of citrus canker in lime plants. Trop Life Sci Res 30:73–88
Davey ME, O’toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol R 64:847–867
De Carvalho SA, De Carvalho Nunes WM, Belasque J et al (2015) Comparison of resistance to asiatic citrus canker among different genotypes of citrus in a long-term canker-resistance field screening experiment in Brazil. Plant Dis 99:207–218
De Oliveira MLP, De Lima Silva CC, Abe VY et al (2013) Increased resistance against citrus canker mediated by a citrus mitogen-activated protein kinase. Mol Plant Microbe Interact 26:1190–1199
De Oliveira AG, Spago FR, Simionato AS et al (2016) Bioactive organocopper compound from Pseudomonas aeruginosa inhibits the growth of Xanthomonas citri subsp. citri. Front Microbiol 7:113
de Souza AA, Ionescu M, Baccari C et al (2013) Phenotype overlap in Xylella fastidiosa is controlled by the cyclic di-GMP phosphodiesterase eal in response to antibiotic exposure and diffusible signal factor-mediated cell-cell signaling. Appl Environ Microbiol 79:3444–3454
de Souza TA, Soprano AS, de Lira NPV et al (2012) The TAL effector PthA4 interacts with nuclear factors involved in RNA-dependent processes including a HMG protein that selectively binds poly(U) RNA. PLoS ONE 7:e32305
Deng XX (2008) Citrus breeding and genetic improvement programme in China. Acta Horticulturae 773:17–24
Di Lorenzo F, Silipo A, Andersen Gersby LB, Palmigiano A, Lanzetta R, Garozzo D, Boyer C, Pruvost O, Newman M-A, Molinaro A (2017) Xanthomonas citri pv. citri Pathotypes: LPS Structure and Function as Microbe-Associated Molecular Patterns. ChemBioChem 18:772–781
Domingues MN, de Campos BM, de Oliveira MLP et al (2012) Tal effectors target the C-terminal domain of RNA Polymerase II (CTD) by inhibiting the prolyl-isomerase activity of a CTD-associated cyclophilin. PLoS ONE 7:e41553
Domingues MN, De Souza TA, Cernadas RA et al (2010) The Xanthomonas citri effector protein PthA interacts with citrus proteins involved in nuclear transport, protein folding and ubiquitination associated with DNA repair. Mol Plant Pathol 11:663–675
Domínguez A, Fagoaga C, Navarro L et al (2002) Regeneration of transgenic citrus plants under non selective conditions results in high-frequency recovery of plants with silenced transgenes. Mol Genet Genom 267:544–556
Dong H, Delaney TP, Bauer DW, Beer SV (1999) Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. The Plant Journal for Cell Molecular Biology 20:207–215
Dong OX, Ronald PC (2019) Genetic engineering for disease resistance in plants: Recent progress and future perspectives. Plant Physiol 180:26–38
Donmez D, Simsek O, Izgu T et al (2013) Genetic Transformation in Citrus. Plant Biotechnol 2013: 491207
Duan S, Jia H, Pang Z et al (2018) Functional characterization of the citrus canker susceptibility gene CsLOB1. Mol Plant Pathol 19:1908–1916
Dunger G, Garofalo CG, Gottig N et al (2012) Analysis of three Xanthomonas axonopodis pv. citri effector proteins in pathogenicity and their interactions with host plant proteins. Mol Plant Pathol 13:865–876
Durairaj K, Velmurugan P, Park J-H et al (2017) Potential for plant biocontrol activity of isolated Pseudomonas aeruginosa and Bacillus stratosphericus strains against bacterial pathogens acting through both induced plant resistance and direct antagonism. FEMS Microbiol Lett 364
Enebe MC, Babalola OO (2019) The impact of microbes in the orchestration of plants’ resistance to biotic stress: a disease management approach. Appl Microbiol Biotechnol 103:9–25
Engström P, Carlsson A, Engström A et al (1984) The antibacterial effect of attacins from the silk moth Hyalophora cecropia is directed against the outer membrane of Escherichia coli. EMBO J 3:3347–3351
Enrique R, Siciliano F, Favaro MA et al (2011) Novel demonstration of RNAi in citrus reveals importance of citrus callose synthase in defence against Xanthomonas citri subsp. citri. Plant Biotechnol J 9:394–407
Fan Z, Shi J, Bao X (2018) Synthesis and antimicrobial evaluation of novel 1,2,4-triazole thioether derivatives bearing a quinazoline moiety. Mol Divers 22:657–667
Febres V, Fisher L, Khalaf A, A. G (2011) Citrus Transformation: Challenges and Prospects. In: Genetic Transformation, InTechOpen
Feng CT, Su HJ, Chen CT et al (2012) Inhibitory effects of Chinese medicinal herbs on plant-pathogenic bacteria and identification of the active components from gallnuts of Chinese sumac. Plant Dis 96:1193–1197
Ference CM, Gochez AM, Behlau F et al (2018) Recent advances in the understanding of Xanthomonas citri ssp. citri pathogenesis and citrus canker disease management. Mol Plant Pathol 19:1302–1318
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633
Fonseca NP, Patané JSL, Varani AM et al (2019) Analyses of Seven New Genomes of Xanthomonas citri pv. aurantifolii Strains, Causative Agents of Citrus Canker B and C, Show a Reduced Repertoire of Pathogenicity-Related Genes. Front Microbiol 10:2361
Frampton RA, Pitman AR, Fineran PC (2012) Advances in Bacteriophage-Mediated Control of Plant Pathogens. Int J Microbiol 2012:326452
Francis MI, Redondo A, Burns JK, Graham JH (2009) Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker. Eur J Plant Pathol 124:283–292
Fu X-Z, Liu J-H (2013) Transcriptional profiling of canker-resistant transgenic sweet orange (Citrus sinensis Osbeck) constitutively overexpressing a spermidine synthase gene. Biomed Res Int 2013:918136
Fu XZ, Chen CW, Wang Y et al (2011) Ectopic expression of MdSPDS1 in sweet orange (Citrus sinensis Osbeck) reduces canker susceptibility: Involvement of H2O2 production and transcriptional alteration. BMC Plant Biol 11:55
Fu XZ, Gong XQ, Zhang YX et al (2012) Different transcriptional response to Xanthomonas citri subsp. citri between kumquat and sweet orange with contrasting canker tolerance. PLoS ONE 7:e41790
Furman N, Kobayashi K, Zanek MC et al (2013) Transgenic sweet orange plants expressing a dermaseptin coding sequence show reduced symptoms of citrus canker disease. J Biotechnol 167:412–419
Garavaglia BS, Zimaro T, Abriata LA et al (2016) XacFhaB adhesin, an important Xanthomonas citri ssp. citri virulence factor, is recognized as a pathogen-associated molecular pattern. Mol Plant Pathol 17:1344–1353
Gholami D, Goodarzi T, Aminzadeh S et al (2015) Bacterial secretome analysis in hunt for novel bacteriocins with ability to control Xanthomonas citri subsp. citri. Iran J Biotechnol 13:10–19
Gois IB, Borém A, Cristofani-Yaly M et al (2016) Genome wide selection in citrus breeding. Genet Mol Res 15
Gottig N, Garavaglia BS, Garofalo CG et al (2009) A Filamentous Hemagglutinin-Like Protein of Xanthomonas axonopodis pv. citri, the Phytopathogen Responsible for Citrus Canker, Is Involved in Bacterial Virulence. PLoS ONE 4:e4358
Gottig N, Vranych CV, Sgro GG et al (2018) HrpE, the major component of the Xanthomonas type three protein secretion pilus, elicits plant immunity responses. Sci Rep 8:9842
Graham JH, Gottwald TR, Cubero J, Achor DS (2004) Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Mol Plant Pathol 5:1–15
Graham JH, Johnson EG, Myers ME et al (2016) Potential of nano-formulated zinc oxide for control of citrus canker on grapefruit trees. Plant Dis 100:2442–2447
Graham JH, Leite RP, Yonce HD, Myers M (2008) Streptomycin Controls Citrus Canker on Sweet Orange in Brazil and Reduces Risk of Copper Burn on Grapefruit in Florida. Proceedings of the Florida State Horticultural Society. 121:118–123
Graham JH, Myers ME (2011) Soil application of SAR inducers imidacloprid, thiamethoxam, and acibenzolar-S-methyl for citrus canker control in young grapefruit trees. Plant Dis 95:725–728
Granato LM, Picchi SC, De Oliveira Andrade M et al (2016) The ATP-dependent RNA helicase HrpB plays an important role in motility and biofilm formation in Xanthomonas citri subsp. citri. BMC Microbiol 16:55
Granato LM, Picchi SC, De Oliveira Andrade M et al (2019) The EcnA antitoxin is important not only for human pathogens: Evidence of Its Role in the Plant Pathogen Xanthomonas citri subsp. citri. J Bacteriol 201:e00796-18
Guo W, Li D, Duan Y (2007) Citrus Transgenics: Current Status and Prospects. Transgenic Plant J 1:202–209
Hammerbacher A, Coutinho TA, Gershenzon J (2019) Roles of plant volatiles in defence against microbial pathogens and microbial exploitation of volatiles. Plant Cell Environ 42:2827–2843
Hao G, Stover E, Gupta G (2016) Overexpression of a modified plant Thionin enhances disease resistance to Citrus canker and Huanglongbing (HLB). Front Plant Sci 7:1078
Hao G, Zhang S, Stover E (2017) Transgenic expression of antimicrobial peptide D2A21 confers resistance to diseases incited by Pseudomonas syringae pv. tabaci and Xanthomonas citri, but not Candidatus Liberibacter asiaticus. PLoS ONE 12:e0186810
He Y, Chen S, Peng A et al (2011) Production and evaluation of transgenic sweet orange (Citrus sinensis Osbeck) containing bivalent antibacterial peptide genes (Shiva A and Cecropin B) via a novel Agrobacterium-mediated transformation of mature axillary buds. Scientia Horticulturae 128:99–107
He Y, Jia R, Qi J et al (2019) Functional analysis of citrus AP2 transcription factors identified CsAP2-09 involved in citrus canker disease response and tolerance. Gene 707:178–188
Hidaka T, Omura M (1993) Transformation of Citrus Protoplasts by Electroporation. J JPN Soc Hortic Sci 62:371–376
Hidaka T, Omura M, Ugaki M et al (1990) Agrobacterium-mediated transformation and regeneration of Citrus spp. from suspension cells. JPN J Breed 40:199–207
Hippler FWR, Petená G, Boaretto RM et al (2018) Mechanisms of copper stress alleviation in Citrus trees after metal uptake by leaves or roots. Environ Sci Pollut Res 25:13134–13146
Hu Y, Zhang J, Jia H et al (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Nat Acad Sci U.S.A. 111:E521–E529
Huang M, Roose ML, Yu Q et al (2018) Construction of high-density genetic maps and detection of QTLs associated with huanglongbing tolerance in citrus. Front Plant Sci 9:1694
Huang PY, Zimmerli L (2014) Enhancing crop innate immunity: New promising trends. Front Plant Sci 5:624
Huang TP, Tzeng DDS, Wong ACL et al (2012) DNA polymorphisms and biocontrol of Bacillus antagonistic to citrus bacterial canker with indication of the interference of phyllosphere biofilms. PLoS ONE 7:e42124
Hyun JW, Kim HJ, Yi PH et al (2012) Mode of action of streptomycin resistance in the citrus canker pathogen (Xanthomonas smithii subsp. citri) in Jeju island. Plant Pathol J 28:207–211
Ibrahim YE, Saleh AA, Al-Saleh MA (2017) Management of asiatic citrus canker under field conditions in Saudi Arabia using bacteriophages and acibenzolar-s-methyl. Plant Dis 101:761–765
Iglesias DJ, Cercós M, Colmenero-Flores JM et al (2007) Physiology of citrus fruiting. Braz J Plant Physiol 19:333–362
Imai A, Kuniga T, Yoshioka T et al (2018) Predicting segregation of multiple fruit-quality traits by using accumulated phenotypic records in citrus breeding. PLoS ONE 13:e0202341
Inglese P, Sortino G (2019) Citrus History, Taxonomy, Breeding, and Fruit Quality Citrus History, Taxonomy, Breeding, and Fruit Quality Summary and Keywords. In Oxford Research Encyclopedia of Environmental Science. Oxford University Press USA
Inui Kishi RN, Stach-Machado D, Singulani JL et al (2018) Evaluation of cytotoxicity features of antimicrobial peptides with potential to control bacterial diseases of citrus. PLoS One 13(9):e0203451
Ionescu M, Baccari C, Da Silva AM et al (2013) Diffusible signal factor (DSF) synthase RpfF of Xylella fastidiosa is a multifunction protein also required for response to DSF. J Bacteriol 195:5273–5284
Jia H, Orbovic V, Jones JB, Wang N (2016) Modification of the PthA4 effector binding elements in Type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating Xcc∆pthA4: DCsLOB1.3 infection. Plant Biotechnol J 14:1291–1301
Jia H, Zhang Y, Orbović V et al (2017) Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15:817–823
Jia H, Orbovi?? V, Wang N. (2019) CRISPR-LbCas12a-mediated modification of citrus. Plant Biotechnol J. 17:1928–1937
Kering KK, Kibii BJ, Wei H (2019) Biocontrol of phytobacteria with bacteriophage cocktails. Pest Manag Sci 75:1775–1781
Khalaf AA, Gmitter FG, Conesa A et al (2011) Fortunella margarita Transcriptional Reprogramming Triggered by Xanthomonas citri subsp. citri. BMC Plant Biol 11:159
Kishi RNI, Stach-Machado D, de Lacorte Singulani J et al (2018) Evaluation of cytotoxicity features of antimicrobial peptides with potential to control bacterial diseases of citrus. PLoS ONE 13:e0203451
Kobayashi AK, Gonzaga Vieira LE, Carlos Bespalhok Filho J et al (2017) Enhanced resistance to citrus canker in transgenic sweet orange expressing the sarcotoxin IA gene. Eur J Plant Pathol 149:865–873
Kobayashi S, Uchimiya H (1989) Expression and integration of a foreign gene in orange (Citrus sinensis Osb.) protoplasts by direct DNA transfer. JPN J Genet 64:91–97
Król E, de Sousa Borges A, da Silva I et al (2015) Antibacterial activity of alkyl gallates is a combination of direct targeting of FtsZ and permeabilization of bacterial membranes. Front Microbiol 6:390
Lacombe S, Rougon-Cardoso A, Sherwood E et al (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28:365–369
Lee JY, Moon SS, Hwang BK (2003) Isolation and in vitro and in vivo activity against Phytophthora capsici and Colletotrichum orbiculare of phenazine-1-carboxylic acid from Pseudomonas aeruginosa strain GC-B26. Pest Manag Sci 59:872–882
Li J, Wang N (2014) Foliar application of biofilm formation-inhibiting compounds enhances control of citrus canker caused by Xanthomonas citri subsp. citri. Phytopathology 104:134–142
Li DL, Xiao X, Guo WW (2014a) Production of transgenic anliucheng sweet orange (citrus sinensis osbeck) with xa21 gene for potential canker resistance. J Integr Agric 13:2370–2377
Li Z, Zou L, Ye G et al (2014b) A potential disease susceptibility gene CsLOB of citrus is targeted by a major virulence effector PthA of Xanthomonas citri subsp. citri. Mol Plant 7:912–5
Li L, Li J, Zhang Y et al (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
Li P, Ma Y, Zhou J et al (2015) The efficacy and underlying mechanism of sulfone derivatives containing 1,3,4-oxadiazole on Citrus Canker. Molecules. 20(8):14103–14117.
Liu SH, Rawal TB, Soliman M et al (2019) Antimicrobial Zn-Based TSOL for Citrus Greening Management: Insights from Spectroscopy and Molecular Simulation. J Agric Food Chem 67:6970–6977
Magalhães DM, Scholte LLS, Silva NV et al (2016) LRR-RLK family from two Citrus species: genome-wide identification and evolutionary aspects. BMCGenomics 17:623
Malamud F, Torres PS, Roeschlin R et al (2011) The Xanthomonas axonopodis pv. citri flagellum is required for mature biofilm and canker development. Microbiology 157:819–829
Marin TGS, Galvanin AL, Lanza FE, Behlau F (2019) Description of copper tolerant Xanthomonas citri subsp. citri and genotypic comparison with sensitive and resistant strains. Plant Pathol 68:1088–1098
Martins PMM, Machado MA, Silva NV et al (2016) Type II toxin-antitoxin distribution and adaptive aspects on Xanthomonas genomes: Focus on Xanthomonas citri. Front Microbiol 7:652
Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense Priming: An Adaptive Part of Induced Resistance. Annu Rev Plant Biol 68:485–512
McKenna M (2019) Antibiotics set to flood Florida’s troubled orange orchards. Nature 567:302–303
McManus PS, Stockwell VO, Sundin GW, Jones AL (2002) Antibiotic use in plant agriculture. Ann Rev Phytopathol 40:443–465
Mendes BMJ, Cardoso SC, Boscariol-Camargo RL et al (2010) Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathol 59:68–75
Michavila G, Adler C, De Gregorio PR et al (2017) Pseudomonas protegens CS1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent. Plant Biol 19:608–617
Mirzaei-Najafgholi H, Tarighi S, Golmohammadi M, Taheri P (2017) The effect of citrus essential oils and their constituents on growth of Xanthomonas citri subsp. citri. Molecules 22:591
Mitchell AM, Strobel GA, Moore E et al (2010) Volatile antimicrobials from Muscodor crispans, a novel endophytic fungus. Microbiology 156:270–277
Montesinos E (2007) Antimicrobial peptides and plant disease control. FEMS Microbiol Lett 270:1–11
Moore GA, Jacono CC, Neidigh JL et al (1992) Agrobacterium-mediated transformation of Citrus stem segments and regeneration of transgenic plants. Plant Cell Rep 11:238–242
Muller MP, MacDougall C, Lim M et al (2016) Antimicrobial surfaces to prevent healthcare-associated infections: A systematic review. J Hosp Infect 92:7–13
Muranaka LS, Giorgiano TE, Takita MA et al (2013) N-Acetylcysteine in Agriculture, a Novel Use for an Old Molecule: Focus on Controlling the Plant-Pathogen Xylella fastidiosa. PLoS ONE 8:e72937
Murata MM, Omar AA, Mou Z et al (2019) Novel plastid-nuclear genome combinations enhance resistance to citrus canker in cybrid grapefruit. Front Plant Sci 9:1858
Murate LS, Oliveira AG de, Higashi AY et al (2015) Activity of Secondary Bacterial Metabolites in the Control of Citrus Canker. Agric Sci 06:295–303
Nilsson AS (2014) Phage therapy-constraints and possibilities. Upsala J Med Sci 119:192–198
Oard SV (2011) Deciphering a mechanism of membrane permeabilization by α-hordothionin peptide. Biochim Biophys Acta Biomembr 1808:1737–1745
Omar AA, Murata MM, El-Shamy HA et al (2018) Enhanced resistance to citrus canker in transgenic mandarin expressing Xa21 from rice. Transgenic Res 27:179–191
Orbović V, Shankar A, Peeples ME et al (2015) Citrus transformation using mature tissue explants. Methods Mol Biol 1224:259–273
Osusky M, Osuska L, Kay W, Misra S (2005) Genetic modification of potato against microbial diseases: In vitro and in planta activity of a dermaseptin B1 derivative, MsrA2. Theor Appl Genet 111:711–722
Pal C, Asiani K, Arya S et al (2017) Metal Resistance and Its Association With Antibiotic Resistance. Adv Microb Physiol 70:261–313
Pandey AK, Kumar P, Singh P et al (2017) Essential oils: Sources of antimicrobials and food preservatives. Front Microbiol 7:2161
Patané JSL, Martins J, Rangel LT et al (2019) Origin and diversification of Xanthomonas citri subsp. citri pathotypes revealed by inclusive phylogenomic, dating, and biogeographic analyses. BMC Genomics 20:700
Patel H, Shirkhedkar A, Bari S et al (2018) Quinazolino-thiadiazoles as antimicrobial agents. Bull Fac Pharm Cairo Univ 56:83–90
Peng A, Chen S, Lei T et al (2017) Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J 15:1509–1519
Peña L, Cervera M, Juárez J et al (1995a) Agrobacterium-mediated transformation of sweet orange and regeneration of transgenic plants. Plant Cell Rep 14:616–619
Peña L, Cervera M, Juárez J et al (1995b) High efficiency Agrobacterium-mediated transformation and regeneration of citrus. Plant Sci 104:183–191
Peña L, Martín-Trillo M, Juárez J et al (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat Biotechnol 19:263–267
Pereira ALA, Carazzolle MF, Abe VY et al (2014) Identification of putative TAL effector targets of the citrus canker pathogens shows functional convergence underlying disease development and defense response. BMC Genomics 15:157
Perez-Quintero AL, Szurek B (2019) A Decade Decoded: Spies and Hackers in the History of TAL Effectors Research. Annu Rev Phytopathol 57:459–481
Petrocelli S, Tondo ML, Daurelio LD, Orellano EG (2012) Modifications of Xanthomonas axonopodis pv. citri lipopolysaccharide affect the basal response and the virulence process during citrus canker. PLoS ONE 7:e40051
Picchi SC, de Sousa AA, Della Coletta H (2017) Uma nova opção no manejo do Cancro Cítrico. Citricultura Atual 113:14–16
Picchi SC, Takita MA, Coletta-Filho HD et al (2016) N -acetylcysteine interferes with the biofilm formation, motility and epiphytic behaviour of Xanthomonas citri subsp. citri. Plant Pathol 65:561–569
Pitino M, Armstrong CM, Duan Y (2015) Rapid screening for citrus canker resistance employing pathogen-associated molecular pattern-triggered immunity responses. Hortic Res 2:15042
Poole K (2017) At the nexus of antibiotics and metals: the impact of Cu and Zn on antibiotic activity and resistance. Trends Microbiol 25:820–832
Pruitt RN, Joe A, Zhang W et al (2017) A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone. New Phytol 215:725–736
Pruvost O, Magne M, Boyer K et al (2014) A MLVA genotyping scheme for global surveillance of the citrus pathogen Xanthomonas citri pv. citri suggests a worldwide geographical expansion of a single genetic lineage. PLoS ONE 9:e98129
Rabbee MF, Ali MS, Baek K-H (2019) Endophyte Bacillus velezensis isolated from Citrus spp. Controls streptomycin-resistant Xanthomonas citri subsp. citri that causes citrus bacterial canker. Agronomy 9:470
Rensing C, Moodley A, Cavaco LM, McDevitt SF (2018) Resistance to Metals Used in Agricultural Production. Microbiol Spectr 6
Riera N, Wang H, Li Y et al (2018) Induced systemic resistance against citrus canker disease by rhizobacteria. Phytopathology 108:1038–1045
Rigano L, Siciliano F, Enrique R et al (2007) Biofilm formation, epiphytic fitness, and canker development in Xanthomonas axonopodis pv. citri. Mol Plant Microbe Interact 20:1222–1230
Ríos JL (2016) Essential oils: What they are and how the terms are used and defined. In: Essential Oils in Food Preservation, Flavor and Safety. Elsevier Academic Press
Rivero M, Furman N, Mencacci N et al (2012) Stacking of antimicrobial genes in potato transgenic plants confers increased resistance to bacterial and fungal pathogens. J Biotechnol 157:334–343
Rodríguez A, Andrés VS, Cervera M et al (2011) Terpene down-regulation in orange reveals the role of fruit aromas in mediating interactions with insect herbivores and pathogens. Plant Physiol 156:793–802
Rodríguez A, Shimada T, Cervera M et al (2015) Resistance to pathogens in terpene down-regulated orange fruits inversely correlates with the accumulation of D-limonene in peel oil glands. Plant Signal Behav 10:e1028704
Roeschlin RA, Favaro MA, Chiesa MA et al (2017) Resistance to citrus canker induced by a variant of Xanthomonas citri ssp. citri is associated with a hypersensitive cell death response involving autophagy-associated vacuolar processes. Mol Plant Pathol 18:1267–1281
Roeschlin RA, Uviedo F, García L et al (2019) PthA4AT, a 7.5-repeats transcription activator-like (TAL) effector from Xanthomonas citri ssp. citri, triggers citrus canker resistance. Mol Plant Pathol 20:1394–1407
Ronald PC, Albano B, Tabien R et al (1992) Genetic and physical analysis of the rice bacterial blight disease resistance locus, Xa21. Mol Gen Genet: MGG 236:113–20
Ruiz M, Pensabene-Bellavia G, Quiñones A et al (2018) Molecular characterization and stress tolerance evaluation of new allotetraploid somatic hybrids between carrizo citrange and Citrus macrophylla W. rootstocks. Front Plant Sci 9:901
Sathoff AE, Samac DA (2019) Antibacterial activity of plant defensins. Mol Plant Microbe Interact 32:507–514
Savietto A, Polaquini CR, Kopacz M et al (2018) Antibacterial activity of monoacetylated alkyl gallates against Xanthomonas citri subsp. citri. Arch Microbiol 200:929–937
Sendín LN, Filippone MP, Orce IG et al (2012) Transient expression of pepper Bs2 gene in Citrus limon as an approach to evaluate its utility for management of citrus canker disease. Plant Pathol 61:648–657
Sendín LN, Orce IG, Gómez RL et al (2017) Inducible expression of Bs2 R gene from Capsicum chacoense in sweet orange (Citrus sinensis L. Osbeck) confers enhanced resistance to citrus canker disease. Plant Mol Biol 93:607–621
Sgro GG, Ficarra FA, Dunger G et al (2012) Contribution of a harpin protein from Xanthomonas axonopodis pv. citri to pathogen virulence. Mol Plant Pathol 13:1047–1059
Shantharaj D, Römer P, Figueiredo JFL et al (2017) An engineered promoter driving expression of a microbial avirulence gene confers recognition of TAL effectors and reduces growth of diverse Xanthomonas strains in citrus. Mol Plant Pathol 18:976–989
Shi Q, Febres VJ, Jones JB, Moore GA (2015) Responsiveness of different citrus genotypes to the Xanthomonas citri ssp. citri-derived pathogen-associated molecular pattern (PAMP) flg22 correlates with resistance to citrus canker. Mol Plant Pathol 16:507–520
Shi Q, Febres VJ, Jones JB, Moore GA (2016) A survey of FLS2 genes from multiple citrus species identifies candidates for enhancing disease resistance to Xanthomonas citri ssp. citri. Hortic Res 3:16022
Shimada T, Endo T, Rodríguez A et al (2017) Ectopic accumulation of linalool confers resistance to Xanthomonas citri subsp. citri in transgenic sweet orange plants. Tree Physiol 37:654–664
Shimo HM, Terassi C, Lima Silva CC et al (2019) Role of the citrus sinensis RNA deadenylase CsCAF1 in citrus canker resistance. Mol Plant Patho 20(8):1105–1118.
Silva IC, Polaquini CR, Regasini LO et al (2017) Evaluation of cytotoxic, apoptotic, mutagenic, and chemopreventive activities of semi-synthetic esters of gallic acid. Food Chem Toxicol 105:300–307
Silva IC, Regasini LO, Petrãnio MS et al (2013) Antibacterial activity of alkyl gallates against Xanthomonas citri subsp. citri. J Bacteriol 195:85–94
Silva KJP, Mahna N, Mou Z, Folta KM (2018) NPR1 as a transgenic crop protection strategy in horticultural species. Hortic Res 5:15
Soler N, Plomer M, Fagoaga C et al (2019) Methods for Producing Transgenic Plants Resistant to CTV. In: Methods in Molecular Biology. Humana Press Inc
Song WY, Wang GL, Chen LL et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804
Soprano AS, Abe VY, Smetana JHC, Benedetti CE (2013) Citrus MAF1, a repressor of RNA polymerase III, binds the Xanthomonas citri canker elicitor PthA4 and suppresses citrus canker development. Plant Physiol 163:232–242
Soprano AS, Giuseppe PO de, Shimo HM et al (2017) Crystal structure and regulation of the citrus pol III repressor MAF1 by auxin and phosphorylation. Structure 25:1360–1370.e4
Souza DP, Oka GU, Alvarez-Martinez CE et al (2015) Bacterial killing via a type IV secretion system. Nat Commun 6:6453
Spago FR, Ishii Mauro CS, Oliveira AG et al (2014) Pseudomonas aeruginosa produces secondary metabolites that have biological activity against plant pathogenic Xanthomonas species. Crop Prot 62:46–54
Stockwell VO, Duffy B (2012) Use of antibiotics in plant agriculture. OIE Rev Sci Tech 31:199–210
Stork W, Kim JG, Mudgett MB (2015) Functional analysis of plant defense suppression and activation by the Xanthomonas core type III effector XopX. Mol Plant Microbe Interact 28:180–194
Stover ED, Stange RR, Mccollum TG et al (2013) Screening antimicrobial peptides in vitro for use in developing transgenic citrus resistant to huanglongbing and citrus canker. J Am Soc Hortic Sci 138:142–148
Strange RN, Scott PR (2005) Plant Disease: A Threat to Global Food Security. Annu Rev Phytopathol 43:83–116. https://doi.org/10.1146/annurev.phyto.43.113004.133839
Sun X, Stall RE, Jones JB et al (2004) Detection and characterization of a new strain of citrus canker bacteria from key/Mexican lime and alemow in South Florida. Plant Dis 88:1179–1188
Tai TH, Dahlbeck D, Clark ET et al (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci U.S.A. 96:14153–14158
Taveira GB, Mello ÉO, Carvalho AO et al (2017) Antimicrobial activity and mechanism of action of a thionin-like peptide from Capsicum annuum fruits and combinatorial treatment with fluconazole against Fusarium solani. Biopolymers 108
Thomas NC, Oksenberg N, Liu F et al (2018) The rice XA21 ectodomain fused to the Arabidopsis EFR cytoplasmic domain confers resistance to Xanthomonas oryzae pv. oryzae. PeerJ 2018:e4456
Trdá L, Boutrot F, Ciaverie J et al (2015) Perception of pathogenic or beneficial bacteria and their evasion of host immunity: Pattern recognition receptors in the frontline. Front Plant Sci 6:219
Uzun A, Seday U, Gulsen O, Kafa G (2015) Hybridization-Based citrus breeding program in turkey. Acta Horticulturae 1065:557–559
Vardi A, Bleichman S, Aviv D (1990) Genetic transformation of citrus protoplasts and regeneration of transgenic plants. Plant Sci 69:199–206
Verma G, Mondal KK, Kulshreshtha A, Sharma M (2019) XopR T3SS-effector of Xanthomonas oryzae pv. oryzae suppresses cell death-mediated plant defense response during bacterial blight development in rice. 3 Biotech 9:272
Vieira G, Purić J, Morão LG et al (2018) Terrestrial and marine Antarctic fungi extracts active against Xanthomonas citri subsp. citri. Lett Appl Microbiol 67:64–71
Wang L, Chen S, Peng A et al (2019) 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
Wang P, Gao M, Zhou L et al (2016a) Synthesis and antibacterial activity of pyridinium-tailored aromatic amphiphiles. Bioorg Med Chem Lett 26:1136–1139
Wang PY, Fang HS, Shao W, Bin et al (2017) Synthesis and biological evaluation of pyridinium-functionalized carbazole derivatives as promising antibacterial agents. Bioorg Med Chem Lett 27:4294–4297
Wang PY, Zhou L, Zhou J et al (2016b) Synthesis and antibacterial activity of pyridinium-tailored 2,5-substituted-1,3,4-oxadiazole thioether/sulfoxide/sulfone derivatives. Bioorg Med Chem Lett 26:1214–1217
Wang X, Yan J, Wang M et al (2018) Synthesis and three-dimensional quantitative structure-activity relationship study of quinazoline derivatives containing a 1,3,4-oxadiazole moiety as efficient inhibitors against Xanthomonas axonopodis pv. citri. Mol Divers 22:791–802
Wang Y, Liu JH (2012) Exogenous treatment with salicylic acid attenuates occurrence of citrus canker in susceptible navel orange (Citrus sinensis Osbeck). J Plant Physiol 169:1143–1149
Wattana-Amorn P, Charoenwongsa W, Williams C et al (2016) Antibacterial activity of cyclo(L-Pro-L-Tyr) and cyclo(D-Pro-L-Tyr) from Streptomyces sp. strain 22 – 4 against phytopathogenic bacteria. Nat Prod Res 30:1980–1983
Wei ZM, Laby RJ, Zumoff CH et al (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85–88
Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: Looking back over 30 years. Phytopathology 97:250–256
Wu Q, Patočka J, Kuča K (2018) Insect antimicrobial peptides, a mini review. toxins 10:461
Wulff BBH, Horvath DM, Ward ER (2011) Improving immunity in crops: New tactics in an old game. Curr Opin Plant Biol 14:468–476
Yan Q, Hu X, Wang N (2012) The novel virulence-related gene nlxA in the lipopolysaccharide cluster of Xanthomonas citri ssp. citri is involved in the production of lipopolysaccharide and extracellular polysaccharide, motility, biofilm formation and stress resistance. Mol Plant Pathol 13:923–934
Yan X, Tao J, Luo HL et al (2019) A type III effector XopLXcc8004 is vital for Xanthomonas campestris pv. campestris to regulate plant immunity. Res Microbiol 170:138–146
Yang L, Ge S, Huang J, Bao X (2018) Synthesis of novel (E)-2-(4-(1H-1,2,4-triazol-1-yl)styryl)-4- (alkyl/arylmethyleneoxy)quinazoline derivatives as antimicrobial agents. Mol Divers 22:71–82
Yang L, Hu C, Li N et al (2011) Transformation of sweet orange [Citrus sinensis (L.) Osbeck] with pthA-nls for acquiring resistance to citrus canker disease. Plant Mol Biol 75:11–23
Yevtushenko DP, Misra S (2019) Enhancing disease resistance in poplar through modification of its natural defense pathway. Plant Mol Biol 100:481–494
Yoshikawa G, Askora A, Blanc-Mathieu R et al (2018) Xanthomonas citri jumbo phage XacN1 exhibits a wide host range and high complement of tRNA genes. Sci Rep 8:4486
Yu X, Armstrong CM, Zhou M, Duan Y (2016) Bismerthiazol inhibits Xanthomonas citri subsp. citri growth and induces differential expression of citrus defense-related genes. Phytopathology 106:693–701
Zhang X, Francis MI, Dawson WO et al (2010) Over-expression of the Arabidopsis NPR1 gene in citrus increases resistance to citrus canker. European J Plant Pathol 128:91–100
Zhou P, Jia R, Chen S et al (2017) Cloning and expression analysis of four citrus WRKY genes responding to Xanthomonas axonopodis pv. citri. Acta Hortic Sinica 44:452–462
Acknowledgements
This work was supported by a research grant from INCT Citrus (Proc. CNPQ 465440/2014-2 and FAPESP 2014/50880-0) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP − 2013/10957-0 and 2018/08535-4). P. M. M. Martins and M. O. Andrade are postdoctoral fellows (FAPESP 2016/01273-9, 2018/18550-0 and 2017/18570-9). C. E. Benedetti are recipients of a research fellowship from CNPq (grants 303238/2016-0 and 301803/2019-6, respectively). The authors declare no competing or financial interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Martins, P.M.M., de Oliveira Andrade, M., Benedetti, C.E. et al. Xanthomonas citri subsp. citri: host interaction and control strategies. Trop. plant pathol. 45, 213–236 (2020). https://doi.org/10.1007/s40858-020-00376-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40858-020-00376-3