Transcriptome analysis of two lines of Brassica oleracea in response to early infection with Xanthomonas campestris pv. campestris

References

• Ade J, DeYoung BJ, Golstein C, Innes RW. 2007. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci USA. 104:2531–2536. doi:10.1073/pnas.0608779104.
   PubMed Web of Science ®Google Scholar
• Afrin KS, Rahim MA, Park J, Natarajan S, Kim H, Nou I. 2018. Identification of NBS-encoding genes linked to black rot resistance in cabbage (Brassica oleracea var. capitata). Mol Biol Rep. 45:773–785. doi:10.1007/s11033-018-4217-5.
   PubMed Web of Science ®Google Scholar
• Aires A, Mota VR, Saavedra MJ, Monteiro AA, Simões M, Rosa EAS, Bennett RN. 2009. Initial in vitro evaluations of the antibacterial activities of glucosinolate enzymatic hydrolysis products against plant pathogenic bacteria. J Appl Microbiol. 106:2096–2105. doi:10.1111/j.1365-2672.2009.04181.x.
   PubMed Web of Science ®Google Scholar
• Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K. 2004. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell. 16:3460–3479. doi:10.1105/tpc.104.025833.
   PubMed Web of Science ®Google Scholar
• Andrade AE, Silva LP, Pereira JL, Noronha EF, Reis FB, Carlos B, Santos MFD, Domont GB, Franco OL, Angela M. 2010. In vivo proteome analysis of Xanthomonas campestris pv. campestris in the interaction with the host plant Brassica oleracea. FEMS Microbiol Lett. 281:167–174. doi:10.1111/j.1574-6968.2008.01090.x.
   Web of Science ®Google Scholar
• Benjamini YHY. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 57:289–300.
   Google Scholar
• Bent AF, Mackey D. 2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol. 45:399–436. doi:10.1146/annurev.phyto.45.062806.094427.
   PubMed Web of Science ®Google Scholar
• Berger S, Sinha AK, Roitsch T. 2007. Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions. J Exp Bot. 58:4019–4026. doi:10.1093/jxb/erm298.
   PubMed Web of Science ®Google Scholar
• Burlakoti RR, Chen JR, Hsu CF, Burlakoti P, Kenyon L. 2018. Molecular characterization, comparison of screening methods, and evaluation of cross‐pathogenicity of black rot (Xanthomonas campestris pv. Campestris) Strains from Cabbage, Choy Sum, Leafy Mustard and Pak Choi from Taiwan. Plant Pathol. 67:1589–1600.
   Web of Science ®Google Scholar
• Buxdorf K, Yaffe H, Barda O, Levy M. 2013. The effects of glucosinolates and their breakdown products on necrotrophic fungi. PLoS One. 8:e70771. doi:10.1371/journal.pone.0070771.
   PubMed Web of Science ®Google Scholar
• Cai B, Li Q, Xu Y, Yang L, Bi H, Ai X. 2016. Genome-wide analysis of the fructose 1,6-bisphosphate aldolase (FBA) gene family and functional characterization of FBA7 in tomato. Plant Physiol Bioch. 108:251–265. doi:10.1016/j.plaphy.2016.07.019.
   PubMed Web of Science ®Google Scholar
• Chen J, Pang W, Chen B, Zhang C, Piao Z. 2016. Transcriptome analysis of Brassica rapa near-isogenic lines carrying clubroot-resistant and -susceptible alleles in response to Plasmodiophora brassicae during early infection. Front Plant Sci. 6:1183. doi:10.3389/fpls.2015.01183.
   PubMed Web of Science ®Google Scholar
• Chen K, Du L, Chen Z. 2003. Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis. Plant Mol Biol. 53:61–74. doi:10.1023/B:PLAN.0000009265.72567.58.
   PubMed Web of Science ®Google Scholar
• Cook A, Walker J, Larson R. 1952. Studies on the disease cycle of crucifer black rot. Phytopathology. 42:162–167.
   Web of Science ®Google Scholar
• Cruz J, Tenreiro R, Cruz L. 2017. Assessment of diversity of Xanthomonas campestris pathovars affecting cruciferous plants in portugal and disclosure of two novel X. campestris pv. campestris races. J Plant Pathol. 99:403–414.
   Web of Science ®Google Scholar
• Czernic P, Visser B, Sun W, Savouré A, Deslandes L, Marco Y, Van Montagu M, Verbruggen N. 1999. Characterization of an Arabidopsis thaliana receptor-like protein kinase gene activated by oxidative stress and pathogen attack. Plant J. 18:321–327. doi:10.1046/j.1365-313X.1999.00447.x.
   PubMed Web of Science ®Google Scholar
• Dangl JL, Jones JDG. 2001. Plant pathogens and integrated defence responses to infection. Nature. 411:826–833. doi:10.1038/35081161.
   PubMed Web of Science ®Google Scholar
• Dey SS, Sharma K, Bhatia Dey R, Sandeep Kumar GM, Singh D, Kumar R, Parkash C. 2015. Inter specific hybridization (Brassica carinata × Brassica oleracea) for introgression of black rot resistance genes into indian cauliflower (B. oleracea var. botrytis L.). Euphytica. 204:149–162. doi:10.1007/s10681-015-1352-0.
   Web of Science ®Google Scholar
• El Kasmi F, Chung E, Anderson RG, Li J, Wan L, Eitas TK, Gao Z, Dangl JL. 2017. Signaling from the plasma-membrane localized plant immune receptor RPM1 requires self-association of the full-length protein. Proc Natl Acad Sci USA. 114:E7385–E7394. doi:10.1073/pnas.1708288114.
   PubMed Web of Science ®Google Scholar
• Fargier E, Manceau C. 2007. Pathogenicity assays restrict the species Xanthomonas campestris into three pathovars and reveal nine races within X. campestris pv. campestris. Plant Pathol. 56:805–818. doi:10.1111/j.1365-3059.2007.01648.x.
   Web of Science ®Google Scholar
• Flor HH. 1971. Current status of the gene-for-gene concept. Annu Rev Phytopathol. 9:275–296. doi:10.1146/annurev.py.09.090171.001423.
   Web of Science ®Google Scholar
• Gao Z, Chung EH, Eitas TK, Dangl JL. 2011. Plant intracellular innate immune receptor resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. Proc Natl Acad Sci USA. 108:7619–7624. doi:10.1073/pnas.1104410108.
   PubMed Web of Science ®Google Scholar
• Garavaglia BS, Thomas L, Gottig N, Zimaro T, Garofalo CG, Gehring C, Ottado J. 2010. Shedding light on the role of photosynthesis in pathogen colonization and host defense. Commun Integr Biol. 3:382–384. doi:10.4161/cib.3.4.12029.
   PubMedGoogle Scholar
• Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol. 43:205–227. doi:10.1146/annurev.phyto.43.040204.135923.
   PubMed Web of Science ®Google Scholar
• Grant JJ, Chini A, Basu D, Loake GJ. 2003. Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol Plant Microbe In. 16:669–680. doi:10.1094/MPMI.2003.16.8.669.
   PubMed Web of Science ®Google Scholar
• Griesbach E, Loptien H, Miersch U. 2003. Resistance to Xanthomonas campestris pv. campestris (Pammel) Dowson in cabbage Brassica oleracea L. J Plant Dis Protect. 110:461–475. doi:10.1007/BF03356123.
   Web of Science ®Google Scholar
• Griffiths PD, Marek LF, Robertson LD. 2009. Identification of crucifer accessions from the NC-7 and NE-9 plant introduction collections that are resistant to black rot (Xanthomonas campestris pv. campestris) races 1 and 4. Hortscience. 44:284–288. doi:10.21273/HORTSCI.44.2.284.
   Web of Science ®Google Scholar
• Grubb CD, Abel S. 2006. Glucosinolate metabolism and its control. Trends Plant Sci. 11:89–100. doi:10.1016/j.tplants.2005.12.006.
   PubMed Web of Science ®Google Scholar
• Hatakeyama K, Suwabe K, Tomita RN, Kato T, Nunome T, Fukuoka H, Matsumoto S. 2013. Identification and characterization of Crr1a, a gene for resistance to clubroot disease (Plasmodiophora brassicae Woronin) in Brassica rapa L. PLoS One. 8:e54745. doi:10.1371/journal.pone.0054745.
   PubMed Web of Science ®Google Scholar
• He Y, Zhou J, Shan L, Meng X. 2018. Plant cell surface receptor-mediated signaling – a common theme amid diversity. J Cell Sci. 131:jcs209353. doi:10.1242/jcs.209353.
   PubMed Web of Science ®Google Scholar
• Holub EB. 2007. Natural variation in innate immunity of a pioneer species. Curr Opin Plant Biol. 10:415–424. doi:10.1016/j.pbi.2007.05.003.
   PubMed Web of Science ®Google Scholar
• Izzah N, Lee J, Jayakodi M, Perumal S, Jin M, Park B, Ahn K, Yang T. 2014. Transcriptome sequencing of two parental lines of cabbage (Brassica oleracea L. var. capitata L.) and construction of an EST-based genetic map. BMC Genomics. 15:149. doi:10.1186/1471-2164-15-149.
   PubMed Web of Science ®Google Scholar
• Jalloul A, Montillet JL, Assigbetsé K, Agnel JP, Delannoy E, Triantaphylidès C, Daniel JF, Marmey P, Geiger JP, Nicole M. 2002. Lipid peroxidation in cotton: xanthomonas interactions and the role of lipoxygenases during the hypersensitive reaction. Plant J. 32:1–12. doi:10.1046/j.1365-313X.2002.01393.x.
   PubMed Web of Science ®Google Scholar
• Jamwal RS, Sharma PP. 1986. Inheritance of resistance to black rot (Xanthomonas campestris pv. campestris) in cauliflower (Brassica oleracea var. Botrytis). Euphytica. 35:941–943. doi:10.1007/BF00028603.
   Web of Science ®Google Scholar
• Jones JDG, Dangl JL. 2006. The plant immune system. Nature. 444:323–329. doi:10.1038/nature05286.
   PubMed Web of Science ®Google Scholar
• Kamoun S. 1992. Incompatible interactions between crucifers and Xanthomonas campestris involve a vascular hypersensitive response: role of the hrpX locus. Mol Plant Microbe In. 5:22–33. doi:10.1094/MPMI-5-022.
   Web of Science ®Google Scholar
• Keshavarzi M, Soylu S, Brown I, Bonas U, Nicole M, Rossiter J, Mansfield J. 2004. Basal defenses induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria. Mol Plant Microbe In. 17:805–815. doi:10.1094/MPMI.2004.17.7.805.
   PubMed Web of Science ®Google Scholar
• Lee J, Izzah N, Jayakodi M, Perumal S, Joh H, Lee H, Lee S, Park J, Yang K, Nou I, et al. 2015. Genome-wide SNP identification and QTL mapping for black rot resistance in cabbage. BMC Plant Biol. 15:32. doi:10.1186/s12870-015-0424-6.
   PubMed Web of Science ®Google Scholar
• Levine A, Tenhaken R, Dixon R, Lamb C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 79:583–593. doi:10.1016/0092-8674(94)90544-4.
   PubMed Web of Science ®Google Scholar
• Li Z, Huang J, Wang Z, Meng F, Zhang S, Wu X, Zhang Z, Gao Z. 2019. Overexpression of Arabidopsis nucleotide-binding and leucine-rich repeat genes RPS2 and RPM1(D505V) confers broad-spectrum disease resistance in rice. Front Plant Sci. 10:417. doi:10.3389/fpls.2019.00417.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 25:402–408. doi:10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar
• Lushchak VI. 2011. Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Phys C. 153:175–190.
   PubMed Web of Science ®Google Scholar
• Lv H, Fang Z, Yang L, Zhang Y, Wang Q, Liu Y, Zhuang M, Yang Y, Xie B, Liu B, et al. 2014. Mapping and analysis of a novel candidate Fusarium wilt resistance gene FOC1 in Brassica oleracea. BMC Genomics. 15:1094. doi:10.1186/1471-2164-15-1094.
   PubMed Web of Science ®Google Scholar
• Madloo P, Lema M, Francisco M, Soengas P. 2019. Role of major glucosinolates in the defense of kale against sclerotinia sclerotiorum and Xanthomonas campestris pv. campestris. Phytopathology. 109:1246–1256. doi:10.1094/PHYTO-09-18-0340-R.
   PubMed Web of Science ®Google Scholar
• McDowell JM, Dhandaydham M, Long TA, Aarts MGM, Goff S, Holub EB, Dangl JL. 1998. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. The Plant Cell. 10:1861–1874.
   PubMed Web of Science ®Google Scholar
• Mohr TJ, Mammarella ND, Hoff T, Woffenden BJ, Jelesko JG, McDowell JM. 2010. The Arabidopsis downy mildew resistance gene RPP8 is induced by pathogens and salicylic acid and is regulated by W box cis elements. Mol Plant Microbe In. 23:1303–1315. doi:10.1094/MPMI-01-10-0022.
   PubMed Web of Science ®Google Scholar
• Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods. 5:621–628. doi:10.1038/nmeth.1226.
   PubMed Web of Science ®Google Scholar
• O’Donnell PJ, Jones JB, Antoine FR, Ciardi J, Klee HJ, Chen J, Pang W, Chen B, Zhang C, Piao Z. 2001. Ethylene-dependent salicylic acid regulates an expanded cell death response to a plant pathogen. Plant J. 25:315–323. doi:10.1046/j.1365-313x.2001.00968.x.
   PubMed Web of Science ®Google Scholar
• Parkin IA, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, et al. 2014. Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol. 15:R77.
   PubMed Web of Science ®Google Scholar
• Pastorczyk M, Bednarek P. 2016. The function of glucosinolates and related metabolites in plant innate immunity. Adv Bot Res. 7:171–198.
   Web of Science ®Google Scholar
• Patil MA, Pierce ML, Phillips AL, Venters BJ, Essenberg M. 2005. Identification of genes up-regulated in bacterial-blight-resistant upland cotton in response to inoculation with Xanthomonas campestris pv. malvacearum. Physiol Mol Plant P. 67:319–335.
   Web of Science ®Google Scholar
• Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM. 2009. Networking by small-molecule hormones in plant immunity. Nat Chem Biol. 5:308–316.
   PubMed Web of Science ®Google Scholar
• Prerostova S, Dobrev P, Konradyova V, Knirsch V, Gaudinova A, Kramna B, Kazda J, Ludwig-Müller J, Vankova R. 2018. Hormonal responses to Plasmodiophora brassicae infection in Brassica napus cultivars differing in their pathogen resistance. Int J Mol Sci. 19:4024.
   Web of Science ®Google Scholar
• Ribeiro DG, Cunha GCRD, Santos CD, Silva LP, Oliveira Neto OBD, Labuto LBD, Mehta A. 2018. Brassica oleracea resistance-related proteins identified at an early stage of black rot disease. Physiol Mol Plant P. 104:9–14.
   Web of Science ®Google Scholar
• Roberts SJ, Koenraadt H. 2014. 7-019a: detection of Xanthomonas campestris pv. campestris on Brassica spp. The International Seed Testing Association (ISTA). http://seedtest.org/upload/cms/user/SH-07-019a-2014.pdf.
   Google Scholar
• Rubel MH, Robin AHK, Natarajan S, Vicente JG, Kim H, Park J, Nou I. 2017. Whole-genome re-alignment facilitates development of specific molecular markers for races 1 and 4 of Xanthomonas campestris pv. campestris, the cause of black rot disease in Brassica oleracea. Int J Mol Sci. 18:2523.
   Web of Science ®Google Scholar
• Saha P, Kalia P, Sharma M, Singh D. 2016. New source of black rot disease resistance in Brassica oleracea and genetic analysis of resistance. Euphytica. 207:35–48.
   Web of Science ®Google Scholar
• Santos C, Nogueira FCS, Domont GB, Fontes W, Prado GS, Habibi P, Santos VO, Oliveira-Neto OB, Grossi-de-Sá MF, Jorrín-Novo JV, et al. 2019a. Proteomic analysis and functional validation of a Brassica oleracea endochitinase involved in resistance to Xanthomonas campestris. Front Plant Sci. 10:414.
   PubMed Web of Science ®Google Scholar
• Santos LS, Maximiano MR, Megias E, Pappas M, Ribeiro SG, Mehta A. 2019b. Quantitative expression of microRNAs in Brassica oleracea infected with Xanthomonas campestris pv. campestris. Mol Biol Rep. 46:3523–3529.
   PubMed Web of Science ®Google Scholar
• Sharma BB, Kalia P, Singh D, Sharma TR. 2017. Introgression of black rot resistance from Brassica carinata to cauliflower (Brassica oleracea botrytis Group) through embryo rescue. Front Plant Sci. 8:1255.
   PubMed Web of Science ®Google Scholar
• Sharma BB, Kalia P, Yadava DK, Singh D, Sharma TR. 2016. Genetics and molecular mapping of black rot resistance locus Xca1bc on chromosome B-7 in ethiopian mustard (Brassica carinata A. Braun). PLoS One. 11:1–13.
   Web of Science ®Google Scholar
• Sharma BR, Swarup V, Chatterjee SS. 1972. Inheritance of resistance to black rot in cauliflower. Genome. 14:363–370.
   Google Scholar
• Singh D, S D, Yadava DK. 2011. Genetic and pathogenic variability of indian strains of Xanthomonas campestris pv. campestris causing black rot disease in crucifers. Curr Microbiol. 63:551–560.
   PubMed Web of Science ®Google Scholar
• Singh S, Dey SS, Bhatia R, Batley J, Kumar R. 2018. Molecular breeding for resistance to black rot [Xanthomonas campestris pv. campestris (Pammel) Dowson] in Brassicas: recent advances. Euphytica. 214:196.
   Web of Science ®Google Scholar
• Taylor JD, Conway J, Roberts SJ, Astley D, Vicente JG. 2002. Sources and origin of resistance to Xanthomonas campestris pv. campestris in brassica genomes. Phytopathology. 92:105–111.
   PubMed Web of Science ®Google Scholar
• Tonguç M, Griffiths PD. 2004. Development of black rot resistant interspecific hybrids between Brassica oleracea L. cultivars and Brassica accession A 19182, using embryo rescue. Euphytica. 136:313–318.
   Web of Science ®Google Scholar
• Tonu NN, Doullah MA, Shimizu M, Karim MM, Kawanabe T, Fujimoto R, Okazaki K. 2013. Comparison of positions of QTLs conferring resistance to Xanthomonas campestris pv. campestris in Brassica oleracea. Am J Plant Sci. 04:11–20.
   Google Scholar
• Ueno H, Matsumoto E, Aruga D, Kitagawa S, Matsumura H, Hayashida N. 2012. Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Mol Biol. 80:621–629.
   PubMed Web of Science ®Google Scholar
• Velasco P, Lema M, Francisco M, Soengas P, Cartea M. 2013. vivo and in vitro effects of secondary metabolites against Xanthomonas campestris pv. campestris. Molecules. 18:11131–11143.
   PubMed Web of Science ®Google Scholar
• Vicente JG, Conway J, Roberts SJ, Taylor JD. 2001. Identification and origin of Xanthomonas campestris pv. campestris races and related pathovars. Phytopathology. 91:492–499.
   PubMed Web of Science ®Google Scholar
• Vicente JG, Holub EB. 2013. Xanthomonas campestris pv. campestris (cause of black rot of crucifers) in the genomic era is still a worldwide threat to brassica crops. Mol Plant Pathol. 14:2–18.
   PubMed Web of Science ®Google Scholar
• Villeth GR, Reis FB, Tonietto A, Huergo L, de Souza EM, Pedrosa FO, Franco OVL, Mehta A. 2009. Comparative proteome analysis of Xanthomonas campestris pv. campestris in the interaction with the susceptible and the resistant cultivars of Brassica oleracea. FEMS Microbiol Lett. 298:260–266.
   PubMed Web of Science ®Google Scholar
• Villeth GRC, Carmo LST, Silva LP, Santos MF, de Oliveira Neto OB, Grossi-de-Sá MF, Ribeiro IS, Dessaune SN, Fragoso RR, Franco OL, et al. 2016. Identification of proteins in susceptible and resistant Brassica oleracea responsive to Xanthomonas campestris pv. campestris infection. J Proteomics. 143:278–285.
   PubMed Web of Science ®Google Scholar
• Wang S, Yu F, Zhang W, Tang J, Li J, Yu L, Wang H, Jiang J. 2019. Comparative transcriptomic analysis reveals gene expression changes during early stages of Plasmodiophora brassicae infection in cabbage (Brassica oleracea var. capitata L.). Can J Plant Pathol. 41:188–199.
   Web of Science ®Google Scholar
• Wasternack C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot London. 100:681–697.
   PubMed Web of Science ®Google Scholar
• Williams PH. 1980. Black rot: a continuing threat to world crucifers. Plant Dis. 64:736–742.
   Google Scholar
• Zhang J, Zhou J. 2010. Plant immunity triggered by microbial molecular signatures. Mol Plant. 3:783–793.
   PubMed Web of Science ®Google Scholar