Comparative transcriptomic analysis reveals gene expression changes during early stages of Plasmodiophora brassicae infection in cabbage (Brassica oleracea var. capitata L.)

References

• Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci USA. 95:10306–10311.
   PubMed Web of Science ®Google Scholar
• Agarwal A, Kaul V, Faggian R, Cahill DM. 2009. Development and use of a model system to monitor clubroot disease progression with an australian field population of plasmodiophora brassicae. Australas Plant Path. 38:120-127.
   Web of Science ®Google Scholar
• Agarwal A, Kaul V, Faggian R, Rookes JE, Ludwigmuller J, Cahill DM. 2011. Analysis of global host gene expression during the primary phase of the Arabidopsis thaliana–plasmodiophora brassicae interaction. Func Plant Biol. 38:462–478.
   PubMed Web of Science ®Google Scholar
• Anders S, Huber W, Halsall JA, Page P, Illingworth RS, Taylor AMR, Davison V, O’Neill LP, Turner BM. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Yekutieli D. 2001. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 29:1165–1188.
   Web of Science ®Google Scholar
• Bi K, He Z, Gao Z, Zhao Y, Fu Y, Cheng J, Xie J, Jiang D, Chen T. 2016. Integrated omics study of lipid droplets from Plasmodiophora brassicae. Sci Rep. 6:36965.
   PubMed Web of Science ®Google Scholar
• Bleecker AB, Kende H. 2000. Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol. 16:1–18.
   PubMed Web of Science ®Google Scholar
• Blein J, Coutosthevenot P, Marion D, Ponchet M. 2002. From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci. 7:293–296.
   PubMed Web of Science ®Google Scholar
• Buczacki ST, Toxopeus H, Mattusch P, Johnston TD, Dixon GR, Hobolth LA. 1975. Study of physiologic specialization in Plasmodiophora brassicae: proposals for attempted rationalization through an international approach. Trans Brit Mycol Soc. 65:295–303.
   Web of Science ®Google Scholar
• Burki F, Kudryavtsev A, Matz MV, Aglyamova GV, Bulman S, Fiers M, Keeling PJ, Pawlowski J. 2010. Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evol Biol. 10:377.
   PubMed Web of Science ®Google Scholar
• Chen J, Jing J, Zhan Z, Zhang T, Zhang C, Piao Z, Schönbach C. 2013. Identification of novel QTLs for isolate-specific partial resistance to Plasmodiophora brassicae in Brassica rapa. PLoS One. 8:e85307.
   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.
   PubMed Web of Science ®Google Scholar
• Chen L, Zou W, Wu G, Lin H, Xi D. 2018. Tobacco alpha-expansin EXPA4 plays a role in Nicotiana benthamiana defence against Tobacco mosaic virus. Planta. 247:355–368.
   PubMed Web of Science ®Google Scholar
• Chen Y, Lee C, Cheng K, Chang W, Huang R, Nam HG, Chen Y. 2014. Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. Plant Cell. 26:4135–4148.
   PubMed Web of Science ®Google Scholar
• Cho H, Cosgrove DJ. 2002. Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell. 14:3237–3253.
   PubMed Web of Science ®Google Scholar
• Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. 2009. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science. 323:95–101.
   PubMed Web of Science ®Google Scholar
• Dixon GR. 2009. The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J Plant Growth Regul. 28:194–202.
   Web of Science ®Google Scholar
• Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. 11:539–548.
   PubMed Web of Science ®Google Scholar
• Gfeller A, Liechti R, Farmer EE. 2010. Arabidopsis jasmonate signaling pathway. Sci Signal. 3:cm4.
   PubMed Web of Science ®Google Scholar
• Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol. 43:205–227.
   PubMed Web of Science ®Google Scholar
• Hatakeyama K, Niwa T, Kato T, Ohara T, Kakizaki T, Matsumoto S. 2017. The tandem repeated organization of NB-LRR genes in the clubroot-resistant CRb locus in Brassica rapa L. Mol Genet Gen. 292:397–405.
   PubMed Web of Science ®Google Scholar
• Hatakeyama K, Suwabe K, Tomita RN, Kato T, Nunome T, Fukuoka H, Matsumoto S, Wu K. 2013. Identification and characterization of Crr1a, a gene for resistance to clubroot disease (Plasmodiophora brassicae Woronin) in Brassica rapa L. PLoS One. 8:e54745.
   PubMed Web of Science ®Google Scholar
• Hwang SF, Howard RJ, Strelkov SE, Gossen BD, Peng G. 2014. Management of clubroot (Plasmodiophora brassicae) on canola (Brassica napus) in western Canada. Can J Plant Pathol. 36(Supp.1):49–65.
   Web of Science ®Google Scholar
• Irani S, Trost B, Waldner M, Nayidu NK, Tu J, Kusalik A, Todd CD, Wei Y, Bonhamsmith PC. 2018. Transcriptome analysis of response to Plasmodiophora brassicae infection in the Arabidopsis shoot and root. BMC Genomics. 19:23.
   PubMed Web of Science ®Google Scholar
• Ji R, Zhao L, Xing M, Shen X, Bi Q, Peng S, Feng H. 2014. Infection of Plasmodiophora brassicae in Chinese cabbage. Genet Mol Res. 13:10976–10982.
   PubMed Web of Science ®Google Scholar
• Jia H, Wei XC, Yang Y, Yuan YX, Wei F, Zhao YY, Yang SJ, Yao QJ, Wang ZY, Tian BM, et al. 2017. Root RNA-seq analysis reveals a distinct transcriptome landscape between clubroot-susceptible and clubroot-resistant Chinese cabbage lines after Plasmodiophora brassicae infection. Plant Soil. 421:93–105.
   Web of Science ®Google Scholar
• Jones JD, Dangl JL. 2006. The plant immune system. Nature. 444:323–329.
   PubMed Web of Science ®Google Scholar
• Jubault M, Lariagon C, Taconnat L, Renou J, Gravot A, Delourme R, Manzanaresdauleux MJ. 2013. Partial resistance to clubroot in Arabidopsis is based on changes in the host primary metabolism and targeted cell division and expansion capacity. Funct Integr Genomic. 13:191–205.
   PubMed Web of Science ®Google Scholar
• Kageyama K, Asano T. 2009. Life cycle of Plasmodiophora brassicae. J Plant Growth Regul. 28:203–211.
   Web of Science ®Google Scholar
• Kim KH, Kang YJ, Kim DH, Yoon MY, Moon JK, Kim MY, Van K, Lee SH. 2011. RNA-Seq analysis of a soybean near-isogenic line carrying bacterial leaf pustule-resistant and -susceptible alleles. DNA Res. 18:483–497.
   PubMed Web of Science ®Google Scholar
• Latge J, Beauvais A. 2014. Functional duality of the cell wall. Curr Opin Microbiol. 20:111–117.
   PubMed Web of Science ®Google Scholar
• Liu MJ, Sugimoto K, Uygun S, Panchy N, Campbell MS, Yandell M, Howe GA, Shiu SH. 2018a. Regulatory divergence in wound-responsive gene expression between domesticated and wild tomato. Plant Cell. 30:1445–1460.
   PubMed Web of Science ®Google Scholar
• Liu Y, Xu A, Liang F, Yao X, Wang Y, Liu X, Zhang Y, Dalelhan J, Zhang B, Qin M, et al. 2018b. Screening of clubroot-resistant varieties and transfer of clubroot resistance genes to Brassica napus using distant hybridization. Breed Sci. 68:258–267.
   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.
   PubMed Web of Science ®Google Scholar
• Louvet R, Cavel E, Gutierrez L, Guenin S, Roger D, Gillet F, Guerineau F, Pelloux J. 2006. Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta. 224:782–791.
   PubMed Web of Science ®Google Scholar
• Lu L, Xu S, Zeng L, Zheng X, Yu T. 2014. Rhodosporidium paludigenum induced resistance in Ponkan mandarin against Penicillium digitatum requires ethylene-dependent signaling pathway. Postharvest Biol Tech. 97:93–101.
   Web of Science ®Google Scholar
• Marowa P, Ding A, Kong Y. 2016. Expansins: roles in plant growth and potential applications in crop improvement. Plant Cell Rep. 35:949–965.
   PubMed Web of Science ®Google Scholar
• Pandey SP, Somssich IE. 2009. The role of WRKY transcription factors in plant immunity. Plant Physiol. 150:1648–1655.
   PubMed Web of Science ®Google Scholar
• Parkin IAP, 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
• Pelloux J, Rusterucci C, Mellerowicz EJ. 2007. New insights into pectin methylesterase structure and function. Trends Plant Sci. 12:267–277.
   PubMed Web of Science ®Google Scholar
• Peng G, Lahlali R, Hwang SF, Pageau D, Hynes RK, Mcdonald MR, Gossen BD, Strelkov SE. 2014. Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Can J Plant Pathol. 36:99–112.
   Web of Science ®Google Scholar
• Piao Z, Ramchiary N, Yong PL. 2009. Genetics of clubroot resistance in Brassica species. J Plant Growth Regul. 28:252–264.
   Web of Science ®Google Scholar
• Rayapuram C, Jensen MK, Maiser F, Shanir JV, Hornshoj H, Rung JH, Gregersen PL, Schweizer P, Collinge DB, Lyngkjaer MF. 2012. Regulation of basal resistance by a powdery mildew-induced cysteine-rich receptor-like protein kinase in barley. Mol Plant Pathol. 13:135–147.
   PubMed Web of Science ®Google Scholar
• Regente M, Giudici AM, Villalain J, La Canal LD. 2005. The cytotoxic properties of a plant lipid transfer protein involve membrane permeabilization of target cells. Lett Appl Microbiol. 40:183–189.
   PubMed Web of Science ®Google Scholar
• Sagi M, Fluhr R. 2001. Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126:1281–1290.
   PubMed Web of Science ®Google Scholar
• Scheible W, Fry BA, Kochevenko A, Schindelasch D, Zimmerli L, Somerville S, Loria R, Somerville C. 2003. An Arabidopsis mutant resistant to thaxtomin A, a cellulose synthesis inhibitor from Streptomyces species. Plant Cell. 15:1781–1794.
   PubMed Web of Science ®Google Scholar
• Schuller A, Kehr J, Ludwig-Müller J. 2014. Laser microdissection coupled to transcriptional profiling of Arabidopsis roots inoculated by Plasmodiophora brassicae indicates a role for brassinosteroids in clubroot formation. Plant Cell Physiol. 55:392–411.
   PubMed Web of Science ®Google Scholar
• Siemens J, Keller I, Sarx J, Kunz S, Schuller A, Nagel W, Schmulling T, Parniske M, Ludwig-Muller J. 2006. Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol Plant-Microbe Interact. 19:480–494.
   PubMed Web of Science ®Google Scholar
• Song T, Chu M, Lahlali R, Yu F, Peng G. 2016. Shotgun label-free proteomic analysis of clubroot (Plasmodiophora brassicae) resistance conferred by the gene Rcr1 in Brassica rapa. Front Plant Sci. 7:1013.
   PubMed Web of Science ®Google Scholar
• Stringlis IA, Yu K, Feussner K, de Jonge R, van Bentum S, Van Verk MC, Berendsen RL, Bakker P, Feussner I, Pieterse CMJ. 2018. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci USA. 115:E5213–E5222.
   PubMed Web of Science ®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
• Wang SY, Qiang W, Hong W, Li Y, Jianbin L, Wanxia D. 2016. Identification of Plasmodiophora brassicae Wor. and resistance assessment of cabbage (Brasisica oleracea var. capitata L.) germplasm. J Plant Genet Resour. 17:1123–1132. in Chinese.
   Google Scholar
• You J, Chan Z. 2015. ROS regulation during abiotic stress responses in crop plants. Front Plant Sci. 6:1092.
   PubMed Web of Science ®Google Scholar
• Zipfel C. 2009. Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol. 12:414–420.
   PubMed Web of Science ®Google Scholar