Abstract
Key message
Fusarium yellows resistant and susceptible lines in Brassica rapa showed different salicylic acid responses; the resistant line showed a similar response to previous reports, but the susceptible line differed.
Abstract
Fusarium yellows caused by Fusarium oxysporum f. sp. conglutinans (Foc) is an important disease. Previous studies showed that genes related to salicylic acid (SA) response were more highly induced following Foc infection in Brassica rapa Fusarium yellows resistant lines than susceptible lines. However, SA-induced genes have not been identified at the whole genome level and it was unclear whether they were up-regulated by Foc inoculation. Transcriptome analysis with and without SA treatment in the B. rapa Fusarium yellows susceptible line ‘Misugi’ and the resistant line ‘Nanane’ was performed to obtain insights into the relationship between SA sensitivity/response and Fusarium yellows resistance. ‘Nanane’s up-regulated genes were related to SA response and down-regulated genes were related to jasmonic acid (JA) or ethylene (ET) response, but differentially expressed genes in ‘Misugi’ were not. This result suggests that Fusarium yellows resistant and susceptible lines have a different SA response and that an antagonistic transcription between SA and JA/ET responses was found only in a Fusarium yellows resistant line. SA-responsive genes were induced by Foc inoculation in Fusarium yellows resistant (RJKB-T23) and susceptible lines (RJKB-T24). By contrast, 39 SA-induced genes specific to RJKB-T23 might function in the defense response to Foc. In this study, SA-induced genes were identified at the whole genome level, and the possibility, the defense response to Foc observed in a resistant line could be mediated by SA-induced genes, is suggested. These results will be useful for future research concerning the SA importance in Foc or other diseases resistance in B. rapa.
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The RNA-sequencing data have been deposited with DDBJ (https://www.ddbj.nig.ac.jp) under DRA010766.
References
Abe H, Narusaka Y, Sasaki I et al (2011) Development of full-length cDNAs from Chinese cabbage (Brassica rapa subsp. pekinensis) and identification of marker genes for defence response. DNA Res 18:277–289
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Blanco F, Salinas P, Cecchini NM et al (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70:79–102
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Caarls L, Pieterse CMJ, Van Wees SCM (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170
Cao J, Zeng K, Jiang W (2006) Enhancement of postharvest disease resistance in Ya Li pear (Pyrus bretschneideri) fruit by salicylic acid sprays on the trees during fruit growth. Eur J Plant Pathol 114:363–370
Chen L, Zhang L, Yu D (2010) Wounding-induced WRKY8 is involved in basal defense in Arabidopsis. Mol Plant-Microbe Interact 23:558–565
Chung S, Lee K, Oh K et al (2005) Molecular characterization of a PR4 gene in Chinese cabbage. Integr Biosci 9:239–244
Daly P, Tomkins B (1995) Production and postharvest handling of Chinese cabbage (Brassica rapa var. pekinensis). RIRDC 97:41
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548
Du Z, Zhou X, Ling Y et al (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70
Dubos C, Stracke R, Grotewold E et al (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581
Edgar CI, McGrath KC, Dombrecht B et al (2006) Salicylic acid mediates resistance to the vascular wilt pathogen Fusarium oxysporum in the model host Arabidopsis thaliana. Australas Plant Pathol 35:581–591
Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371
Eulgem T, Rushton PJ, Robatzek S et al (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206
Fasani E, DalCorso G, Costa A et al (2019) The Arabidopsis thaliana transcription factor MYB59 regulates calcium signalling during plant growth and stress response. Plant Mol Biol 99:517–534
Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863
Fujimoto R, Sasaki T, Nishio T (2006) Characterization of DNA methyltransferase genes in Brassica rapa. Genes Genet Syst 81:235–242
Gigolashvili T, Yatusevich R, Berger B et al (2007) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 51:247–261
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329
Journot-Catalino H, Somssich IE, Roby D et al (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18:3289–3302
Kanehisa M, Sato Y (2020) KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci 29:28–35
Kawamura K, Kawanabe T, Shimizu M et al (2016) Genetic characterization of inbred lines of Chinese cabbage by DNA markers; towards the application of DNA markers to breeding of F1 hybrid cultivars. Data Brief 6:229–237
Kim KC, Lai Z, Fan B et al (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with Histone Deacetylase 19 in basal defense. Plant Cell 20:2357–2371
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360
Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350
Kitajima S, Sato F (1999) Plant pathogenesis-related proteins: molecular mechanisms of gene expression and protein function. J Biochem 125:1–8
Klessig DF, Choi HW, Dempsey DA (2018) Systemic acquired resistance and salicylic acid: past, present, and future. Mol Plant-Microbe Interact 31:871–888
Knepper C, Savory EA, Day B (2011) Arabidopsis NDR1 is an integrin-like protein with a role in fluid loss and plasma membrane-cell wall adhesion. Plant Physiol 156:286–300
Kumar D (2014) Salicylic acid signaling in disease resistance. Plant Sci 228:127–134
Lee K, Cho T (2003) Characterization of a salicylic acid- and pathogen-induced lipase-like gene in Chinese cabbage. J Biochem Mol Biol 36:433–441
Lv H, Fang Z, Yang L et al (2014) Mapping and analysis of a novel candidate Fusarium wilt resistance gene FOC1 in Brassica oleracea. BMC Genom 15:1094
Lv H, Miyaji N, Osabe K et al (2020) The importance of genetic and epigenetic research in the Brassica vegetables in the face of climate change. In: Kole C (ed) Genomic designing of climate-smart vegetable crops, 1st edn. Springer, Berlin, pp 161–255
Mandal S, Mallick N, Mitra A (2009) Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. Plant Physiol Biochem 47:642–649
Mehraj H, Akter A, Miyaji N et al (2020) Genetics of clubroot and fusarium wilt disease resistance in Brassica vegetables: the application of marker assisted breeding for disease resistance. Plants 9:726
Miyaji N, Shimizu M, Miyazaki J et al (2017) Comparison of transcriptome profiles by Fusarium oxysporum inoculation between Fusarium yellows resistant and susceptible lines in Brassica rapa L. Plant Cell Rep 36:1841–1854
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Narusaka Y, Narusaka M, Horio T et al (1999) Comparison of local and systemic induction of acquired disease resistance in cucumber plants treated with benzothiadiazoles or salicylic acid. Plant Cell Physiol 40:388–395
Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655
Park YS, Min HJ, Ryang SH et al (2003) Characterization of salicylic acid-induced genes in Chinese cabbage. Plant Cell Rep 21:1027–1034
Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LGG et al (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:D822–D827
Pieterse CMJ, Van der Does D, Zamioudis C et al (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521
Pu Z, Shimizu M, Zhang Y et al (2012) Genetic mapping of a fusarium wilt resistance gene in Brassica oleracea. Mol Breed 30:809–818
Pu Z, Ino Y, Kimura Y et al (2016) Changes in the proteome of xylem sap in Brassica oleracea in response to Fusarium oxysporum stress. Front Plant Sci 7:31
Rekhter D, Lüdke D, Ding Y et al (2019) Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science 365:498–502
Seo M, Kim JS (2017) Understanding of MYB transcription factors involved in glucosinolate biosynthesis in Brassicaceae. Molecules 22:1549
Shigenaga AM, Argueso CT (2016) No hormone to rule them all: interactions of plant hormones during the responses of plants to pathogens. Semin Cell Dev Biol 56:174–189
Shigenaga AM, Berens ML, Tsuda K et al (2017) Towards engineering of hormonal crosstalk in plant immunity. Curr Opin Plant Biol 38:164–172
Shimizu M, Fujimoto R, Ying H et al (2014) Identification of candidate genes for fusarium yellows resistance in Chinese cabbage by differential expression analysis. Plant Mol Biol 85:247–257
Shimizu M, Pu Z, Kawanabe T et al (2015) Map-based cloning of a candidate gene conferring Fusarium yellows resistance in Brassica oleracea. Theor Appl Genet 128:119–130
Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100
Sun T, Huang J, Xu Y et al (2020) Redundant CAMTA transcription factors negatively regulate the biosynthesis of salicylic acid and N-Hydroxypipecolic acid by modulating the expression of SARD1 and CBP60g. Mol Plant 13:144–156
Thomma BPHJ, Eggermont K, Penninckx IAMA et al (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci U S A 95:15107–15111
Trapnell C, Roberts A, Goff L et al (2013) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578
Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206
Walker JC (1930) Inheritance of fusarium resistance in cabbage. J Agric Res 40:721–745
Wang L, Tsuda K, Sato M et al (2009) Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog 5:e1000301
Wang L, Tsuda K, Truman W et al (2011) CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J 67:1029–1041
Xie YD, Li W, Guo D et al (2010) The Arabidopsis gene SIGMA FACTOR-BINDING PROTEIN 1 plays a role in the salicylate- and jasmonate-mediated defence responses. Plant Cell Environ 33:828–839
Xing DH, Lai ZB, Zheng ZY et al (2008) Stress- and pathogen-induced Arabidopsis WRKY48 is a transcriptional activator that represses plant basal defense. Mol Plant 1:459–470
Xu X, Chen C, Fan B et al (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310–1326
Yan S, Dong X (2014) Perception of the plant immune signal salicylic acid. Curr Opin Plant Biol 20:64–68
Yanhui C, Xiaoyuan Y, Kun H et al (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124
Yao H, Tian S (2005) Effects of pre- and post-harvest application of salicylic acid or methyl jasmonate on inducing disease resistance of sweet cherry fruit in storage. Postharvest Biol Technol 35:253–262
Yi GE, Robin AHK, Yang K et al (2016) Exogenous methyl jasmonate and salicylic acid induce subspecies-specific patterns of glucosinolate accumulation and gene expression in Brassica oleracea L. Molecules 21:1417
Zeng K, Cao J, Jiang W (2006) Enhancing disease resistance in harvested mango (Mangifera indica L. cv. ‘Matisu’) fruit by salicylic acid. J Sci Food Agric 86:694–698
Zhang Y, Zhao L, Zhao J et al (2017) S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis. Plant Physiol 175:1082–1093
Zhang W, Zhao F, Jiang L et al (2018) Different pathogen defense strategies in Arabidopsis: more than pathogen recognition. Cells 7:252
Acknowledgements
Computations were partially performed on the NIG supercomputer at ROIS National Institute of Genetics.
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This work was funded by Grant-in-Aid for JSPS Research Fellow to NM and grants from Project of the NARO Bio-oriented Technology Research Advancement Institution (Research program on development of innovation technology) to RF.
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RF, ESD, and TTY designed research. NM performed research. NM and MS analyzed the RNA-seq data. NM, RF, and ESD wrote the paper.
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Miyaji, N., Shimizu, M., Takasaki-Yasuda, T. et al. The transcriptional response to salicylic acid plays a role in Fusarium yellows resistance in Brassica rapa L.. Plant Cell Rep 40, 605–619 (2021). https://doi.org/10.1007/s00299-020-02658-1
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DOI: https://doi.org/10.1007/s00299-020-02658-1