Skip to main content
Log in

Fine-mapping of a major QTL (Fwr1) for fusarium wilt resistance in radish

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

A major radish QTL (Fwr1) for fusarium wilt resistance was fine-mapped. Sequence and expression analyses suggest that a gene encoding a serine/arginine-rich protein kinase is a candidate gene for Fwr1.

Abstract

Fusarium wilt resistance locus 1 (Fwr1) is a major quantitative trait locus (QTL) mediating the resistance of radish inbred line ‘B2’ to Fusarium oxysporum, which is responsible for fusarium wilt. We previously detected Fwr1 on radish linkage group 3 (i.e., chromosome 5). In this study, a high-resolution genetic map of the Fwr1 locus was constructed by analyzing 354 recombinant F2 plants derived from a cross between ‘B2’ and ‘835’, the latter of which is susceptible to fusarium wilt. The Fwr1 QTL was fine-mapped to a 139.8-kb region between markers FM82 and FM87 in the middle part of chromosome 5. Fifteen candidate genes were predicted in this region based on a sequence comparison with the ‘WK10039’ radish reference genome. Additionally, we examined the time-course expression patterns of these predicted genes following an infection by the fusarium wilt pathogen. The ORF4 expression level was significantly higher in the resistant ‘B2’ plants than in the susceptible ‘835’ plants. The ORF4 sequence was predicted to encode a serine/arginine-rich protein kinase and includes SNPs that result in nonsynonymous mutations, which may have important functional consequences. This study reveals a novel gene responsible for fusarium wilt resistance in radish. Further analyses of this gene may elucidate the molecular mechanisms underlying the fusarium wilt resistance of plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Branham SE, Levi A, Katawczik M, Fei Z, Wechter WP (2018) Construction of a genome-anchored, high-density genetic map for melon (Cucumis melo L.) and identification of Fusarium oxysporum f. sp. melonis race 1 resistance QTL. Theor Appl Genet 131(4):829–837

    Article  CAS  PubMed  Google Scholar 

  • Brotman Y, Normantovich M, Goldenberg Z, Zvirin Z, Kovalski I, Stovbun N, Doniger T, Bolger AM, Troadec C, Bendahmane A, Cohen R, Katzir N, Pitrat M, Dogimont C, Perl-Treves R (2013) Dual resistance of melon to Fusarium oxysporum races 0 and 2 and to Papaya ring-spot virus is controlled by a pair of head-to-head-oriented NB-LRR genes of unusual architecture. Mol Plant 6:235–238

    Article  CAS  PubMed  Google Scholar 

  • Brueggeman R, Druka A, Nirmala J, Cavileer T, Drader T, Rostoks N, Mirlohi A, Bennypaul H, Gill U, Kudrna D, Whitelaw C, Kilian A, Han F, Sun Y, Gill K, Steffenson B, Kleinhofs A (2008) The stem rust resistance gene Rpg5 encodes a protein with nucleotide-binding-site, leucine-rich, and protein kinase domains. Proc Natl Acad Sci 105:14970–14975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu D, Wang X, Chen P (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc Natl Acad Sci 108:7727–7732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catanzariti AM, Lim GT, Jones DA (2015) The tomato I-3 gene: a novel gene for resistance to Fusarium wilt disease. New Phytol 207:106–118

    Article  CAS  PubMed  Google Scholar 

  • Catanzariti AM, Do HT, Bru P, de Sain M, Thatcher LF, Rep M, Jones DA (2017) The tomato I gene for Fusarium wilt resistance encodes an atypical leucine-rich repeat receptor-like protein whose function is nevertheless dependent on SOBIR 1 and SERK 3/BAK 1. Plant J 89(6):1195–1209

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty J, Ghosh P, Sen S, Nandi AK, Das S (2019) CaMPK9 increases the stability of CaWRKY40 transcription factor which triggers defense response in chickpea upon Fusarium oxysporum f. sp. ciceri Race1 infection. Plant Mol Biol 100:411–431

    Article  CAS  PubMed  Google Scholar 

  • Cole SJ, Diener AC (2013) Diversity in receptor-like kinase genes is a major determinant of quantitative resistance to Fusarium oxysporum f.sp. matthioli. New Phytol 200(1):172–184

    Article  CAS  PubMed  Google Scholar 

  • de Boer M, Bom P, Kindt F, Keurentjes JJ, van der Sluis I, van Loon LC, Bakker PA (2003) Control of fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Phytopathol 93:626–632

    Article  Google Scholar 

  • van Bentem S, Anrather D, Roitinger E, Djamei A, Hufnagl T, Barta A, Csaszar E, Dohnal I, Lecourieux D, Hirt H (2006) Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism. Nucleic Acids Res 34:3267–3278

    Article  CAS  Google Scholar 

  • Diener AC, Ausubel FM (2005) Resistance to Fusarium Oxysporum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171:305–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dinesh-Kumar SP, Baker BJ (2000) Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci 97:1908–1913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dinolfo MI, Castanares E, Stenglein SA (2017) Fusarium-plant interaction: state of the art—a review. Plant Protect Sci 53:61–70

    Article  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  CAS  PubMed  Google Scholar 

  • Edgar CI, McGrath KC, Dombrecht B, Manners JM, Maclean DC, Schenk PM, Kazan K (2006) Salicylic acid mediates resistance to the vascular wilt pathogen Fusarium oxysporum in the model host Arabidopsis thaliana. Australas Plant Path 35(6):581–591

    Article  CAS  Google Scholar 

  • Giannakouros T, Nikolakaki E, Mylonis I, Georgatsou E (2011) Serine-arginine protein kinases: a small protein kinase family with a large cellular presence. FEBS J 278(4):570–586

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Cendales Y, Catanzariti AM, Baker B, McGrath DJ, Jones DA (2016) Identification of I-7 expands the repertoire of genes for resistance to Fusarium wilt in tomato to three resistance gene classes. Mol Plant Pathol 17(3):448–463

    Article  CAS  PubMed  Google Scholar 

  • Hanks SK (2003) Genomic analysis of the eukaryotic protein kinase superfamily: a perspective. Genome Biol 4:111

    Article  PubMed  PubMed Central  Google Scholar 

  • Hemming MN, Basuki S, McGrath DJ, Carroll BJ, Jones DA (2004) Fine mapping of the tomato I-3 gene for fusarium wilt resistance and elimination of a co-segregating resistance gene analogue as a candidate for I-3. Theor Appl Genet 109:409–418

    Article  CAS  PubMed  Google Scholar 

  • Husaini AM, Sakina A, Cambay SR (2018) Host–pathogen interaction in Fusarium oxysporum infections: Where do we stand? Mol Plant Microbe In 31:889–898

    Article  CAS  Google Scholar 

  • Joobeur T, King JJ, Nolin SJ, Thomas CE, Dean RA (2004) The Fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features. Plant J 39:283–297

    Article  CAS  PubMed  Google Scholar 

  • Kamei A, Tsuro M, Kubo N, Hayashi T, Wang N, Fujimura T, Hirai M (2010) QTL mapping of clubroot resistance in radish (Raphanus sativus L.). Theor Appl Genet 120:1021–1027

    Article  PubMed  Google Scholar 

  • Kaneko Y, Kimizukaa-Takagi C, Bang SW, Matsuzawa Y (2007) Radish. In: Kole C (ed) Genome mapping and nolecular breeding in plant, vol 5. Springer, New York, pp 141–160

    Google Scholar 

  • Kim H, Hwang SM, Lee JH, Oh M, Han JW, Choi GJ (2017) Specific PCR detection of Fusarium oxysporum f. sp. raphani: a causal agent of Fusarium wilt on radish plants. Lett Appl Microbiol 65:133–140

    Article  CAS  PubMed  Google Scholar 

  • Kitashiba H, Li F, Hirakawa H, Kawanabe T, Zou Z, Hasegawa Y, Tonosaki K, Shirasawa S, Fukushima A, Yokoi S, Takahata Y, Kakizaki T, Ishida M, Okamoto S, Sakamoto K, Shirasawa K, Tabata S, Nishio T (2014) Draft sequences of the radish (Raphanus sativus L.) genome. DNA Res 21:481–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar Y, Zhang L, Panigrahi P, Dholakia BB, Dewangan V, Chavan SG, Kunjir SM, Wu X, Li N, Rajmohanan PR, Kadoo NY, Giri AP, Tang H, Gupta VS (2016) Fusarium oxysporum mediates systems metabolic reprogramming of chickpea roots as revealed by a combination of proteomics and metabolomics. Plant Biotechnol J 14:1589–1603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lievens B, Rep M, Thomma BP (2008) Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum. Pest Manag Sci 64(8):781–788

    Article  CAS  PubMed  Google Scholar 

  • Lv H, Fang Z, Yang L, Zhang Y, Wang Q, Liu Y, Zhuang M, Yang Y, Xie B, Liu B, Liu J, Kang J, Wang X (2014) Mapping and analysis of a novel candidate Fusarium wilt resistance gene FOC1 in Brassica oleracea. BMC Genom 15:1094

    Article  CAS  Google Scholar 

  • Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2014) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436

    Article  CAS  PubMed  Google Scholar 

  • Matic S, Gilardi G, Gullino ML, Garibaldi A (2018) Evidence for an expanded host range of Fusarium oxysporum f. sp chrysanthemi. J Plant Pathol 100:97–104

    Article  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 10:311–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mun JH, Chung H, Chung WH, Oh M, Jeong YM, Kim N, Ahn BO, Park BS, Park S, Lim KB, Hwang YJ, Yu HJ (2015) Construction of a reference genetic map of Raphanus sativus based on genotyping by whole-genome resequencing. Theor Appl Genet 128(2):259–272

    Article  CAS  PubMed  Google Scholar 

  • Oumouloud A, El-Otmani M, Chikh-Rouhou H, Claver AG, Torres RG, Perl-Treves R, Alvarez JM (2013) Breeding melon for resistance to Fusarium wilt: recent developments. Euphytica 192:155–169

    Article  CAS  Google Scholar 

  • Perchepied L, Pitrat M (2004) Polygenic inheritance of partial resistance to Fusarium oxysporum f. sp. melonis Race 1.2 in Melon. Phytopathology 94:1331–1336

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, Jiao D, Gong G, Zhang H, Guo S, Zhang J, Xu Y (2015) Genetic analysis and chromosome mapping of resistance to Fusarium oxysporum f. sp. niveum (FON) race 1 and race 2 in watermelon (Citrullus lanatus L.). Mol Breed 35:183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Romeis T (2001) Protein kinases in the plant defence response. Curr Opin Plant Biol 4:407–414

    Article  CAS  PubMed  Google Scholar 

  • Rommens CM, Salmeron JM, Oldroyd GE, Staskawicz BJ (1995) Intergeneric transfer and functional expression of the tomato disease resistance gene Pto. Plant Cell 7:1537–1544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542

    Article  CAS  PubMed  Google Scholar 

  • Shen Y, Diener AC (2013) Arabidopsis thaliana resistance to fusarium oxysporum 2 implicates tyrosine-sulfated peptide signaling in susceptibility and resistance to root infection. PLoS Genet 9:e1003525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu M, Fujimoto R, Ying H, Pu ZJ, Ebe Y, Kawanabe T, Saeki N, Taylor JM, Kaji M, Dennis ES, Okazaki K (2014) Identification of candidate genes for Fusarium yellows resistance in Chinese cabbage by differential expression analysis. Plant Mol Biol 85:247–257

    Article  CAS  PubMed  Google Scholar 

  • Shimizu M, Pu ZJ, Kawanabe T, Kitashiba H, Matsumoto S, Ebe Y, Sano M, Funaki T, Fukai E, Fujimoto R, Okazaki K (2015) Map-based cloning of a candidate gene conferring Fusarium yellows resistance in Brassica oleracea. Theor Appl Genet 128:119–130

    Article  CAS  PubMed  Google Scholar 

  • Shirasawa K, Oyama M, Hirakawa H, Sato S, Tabata S, Fujioka T, Kimizuka-Takagi C, Sasamoto S, Watanabe A, Kato M, Kishida Y, Kohara M, Takahashi C, Tsuruoka H, Wada T, Sakai T, Isobe S (2011) An EST-SSR linkage map of Raphanus sativus and comparative genomics of the Brassicaceae. DNA Res 18:221–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, Diergaarde P, Van der Lee T, Bleeker M, Onstenk J, de Both M, Haring M, Mes J, Cornelissen B, Zabeau M, Vos P (1998) Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055–1068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

    Article  CAS  PubMed  Google Scholar 

  • Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744

    Article  CAS  Google Scholar 

  • Swarupa V, Ravishankar KV, Rekha A (2014) Plant defense response against Fusarium oxysporum and strategies to develop tolerant genotypes in banana. Planta 239(4):735–751

    Article  CAS  PubMed  Google Scholar 

  • Swiderski MR, Innes RW (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J 26:101–112

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40(15):e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Ooijen JW (2006) JoinMap®4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2006) Windows QTL Cartographer V2.5. User manual. Bioinformatics Research Centre; North Carolina State University, Raleigh

  • Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998) A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10:1439–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing M, Lv H, Ma J, Xu D, Li H, Yang L, Kang J, Wang X, Fang Z (2016) Transcriptome profiling of resistance to Fusarium oxysporum f. sp. conglutinans in Cabbage (Brassica oleracea) roots. PLoS ONE 11:e0148048

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu X, Choi SR, Ramchiary N, Miao X, Lee SH, Sun HJ, Kim S, Ahn CH, Lim YP (2013) Comparative mapping of Raphanus sativus genome using Brassica markers and quantitative trait loci analysis for the Fusarium wilt resistance trait. Theor Appl Genet 126:2553–2562

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Choi SR, Dhandapani V, Rameneni JJ, Li X, Pang W, Lee JY, Lim YP (2016) Quantitative trait loci for morphological traits and their association with functional genes in Raphanus sativus. Front Plant Sci 7:255

    PubMed  PubMed Central  Google Scholar 

  • Zhang XC, Gassmann W (2003) RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. Plant Cell 15:2333–2342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou Z, Ishida M, Li F, Kakizaki T, Suzuki S, Kitashiba H, Nishio T (2013) QTL analysis using SNP markers developed by next-generation sequencing for identification of candidate genes controlling 4-methylthio-3-butenyl glucosinolate contents in roots of radish, Raphanus sativus L. PloS One 8:e53541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries through the Golden Seed Project, which is funded by the Ministry of Agriculture, Food and Rural Affairs (Grant Numbers 213006-05-3-SBO20 and 213006-05-3-SB110).

Author information

Authors and Affiliations

Authors

Contributions

XY and LL designed the experiment, carried out the marker development, analyzed all data, and drafted the manuscript. LL and YM were participated in phenotype evaluations, and marker survey and genotyping, candidate gene identification. SSC participated in data analysis and modification of the manuscript. SYY interpreted the data and designed the experiment. YPL provided plant materials, conceived the study, and finalized the manuscript. SRC conceived and designed the study, participated as a director, and wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Su Ryun Choi.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by Carlos F. Quiros.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1(a)

Multiple sequence alignment and phylogenetic analysis of the following Cruciferae species and proteins: Arabidopsis thaliana (AT3G53030), Raphanus sativus paralog of RS258060 (Rs568250), R. sativus SRPK reference sequence (Rs258060), ‘B2’ SRPK (Rs258060), ‘835’ SRPK (Rs258060), Brassica rapa (Bra006970), Brassica oleracea (Bol025090), Brassica napus (GSBRNA2T00109131001), Brassica juncea (BjuA035510), Zea mays (ONM09221.1), Oryza sativa (XP_015630587.1), Solanum lycopersicum (XP_004250999.1), and Capsicum annuum (XP_016547285.1). (a) Multiple sequence alignment of 13 sequences. The fully conserved residues are indicated in black, whereas the residues with a lower degree of conservation are indicated in gray. Various conserved kinase subdomains are marked with Roman numerals above the aligned sequences (PDF 1193 kb)

Supplementary Fig. 1(b)

Phylogenetic relationships among 13 SRPK sequences from radish (‘B2’ and ‘835’) and other plant species. The ‘B2’ SRPK is relatively closely related to a sequence encoded in the radish reference genome. The phylogenetic tree was constructed according to the neighbor-joining method of CLUSTAL W (Thompson et al. 1997). (TIFF 468 kb)

Supplementary material 3 (XLSX 16 kb)

Supplementary material 4 (XLSX 12 kb)

Supplementary material 5 (XLSX 10 kb)

Supplementary material 6 (XLSX 9 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, X., Lu, L., Ma, Y. et al. Fine-mapping of a major QTL (Fwr1) for fusarium wilt resistance in radish. Theor Appl Genet 133, 329–340 (2020). https://doi.org/10.1007/s00122-019-03461-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03461-7

Navigation