Abstract
Key message
A major novel quantitative disease resistance locus, qRfg_Gm06, for Fusarium graminearum was genetically mapped to chromosome 6. Genomic-assisted haplotype analysis within this region identified three putative candidate genes.
Abstract
Fusarium graminearum causes seed, root rot, and seedling damping-off in soybean which contributes to reduced stands and yield. A cultivar Magellan and PI 567516C were identified with low and high levels of partial resistance to F. graminearum, respectively. Quantitative disease resistance loci (QDRL) were mapped with 241 F7:8 recombinant inbred lines (RILs) derived from a cross of Magellan × PI 567516C. Phenotypic evaluation for resistance to F. graminearum used the rolled towel assay in a randomized incomplete block design. The genetic map was constructed from 927 polymorphic single nucleotide polymorphism (SNP) and simple sequence repeat (SSR) markers. One major QDRL qRfg_Gm06 was detected and mapped to chromosome 6 with a LOD score of 20.3 explaining 40.2% of the total phenotypic variation. This QDRL was mapped to a ~400 kb genomic region of the Williams 82 reference genome. Genome mining of this region identified 14 putative candidate disease resistance genes. Haplotype analysis of this locus using whole genome re-sequencing (WGRS) of 106 diverse soybean lines narrowed the list to three genes. A SNP genotyping Kompetitive allele-specific PCR (KASP) assay was designed for one of the genes and was validated in a subset of the RILs and all 106 diverse lines.
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References
Acharya B (2014) Evaluation of soybean germplasm for additional sources of resistance and characterization of resistance towards Fusarium graminearum. M.S. Thesis, The Ohio State University
Acharya B, Lee S, Mian MAR, Jun TH, McHale LK, Michel AP, Dorrance AE (2015) Identification and mapping of quantitative trait loci (QTL) conferring resistance to Fusarium graminearum from soybean PI 567301B. Theor Appl Genet 128:827–838
Anderson JA, Stack RW, Liu S, Waldron BL, Fjeld AD, Coyne C, Moreno-Sevilla B, Fetch JM, Song QJ, Cregan PB, Frohberg RC (2001) DNA markers for Fusarium head blight resistance QTLs its two wheat populations. Theor Appl Genet 102:1164–1168
Arelli PR, Concibido VC, Young LD (2010) QTLs associated with resistance in soybean PI567516C to synthetic nematode population infecting cv. Hartwig. J Crop Sci Biotech 13:163–167
Asekova S, Kulkarni KP, Patil G, Kim M, Song JT, Nguyen HT, Shannon JG, Lee JD (2016) Genetic analysis of shoot fresh weight in a cross of wild (G. soja) and cultivated (G. max) soybean. Mol Breed 36:103. doi:10.1007/s11032-016-0530-7
Bai GH, Kolb FL, Shaner G, Domier LL (1999) Amplified fragment length polymorphism markers linked to a major quantitative trait locus controlling scab resistance in wheat. Phytopathology 89:343–348
Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442
Bergamini E, Catellani D, Dall’asta C, Galaverna G, Dossena A, Marchelli R, Suman M (2010) Fate of Fusarium mycotoxins in the cereal product supply chain: the deoxynivalenol (DON) case within industrial bread-making technology. Food Addit Contam A 27:677–687
Bernardo AN, Ma HX, Zhang DD, Bai GH (2012) Single nucleotide polymorphism in wheat chromosome region harboring Fhb1 for Fusarium head blight resistance. Mol Breed 29:477–488
Broders KD, Lipps PE, Paul PA, Dorrance AE (2007) Evaluation of Fusarium graminearum associated with corn and soybean seed and seedling disease in Ohio. Plant Dis 91:1155–1160
Bruns TL (2015) The role of Fusarium mycotoxins in seedling infection of soybeans, wheat and maize. Graduate Theses and Dissertations. Paper 14676. http://lib.dr.iastate.edu/etd/14676
Chaudhary J, Patil GB, Sonah H, Deshmukh RK, Vuong TD, Valliyodan B, Nguyen HT (2015) Expanding omics resources for improvement of soybean seed composition traits. Front Plant Sci 6:1021. doi: 10.3389/fpls.2015.01021
Choi Y, Sims GE, Murphy S, Miller JR, Chan AP (2012) Predicting the functional effect of amino acid substitutions and indels. PLoS One 7(10):e46688
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Díaz Arias MM, Leandro LF, Munkvold GP (2013) Aggressiveness of Fusarium species and impact of root infection on growth and yield of soybeans. Phytopathology 103:822–832
Ellis ML, Broders KD, Paul PA, Dorrance AE (2011) Infection of soybean seed by Fusarium graminearum and effect of seed treatments on disease under controlled conditions. Plant Dis 95:401–407
Ellis ML, Wang HH, Paul PA, St Martin SK, McHale LK, Dorrance AE (2012) Identification of soybean genotypes resistant to Fusarium graminearum and genetic mapping of resistance quantitative trait loci in the cultivar Conrad. Crop Sci 52:2224–2233
Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START 7-gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–1360
Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001
He J, Zhao X, Laroche A, Lu Z-X, Liu H, Li Z (2014) Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5:484
Jiao YQ, Vuong TD, Liu Y, Li ZL, Noe J, Robbins RT, Joshi T, Xu D, Shannon JG, Nguyen HT (2015) Identification of quantitative trait loci underlying resistance to southern root-knot and reniform nematodes in soybean accession PI 567516C. Mol Breed 35:131–141
Jun TH, Mian MAR, Kang ST, Michel AP (2012a) Genetic mapping of the powdery mildew resistance gene in soybean PI 567301B. Theor Appl Genet 125:1159–1168
Jun TH, Mian MAR, Michel AP (2012b) Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theor Appl Genet 124:13–22
Kadam S, Vuong TD, Qiu D, Meinhardt CG, Song L, Deshmukh R, Patil G, Wan J, Valliyodan B, Scaboo AM (2015) Genomic-assisted phylogenetic analysis and marker development for next generation soybean cyst nematode resistance breeding. Plant Sci 242:342–350. doi:10.1016/j.plantsci.2015.08.015
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363
Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103
Minor HC, Wiebold W (1998) Wheat-soybean double-crop management in Missouri. University of Missouri Extension. http://extension.missouri.edu/
Niblack TL, Lambert KN, Tylka GL (2006) A model plant pathogen from the kingdom Animalia: Heterodera glycines, the soybean cyst nematode. Annu Rev Phytopathol 44:283–303
Park YJ, Lee HJ, Kwak KJ, Lee K, Hong SW, Kang H (2014) MicroRNA400-guided cleavage of pentatricopeptide repeat protein mRNAs renders Arabidopsis thaliana more susceptible to pathogenic bacteria and fungi. Plant Cell Physiol 55:1660–1668
Patil G, Do T, Vuong TD, Valliyodan B, Lee JD, Chaudhary J, Shannon JG, Nguyen HT (2016) Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean. Sci Rep-Uk 6:19199
Pestka JJ (2010) Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch Toxicol 84:663–679
Pioli RN, Mozzoni L, Morandi EN (2004) First report of pathogenic association between Fusarium graminearum and soybean. Plant Dis 88:220–220
Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R, Kuchler K, Glössl J, Luschnig C, Adam G (2003) Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J Biol Chem 278:47905–47914
Pumphrey MO, Bernardo R, Anderson JA (2007) Validating the Fhb1 QTL for Fusarium head blight resistance in near-isogenic wheat lines developed from breeding populations. Crop Sci 47:200–206
Qi X, Li MW, Xie M et al (2014) Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Commun 5:4340
Rawat N, Pumphrey MO, Liu S, Zhang X, Tiwari VK, Ando K, Trick HN, Bockus WW, Akhunov E, Anderson JA, Gill BS (2016) Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nat Genet 12:1576–1580
Schapire AL, Valpuesta V, Botella MA (2006) TPR proteins in plant hormone signaling. Plant Signal Behav 1:229–230
Schweiger W, Steiner B, Ametz C, Siegwart G, Wiesenberger G, Berthiller F, Lemmens M, Jia H, Adam G, Muehlbauer GJ, Kreil DP, Buerstmayr H (2013) Transcriptomic characterization of two major Fusarium resistance quantitative trait loci (QTLs), Fhb1 and Qfhs.ifa-5A, identifies novel candidate genes. Mol Plant Pathol 14:772–785
Sekhwal MK, Li PC, Lam I, Wang XE, Cloutier S, You FM (2015) Disease resistance gene analogs (RGAs) in plants. Int J Mol Sci 16:19248–19290
Sella L, Gazzetti K, Castiglioni C, Schafer W, Favaron F (2014) Fusarium graminearum possesses virulence factors common to Fusarium head blight of wheat and seedling rot of soybean but differing in their impact on disease severity. Phytopathology 104:1201–1207
Semagn K, Babu R, Hearne S, Olsen M (2014) Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Mol Breed 33:1–14
St Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48:247–268
Stasko A, Wickramasinghe D, Nauth B, Acharya B, Ellis M, Taylor C, McHale L, Dorrance A (2016) High density mapping of resistance QTL towards Phytophthora sojae, Pythium irregulare, and Fusarium graminearum in the same soybean population. Crop Sci 56:1–17
Valliyodan B, Dan Q, Patil G, Zeng P, Huang J, Dai L, Chen C, Li Y, Joshi T, Song L, Vuong TD, Musket TA, Xu D, Shannon JG, Shifeng C, Liu X, Nguyen HT (2016) Landscape of genomic diversity and trait discovery in soybean. Sci Rep-Uk 6:23598
Van Ooijen JW (2004) MapQTL ® 5, Software for the mapping of quantitative trait loci in experimental populations Kyazma B. V. Wageningen, Netherlands
Van Ooigen JW (2006) JoinMap 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma B. V. Wageningen, Netherlands
Vuong TD, Sleper DA, Shannon JG, Nguyen HT (2010) Novel quantitative trait loci for broad-based resistance to soybean cyst nematode (Heterodera glycines Ichinohe) in soybean PI 567516C. Theor Appl Genet 121:1253–1266
Xue AG, Cober E, Voldeng HD, Babcock C, Clear RM (2007) Evaluation of the pathogenicity of Fusarium graminearum and Fusarium pseudograminearum on soybean seedlings under controlled conditions. Can J Plant Pathol 29:35–40
Yuan J, Wen Z, Gu C, Wang D (2014) Introduction of high throughput and cost effective SNP genotyping platforms in soybean. Plant Genet Genomics. Biotech 2(1):90–94
Acknowledgements
We thank Dr. H. Ye, D. J. Veney, M. Eyre, and L. Weber for technical assistance and T. Musket for editing of the manuscript. Funding for this project was provided by the United Soybean Board, the National Center for Soybean Biotechnology (University of Missouri), the Ohio Soybean Council, and the Ohio State University Center for Applied Plant Sciences. Salaries and research support for this project was provided by State and Federal Funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University and the National Institute of Food and Agriculture, U.S. Department of Agriculture, and Hatch project Development of Disease Management Strategies for Soybean Pathogens in Ohio OHO01303.
Additional support was provided by the Ohio State University Center for Applied Plant Sciences as part of the Soybean Resistance Team project.
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Communicated by Volker Hahn.
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122_2017_2866_MOESM1_ESM.docx
Supplementary Figure S1. QTL-based haplotype clustering of target QTL region in 106 WGRS lines. Base position identical to reference (Williams 82) are light sky blue, black – different. Gene id below the haplotype showing approximate position of candidate genes. Four haplotype groups (HG-I–IV) were identified and highlighted. Approximate position of underlying genes is shown at bottom and three putative candidate highlighted in red text. (DOCX 315 KB)
122_2017_2866_MOESM2_ESM.xlsx
Supplementary Table S1. A. Identification of sequence variants in three candidate genes in 106 WGRS lines. The syn and non_syn SNPs are mentioned above SNP position. B. Prediction of amino acid change on protein function. (XLSX 39 KB)
122_2017_2866_MOESM3_ESM.docx
Supplementary Table S2. Letters A, B, and C represent independent experiments that each contain 3 replications completed at different times. The means of each category is the mean of all 3 replicates within each experiment. (DOCX 15 KB)
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Cheng, P., Gedling, C.R., Patil, G. et al. Genetic mapping and haplotype analysis of a locus for quantitative resistance to Fusarium graminearum in soybean accession PI 567516C. Theor Appl Genet 130, 999–1010 (2017). https://doi.org/10.1007/s00122-017-2866-8
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DOI: https://doi.org/10.1007/s00122-017-2866-8