Abstract
Key message
Different loci associated with root resistance to F. virguliforme colonization and foliar resistance to phytotoxin damage in soybean.
Abstract
Use of resistant cultivars is the most efficacious approach to manage soybean sudden death syndrome (SDS), caused by Fusarium virguliforme. The objectives of this study were to (1) map the loci associated with root and foliar resistance to F. virguliforme infection and (2) decipher the relationships between root infection, foliar damage, and plot yield. A mapping population consisting of 153 F4-derived recombinant inbred lines from the cross U01-390489 × E07080 was genotyped by SoySNP6 K BeadChip assay. Both foliar damage and F. virguliforme colonization in roots were investigated in the field, and a weak positive correlation was identified between them. Foliar damage had a stronger negative correlation with plot yield than F. virguliforme colonization. Twelve loci associated with foliar damage were identified, and four of them were associated with multiple traits across environments. In contrast, only one locus associated with root resistance to F. virguliforme colonization was identified and mapped on Chromosome 18. It colocalized with the locus associated with foliar damage in the same environment. The locus on Chromosome 6, qSDS6-2, and the locus on Chromosome 18, qSDS18-1, were associated with resistance to SDS phytotoxins and resistance to F. virguliforme colonization of roots, respectively. Both loci affected plot yield. Foliar damage-related traits, especially disease index, are valuable indicators for SDS resistance breeding because of consistency of the identified loci and their stronger correlation with plot yield. The information provided by this study will facilitate marker-assisted selection to improve SDS resistance in soybean.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdelmajid KM, Meksem K, Wood AJ, Lightfoot DA (2007) Loci underlying SDS and SCN resistance mapped in the “Essex” by “Forrest” soybean recombinant inbred lines. Rev Biol Biotechnol 6:2–10
Abdelmajid KM, Ramos L, Leandro L et al (2012) The “PI 438489B” by “Hamilton” SNP-based genetic linkage map of soybean [Glycine max (L.) Merr.] identified quantitative trait loci that underlie seedling SDS resistance. J Plant Genome Sci 1:18–30. https://doi.org/10.5147/jpgs.2012.0053
Ahn SJ, Costa J, Emanuel JR (1996) PicoGreen quantitation of DNA: effective evaluation of samples pre- or post-PCR. Nucleic Acids Res 24:2623–2625. https://doi.org/10.1093/nar/24.13.2623
Anderson J, Akond M, Kassem MA et al (2015) Quantitative trait loci underlying resistance to sudden death syndrome (SDS) in MD96-5722 by “Spencer” recombinant inbred line population of soybean. 3 Biotech 5:203–210. https://doi.org/10.1007/s13205-014-0211-3
Aoki T, O’donnell K, Homma Y, Lattanzi AR (2003) Sudden-death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex—F.virguliforme in North America and F.tucumaniae in South America. Mycologia 95:660–684. https://doi.org/10.2307/3761942
Bao Y, Kurle JE, Anderson G, Young ND (2015) Association mapping and genomic prediction for resistance to sudden death syndrome in early maturing soybean germplasm. Mol Breed 35:1–14. https://doi.org/10.1007/s11032-015-0324-3
Bhattarai KK, Atamian HS, Kaloshian I et al (2010) WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant J 63:229–240
Brar HK, Bhattacharyya MK (2012) Expression of a single-chain variable-fragment antibody against a Fusarium virguliforme toxin peptide enhances tolerance to sudden death syndrome in transgenic soybean plants. Mol Plant Microbe Interact 25:817–824. https://doi.org/10.1094/MPMI-12-11-0317
Brar HK, Swaminathan S, Bhattacharyya MK (2011) The Fusarium virguliforme toxin FvTox1 causes foliar sudden death syndrome-like symptoms in soybean. Mol Plant Microbe Interact 24:1179–1188. https://doi.org/10.1094/MPMI-12-10-0285
Brzostowski LF, Schapaugh WT, Rzodkiewicz PA et al (2014) Effect of host resistance to Fusarium virguliforme and Heterodera glycines on sudden death syndrome disease severity and soybean yield. Plant Health Prog 15:1–8. https://doi.org/10.1094/PHP-RS-13-0100
Chang SJC, Doubler TW, Kilo V et al (1996) Two additional loci underlying durable field resistance to soybean sudden death syndrome (SDS). Crop Sci 36:1684–1688. https://doi.org/10.2135/cropsci1996.0011183X003600060044x
Chang H-X, Domier LL, Radwan O et al (2016) Identification of multiple phytotoxins produced by Fusarium virguliforme including a phytotoxic effector (FvNIS1) associated with sudden death syndrome foliar symptoms. Mol Plant Microbe Interact 29:96–108. https://doi.org/10.1094/MPMI-09-15-0219-R
Chong SK, Hildebrand KK, Luo Y et al (2005) Mapping soybean sudden death syndrome as related to yield and soil/site properties. Soil Tillage Res 84:101–107. https://doi.org/10.1016/j.still.2004.09.001
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971. https://doi.org/10.1534/genetics.107.080101
De Farias Neto AL, Hashmi R, Schmidt M et al (2007) Mapping and confirmation of a new sudden death syndrome resistance QTL on linkage group D2 from the soybean genotypes PI 567374 and “Ripley”. Mol Breed 20:53–62. https://doi.org/10.1007/s11032-006-9072-8
Falk A, Feys BJ, Frost LN et al (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci 96:3292–3297
Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931. https://doi.org/10.2135/cropsci1971.0011183X001100060051x
Gao X, Jackson TA, Hartman GL, Niblack TL (2006) Interactions between the soybean cyst nematode and Fusarium solani f. sp. glycines based on greenhouse factorial experiments. Phytopathology 96:1409–1415. https://doi.org/10.1094/PHYTO-96-1409
Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:843–846. https://doi.org/10.1093/nar/gkp798
Hartman GL, Chang HX, Leandro LF (2015) Research advances and management of soybean sudden death syndrome. Crop Prot 73:60–66. https://doi.org/10.1016/j.cropro.2015.01.017
Hnetkovsky N, Chang SJC, Doubler TW et al (1996) Genetic mapping of loci underlying field resistance to soybean sudden death syndrome (SDS). Crop Sci 36:393–400. https://doi.org/10.2135/cropsci1996.0011183X003600020030x
Höwing T, Huesmann C, Hoefle C et al (2014) Endoplasmic reticulum KDEL-tailed cysteine endopeptidase 1 of Arabidopsis (AtCEP1) is involved in pathogen defense. Front Plant Sci 5:58
Iqbal MJ, Meksem K, Njiti VN et al (2001) Microsatellite markers identify three additional quantitative trait loci for resistance to soybean sudden-death syndrome (SDS) in Essex × Forrest RILs. Theor Appl Genet 102:187–192. https://doi.org/10.1007/s001220051634
Kandel YR, Haudenshield JS, Srour AY et al (2015) Multilaboratory comparison of quantitative PCR assays for detection and quantification of Fusarium virguliforme from soybean roots and soil. Phytopathology 105:1601–1611. https://doi.org/10.1094/PHYTO-04-15-0096-R
Kazi S, Shultz J, Afzal J et al (2008) Separate loci underlie resistance to root infection and leaf scorch during soybean sudden death syndrome. Theor Appl Genet 116:967–977. https://doi.org/10.1007/s00122-008-0728-0
Kisha TJ, Sneller CH, Diers BW (1997) Relationship between genetic distance among parents and genetic variance in populations of soybean. Crop Sci 37:1317–1325. https://doi.org/10.2135/cropsci1997.0011183X003700040048x
Koenning SR, Wrather JA (2010) Suppression of soybean yield potential in the continental United States by plant diseases from 2006 to 2009. Plant Health Prog. https://doi.org/10.1094/php-2010-122-01-rs
Li D, Sun M, Han Y et al (2010) Identification of QTL underlying soluble pigment content in soybean stems related to resistance to soybean white mold (Sclerotinia sclerotiorum). Euphytica 172:49–57. https://doi.org/10.1007/s10681-009-0036-z
Luckew AS, Leandro LF, Bhattacharyya MK et al (2013) Usefulness of 10 genomic regions in soybean associated with sudden death syndrome resistance. Theor Appl Genet 126:2391–2403. https://doi.org/10.1007/s00122-013-2143-4
Luckew AS, Swaminathan S, Leandro LF et al (2017) “MN1606SP” by “Spencer” filial soybean population reveals novel quantitative trait loci and interactions among loci conditioning SDS resistance. Theor Appl Genet. https://doi.org/10.1007/s00122-017-2947-8
Marburger D, Conley S, Esker P et al (2014) Relationship between Fusarium virguliforme and Heterodera glycines in commercial soybean fields in Wisconsin. Plant Health Prog 15:11–18. https://doi.org/10.1094/PHP-RS-13-0107
Meksem K, Doubler TW, Chancharoenchai K et al (1999) Clustering among loci underlying soybean resistance to Fusarium solani, SDS and SCN in near-isogenic lines. Theor Appl Genet 99:1131–1142. https://doi.org/10.1007/s001220051317
Njiti VN, Doubler TW, Suttner RJ et al (1998) Resistance to soybean sudden death syndrome and root colonization by Fusarium solani f. sp. glycines in near-isogeneic lines. Crop Sci 38:472–477
Njiti VN, Lightfoot DA (2006) Genetic analysis infers Dt loci underlie resistance to Fusarium solani f. sp glycines in indeterminate soybeans. Can J Plant Sci 86:83–90. https://doi.org/10.4141/P05-046
Njiti VN, Meksem K, Iqbal MJ et al (2002) Common loci underlie field resistance to soybean sudden death syndrome in Forrest, Pyramid, Essex, and Douglas. Theor Appl Genet 104:294–300. https://doi.org/10.1007/s001220100682
Nyquist W, Baker R (1991) Estimation of heritability and prediction of selection response in plant populations. Crit Rev Plant Sci 10:235–322
Prabhu RR, Njiti VN et al (1999) Selecting soybean cultivars for dual resistance to soybean cyst nematode and sudden death syndrome using two DNA markers. Crop Sci 39:982–987
Pudake RN, Swaminathan S, Sahu BB et al (2013) Investigation of the Fusarium virguliforme fvtox1 mutants revealed that the FvTox1 toxin is involved in foliar sudden death syndrome development in soybean. Curr Genet 59:107–117. https://doi.org/10.1007/s00294-013-0392-z
Rogovska N, Laird D, Leandro L, Aller D (2017) Biochar effect on severity of soybean root disease caused by Fusarium virguliforme. Plant Soil 413:111–126. https://doi.org/10.1007/s11104-016-3086-8
Roy KW, State M, Rupe JC et al (1997) Sudden death syndrome of soybean. Plant Dis 81:1100–1111
Sanogo S, Yang XB (2001) Relation of sand content, pH, and potassium and phosphorus nutrition to the development of sudden death syndrome in soybean. Can J Plant Pathol 23:174–180. https://doi.org/10.1080/07060660109506927
Scherm H, Yang XB, Lundeen P (1998) Soil variables associated with sudden death syndrome in soybean fields in Iowa. Plant Dis 82:1152–1157. https://doi.org/10.1094/PDIS.1998.82.10.1152
Song QJ, Marek LF, Shoemaker RC et al (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122–128. https://doi.org/10.1007/s00122-004-1602-3
Srour AY, Gibson DJ, Leandro LFS et al (2017) Unraveling microbial and edaphic factors affecting the development of sudden death syndrome in soybean. Phytobiomes 1:91–101. https://doi.org/10.1094/PBIOMES-02-17-0009-R
Swaminathan S, Abeysekara NS, Liu M et al (2016) Quantitative trait loci underlying host responses of soybean to Fusarium virguliforme toxins that cause foliar sudden death syndrome. Theor Appl Genet 129:495–506. https://doi.org/10.1007/s00122-015-2643-5
Takahashi T, Murano T, Ishikawa A (2018) SOBIR1 and AGB1 independently contribute to nonhost resistance to Pyricularia oryzae (syn. Magnaporthe oryzae) in Arabidopsis thaliana. Biosci Biotechnol Biochem 82:1922–1930
Tan R, Serven B, Collins PJ et al (2018) QTL mapping and epistatic interaction analysis of field resistance to sudden death syndrome (Fusarium virguliforme) in soybean. Theor Appl Genet. https://doi.org/10.1007/s00122-018-3110-x
Teng W, Han Y, Du Y et al (2009) QTL analyses of seed weight during the development of soybean (Glycine max L. Merr.). Heredity 102:371–380
Tischner T, Allphin L, Chase K et al (2003) Genetics of seed abortion and reproductive traits in soybean. Crop Sci 43:464–473. https://doi.org/10.2135/cropsci2003.0464
Triwitayakorn K, Njiti VN, Iqbal MJ et al (2005) Genomic analysis of a region encompassing QRfs1 and QRfs2: genes that underlie soybean resistance to sudden death syndrome. Genome 48:125–138. https://doi.org/10.1139/g04-103
Van Ooijen J (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77
Wang S, Basten CJ, Zeng Z-B (2012) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
Wang J, Jacobs JL, Byrne JM, Chilvers MI (2015) Improved diagnoses and quantification of Fusarium virguliforme, causal agent of soybean sudden death syndrome. Phytopathology 105:378–387. https://doi.org/10.1094/PHYTO-06-14-0177-R
Wen Z, Tan R, Yuan J et al (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genom 15:809
Westphal A, Li C, Xing L et al (2014) Contributions of Fusarium virguliforme and Heterodera glycines to the disease complex of sudden death syndrome of soybean. PLoS ONE 9:1–13. https://doi.org/10.1371/journal.pone.0099529
Xing LJ, Westphal A (2006) Interaction of Fusarium solani f. sp. glycines and Heterodera glycines in sudden death syndrome of soybean. Phytopathology 96:763–770. https://doi.org/10.1094/PHYTO-96-0763
Zhang J, Singh A, Mueller DS, Singh AK (2015) Genome-wide association and epistasis studies unravel the genetic architecture of sudden death syndrome resistance in soybean. Plant J 84:1124–1136. https://doi.org/10.1111/tpj.13069
Acknowledgements
This work was supported by North Central Soybean Research Program, Michigan Soybean Promotion Committee, USDA National Institute of Food and Agriculture, Hatch project 1011788 and MSU AgBioResearch. We thank George L. Graef from the Department of Agronomy and Horticulture at the University of Nebraska–Lincoln for providing one of the parental lines, U01-390489. We thank Adam Byrne, Yingdong Bi, Shichen Zhang, Wenyan Du, Jiazheng Yuan, Lihong Li, Wei Xiao, and Zhimin Dong for assistance during the conduction of this research. This study was reviewed by Dr. James Kelly and Dr. Amy Iezzoni from Michigan State University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Ethical standards
This work complies with the current law of the USA.
Additional information
Communicated by Volker Hahn.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tan, R., Collins, P.J., Wang, J. et al. Different loci associated with root and foliar resistance to sudden death syndrome (Fusarium virguliforme) in soybean. Theor Appl Genet 132, 501–513 (2019). https://doi.org/10.1007/s00122-018-3237-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-018-3237-9