Abstract
Key message
The candidate genes involved in resistance to Fusarium equiseti in soybean PI 437654 were identified through comparative genomic analyses of mutants via whole genome re-sequencing.
Abstract
The fungus Fusarium infects each stage of the growth and development of soybean and causes soybean (Glycine max (L.)) seed and root rot and seedling damping-off and wilt with a large quantity of annual yield loss worldwide. It is very important to identify the resistant genes in soybean to prevent and control this pathogen. One Fusarium equiseti isolate was previously identified to be incompatible with ‘PI 437654’ but compatible with a Chinese soybean cultivar ‘Zhonghuang 13’. In this study, with the infection of this isolate on the seedling roots of developed PI 437654 mutants, 6 mutants were identified from 500 mutants to significantly alter their phenotypes to F. equiseti compared to wild-type PI 437654. Then, two identified segregating mutants were selected to directly perform whole genome re-sequencing. Finally, through comparative genomic analyses 7 genes including one cluster of 4 nucleotide binding site-leucine-rich repeat genes on one genomic region of chromosome 7, a 60S ribosomal protein L12 gene and 2 uncharacterized genes were identified to be likely involved in the resistance to F. equiseti. These genes will facilitate the breeding of resistant germplasm resources and the identification of resistance of soybean to Fusarium spp.
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Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178
Acharya B, Lee S, Rouf Mian MA, 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
Afzal AJ, Srour A, Saini N, Hemmati N, El Shemy HA, Lightfoot DA (2012) Recombination suppression at the dominant Rhg1/Rfs2 locus underlying soybean resistance to the cyst nematode. Theor Appl Genet 124:1027–1039
Afzal AJ, Srour A, Goil A, Vasudaven S, Liu T, Samudrala R, Dogra N, Kohli P, Malakar A, Lightfoot DA (2013) Homo-dimerization and ligand binding by the leucine-rich repeat domain at RHG1/RFS2 underlying resistance to two soybean pathogens. BMC Plant Biol 13:43
Anderson J, Akond M, Kassem MA, Meksem K, Kantartzi SK (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(2):203–210
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
Bai GH, Plattner R, Desjardins A, Kolb F, McIntosh RA (2001) Resistance to Fusarium head blight and deoxynivalenol accumulation in wheat. Plant Breed 120:1–6
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
Brar HK, Swaminathan S, Bhattacharyya MK (2011) The Fusarium virguliforme toxin FvTox1 causes foliar sudden death syndrome-like symptoms in soybean. Mol Plant Microb Interact 24:1179–1188
Brito N, Espino JJ, González C (2006) The endo-beta-1,4-xylanase xyn11A is required for virulence in Botrytis cinerea. Mol Plant Microb Interact 19:25–32
Chang SJC, Doubler TW, Kilo V, Suttner R, Klein J, Schmidt ME, Gibson PT, Lightfoot DA (1996) Two additional loci underlying durable field resistance to soybean sudden death syndrome (SDS). Crop Sci 36:1684–1688
Chang C, Tian L, Ma L, Li W, Nasir F, Li X, Tran LP, Tian C (2018) Differential responses of molecular mechanisms and physiochemical characters in wild and cultivated soybeans against invasion by the pathogenic Fusarium oxysporum Schltdl. Physiol Plant. https://doi.org/10.1111/ppl.12870
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890
Cheng P, Gedling CR, Patil G, Vuong TD, Shannon JG, Dorrance AE, Nguyen HT (2017) 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
Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Xu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80–92
Cooper RM, Longman D, Campbell A, Henry M, Lees PE (1998) Enzymic adaptation of cereal pathogens to the monocotyledonous primary wall. Physiol Mol Plant Pathol 32:33–47
de Farias Neto AL, Hashmi R, Schmidt M, Carlson SR, Hartman GL, Li S, Nelson RL, Diers BW (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
Ge FY, Zheng N, Zhang LP, Huang WK, Peng DL, Liu SM (2018) Chemical mutagenesis and soybean mutants potential for identification of novel genes conferring resistance to soybean cyst nematode. J Integr Agric 17:2734–2744
Iqbal MJ, Meksem K, Njiti VN, Kassem MA, Lightfoot DA (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
Islam KT, Bond JP, Fakhoury AM (2017) FvSTR1, a striatin orthologue in Fusarium virguliforme, is required for asexual development and virulence. Appl Microbiol Biotechnol 101:6431–6445
Jayasinghe CK, Wijayaratne SC, Fernando TH (2004) Characterization of cell wall degrading enzymes of Thanatephorus cucumeris. Mycopathologia 157:73–79
Kassem MA, Shultz J, Meksem K, Cho Y, Wood AJ, Iqbal MJ, Lightfoot DA (2006) An updated ‘Essex’ by ‘Forrest’ linkage map and first composite interval map of QTL underlying six soybean traits. Theor Appl Genet 113:1015–1026
Kassem MA, 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
Kassem MA, Ramos L, Leandro L, Mbofung G, Hyten DL, Kantartzi SK, Grier RL, Njiti VN, Cianzio S, Meksem K (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
Kazi S, Shultz J, Afzal J, Johnson J, Njiti VN, Lightfoot DA (2008) Separate loci underlie resistance to root infection and leaf scorch during soybean sudden death syndrome. Theor Appl Genet 116:967–977
Lanubile A, Muppirala UK, Severin AJ, Marocco A, Munkvold GP (2015) Transcriptome profiling of soybean (Glycine max) roots challenged with pathogenic and non-pathogenic isolates of Fusarium oxysporum. BMC Genom 16:1089
Li H, Durbin R (2010) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map (SAM) format and SAMtools. Bioinformatics 25:2078–2079
Liu S, Kandoth PK, Lakhssassi N, Kang J, Colantonio V, Heinz R, Yechel G, Zhou Z, Bekal S, Dapprich J, Rotter B, Cianzio S, Mitchum MG, Meksem K (2017) The soybean GmSNAP18 gene underlies two types of resistance to soybean cyst nematode. Nat Commun 8:14822
Luckew AS, Leandro LF, Bhattacharyya MK, Nordman DJ, Lightfoot DA, Cianzio SR (2013) Usefulness of 10 genomic regions in soybean associated with sudden death syndrome resistance. Theor Appl Genet 126:2391–2403
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
Meksem K, Doubler TW, Chancharoenchai K, Njiti VN, Chang SJC, Rao-Arelli AP, Cregan PE, Gray LE, Gibson PT, Lightfoot DA (1999) Clustering among loci underlying soybean resistance to Fusarium solani, SDS and SCN in near-isogenic lines. Theor Appl Genet 99:1131–1142
Mueller DS, Hartman GL, Nelson RL, Pedersen WL (2002) Evaluation of Glycine max germ plasm for resistance to Fusarium solani f. sp. glycines. Plant Dis 86:741–746
Ngaki MN, Wang B, Sahu BB, Srivastava SK, Farooqi MS, Kambakam S, Swaminathan S, Bhattacharyya MK (2016) Tanscriptomic study of the soybean-Fusarium virguliforme interaction revealed a novel ankyrin-repeat containing defense gene, expression of whose during infection led to enhanced resistance to the fungal pathogen in transgenic soybean plants. PLoS ONE 11:e0163106
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
Njiti VN, Doubler TW, Suttner RJ, Gray LE, Gibson PT, Lightfoot DA (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, Meksem K, Iqbal MJ, Johnson JE, Kassem MA, Zobrist KF, Kilo VY, Lightfoot DA (2002) Common loci underlie field resistance to soybean sudden death syndrome in Forrest, Pyramid, Essex, and Douglas. Theor Appl Genet 104:294–300
Nomura T, Mochizuki R, Dabbs ER, Shimizu Y, Ueda T, Hachinori A (2003) A point mutation in ribosomal protein L7/L12 reduces its ability to form a compact dimer structure and to assemble into the GTPase center. Biochemistry 42:4691–4698
Paccanaro MC, Sella L, Castiglioni C, Giacomello F, Martínez-Rocha AL, D’Ovidio R, Schäfer W, Favaron F (2017) Synergistic effect of different plant cell wall-degrading enzymes is important for virulence of Fusarium graminearum. Mol Plant Microbe Interact 30:886–895
Petrov AN, Meskauskas A, Roshwalb SC, Dinman JD (2008) Yeast ribosomal protein L10 helps coordinate tRNA movement through the large subunit. Nucleic Acid Res 36:6187–6198
Pottorff M, Wanamaker S, Ma YQ, Ehlers JD, Roberts PA, Close TJ (2012) Genetic and physical mapping of candidate genes for resistance to Fusarium oxysporum f. sp. tracheiphilum race 3 in cowpea [Vigna unguiculata (L.) Walp]. PLoS ONE 7:e41600
Prabhu RR, Njiti VN, Johnson JE, Schmidt ME, Klein RJ, Lightfoot DA (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, Leandro LF, Bhattacharyya MK (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
Rosado A, Sohn EJ, Drakakaki G, Pan S, Swidergal A, Xiong Y, Kang BH, Bressan RA, Raikhel NV (2010) Auxin-mediated ribosomal biogenesis regulates vacuolar trafficking in Arabidopsis. Plant Cell 22:143–158
Roy KW (1997) Fusarium solani on soybean roots: nomenclature of the causal agent of sudden death syndrome and identity and relevance of F. solani form B. Plant Dis 81:259–266
Srivastava SK, Huang X, Brar HK, Fakhoury AM, Bluhm BH, Bhattacharyya MK (2014) The genome sequence of the fungal pathogen Fusarium virguliforme that causes sudden death syndrome in soybean. PLoS ONE 9:e81832
Srour A, Afzal AJ, Blahut-Beatty L, Hemmati N, Simmonds DH, Li W, Liu M, Town CD, Sharma H, Arelli P, Lightfoot DA (2012) The receptor like kinase at Rhg1-a/Rfs2 caused pleiotropic resistance to sudden death syndrome and soybean cyst nematode as a transgene by altering signaling responses. BMC Genom 13:368
Swaminathan S, Abeysekara NS, Liu M, Cianzio SR, Bhattacharyya MK (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
Swaminathan S, Abeysekara NS, Knight JM, Liu M, Dong J, Hudson ME, Bhattacharyya MK, Cianzio SR (2018) Mapping of new quantitative trait loci for sudden death syndrome and soybean cyst nematode resistance in two soybean populations. Theor Appl Genet 131:1047–1062
Swaminathan S, Das A, Assefa T, Knight JM, Da Silva AF, Carvalho JPS, Hartman GL, Huang X, Leandro LF, Cianzio SR, Bhattacharyya MK (2019) Genome wide association study identifies novel single nucleotide polymorphic loci and candidate genes involved in soybean sudden death syndrome resistance. PLoS ONE 14:e0212071
Tai LM, Xu YL, Yan FY (2006) Effects of Fusarium oxysporium toxin on the ultrastructure of soybean radicle tissue. Act Phytopathol Sin 36:512–516
Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183
Takagi H, Tamiru M, Abe A, Yoshida K, Uemura A, Yaegashi H, Obara T, Oikawa K, Utsushi H, Kanzaki E, Mitsuoka C, Natsume S, Kosugi S, Kanzaki H, Matsumura H, Urasaki N, Kamoun S, Terauchi R (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nat Biotechnol 33:445–449
Tan R, Serven B, Collins PJ, Zhang Z, Wen Z, Boyse JF, Gu C, Chilvers MI, Diers BW, Wang D (2018) QTL mapping and epistatic interaction analysis of field resistance to sudden death syndrome (Fusarium virguliforme) in soybean. Theor Appl Genet 131:1729–1740
Tan R, Collins PJ, Wang J, Wen Z, Boyse JF, Laurenz RG, Gu C, Jacobs JL, Song Q, Chilvers MI, Wang D (2019) Different loci associated with root and foliar resistance to sudden death syndrome (Fusarium virguliforme) in soybean. Theor Appl Genet 132:501–513
Triwitayakorn K, Njiti VN, Iqbal MJ, Yaegashi S, Town C, Lightfoot DA (2005) Genomic analysis of a region encompassing QRfs1 and QRfs2: genes that underlie soybean resistance to sudden death syndrome. Genome 48:125–138
Wang B, Swaminathan S, Bhattacharyya MK (2015) Identification of Fusarium virguliforme FvTox1-interacting synthetic peptides for enhancing foliar sudden death syndrome resistance in soybean. PLoS ONE 10:e0145156
Wen Z, Tan R, Yuan J, Bales C, Du W, Zhang S, Chilvers MI, Schmidt C, Song Q, Cregan PB, Wang D (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genom 15:809
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
Zhang C, Zhao X, Qu Y, Teng W, Qiu L, Zheng H, Wang Z, Han Y, Li W (2019) Loci and candidate genes in soybean that confer resistance to Fusarium graminearum. Theor Appl Genet 132:431–441
Zheng N, Zheng N, Zhang LP, Ge FY, Huang WK, Kong LA, Peng DL, Liu SM (2018) Conidia of one Fusarium solani isolate from a soybean-production field enable to be virulent to soybean and make soybean seedlings wilted. J Integr Agric 17:2042–2053
Acknowledgements
This work was financially supported by the Innovation Program and Youth Elite Program of Chinese Academy of Agricultural Sciences and the Special Fund for Agro-scientific Research in the Public Interest of China (201503114). We thank the staff at OE Biotech, China, for sequencing and analyzing the original sequencing data.
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Zhang, L., Huang, W., Peng, D. et al. Comparative genomic analyses of two segregating mutants reveal seven genes likely involved in resistance to Fusarium equiseti in soybean via whole genome re-sequencing. Theor Appl Genet 132, 2997–3008 (2019). https://doi.org/10.1007/s00122-019-03401-5
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DOI: https://doi.org/10.1007/s00122-019-03401-5