Abstract
Key message
The first single dominant resistance gene contributing major resistance to the oomycete pathogen Phytophthora sansomeana was identified and mapped from soybean ‘Colfax’.
Abstract
Phytophthora root rot (PRR) is one of the most important diseases in soybean (Glycine max). PRR is well known to be caused by Phytophthora sojae, but recent studies showed that P. sansomeana also causes extensive root rot of soybean. Depending upon the isolate, it might produce aggressive symptoms, especially in seeds and seedlings. Unlike P. sojae which can be effectively managed by Rps genes, no known major resistance genes have yet been reported for P. sansomeana. Our previous study screened 470 soybean germplasm lines for resistance to P. sansomeana and found that soybean ‘Colfax’ (PI 573008) carries major resistance to the pathogen. In this study, we crossed ‘Colfax’ with a susceptible parent, ‘Senaki’, and developed three mapping populations with a total of 234 F2:3 families. Inheritance pattern analysis indicated a 1:2:1 ratio for resistant: segregating: susceptible lines among all the three populations, indicating a single dominant gene conferring the resistance in ‘Colfax’ (designated as Rpsan1). Linkage analysis using extreme phenotypes anchored Rpsan1 to a 30 Mb region on chromosome 3. By selecting nine polymorphic SNP markers within the region, Rpsan1 was genetically delimited into a 21.3 cM region between Gm03_4487138_A_C and Gm03_5451606_A_C, which corresponds to a 1.06 Mb genomic region containing nine NBS-LRR genes based on Gmax2.0 assembly. The mapping results were then validated using two breeding populations derived from ‘E12076T-03’ × ‘Colfax’ and ‘E16099’ × ‘Colfax’. Marker-assisted resistance spectrum analyses with 9 additional isolates of P. sansomeana indicated that Rpsan1 may be effective towards a broader range of P. sansomeana isolates and has strong merit in protecting soybean to this pathogen in the future.
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The phenotype and genotype data generated in this study is available in ‘Supplementary Data’. Additional information is available upon request.
References
An TJ, Park MS, Jeong JT, Kim YG, Kim YI, Lee ES, Chang JK (2019) Occurrence of the phytophthora blight caused by Phytophthora sansomeana in Atractylodes macrocephala Koidz. Korean J Med Crop Sci 27:404–411
Anderson RG, Deb D, Fedkenheuer K, McDowell JM (2015) Recent progress in RXLR effector research. Mol Plant Microbe Interact 28:1063–1072
Allen TW, Bradley CA, Sisson AJ, Byamukama E, Chilvers MI, Coker CM, Collins AA, Damicone JP, Dorrance AE, Dufault NS, Esker PD (2017) Soybean yield loss estimates due to diseases in the United States and Ontario Canada from 2010 to 2014. Plant Health Progress 18:19–27
Bhattacharyya MK, Narayanan NN, Gao H, Santra DK, Salimath SS, Kasuga T, Liu Y, Espinosa B, Ellison L, Marek L, Shoemaker R, Gijzen M, Buzzell RI (2005) Identification of a large cluster of coiled coil-nucleotide binding site–leucine rich repeat-type genes from the Rps1 region containing Phytophthora resistance genes in soybean. Theor Appl Genet 111:75–86
Bienapfl JC, Malvick DK, Percich JA (2011) Specific molecular detection of Phytophthora sojae using conventional and real-time PCR. Fungal Biol 115:733–740
Cerritos-Garcia DG, Huang SY, Kleczewski NM, Mideros SX (2023) Aggressiveness and fungicide sensitivity of Phytophthora spp associated with soybean in Illinois. Plant Dis 107:1785–1793
Chang KF, Hwang SF, Ahmed HU, Fu H, Zhou Q, Strelkov SE, Turnbull GD (2017) First report of Phytophthora sansomeana causing root rot in field pea in Alberta Canada. Crop Prot 101:1–4
Detranaltes CE, Ma J, Cai G (2022) Phytophthora sansomeana an emerging threat to soybean production. Agronomy 12:1769
Dorrance AE, Jia H, Abney TS (2004) Evaluation of soybean differentials for their interaction with Phytophthora sojae. Plant Health Progr 5:9
Dorrance AE (2018) Management of Phytophthora sojae of soybean: a review and future perspectives. Can J Plant Pathol 40:210–219
Hacker CV, Brasier CM, Buck KW (2005) A double-stranded RNA from a Phytophthora species is related to the plant endornaviruses and contains a putative UDP glycosyltransferase gene. J Gen Virol 86:1561–1570
Hansen EM, Wilcox WF, Reeser PW, Sutton W (2009) Phytophthora rosacearum and P sansomeana new species segregated from the Phytophthora megasperma “complex.” Mycologia 101:129–135
Hebb LM, Bradley CA, Telenko DE, Wise K, Dorrance AE (2023a) Isolates of Phytophthora sansomeana display a range of aggressiveness on soybean seedlings. Plant Health Progr 24:171–179
Hebb L, Poelstra JW, Dorrance AE (2023b) Genome resource announcement for two isolates of Phytophthora sansomeana with varying levels of pathogenicity on soybean. PhytoFrontiers 3:738–743
Lander ESP, Green J, Abrahamson A, Barlow MJ, Daly SE, Lincoln LN (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental populations. Genomics 1:174–181
Lin F, Chhapekar SS, Vieira CC, Da Silva MP, Rojas A, Lee D, Liu N, Pardo EM, Lee YC, Dong Z, Pinheiro JB (2022) Breeding for disease resistance in soybean: a global perspective. Theor Appl Genet 135:3773–3872
Lin F, Li W, McCoy AG, Gao X, Collins PJ, Zhang N, Wen Z, Cao S, Wani SH, Gu C, Chilvers MI (2021) Molecular mapping of quantitative disease resistance loci for soybean partial resistance to Phytophthora sansomeana. Theor Appl Genet 134:1977–1987
Lin F, Zhao M, Ping J, Johnson A, Zhang B, Abney TS, Hughes TJ, Ma J (2013) Molecular mapping of two genes conferring resistance to Phytophthora sojae in a soybean landrace PI 567139B. Theor Appl Genet 126:2177–2185
Malvick DK, Grunden E (2004) Traits of soybean-infecting Phytophthora populations from Illinois agricultural fields. Plant Dis 88:1139–1145
McCoy AG, Byrne AM, Jacobs JL, Anderson G, Kurle JE, Telenko DE, Chilvers MI (2022) Oomicide treated soybean seeds reduce early season stand loss to Phytophthora sojae. Crop Prot 157:105984
McCoy AG, Jacobs JL, Chilvers M (2018) Phytophthora sansomeana host characterization in Michigan field crops. In: International congress of plant pathology (ICPP) plant health in a global economy. APSNET
Michelmore RW, Paran I, Kesseli R (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci 88:9828–9832
Rahman MZ, Uematsu S, Suga H, Kageyama K (2015) Diversity of Phytophthora species newly reported from Japanese horticultural production. Mycoscience 56:443–459
Reeser PW, Scott DH, Ruhl DE (1991) Recovery of race non-classifiable Phytophthora megasperma f sp glycinea from soybean roots in Indiana in 1990. Phytopathology 81:1201
Ribaut JM, Hoisington D (1998) Marker-assisted selection: new tools and strategies. Trends Plant Sci 3:236–239
Rojas JA, Miles TD, Coffey MD, Martin FN, Chilvers MI (2017) Development and application of qPCR and RPA genus-and species-specific detection of Phytophthora sojae and P sansomeana root rot pathogens of soybean. Plant Dis 101:1171–1181
Rojas JA, Witte A, Noel ZA, Jacobs JL, Chilvers MI (2019) Diversity and characterization of oomycetes associated with corn seedlings in Michigan. Phytobiomes J 3:224–234
Safaiefarahani B, Mostowfizadeh-Ghalamfarsa R, Hardy GSJ, Burgess TI (2016) Characterization of Phytophthora pseudocryptogea × P sansomeana associated with sugarbeet root rot in Fars Province. Turk J Agric for 44:6
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW, Nelson RL, Cregan PB (2013) Development and evaluation of SoySNP50K a high-density genotyping array for soybean. PLoS ONE 8:54985
Tande C, Dorrance AE, Schwarzrock D, Mahecha E, Byamukama E (2020) First Report of Phytophthora sansomeana causing root rot of soybean in South Dakota. Plant Dis 104:1877–1877
Tang QH, Gao F, Li GY, Wang H, Zheng XB, Wang YC (2010) First report of root rot caused by Phytophthora sansomeana on soybean in China. Plant Dis 94:378–378
Wang W, Chen L, Fengler K, Bolar J, Llaca V, Wang X, Clark CB, Fleury TJ, Myrvold J, Oneal D, van Dyk MM (2021) A giant NLR gene confers broad-spectrum resistance to Phytophthora sojae in soybean. Nat Commun 12:6263
Zelaya-Molina LX, Ellis ML, Berry SA, Dorrance AE (2010) First report of Phytophthora sansomeana causing wilting and stunting on corn in Ohio. Plant Dis 94:125–125
Acknowledgements
We thank the funding support from Michigan Soybean Committee, USDA National Institute of Food and Agriculture (Hatch project 1011788), AgBioResearch at Michigan State University (Project No. MICL02013), and United Soybean Board (24-209-S-A-1-A and 2331-202-0201). We also thank the Overseas Training Program for Young-Backbone Teachers of Hebei Agricultural University to WL. We are also thankful to the State Scholarship Fund from China Scholarship Council (201908230370) for Zhanguo Zhang.
Funding
United Soybean Board (24-209-S-A-1-A and 2331-202-0201). AgBioResearch at Michigan State University (Project No. MICL02824).
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DW and FL designed the research. FL, MS, ZZ, AGM, WL, RTM, DM, MX, and CG carried out the experiments. FL and MS analyzed the data and developed the draft manuscript. AGM, MIC, and DW edited the manuscript. All authors revised the manuscript and contributed to the final manuscript.
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Lin, F., Salman, M., Zhang, Z. et al. Identification and molecular mapping of a major gene conferring resistance to Phytophthora sansomeana in soybean ‘Colfax’. Theor Appl Genet 137, 55 (2024). https://doi.org/10.1007/s00122-024-04556-6
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DOI: https://doi.org/10.1007/s00122-024-04556-6