Mapping crown rust resistance at multiple time points in elite oat germplasm.


Journal

The plant genome
ISSN: 1940-3372
Titre abrégé: Plant Genome
Pays: United States
ID NLM: 101273919

Informations de publication

Date de publication:
03 2020
Historique:
received: 15 08 2019
accepted: 22 10 2019
entrez: 5 10 2020
pubmed: 6 10 2020
medline: 10 10 2020
Statut: ppublish

Résumé

Crown rust, caused by Puccinia coronata f. sp. avenae Erikss., is the most important disease impacting cultivated oat (Avena sativa L.). Genetic resistance is the most desirable management strategy. The genetic architecture of crown rust resistance is not fully understood, and previous mapping investigations have mostly ignored temporal variation. A collection of elite oat lines sourced from oat breeding programs in the American Upper Midwest and Canada was genotyped using a high-density genotyping-by-sequencing system and evaluated for crown rust disease severity at multiple time points throughout the growing season in three disease nursery environments. Genome-wide association mapping was conducted for disease severity on each observation date of each trial, area under the disease progress curve for each trial, heading date for each trial, and area under the disease progress curve in a multi-environment model. Crown rust resistance quantitative trait loci (QTL) were detected on linkage groups Mrg05, Mrg12, Mrg15, Mrg18, Mrg20, and Mrg33. None of these QTL were coincident with a days-to-heading QTL detected on Mrg02. Only the QTL detected on Mrg15 was detected in multiple mapping models. The QTL on Mrg05, Mrg12, Mrg18, Mrg20, and Mrg33 were detected on only a single observation date and were not detected on observations just days before and after. This result uncovers the importance of temporal variation in mapping experiments which is usually ignored. It is possible that high density temporal data could be used to more precisely characterize the nature of plant resistance in other systems.

Identifiants

pubmed: 33016637
doi: 10.1002/tpg2.20007
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

e20007

Informations de copyright

© 2020 The Authors. The Plant Genome published by Wiley Periodicals, Inc. on behalf of Crop Science Society of America.

Références

Acevedo, M., Jackson, E. W., Chong, J., Rines, H. W., Harrison, S., & Bonman, J. M. (2010). Identification and validation of quantitative trait loci for partial resistance to crown rust in oat. Phytopathology, 100, 511-521. https://doi.org/10.1094/PHYTO-100-5-0511
Admassu-Yimer, B., Bonman, J. M., & Klos, K. E. (2018). Mapping of crown rust resistance gene Pc53 in oat (Avena sativa). PLOS ONE, 13, e0209105. https://doi.org/10.1371/journal.pone.0209105
Admassu-Yimer, B., Gordon, T., Bonman, J. M., & Esvelt Klos, K. (2019). Development and validation of a quantitative PCR assay method of assessing relative resistance of oat (Avena sativa) to crown rust (Puccinia coronata f. sp. avenae). Plant Pathology, 68, 669-677. https://doi.org/10.1111/ppa.12988
Al-Kherb, S. M., Roelfs, A. P., & Groth, J. V. (1987). Diversity for virulence in a sexually reproducing population of Puccinia coronata. Canadian Journal of Botany, 65, 994-998. https://doi.org/10.1139/b87-137
Arojju, S. A., Conaghan, P., Barth, S., Milbourne, D., Casler, M. D., Hodkinson, T. R., … Byrne, S. L. (2018). Genomic prediction of crown rust resistance in Lolium perenne. BMC Genetics, 19, 35. https://doi.org/10.1186/s12863-018-0613-z
Babiker, E. M., Gordon, T. C., Jackson, E. W., Chao, S., Harrison, S. A., Carson, M. L., … Bonman, J. M. (2015). Quantitative trait loci from two genotypes of oat (Avena sativa) conditioning resistance to Puccinia coronata. Phytopathology, 105, 239-245. https://doi.org/10.1094/PHYTO-04-14-0114-R
Bartos, P., Fleischmann, G., Samborski, D. J., & Shipton, W. A. (1969). Studies on asexual variation in the virulence of oat crown rust, Puccinia coronata f. sp. avenae, and wheat leaf rust, Puccinia recondita. Canadian Journal of Botany, 47, 1383-1387. https://doi.org/10.1139/b69-197
Bekele, W. A., Wight, C. P., Chao, S., Howarth, C. J., & Tinker, N. A. (2018). Haplotype-based genotyping-by-sequencing in oat genome research. Plant Biotechnology Journal, 16, 1452-1463. https://doi.org/10.1111/pbi.12888
Carson, M. L. (2011). Virulences in oat crown rust (Puccinia coronata f. sp. avenae) in the United States from 2006 to 2009. Plant Disease, 95, 1528-1534. https://doi.org/10.1094/PDIS-09-10-0639
Chaffin, A. S., Huang, Y. F., Smith, S., Bekele, W. A., Babiker, E., Gnanesh, B. N., … Tinker, N. A. (2016). A consensus map in cultivated hexaploid oat reveals conserved grass synteny with substantial subgenome rearrangement. Plant Genome, 9, https://doi.org/10.3835/plantgenome2015.10.0102
Chen, J., Upadhyaya, N. M., Ortiz, D., Sperschneider, J., Li, F., Bouton, C., … Dodd, P. N. (2017). Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science, 358, 1607-1610.
Chong, J., Gruenke, J., Dueck, R., Mayert, W., & Woods, S. (2008). Virulence of oat crown rust Puccinia coronata f. sp. avenae in Canada during 2002-2006. Canadian Journal of Plant Pathology, 30, 115-123. https://doi.org/10.1080/07060660809507502
Dehman, A., Ambroise, C., & Neuvial, P. (2015). Performance of a blockwise approach in variable selection using linkage disequilibrium information. BMC Bioinformatics, 16. https://doi.org/10.1186/s12859-015-0556-6
de Mendiburu, F. (2017). Agricolae: Statistical procedures for agricultural research. R package version 1.2-8. Vienna, Austria: R Foundation for Statistical Computing.
Development Core Team, R. (2008). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Diaz-Lago, J. E., Stuthman, D. D., & Abadie, T. E. (2002). Recurrent selection for partial resistance to crown rust in oat. Crop Science, 42, 1475-1482. https://doi.org/10.2135/cropsci2002.1475
Diaz-Lago, J. E., Stuthman, D. D., & Leonard, K. J. (2003). Evaluation of components of partial resistance to oat crown rust using digital image analysis. Plant Disease, 87, 667-674. https://doi.org/10.1094/PDIS.2003.87.6.667
Eloarce, Y., Enavas, E., Epaniagua, C., Efominaya, A., Manjon, J. L., & Eferrer, E. (2016). Identification of genes in a partially resistant genotype of Avena sativa expressed in response to Puccinia coronata infection. Frontiers in Plant Science, 7. https://doi.org/10.3389/fpls.2016.00731
Endelman, J. B. (2011). Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome Journal, 4, 250-255. https://doi.org/10.3835/plantgenome2011.08.0024
Esvelt Klos, K., Huang, Y., Bekele, W. A., Obert, D. E., Babiker, E., Beattie, A. D., … Tinker, N. A. (2016). Population genomics related to adaptation in elite oat germplasm. Plant Genome, 9. https://doi.org/10.3835/plantgenome2015.10.0103
Esvelt Klos, K., Yimer, B. A., Babiker, E. M., Beattie, A. D., Bonman, J. M., Carson, M. L., … Tinker, N. A. (2017). Genome-wide association mapping of crown rust resistance in oat elite germplasm. Plant Genome, 10. https://doi.org/10.3835/plantgenome2016.10.0107
Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
Falcon, C., Horsley, R., Hu, G., Blake, T., & Smith, K. P. (2018). Mapping QTLs for grain protein concentration and agronomic traits under different nitrogen levels in barley. Crop Science, 59, 68-83. https://doi.org/10.2135/cropsci2018.03.0208
Groth, J. V., & Roelfs, A. P. (1982). The effect of sexual and asexual reproduction on race abundance in cereal rust fungus populations. Phytopathology, 72, 1503-1507. https://doi.org/10.1094/Phyto-72-1503
Hoffman, D. L., Chong, J., Jackson, E. W., & Obert, D. E. (2006). Characterization and mapping of a crown rust resistance gene complex (Pc58) in TAM O-301. Crop Science, 46, 2630-2635. https://doi.org/10.2135/cropsci2006.01.0014
Jamann, T. M., Luo, X., Morales, L., Kolkman, J. M., Chung, C. L., & Nelson, R. J. (2015). A remorin gene is implicated in quantitative disease resistance in maize. Theoretical and Applied Genetics, 129, 591-602. https://doi.org/10.1007/s00122-015-2650-6
Jamil, M., Ali, A., Gul, A., Ghafoor, A., Ibrahim, A. M. H., & Mujeeb-Kazi, A. (2018). Genome-wide association studies for spot blotch (Cochliobolus sativus) resistance in bread wheat using genotyping-by-sequencing. Phytopathology, 108, 1307-1314. https://doi.org/10.1094/PHYTO-02-18-0047-R
Jones, D. G. J., & Dangl, J. L. (2006). The plant immune system. Nature, 444, 323-329. https://doi.org/10.1038/nature05286
Kebede, A. Z., Friesen-Enns, J., Gnanesh, B. N., Menzies, J. G., Mitchell Fetch, J. W., Chong, J., … McCartney, C. A. (2019). Mapping oat crown rust resistance gene Pc45 confirms association with PcKM. G3: GENES, GENOMES, GENETICS, 9, 505-511.
Kochman, J. K., & Brown, J. F. (1976a). Host and environmental effects on the prepenetration of oats by Puccinia graminis avenae and Puccinia coronata avenae. Annals of Applied Biology, 82, 251-258. https://doi.org/10.1111/j.1744-7348.1976.tb00560.x
Kochman, J. K., & Brown, J. F. (1976b). Host and environmental effects on the penetration of oats by Puccinia graminis avenae and Puccinia coronata avenae. Annals of Applied Biology, 82, 241-249. https://doi.org/10.1111/j.1744-7348.1976.tb00559.x
Kochman, J. K., & Brown, J. F. (1975). Host and environmental effects on the post-penetration of oats by Puccinia graminis avenae and Puccinia coronata avenae. Annals of Applied Biology, 81, 33-41. https://doi.org/10.1111/j.1744-7348.1975.tb00492.x
Leonard, K. J. (2002). Oat lines with effective adult plant resistance to crown rust. Plant Disease, 86, 593-598. https://doi.org/10.1094/PDIS.2002.86.6.593
Li, J., & Ji, L. (2005). Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity, 95, 221-227. https://doi.org/10.1038/sj.hdy.6800717
Lin, Y., Gnanesh, B. N., Chong, J., Chen, G., Beattie, A. D., Mitchell Fetch, J. W., … McCartney, C. A. (2014). A major quantitative trait locus conferring adult plant partial resistance to crown rust in oat. BMC Plant Biology, 14, 250. https://doi.org/10.1186/s12870-014-0250-2
Luke, H. H., Barnett, R. D., & Pfahler, P. L. (1984). Postpenetration development of Puccinia coronata avenae in slow- and fast-rusting cultivars of Avena byzantina. Phytopathology, 74, 899-903. https://doi.org/10.1094/Phyto-74-899
Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., & Hornik, K. (2019). Cluster: Cluster analysis basics and extensions. R package version 2.0.8. Vienna, Austria: R Foundation for Statistical Computing.
Massman, J., Cooper, B., Horsley, R., Neate, S., Dill-Macky, R., Chao, S., … Smith, K. P. (2011). Genome-wide association mapping of fusarium head blight resistance in contemporary barley breeding germplasm. Molecular Breeding, 27, 439-454. https://doi.org/10.1007/s11032-010-9442-0
May, W. E., Ames, N., Irvine, R. B., Kutcher, H. R., Lafond, G. P., & Shirtliffe, S. J. (2014). Are fungicide applications to control crown rust of oat beneficial? Canadian Journal of Plant Science, 94, 911-922. https://doi.org/10.4141/cjps2013-333
McCallum, B. D., Fetch, T., & Chong, J. (2007). Cereal rust control in Canada. Australian Journal of Agricultural Research, 58, 639-647. https://doi.org/10.1071/AR06145
McCartney, C. A., Stonehouse, R. G., Rossnagel, B. G., Eckstein, P. E., Scoles, G. L., Zatorski, T., … Chong, J. (2011). Mapping of the oat crown rust resistance gene Pc91. Theoretical and Applied Genetics, 122, 317-325. https://doi.org/10.1007/s00122-010-1448-9
Montilla-Bascón, G., Rispail, N., Sanchez-Martin, J., Rubiales, D., Mur, L. A. J., Langdon, T., … Prats, E. (2015). Genome-wide association study for crown rust (Puccinia coronata f. sp. avenae) and powdery mildew (Blumeria graminis f. sp. avenae) resistance in an oat (Avena sativa) collection of commercial varieties and landraces. Frontiers in Plant Science, 6. https://doi.org/10.3389/fpls.2015.00103
Nazareno, E. S., Li, F., Smith, M., Park, R. F., Kianian, S., & Figueroa, M. (2018). Puccinia coronata f. sp. avenae: A threat to global oat production. Molecular Plant Pathology, 19, 1047-1060. https://doi.org/10.1111/mpp.12608
Paradis, E. (2010). pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419-420. https://doi.org/10.1093/bioinformatics/btp696
Parlevliet, J. E. (1978). Further evidence of polygenic inheritance of partial resistance in barley to leaf rust, Puccinia hordei. Euphytica, 27, 369-379. https://doi.org/10.1007/BF00043161
Peterson, R. F., Campbell, A. B., & Hannah, A. E. (1948). A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Canadian Journal of Research, 26c, 496-500. https://doi.org/10.1139/cjr48c-033
Portyanko, V. A., Chen, G., Rines, H. W., Phillips, R. L., Leonard, K. J., Ochocki, G. E., & Stuthman, D. D. (2005). Quantitative trait loci for partial resistance to crown rust, Puccinia coronata, in cultivated oat, Avena sativa L. Theoretical and Applied Genetics, 111, 313-324. https://doi.org/10.1007/s00122-005-2024-6
Rines, H. W., Miller, M. E., Carson, M., Chao, S., Tiede, T., Wiersma, J., & Kianian, S. F. (2018). Identification, introgression, and molecular marker genetic analysis and selection of a highly effective novel oat crown rust resistance from diploid oat, Avena strigosa. Theoretical and Applied Genetics, 131, 721-733. https://doi.org/10.1007/s00122-017-3031-0
Saintenac, C., Jiang, D., Wang, S., & Akhu, E. (2013). Sequence-based mapping of the polyploid wheat genome. G3: GENES, GENOMES, GENETICS, 3, 1105-1114. https://doi.org/10.1534/g3.113.005819
Simons, M. D. (1985). Crown rust. In A. P. Roelfs & W. R. Bushnell (Eds.), The cereal rusts (pp. 131-172). New York: Academic Press.
Simons, M. D., Youngs, V. L., Booth, G. D., & Forsberg, R. A. (1979). Effect of crown rust on protein and groat percentages of oat grain. Crop Science, 19, 703-706. https://doi.org/10.2135/cropsci1979.0011183X001900050039x
Sunstrum, F. G., Bekele, W. A., Wight, C. P., Yan, W., Chen, Y., & Tinker, N. A. (2019). A genetic linkage map in southern-by-spring oat identifies multiple quantitative trait loci for adaptation and rust resistance. Plant Breeding, 138, 82-94.
Tibshirani, R., Walther, G., & Hastie, T. (2001). Estimating the number of clusters in a data set via the gap statistic. Journal of the Royal Statistical Society: Series B (Statistical Methodology), 63(2), 411-423. https://doi.org/10.1111/1467-9868.00293
Tinker, N. A., Bekele, W. A., & Hatori, J. (2016). Haplotag: Software for haplotype-based genotyping-by-sequencing analysis. G3: GENES, GENOMES, GENETICS, 6, 857-863.
Tinker, N. A., Jackson, E. W., Snyder, S., Tiede, T., Azar, C., Babiker, E., … Zwer, P. (2016). Achievements and impact of the Collaborative Oat Research Enterprise. Oat Newsletter, 53(18).
USDA Crop Reporting Board. (1975). Acreage 1975. USDA Statistical Reporting Office, Washington, DC. Retrieved from http://bit.ly/2ZTFgOv
USDA Crop Reporting Board. (2017). Acreage 2017. USDA Statistical Reporting Office, Washington, DC. Retrieved from http://bit.ly/2JaNewN
USDA-ARS Cereal Disease Laboratory. (2016). Small grain losses due to rust. USDA Agricultural Research Service, Cereal Disease Laboratory, St. Paul, MN. Retrieved from http://bit.ly/2PHtHFy
Wamishe, Y. A., Thompson, K. C., & Milus, E. A. (2004). A computer program to improve the efficiency and accuracy of postulating race-specific resistance genes. Plant Disease, 88, 545-549. https://doi.org/10.1094/PDIS.2004.88.5.545
Wight, C. P., O'Donoughue, L. S., Chong, J., Tinker, N. A., & Molnar, S. J. (2004). Discovery, localization, and sequence characterization of molecular markers for the crown rust resistance genes Pc38, Pc39, and Pc48 in cultivated oat (Avena sativa L.). Molecular Breeding, 14, 349-361. https://doi.org/10.1007/s11032-004-0148-z
Winkler, L. R., Bonman, J. M., Chao, S., Yimer, B. A., Bockelman, H., & Esvelt Klos, K. (2016). Population structure and genotype-phenotype associations in a collection of oat landraces and historic cultivars. Frontiers in Plant Science, 7, 1077. https://doi.org/10.3389/fpls.2016.01077
Wolfe, M. D., Rabbi, I. Y., Egesi, C., Hamblin, M., Kawuki, R., Kulakow, P., … Jannink, J. (2016). Genome-wide association and prediction reveals genetic architecture of cassava mosaic disease resistance and prospects for rapid genetic improvement. Plant Genome, 9. https://doi.org/10.3835/plantgenome2015.11.0118
Zadoks, J. C., Chang, T. T., & Konzak, F. C. (1974). A decimal code for the growth stages of cereals. Weed Research, 14, 415-421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
Zegeye, H., Rasheed, A., Makdis, F., Badebo, A., & Ogbonnaya, F. C. (2014). Genome-wide association mapping for seedling and adult plant resistance to stripe rust in synthetic hexaploid wheat. PLOS ONE, 9, e105593. https://doi.org/10.1371/journal.pone.0105593
Zhao, K., Aranzana, M. J., Kim, S., Lister, C., Shindo, C., Tang, C., … Nordborg, M. (2007). An Arabidopsis example of association mapping in structured samples. PLoS Genetics, 3, e4. https://doi.org/10.1371/journal.pgen.0030004

Auteurs

Ian G McNish (IG)

Dep. of Agronomy and Plant Genetics, Univ. of Minnesota, 1991 Upper Buford Circle, 411 Borlaug Hall, St. Paul, MN, 55108.

Cristiano M Zimmer (CM)

Dep. of Crop Science, Federal Univ. of Rio Grande do Sul, Porto Alegre, RS, Brazil.

Alexander Q Susko (AQ)

Dep. of Agronomy and Plant Genetics, Univ. of Minnesota, 1991 Upper Buford Circle, 411 Borlaug Hall, St. Paul, MN, 55108.

D Jo Heuschele (DJ)

Dep. of Agronomy and Plant Genetics, Univ. of Minnesota, 1991 Upper Buford Circle, 411 Borlaug Hall, St. Paul, MN, 55108.

Tyler Tiede (T)

Pepsico, Rhinelander, WI, 54501.

Austin J Case (AJ)

Anheuser-Busch, Fort Collins, CO, 80524.

Kevin P Smith (KP)

Dep. of Agronomy and Plant Genetics, Univ. of Minnesota, 1991 Upper Buford Circle, 411 Borlaug Hall, St. Paul, MN, 55108.

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