Abstract
Key message
Rhynchosporium commune is a globally devastating pathogen of barley. Wild and landrace barley are underutilized, however, contain an abundance of loci that can be used as potential sources of resistance.
Abstract
Rhynchosporium commune, the causal agent of the disease scald or leaf blotch of barley, is a hemibiotrophic fungal pathogen of global importance, responsible for yield losses ranging from 30 to 40% on susceptible varieties. To date, over 150 resistance loci have been characterized in barley. However, due to the suspected location of the R. commune host jump in Europe, European germplasm has been the primary source used to screen for R. commune resistance leaving wild (Hordeum spontaneum) and landrace (H. vulgare) barley populations from the center of origin largely underutilized. A diverse population consisting of 94 wild and 188 barley landraces from Turkey were genotyped using PCR-GBS amplicon sequencing and screened with six Turkish R. commune isolates. The isolates were collected from distinct geographic regions of Turkey with two from the Aegean region, two from central Turkey and two from the Fertile Crescent region. The data set was utilized for association mapping analysis with a total of 21 loci identified, of which 12 were novel, indicating that these diverse primary barley gene pools contain an abundance of novel R. commune resistances that could be utilized for resistance breeding.
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Data availability
Isolates are available upon request. The authors ensure that all data necessary for confirming the conclusions of the article are present within the article, figures, and tables. File SF1 contains phenotyping data. File SF2 contains the mean-squared deviations of each association mapping model tested. Genotyping data, marker positions, population structure and EMMA kinship matrix can be found as File SF1, SF2, SF4, and SF5, respectively, at Figshare: https://doi.org/10.25387/g3.14725311 of Clare et al. (2021).
Change history
23 March 2023
A Correction to this paper has been published: https://doi.org/10.1007/s00122-023-04323-z
References
Abang MM, Baum M, Ceccarelli S et al (2006) Differential Selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 96:1214–1222. https://doi.org/10.1094/PHYTO-96-1214
Abbott DC, Brown AHD, Burdon JJ (1991) Genes for scald resistance from wild barley (Hordeum vulgare ssp. spontaneum) and their linkage to isozyme markers. Euphytica 61:225–231. https://doi.org/10.1007/BF00039662
Avrova A, Knogge W (2012) Rhynchosporium commune: a persistent threat to barley cultivation. Mol Plant Pathol 13:986–997. https://doi.org/10.1111/j.1364-3703.2012.00811.x
Azamparsa MR, Karakaya A (2020) Determination of the pathotypes of Rhynchosporium commune (Zaffarona McDonald & Linde) in some regions of Turkey. Bitk Koruma Bül 60:5–14. https://doi.org/10.15832/ankutbd.441916
Azamparsa MR, Karakaya A, Ergün N et al (2019) Identification of barley landraces and wild barley (Hordeum spontaneum) genotypes resistant to Rhynchosporium commune. Tarım Bilim Derg 25:530–535. https://doi.org/10.15832/ankutbd.441916
Bjørnstad Å, Patil V, Tekauz A et al (2002) Resistance to scald (Rhynchosporium secalis) in barley (Hordeum vulgare) studied by near-isogenic lines: I Markers and differential isolates. Phytopathology 92:710–720. https://doi.org/10.1094/PHYTO.2002.92.7.710
Bradbury PJ, Zhang Z, Kroon DE et al (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Brown JS (1985) Pathogenic variation among isolates of Rhynchosporium secalis from cultivated barley growing in Victoria, Australia. Euphytica 34:129–133. https://doi.org/10.1007/BF00022872
Brueggeman RS, Solanki S, Ameen G et al (2020) Fungal diseases affecting barley. In: Fox G, Li C (eds) Achieving sustainable cultivation of barley. Burleigh Dodds Science Publishing Limited, Cambridge, UK, pp 1–58
Brunner PC, Schürch S, McDonald BA (2007) The origin and colonization history of the barley scald pathogen Rhynchosporium secalis. J Evol Biol 20:1311–1321. https://doi.org/10.1111/j.1420-9101.2007.01347.x
Büttner B, Draba V, Pillen K et al (2020) Identification of QTLs conferring resistance to scald (Rhynchosporium commune) in the barley nested association mapping population HEB-25. BMC Genomics 21:837. https://doi.org/10.1186/s12864-020-07258-7
Çelik Oğuz A, Karakaya A, Ergün N, Sayim İ (2017) Turkish barley landraces resistant to net and spot forms of Pyrenophora teres. Phytopathol Mediterr 56:217–223. https://doi.org/10.14601/Phytopathol_Mediterr-19659
Çelik Oğuz A, Karakaya A, Duran RM, Özbek K (2019) Identification of Hordeum spontaneum genotypes resistant to net blotch disease. Tarım Bilim Derg 25:115–122
Çelik Oğuz A, Ölmez F, Karakaya A, Azamparsa MR (2021) Genetic variation and mating type distribution of Rhynchosporium commune in Turkey. Physiol Mol Plant Pathol 114:101614. https://doi.org/10.1016/j.pmpp.2021.101614
Chełkowski J, Tyrka M, Sobkiewicz A (2003) Resistance genes in barley (Hordeum vulgare L.) and their identification with molecular markers. J Appl Genet 44:291–309
Clare SJ, Wyatt NA, Brueggeman RS, Friesen TL (2020) Research advances in the Pyrenophora teres–barley interaction. Mol Plant Pathol 21:272–288. https://doi.org/10.1111/mpp.12896
Clare SJ, Çelik Oğuz A, Effertz K et al (2021) Genome-wide association mapping of Pyrenophora teres f. maculata and Pyrenophora teres f. teres resistance loci utilizing natural Turkish wild and landrace barley populations. G3 Genes Genomes Genetics. https://doi.org/10.1093/g3journal/jkab269
Cope JE, Norton GJ, George TS, Newton AC (2021) Identifying potential novel resistance to the foliar disease ‘scald’ (Rhynchosporium commune) in a population of Scottish Bere barley landrace (Hordeum vulgare L.). J Plant Dis Prot 128:999–1012. https://doi.org/10.1007/s41348-021-00470-x
Coulter M, Büttner B, Hofmann K et al (2019) Characterisation of barley resistance to rhynchosporium on chromosome 6HS. Theor Appl Genet 132:1089–1107. https://doi.org/10.1007/s00122-018-3262-8
Crous PW, Braun U, McDonald BA et al (2021) Redefining genera of cereal pathogens: Oculimacula, Rhynchosporium and Spermospora. Fungal Syst Evol 7:67–98. https://doi.org/10.3114/fuse.2021.07.04
Daba SD, Horsley R, Brueggeman R et al (2019) Genome-wide association studies and candidate gene identification for leaf scald and net blotch in barley (Hordeum vulgare L.). Plant Dis 103:880–889. https://doi.org/10.1094/PDIS-07-18-1190-RE
Dawson IK, Russell J, Powell W et al (2015) Barley: a translational model for adaptation to climate change. New Phytol 206:913–931. https://doi.org/10.1111/nph.13266
Dracatos PM, Haghdoust R, Singh RP et al (2019) High-density mapping of triple rust resistance in barley using DArT-Seq markers. Front Plant Sci 10:467. https://doi.org/10.3389/fpls.2019.00467
Dreissig S, Fuchs J, Himmelbach A et al (2017) Sequencing of single pollen nuclei reveals meiotic recombination events at megabase resolution and circumvents segregation distortion caused by postmeiotic processes. Front Plant Sci 8:1620. https://doi.org/10.3389/fpls.2017.01620
El-Ahmed AM (1981) Seedling reaction of the 7th IBON to R. secalis in the greenhouse and source of resistance. In: Barley diseases and associated breeding methodology workshop. Rabat, Morocco
Fériani W, Rezgui S, Cherif M (2020) Detection of QTL and QTL × environment interaction for scald resistance in a two-row × six-row cross of barley. Cereal Res Commun 48:187–193. https://doi.org/10.1007/s42976-020-00024-1
Fernández-Calleja M, Casas AM, Igartua E (2021) Major flowering time genes of barley: allelic diversity, effects, and comparison with wheat. Theor Appl Genet 134:1867–1897. https://doi.org/10.1007/s00122-021-03824-z
Gawenda I, Thorwarth P, Günther T et al (2015) Genome-wide association studies in elite varieties of German winter barley using single-marker and haplotype-based methods. Plant Breed 134(28):39. https://doi.org/10.1111/pbr.12237
Genger RK, Williams KJ, Raman H et al (2003) Leaf scald resistance genes in Hordeum vulgare and Hordeum vulgare ssp. spontaneum: parallels between cultivated and wild barley. Aust J Agric Res 54:1335–1342. https://doi.org/10.1071/AR02230
Hanemann A, Schweizer GF, Cossu R et al (2009) Fine mapping, physical mapping and development of diagnostic markers for the Rrs2 scald resistance gene in barley. Theor Appl Genet 119:1507–1522. https://doi.org/10.1007/s00122-009-1152-9
Hautsalo J, Novakazi F, Jalli M et al (2021) Pyramiding of scald resistance genes in four spring barley MAGIC populations. Theor Appl Genet. https://doi.org/10.1007/s00122-021-03930-y
Holtz MD (2021) Distribution and frequency of mating types of Rhynchosporium commune in central Alberta. Can J Plant Path 43:559–566. https://doi.org/10.1080/07060661.2020.1851771
Huang M, Liu X, Zhou Y et al (2019) BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience 8:1–12. https://doi.org/10.1093/gigascience/giy154
IBGSC (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–717. https://doi.org/10.1038/nature11543
Kang HM, Zaitlen NA, Wade CM et al (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709–1723. https://doi.org/10.1534/genetics.107.080101
Kiros-Meles A, Gomez D, McDonald BA et al (2011) Invasion of Rhynchosporium commune onto wild barley in the Middle East. Biol Invasions 13:321–330. https://doi.org/10.1007/s10530-010-9808-6
Li HB, Zhou MX (2011) Quantitative trait loci controlling barley powdery mildew and scald resistances in two different barley doubled haploid populations. Mol Breeding 27:479–490. https://doi.org/10.1007/s11032-010-9445-x
Li M, Liu X, Bradbury P et al (2014) Enrichment of statistical power for genome-wide association studies. BMC Biol 12:73. https://doi.org/10.1186/s12915-014-0073-5
Linde CC, Smith LM, Peakall R (2016) Weeds, as ancillary hosts, pose disproportionate risk for virulent pathogen transfer to crops. BMC Evol Biol 16:101. https://doi.org/10.1186/s12862-016-0680-6
Linde CC, Zala M, McDonald BA (2009) Molecular evidence for recent founder populations and human-mediated migration in the barley scald pathogen Rhynchosporium secalis. Mol Phylogenet Evol 51:454–464. https://doi.org/10.1016/j.ympev.2009.03.002
Liu X, Huang M, Fan B et al (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12:e1005767. https://doi.org/10.1371/journal.pgen.1005767
Looseley ME, Newton AC, Atkins SD et al (2012) Genetic basis of control of Rhynchosporium secalis infection and symptom expression in barley. Euphytica 184:47–56. https://doi.org/10.1007/s10681-011-0485-z
Looseley ME, Griffe LL, Büttner B et al (2018) Resistance to Rhynchosporium commune in a collection of European spring barley germplasm. Theor Appl Genet 131:2513–2528. https://doi.org/10.1007/s00122-018-3168-5
Mamidi S, Chikara S, Goos RJ et al (2011) Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome 4:154–164. https://doi.org/10.3835/plantgenome2011.04.0011
Mascher M, Gundlach H, Himmelbach A et al (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433. https://doi.org/10.1371/journal.pgen.1005767
Mert Z, Karakaya A (2003) Determination of the suitable inoculum concentration for Rhynchosporium secalis seedling assays. J Phytopathol 151:699–701. https://doi.org/10.1046/j.0931-1785.2003.00770.x
Money D, Gardner K, Migicovsky Z et al (2015) LinkImpute: Fast and accurate genotype imputation for nonmodel organisms. G3 Genes Genomes Genetics 5:2383–2390. https://doi.org/10.1534/g3.115.021667
Muñoz-Amatriaín M, Cuesta-Marcos A, Endelman JB et al (2014) The USDA barley core collection: Genetic diversity, population structure, and potential for genome-wide association studies. PLoS One 9:e94688. https://doi.org/10.1371/journal.pone.0094688
Novakazi F, Krusell L, Jensen JD et al (2020) You Had Me at “MAGIC”!: Four barley MAGIC populations reveal novel resistance QTL for powdery mildew. Genes (basel) 11:1512. https://doi.org/10.3390/genes11121512
Novakazi F, Göransson M, Stefánsson TS et al (2021) Virulence of Rhynchosporium commune isolates collected in Iceland. J Plant Pathol 103:935–942. https://doi.org/10.1007/s42161-021-00888-0
Olaniran AO, Hiralal L, Mokoena MP, Pillay B (2017) Flavour-active volatile compounds in beer: production, regulation and control. J Inst Brew 123:13–23. https://doi.org/10.1002/jib.389
Penselin D, Münsterkötter M, Kirsten S et al (2016) Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses. BMC Genomics 17:953. https://doi.org/10.1186/s12864-016-3299-5
Pickering R, Ruge-Wehling B, Johnston PA et al (2006) The transfer of a gene conferring resistance to scald (Rhynchosporium secalis) from Hordeum bulbosum into H. vulgare chromosome 4HS. Plant Breed 125:576–579. https://doi.org/10.1111/j.1439-0523.2006.01253.x
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Read BJ, Raman H, McMichael G et al (2003) Mapping and QTL analysis of the barley population Sloop × Halcyon. Aust J Agric Res 54:1145–1153. https://doi.org/10.1071/AR03037
Richards J, Chao S, Friesen T, Brueggeman R (2016) Fine mapping of the barley chromosome 6H net form net blotch susceptibility locus. G3 Genes Genomes Genetics 6:1809–1818. https://doi.org/10.1534/g3.116.028902
Richards JK, Friesen TL, Brueggeman RS (2017) Association mapping utilizing diverse barley lines reveals net form net blotch seedling resistance/susceptibility loci. Theor Appl Genet 130:915–927. https://doi.org/10.1007/s00122-017-2860-1
Rohe M, Gierlich A, Hermann H et al (1995) The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO J 14:4168–4177. https://doi.org/10.1002/j.1460-2075.1995.tb00090.x
Ruff TM, Marston EJ, Eagle JD et al (2020) Genotyping by multiplexed sequencing (GMS): a customizable platform for genomic selection. PLoS One 15:e0229207. https://doi.org/10.1371/journal.pone.0229207
Russell J, Mascher M, Dawson IK et al (2016) Exome sequencing of geographically diverse barley landraces and wild relatives gives insights into environmental adaptation. Nat Genet 48:1024
Schürch S, Linde CC, Knogge W et al (2004) Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Mol Plant Microbe Interact 17:1114–1125. https://doi.org/10.1094/MPMI.2004.17.10.1114
Schweizer GF, Baumer M, Daniel G et al (1995) RFLP markers linked to scald (Rhynchosporium secalis) resistance gene Rh2 in barley. Theor Appl Genet 90:920–924. https://doi.org/10.1007/BF00222904
Segura V, Vilhjálmsson BJ, Platt A et al (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 44:825–830. https://doi.org/10.1038/ng.2314
Seifollahi E, Sharifnabi B, Javan-Nikkhah M, Linde CC (2018) Low genetic diversity of Rhynchosporium commune in Iran, a secondary centre of barley origin. Plant Pathol 67:1725–1734. https://doi.org/10.1111/ppa.12886
Sharma Poudel R, Al-Hashel AF, Gross T et al (2018) Pyramiding rpg4- and Rpg1-mediated stem rust resistance in barley requires the Rrr1 gene for both to function. Front Plant Sci 9:1789
Spaner D, Shugar LP, Choo TM et al (1998) Mapping of disease resistance loci in barley on the basis of visual assessment of naturally occurring symptoms. Crop Sci 38:843–850
Tamang P, Richards JK, Alhashal A et al (2019) Mapping of barley susceptibility/resistance QTL against spot form net blotch caused by Pyrenophora teres f. maculata using RIL populations. Theor Appl Genetics. https://doi.org/10.1007/s00122-019-03328-x
Wallwork H, Grcic M (2011) The use of differential isolates of Rhynchosporium secalis to identify resistance to leaf scald in barley. Australas Plant Pathol 40:490–496. https://doi.org/10.1007/s13313-011-0065-7
Wallwork H, Grcic M, Li CD et al (2014) Use of specific differential isolates of Rhynchosporium commune to detect minor gene resistance to leaf scald in barley seedlings. Australas Plant Pathol 43:197–203. https://doi.org/10.1007/s13313-013-0264-5
Wang J, Zhang Z (2021) GAPIT Version 3: Boosting power and accuracy for genomic association and prediction. Genomics Proteomics Bioinform 19:629–640. https://doi.org/10.1016/j.gpb.2021.08.005
Wang Q, Tian F, Pan Y et al (2014) A SUPER powerful method for genome wide association study. PLoS One 9:e107684. https://doi.org/10.1371/journal.pone.0107684
Wang Y, Gupta S, Wallwork H et al (2014b) Combination of seedling and adult plant resistance to leaf scald for stable resistance in barley. Mol Breeding 34:2081–2089. https://doi.org/10.1007/s11032-014-0164-6
Xie W, Xiong W, Pan J et al (2018) Decreases in global beer supply due to extreme drought and heat. Nat Plants 4:964–973. https://doi.org/10.1038/s41477-018-0263-1
Yu J, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208. https://doi.org/10.1038/ng1702
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stage of cereals. Weed Res 14:415–421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
Zaffarano PL, McDonald BA, Linde CC (2009) Phylogeographical analyses reveal global migration patterns of the barley scald pathogen Rhynchosporium secalis. Mol Ecol 18:279–293. https://doi.org/10.1111/j.1365-294X.2008.04013.x
Zaffarano PL, McDonald BA, Linde CC (2011) Two new species of Rhynchosporium. Mycologia 103:195–202. https://doi.org/10.3852/10-119
Zantinge J, Xue S, Holtz M et al (2019) The identification of multiple SNP markers for scald resistance in spring barley through restriction-site associated sequencing. Euphytica 215:8. https://doi.org/10.1007/s10681-018-2317-x
Zeng Y, Pu X, Du J et al (2020) Molecular mechanism of functional ingredients in barley to combat human chronic diseases. Oxid Med Cell Longev 2020:3836172. https://doi.org/10.1155/2020/3836172
Zhan J, Fitt BDL, Pinnschmidt HO et al (2008) Resistance, epidemiology and sustainable management of Rhynchosporium secalis populations on barley. Plant Pathol 57:1–14. https://doi.org/10.1111/j.1365-3059.2007.01691.x
Zhang Z, Ersoz E, Lai C-Q et al (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360. https://doi.org/10.1038/ng.546
Zhang X, Ovenden B, Orchard BA et al (2019) Bivariate analysis of barley scald resistance with relative maturity reveals a new major QTL on chromosome 3H. Sci Rep 9:20263. https://doi.org/10.1038/s41598-019-56742-y
Zhang X, Ovenden B, Milgate A (2020) Recent insights into barley and Rhynchosporium commune interactions. Mol Plant Pathol 21:1111–1128. https://doi.org/10.1111/mpp.12945
Zwirek M, Waugh R, McKim SM (2019) Interaction between row-type genes in barley controls meristem determinacy and reveals novel routes to improved grain. New Phytol 221:1950–1965. https://doi.org/10.1111/nph.15548
Acknowledgements
The authors would like to thank Lance Merrick for bioinformatic support and to the staff and research personnel of the Central Research Institute for Field Crops (Ankara, Turkey) for their help.
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The research presented in this manuscript was supported by the United States Department of Agriculture National Institute of Food and Agriculture (USDA-NIFA) award # 2018–67014-28491, the National Science Foundation grant award # 1759030, and the United States Department of Agriculture National Institute of Food and Agriculture Hatch project 1014919, Crop Improvement and Sustainable Production Systems (WSU reference 00011). Any opinions, findings, conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the United States Department of Agriculture National Institute of Food and Agriculture or the National Science Foundation.
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AÇO, AK, and RSB: conceived the study. MRA, AÇO and AK: carried out phenotyping and DNA extractions. KE and SC: carried out genotyping. SC: performed the analysis and wrote the manuscript with contributions from AÇO, KE, AK, and RB: All authors approved the final manuscript.
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Clare, S.J., Çelik Oğuz, A., Effertz, K. et al. Wild barley (Hordeum spontaneum) and landraces (Hordeum vulgare) from Turkey contain an abundance of novel Rhynchosporium commune resistance loci. Theor Appl Genet 136, 15 (2023). https://doi.org/10.1007/s00122-023-04245-w
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DOI: https://doi.org/10.1007/s00122-023-04245-w