Abstract
Key message
Novel rust resistance genes LrP and YrP from Ae. peregrina identified on chromosome 5D and the linked markers will aid deployment of these genes in combination with other major/minor genes.
Abstract
Aegilops peregrina, a wild tetraploid relative of wheat with genome constitution UUSS, displays genetic variation for resistance to leaf and stripe (yellow) rust. The wheat Ae. peregrina introgression line, IL pau16058, harbouring leaf and stripe rust resistance, was crossed with wheat cv. WL711 to generate an F2:3 mapping population. Inheritance studies on this population indicated the transfer of dominant co-segregating resistance to leaf and stripe rust. Ethyl methane sulphonate mutagenesis of IL pau16058 identified independent loss-of-function mutants for leaf and stripe rust resistance, indicating that the leaf and stripe rust resistance is controlled by independent genes, herein designated LrP and YrP, respectively. A high-resolution genetic map of LrP and YrP was constructed using the Illumina Infinium iSelect 90K wheat array and resistance gene enrichment sequencing (RenSeq) markers. The map spans 4.19 cM on the distal-most region of the short arm of chromosome 5D, consisting of eight SNP markers and one microsatellite marker. LrP and YrP co-segregated with markers BS00163889 and 5DS44573_snp and was flanked distally by the SNP marker BS00129707 and proximally by 5DS149010, defining a 15.71 Mb region in the RefSeq v1.0 genome assembly.
Similar content being viewed by others
References
Aggarwal R, Kulshreshtha D, Sharma S, Singh VK, Manjunatha C, Bhardwaj SC, Saharan MS (2018) Molecular characterization of Indian pathotypes of Puccinia striiformis f. sp. tritici and multigene phylogenetic analysis to establish inter- and intraspecific relationships. Genet Mol Biol. https://doi.org/10.1590/1678-4685-gmb-2017-0171
Bansal M (2017) Fine Mapping and identification of candidate genes for a stripe rust and a leaf rust resistance transferred from Aegilops umbellulata to bread wheat (Triticum aestivum). Dissertation, Punjab Agricultural University, Ludhiana, Punjab, India
Bansal M, Kaur S, Dhaliwal HS, Bains NS, Bariana HS, Chhuneja P, Bansal UK (2017) Mapping of Aegilops umbellulata—derived leaf rust and stripe loci in wheat. Plant Pathol 66:38–44
Brabham HJ, Hernández-Pinzón I, Holden S, Lorang J, Moscou MJ (2017) An ancient integration in a plant NLR is maintained as a trans-species polymorphism. BiorRxiv: https://doi.org/10.1101/239541
Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci USA 110:8057–8062
Chhuneja P, Yadav B, Stirnweis D, Hurni S, Kaur S, Elkot AF, Keller B, Wicker T, Sehgal S, Gill BS, Singh K (2015) Fine mapping of powdery mildew resistance genes PmTb7A.1 and PmTb7A.2. In Triticum boeoticum (Boiss.) using the shotgun sequence assembly of chromosome 7AL. Theor Appl Genet 128:2099–2111
Chhuneja P, Kaur S, Dhaliwal HS (2016) Introgression and exploitation of biotic stress tolerance from related wild species in wheat cultivars. In: Rajpal VR et al (eds) Molecular breeding for sustainable crop improvement, sustainable development and biodiversity, vol 11. Springer, Basel, pp 269–324
Curtis CA, Lukaszewski AJ (1991) Genetic linkage between C-bands and storage protein genes in chromosome 1B of tetraploid wheat. Theor Appl Genet 81:245–252. https://doi.org/10.1007/BF00215730
Devos KM, Gale MD (1993) Extended genetic maps of the homoeologous group 3 chromosomes of wheat, rye and barley. Theor Appl Genet 85:649–652
Devos KM, Atkinson MD, Chinoy CN, Francis HA, Harcourt RL, Koebner RMD, Liu CJ, Masojć P, Xie DX, Gale MD (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor Appl Genet 85:673–680
Endo TR (1990) Gametocidal chromosomes and their induction of chromosome mutations in wheat. Jpn J Genet 65:135–152
Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci USA 100:15253–15258
Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296. https://doi.org/10.1146/annurev.py.09.090171.001423
Gale MD, Miller TE (1987) The introduction of alien genetic variation into wheat. In: Lupton FGH (ed) Wheat breeding: its scientific basis. Chapman and Hall, London, pp 173–210
Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156:1–13
International Wheat Genome Sequencing Consortium (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science. https://doi.org/10.1126/science.aar7191
Jiang J, Friebe B, Gill BS (1994) Recent advances in alien gene transfer in wheat. Euphytica 73:199–212
Jupe F, Witek K, Verweij W, Sliwka J, Pritchard L, Etherington GJ (2013) Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J 76:530–544
Kiran K, Rawal HC, Dubey H, Jaswal R, Devanna BN, Gupta DK, Bhardwaj SC, Prasad P, Pal D, Chhuneja P, Balasubramanian P, Kumar J, Swami M, Solanke AU, Gaikwad K, Singh NK, Sharma TR (2016) Draft genome of the wheat rust pathogen (Puccinia triticina) unravels genome-wide structural variations during evolution. Genome Biol Evol 8(9):2702–2721
Klymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A, Chen S, Feng L, Frenkel Z, Krugman T, Lidzbarsky G, Chang W, Jääskeläinen MJ, Schudoma C, Paulin L, Laine P, Bariana H, Sela H, Saleem K, Sørensen CK, Hovmøller MS, Distelfeld A, Chalhoub B, Dubcovsky J, Korol AB, Schulman AH, Fahima T (2018) Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat Commun 9:3735
Kolmer JA, Su Z, Bernardo A, Bai G, Chao S (2018) Mapping and characterization of the new adult plant leaf rust resistance gene Lr77 derived from Santa Fe winter wheat. Theor Appl Genet 131:1553–1560. https://doi.org/10.1007/s00122-018-3097-3
Kourelis J, Van der Hoorn RAL (2018) Nine R gene mechanisms. Plant Cell. https://doi.org/10.1105/tpc.17.00579
Kuraparthy V, Chhuneja P, Dhaliwal HS, Kaur S, Bowden RL, Gill BS (2007) Characterization and mapping of cryptic alien introgression from Aegilops geniculata with new leaf rust and stripe rust resistance genes Lr57 and Yr40 in wheat. Theor Appl Genet 114:1379–1389
Kuruparthy V, Sood S, Chhuneja P, Dhaliwal HS, Kaur S, Bowden RL, Gill BS (2007) A cryptic wheat-Aegilops triuncialis translocation with leaf rust resistance gene Lr58. Crop Sci 47:1995–2003
Mago R, Till B, Periyannan S, Yu G, Wulff BBH, Lagudah E (2017) Generation of loss-of-function mutants for wheat rust disease resistance gene cloning. Methods Mol Biol 1659:199–205. https://doi.org/10.1007/978-1-4939-7249-4_17
Marais GF, McCallum B, Snyman JE, Pretorius ZA, Marais AS (2005) Leaf rust and stripe rust resistance genes Lr54 and Yr37 transferred to wheat from Aegilops kotschyi. Plant Breed 124:538–541
Marchal C, Zhang J, Zhang P, Fenwick P, Steuernagel B, Adamski N, Boyd L, McIntosh R, Wulff BBH, Berry S, Lagudah E, Uauy C (2018) BED-domain containing immune receptors confer diverse resistance spectra to yellow rust. Nat Plants 4:662–668
McIntosh RA (1977) Induced mutations against plant diseases. In: Proceedings of a symposium on the use of induced mutations for improving disease resistance in crop plants; 31 Jan–4 Feb 1977; Vienna. International Atomic Energy Agency, Vienna; 1977. Nature of induced mutations affecting disease reaction in wheat; pp 551–564
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO Publications, East Melbourne
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Xia XC (2017) Catalogue of gene symbols for wheat: 2017 Supplement. http://www.shigen.nig.ac.jp/wheat/komugi/genes/symbolClassList.jsp
Molnár I, Vrána J, Burešová V, Cápal P, Farkas A, Darkó E, Cseh A, Kubaláková M, Molnár-Láng M, Doležel J (2016) Dissecting the U, M, S and C genomes of wild relatives of bread wheat (Aegilops spp.) into chromosomes and exploring their synteny with wheat. Plant J 88(3):452–467. https://doi.org/10.1111/tpj.13266
Narang D, Kaur S, Saini J, Chhuneja P (2018) Development and molecular characterization of wheat-aegilops peregrina introgression lines with resistance to leaf rust and stripe rust. J Crop Improv 32(1):59–70. https://doi.org/10.1080/15427528.2017.1398117
Niu ZX, Klindworth DL, Friesen TL, Chao SM, Jin Y, Cai XW, Xu SS (2011) Targeted introgression of a wheat stem rust resistance gene by DNA marker assisted chromosome engineering. Genetics 187:1011–1021
Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L, Deal K, Luo M, Kong X, Bariana H, Mago R, McIntosh R, Dodds P, Dvorak J, Lagudah E (2013) The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341:786–788
Peterson RF, Campbell AB, Hannah AE (1948) A diagnostic scale for estimating rust severity on leaves and stem of cereals. Can J Res Sect C Bot Sci 26:496–500
Prins R, Marais GF (1999) A genetic study of the gametocidal effect of the Lr19 translocation of common wheat. S Afr J Plant Soil 16:10–14
Ramírez-González RH, Segovia V, Bird N, Fenwick P, Holdgate S, Berry S, Jack P, Caccamo M, Uauy C (2015) RNA-Seq bulked segregant analysis enables the identification of high-resolution genetic markers for breeding in hexaploid wheat. Plant Biotechnol J 13:613–624
Riar AK, Kaur S, Dhaliwal HS, Singh K, Chhuneja P (2012) Introgression of a leaf rust resistance gene from Aegilops caudata to bread wheat. J Genet 91:155–161
Saghai-Maroof MA, Biyashev RM, Yang GP, Zhang Q, Allard RW (1994) Extraordinarily polymorphic microsatellite DNA in barley: species diversity, chromosomal locations and population dynamics. Proc Natl Acad Sci USA 91:5466–5470
Sears ER (1954) The aneuploids of common wheat. Research Bulletin 572, Missouri Agricultural Experiment Station, University of Missouri, Columbia, p 58
Sears ER (1972) Chromosome engineering in wheat. In: Stadler genetics symposium, vol 4. University of Missouri, Columbia, pp 23–38
Singh K, Chhuneja P, Ghai M, Kaur S, Goel RK, Bains NS, Keller B, Dhaliwal HS (2007) Molecular mapping of leaf and stripe rust resistance genes in Triticum monococcum and their transfer to hexaploid wheat. In: Buck H, Nisi JE, Solomon N (eds) Wheat production in stressed environments, 12th edn. Springer, dordrecht, pp 779–786
Somers DJ, Isaac P, Edwards K (2004) A high density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114
Steuernagel B, Jupe F, Witek K, Jones JD, Wulff BBH (2015) NLR-parser: rapid annotation of plant NLR complements. Bioinformatics 31:1665–1667
Steuernagel B, Periyannan SK, Hernandez-Pinzon I, Witek K, Rouse MN, Yu G, Hatta A, Ayliffe M, Bariana H, Jones JDG, Lagudah ES, Wulff BBH (2016) Rapid cloning of disease resistance genes in plants using mutagenesis and sequence capture. Nat Biotechnol 34:652–655
Steuernagel B, Witek K, Jones JDG, Wulff BBH (2017) MutRenSeq: a method for rapid cloning of plant disease resistance genes. Methods Mol Biol 1659:215–229. https://doi.org/10.1007/978-1-4939-7249-4_19
Tiwari VK, Wang S, Danilova T, Koo DH, Vrána J, Kubaláková M, Hribova E, Rawat N, Kalia B, Singh N, Friebe B, Doležel J, Akhunov E, Poland J, Sabir JSM, Gill BS (2015) Exploring the tertiary gene pool of bread wheat: sequence assembly and analysis of chromosome 5Mg of Aegilops geniculata. Plant J 84:733–746
Toor PI, Kaur S, Bansal M, Yadav B, Chhuneja P (2016) Mapping of stripe rust resistance gene in an Aegilops caudata introgression line in wheat and its genetic association with leaf rust resistance. J Genet 95(4):933–938. https://doi.org/10.1007/s12041-016-0718-y
Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, Comai L, Dubcovsky J (2009) A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol. https://doi.org/10.1186/1471-2229-9-115
Uauy C, Wulff BBH, Dubcovsky J (2017) Combining traditional mutagenesis with new high-throughput sequencing and genome editing to reveal hidden variation in polyploid wheat. Annu Rev Genet 51:435–454. https://doi.org/10.1146/annurev-genet-120116-024533
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40(15):115
Voorips RE (2002) Map chart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, Lillemo Hayden M, Akhunov E, International Wheat Genome Sequencing Consortium (2014) Characterization of polyploid wheat genomic diversity using a high-density 90000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796
Yu G, Champouret N, Steuernagel B, Olivera PD, Simmons J, Williams C, Johnson R, Moscou MJ, Hernández-Pinzón I, Green P, Sela H, Millet E, Jones JDG, Ward ER, Steffenson BJ, Wulff BBH (2017) Discovery and characterization of two new stem rust resistance genes in Aegilops sharonensis. Theor Appl Genet 130(6):1207–1222. https://doi.org/10.1007/s00122-017-2882-8
Acknowledgements
This project was funded by the Sustainable Crop Production Research for International Development (SCPRID) and the Crop Genomics and Technologies (CGAT) programmes from the Department of Biotechnology, Ministry of Science and Technology, Government of India, and the Biotechnology and Biological Sciences Research Council, UK, Grant BT/IN/UK/08/PC/2012 (BB/J012017/1) to PC and CU, Grant BT/IN/Indo-UK/CGAT/14/PC/2014-15 (BBS/E/J/000CA572) to PC and BBHW and the BBSRC Designing Future Wheat Programme (BB/P016855/1). The provision of rust cultures by the Directorate of Wheat Research Regional Research Station, Shimla, is thankfully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Aimin Zhang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Narang, D., Kaur, S., Steuernagel, B. et al. Fine mapping of Aegilops peregrina co-segregating leaf and stripe rust resistance genes to distal-most end of 5DS. Theor Appl Genet 132, 1473–1485 (2019). https://doi.org/10.1007/s00122-019-03293-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03293-5