Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture

Nature Biotechnology

Volumn 34, Issue 6, 2016, Pages 652-655

  Steuernagel, Burkhard ^a,b   Periyannan, Sambasivam K ^c   Hernández Pinzón, Inmaculada ^a   Witek, Kamil ^a   Rouse, Matthew N ^d   Yu, Guotai ^b   Hatta, Asyraf ^b,e   Ayliffe, Mick ^c   Bariana, Harbans ^f   Jones, Jonathan D G ^a   Lagudah, Evans S ^c   Wulff, Brande B H ^a,b  

^a SAINSBURY LABORATORY   (United Kingdom)

^b JOHN INNES CENTRE   (United Kingdom)

^c CSIRO   (Australia)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^f UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CLONING; CROPS; DISEASE CONTROL; GENETIC ENGINEERING; MUTAGENESIS; PLANTS (BOTANY);

BREAD WHEAT; CHEMICAL MUTAGENESIS; DISEASE RESISTANCE; DISEASE-RESISTANCE GENES; GENE CLONING; RAPID CLONING; SEQUENCE CAPTURES; STEM RUST RESISTANCE GENES;

GENES;

ARTICLE; BARLEY; BEAN; CHEMICAL MUTAGENESIS; CROP; DISEASE RESISTANCE; EXOME; GENE SEQUENCE; HEXAPLOIDY; MAIZE; MOLECULAR CLONING; MUTAGENESIS; OAT; PEA; PLANT GENE; PRIORITY JOURNAL; RICE; RYE; STEM RUST; TRITICUM AESTIVUM; DNA SEQUENCE; GENETIC ENHANCEMENT; GENETICS; PLANT; PLANT DISEASE; PREVENTION AND CONTROL; PROCEDURES; SITE DIRECTED MUTAGENESIS; TRANSGENIC PLANT;

CLONING, MOLECULAR; DISEASE RESISTANCE; GENES, PLANT; GENETIC ENHANCEMENT; MUTAGENESIS, SITE-DIRECTED; PLANT DISEASES; PLANTS; PLANTS, GENETICALLY MODIFIED; SEQUENCE ANALYSIS, DNA;

EID: 84973657517     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.3543     Document Type: Article

References (41)

1. McDonald, B.A. & Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40, 349-379 (2002).
2. Dangl, J.L., Horvath, D.M. & Staskawicz, B.J. Pivoting the plant immune system from dissection to deployment. Science 341, 746-751 (2013).
3. Kuang, H., Woo, S.S., Meyers, B.C., Nevo, E. & Michelmore, R.W. Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16, 2870-2894 (2004).
4. Smith, S.M., Pryor, A.J. & Hulbert, S.H. Allelic and haplotypic diversity at the rp1 rust resistance locus of maize. Genetics 167, 1939-1947 (2004).
5. Gaut, B.S., Wright, S.I., Rizzon, C., Dvorak, J. & Anderson, L.K. Recombination: an underappreciated factor in the evolution of plant genomes. Nat. Rev. Genet. 8, 77-84 (2007).
6. Hulbert, S.H., Webb, C.A., Smith, S.M. & Sun, Q. Resistance gene complexes: evolution and utilization. Annu. Rev. Phytopathol. 39, 285-312 (2001).
7. Jupe, F. et al. 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 (2013).
8. Andolfo, G. et al. Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol. 14, 120 (2014).
9. Henry, I.M. et al. Efficient genome-wide detection and cataloging of EMS-induced mutations using exome capture and Next-Generation Sequencing. Plant Cell 26, 1382-1397 (2014).
10. Periyannan, S. et al. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341, 786-788 (2013).
11. Gerechter-Amitai, Z.K., Wahl, I., Vardi, A. & Zohary, D. Transfer of stem rust seedling resistance from wild diploid einkorn to tetraploid durum wheat by means of a triploid hybrid bridge. Euphytica 20, 281-285 (1971).
12. The, T.T. Chromosome location of genes conditioning stem rust resistance transferred from diploid to hexaploid wheat. Nat. New Biol. 241, 256 (1973).
13. Olivera Firpo, P. et al. Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in southern Ethiopia in 2013/14. Phytopathology 105, 917-928 (2015).
14. The, T.T. et al. in 7th International Wheat Genetics Symposium (eds. Miller, T.E. & Koebner, R.M.D.) 901-909 (Bath Press, Bath, UK, 1988).
15. Rouse, M.N. & Jin, Y. Stem rust resistance in A-Genome diploid relatives of wheat. Plant Dis. 95, 941-944 (2011).
16. Witek, K. et al. Accelerated cloning of a potato late blight-resistance gene using RenSeq and SMRT sequencing. Nat. Biotechnol. http://dx.doi.org/10.1038/nbt.3540 (2016).
17. Kerber, E.R. & Dyck, P.L. Inheritance in hexaploid wheat of leaf rust resistance and other characters derived from Aegilops squarrosa. Can. J. Genet. Cytol. 11, 639-647 (1969).
18. Marais, G.F., Potgieter, G.F., Roux, H.S. & le Roux, J. An assessment of the variation for stem rust resistance in the progeny of a cross involving the Triticum species aestivum, turgidum and tauschii. S. Afr. J. Plant Soil 11, 15-19 (1994).
19. Periyannan, S. et al. Identification of a robust molecular marker for the detection of the stem rust resistance gene Sr45 in common wheat. Theor. Appl. Genet. 127, 947-955 (2014).
20. Steuernagel, B., Jupe, F., Witek, K., Jones, J.D. & Wulff, B.B. NLR-parser: rapid annotation of plant NLR complements. Bioinformatics 31, 1665-1667 (2015).
21. Saintenac, C. et al. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science 341, 783-786 (2013).
22. International Wheat Genome Sequencing Consortium (IWGSC). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345, 1251788 (2014).
23. Mayer, K.F. et al. A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711-716 (2012).
24. Finn, R.D. et al. Pfam: the protein families database. Nucleic Acids Res. 42, D222-D230 (2014).
25. Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150-3152 (2012).
26. Zhang, Z., Schwartz, S., Wagner, L. & Miller, W. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7, 203-214 (2000).
27. Lagudah, E.S., Appels, R., Brown, A.H.D. & McNeil, D. The molecular-genetic analysis of Triticum tauschii, the D-genome donor to hexaploid wheat. Genome 34, 375-386 (1991).
28. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
29. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
30. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
31. Fiume, M. et al. Savant Genome Browser 2: visualization and analysis for population-scale genomics. Nucleic Acids Res. 40, W615-W621 (2012).
32. Paull, J.G., Pallotta, M.A., Langridge, P. & The, T.T. RFLP markers associated with Sr22 and recombination between chromosome 7A of bread wheat and the diploid species Triticum boeoticum. Theor. Appl. Genet. 89, 1039-1045 (1994).
33. Khan, R.R. et al. Molecular mapping of stem and leaf rust resistance in wheat. Theor. Appl. Genet. 111, 846-850 (2005).
34. Kota, R., Spielmeyer, W., McIntosh, R.A. & Lagudah, E.S. Fine genetic mapping fails to dissociate durable stem rust resistance gene Sr2 from pseudo-black chaff in common wheat (Triticum aestivum L.). Theor. Appl. Genet. 112, 492-499 (2006).
35. Periyannan, S.K., Bansal, U.K., Bariana, H.S., Pumphrey, M. & Lagudah, E.S. A robust molecular marker for the detection of shortened introgressed segment carrying the stem rust resistance gene Sr22 in common wheat. Theor. Appl. Genet. 122, 1-7 (2011).
36. Akhunov, E.D. et al. Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes. BMC Genomics 11, 702 (2010).
37. Luo, M.C. et al. A 4-gigabase physical map unlocks the structure and evolution of the complex genome of Aegilops tauschii, the wheat D-genome progenitor. Proc. Natl. Acad. Sci. USA 110, 7940-7945 (2013).
38. Rouse, M.N. & Jin, Y. Genetics of resistance to race TTKSK of Puccinia graminis f. sp. tritici in Triticum monococcum. Phytopathology 101, 1418-1423 (2011).
39. Krattinger, S.G. et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323, 1360-1363 (2009).
40. Wang, M.B., Li, Z.Y., Matthews, P.R. & Upadhyaya, N.M. Improved vectors for Agrobacterium tumefaciens-mediated transformation of monocot plants. Acta Hortic. 461, 401-408 (1998).
41. Ishida, Y., Tsunashima, M., Hiei, Y. & Komari, T. Wheat (Triticum aestivum L.) transformation using immature embryos. Methods Mol. Biol. 1223, 189-198 (2015).