Genetics of host resistance in wheat

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UKCPVS 07/03/2018 Genetics of host resistance in wheat Keith Gardner

Wagtail association mapping project 4 fungal diseases 4 variable years Multiple trial locations 2015 26,000 SNPs 520 UK/NW Europe wheat varieties 39 disease trials Adult plant resistance (APR) 2 measurement dates

Association mapping results 20-79 hits (fdr<0.05) per disease 14-38 marginal hits (fdr>0.05, -log10p>4) per disease 14-28 hits per disease useful for breeding (resistance allele frequency < 0.7) Useful breeding hits: rusts > ST & PM SR many rare susceptible loci breeding outcome?

Yellow rust * average of individual trials where 0=no sig effect, 0.5= weak effect, 1 = strong effect ** for hits with at least 4 significant trials with 2 disease measurements For UK vs non-uk, large differences highlighted in pink NV - no variation in validation pops HIT by 2012/13 UK trials Non-UK Meta early/late R allele freq R allele freq 2014 trials* min FDR trials* 2012* trials 2012* analysis acting** Wagtail RL 2018 Validation 1 0.39 0.60 0.38 0.25 strong(2014) 0.31 0.56 2 0.17 0.90 0.25 0.00 strong(2014) 0.26 0.20 3 0.08 0.00 0.00 0.25 weak 0.05 0.00 4 0.97 0.55 1.00 1.00 strong(all) 6/6 late 0.12 0.13 5 0.89 0.80 0.88 0.92 strong(all) 3/6 late 0.28 0.56 6 0.47 0.15 0.56 0.50 weak 6/7 late 0.68 0.47 7 0.14 0.00 0.31 0.00 0.21 0.27 8 0.61 0.30 0.94 0.42 weak 6/6 late 0.24 0.16 9 0.08 0.30 0.06 0.00 weak 0.09 0.00 NV 10 0.00 0.00 0.00 0.00 weak 0.08 0.02 NV 11 0.39 0.30 0.31 0.58 weak 0.08 0.18 12 0.25 0.00 0.50 0.08 weak 0.48 0.40 X 13 0.17 0.00 0.13 0.00 weak 0.08 0.20 NV 14 0.06 0.10 0.00 0.17 0.05 0.02 NV 15 0.14 0.00 0.31 0.00 weak 0.61 0.87 X 16 0.61 0.20 0.63 0.75 weak 0.43 0.47 17 0.14 0.30 0.25 0.08 0.18 0.02 18 0.22 0.10 0.19 0.25 5/5 late 0.44 0.40 X 19 0.47 0.35 0.69 0.42 weak 4/5 early 0.34 0.04 X 20 0.08 0.10 0.13 0.08 0.05 0.00 NV 21 0.08 0.25 0.00 0.00 weak 2/4 0.41 0.53 X 22 0.31 0.10 0.38 0.42 weak 5/5 late 0.26 0.04 NV 23 0.47 0.00 0.69 0.42 weak 3/4 late 0.12 0.16 X 24 0.39 0.00 0.44 0.42 weak 2/4 0.23 0.07 X 25 0.39 0.00 0.44 0.42 weak 0.26 0.40 26 0.39 0.10 0.38 0.50 4/5 early 0.29 0.52 27 0.00 0.10 0.00 0.00 0.56 0.71 X 28 0.08 0.00 0.00 0.25 weak 0.37 0.30

Yellow rust - validation 11/13 full hits 3/9 marginal hits Validated hits->uk breeding programs HIT by 2012/13 UK trials Non-UK Meta early/late R allele freq R allele freq 2014 trials* min FDR trials* 2012* trials 2012* analysis acting** Wagtail RL 2018 Validation 1 0.39 0.60 0.38 0.25 strong(2014) 0.31 0.56 2 0.17 0.90 0.25 0.00 strong(2014) 0.26 0.20 3 0.08 0.00 0.00 0.25 weak 0.05 0.00 4 0.97 0.55 1.00 1.00 strong(all) 6/6 late 0.12 0.13 5 0.89 0.80 0.88 0.92 strong(all) 3/6 late 0.28 0.56 6 0.47 0.15 0.56 0.50 weak 6/7 late 0.68 0.47 7 0.14 0.00 0.31 0.00 0.21 0.27 8 0.61 0.30 0.94 0.42 weak 6/6 late 0.24 0.16 9 0.08 0.30 0.06 0.00 weak 0.09 0.00 NV 10 0.00 0.00 0.00 0.00 weak 0.08 0.02 NV 11 0.39 0.30 0.31 0.58 weak 0.08 0.18 12 0.25 0.00 0.50 0.08 weak 0.48 0.40 X 13 0.17 0.00 0.13 0.00 weak 0.08 0.20 NV 14 0.06 0.10 0.00 0.17 0.05 0.02 NV 15 0.14 0.00 0.31 0.00 weak 0.61 0.87 X 16 0.61 0.20 0.63 0.75 weak 0.43 0.47 17 0.14 0.30 0.25 0.08 0.18 0.02 18 0.22 0.10 0.19 0.25 5/5 late 0.44 0.40 X 19 0.47 0.35 0.69 0.42 weak 4/5 early 0.34 0.04 X 20 0.08 0.10 0.13 0.08 0.05 0.00 NV 21 0.08 0.25 0.00 0.00 weak 2/4 0.41 0.53 X 22 0.31 0.10 0.38 0.42 weak 5/5 late 0.26 0.04 NV 23 0.47 0.00 0.69 0.42 weak 3/4 late 0.12 0.16 X 24 0.39 0.00 0.44 0.42 weak 2/4 0.23 0.07 X 25 0.39 0.00 0.44 0.42 weak 0.26 0.40 26 0.39 0.10 0.38 0.50 4/5 early 0.29 0.52 27 0.00 0.10 0.00 0.00 0.56 0.71 X 28 0.08 0.00 0.00 0.25 weak 0.37 0.30

Yellow rust annual changes Average hit magnitude 0.0 0.4 0.8 SR_2012 SR_2014 H1 H3 H5 H7 H9 H11 H13 H15 H17 H19 H21 H23 H25 H27 Trial

Yellow rust annual changes Average hit magnitude 0.0 0.4 0.8 SR_2012 SR_2014 H1 H3 H5 H7 H9 H11 H13 H15 H17 H19 H21 H23 H25 H27 Trial

Yellow rust annual changes Average hit magnitude 0.0 0.4 0.8 SR_2012 SR_2014 H1 H3 H5 H7 H9 H11 H13 H15 H17 H19 H21 H23 H25 H27 Trial

Yellow rust * average of individual trials where 0=no sig effect, 0.5= weak effect, 1 = strong effect ** for hits with at least 4 significant trials with 2 disease measurements For UK vs non-uk, large differences highlighted in pink NV - no variation in validation pops HIT by 2012/13 UK trials Non-UK Meta early/late R allele freq R allele freq 2014 trials* min FDR trials* 2012* trials 2012* analysis acting** Wagtail RL 2018 Validation 1 0.39 0.60 0.38 0.25 strong(2014) 0.31 0.56 2 0.17 0.90 0.25 0.00 strong(2014) 0.26 0.20 3 0.08 0.00 0.00 0.25 weak 0.05 0.00 4 0.97 0.55 1.00 1.00 strong(all) 6/6 late 0.12 0.13 5 0.89 0.80 0.88 0.92 strong(all) 3/6 late 0.28 0.56 6 0.47 0.15 0.56 0.50 weak 6/7 late 0.68 0.47 7 0.14 0.00 0.31 0.00 0.21 0.27 8 0.61 0.30 0.94 0.42 weak 6/6 late 0.24 0.16 9 0.08 0.30 0.06 0.00 weak 0.09 0.00 NV 10 0.00 0.00 0.00 0.00 weak 0.08 0.02 NV 11 0.39 0.30 0.31 0.58 weak 0.08 0.18 12 0.25 0.00 0.50 0.08 weak 0.48 0.40 X 13 0.17 0.00 0.13 0.00 weak 0.08 0.20 NV 14 0.06 0.10 0.00 0.17 0.05 0.02 NV 15 0.14 0.00 0.31 0.00 weak 0.61 0.87 X 16 0.61 0.20 0.63 0.75 weak 0.43 0.47 17 0.14 0.30 0.25 0.08 0.18 0.02 18 0.22 0.10 0.19 0.25 5/5 late 0.44 0.40 X 19 0.47 0.35 0.69 0.42 weak 4/5 early 0.34 0.04 X 20 0.08 0.10 0.13 0.08 0.05 0.00 NV 21 0.08 0.25 0.00 0.00 weak 2/4 0.41 0.53 X 22 0.31 0.10 0.38 0.42 weak 5/5 late 0.26 0.04 NV 23 0.47 0.00 0.69 0.42 weak 3/4 late 0.12 0.16 X 24 0.39 0.00 0.44 0.42 weak 2/4 0.23 0.07 X 25 0.39 0.00 0.44 0.42 weak 0.26 0.40 26 0.39 0.10 0.38 0.50 4/5 early 0.29 0.52 27 0.00 0.10 0.00 0.00 0.56 0.71 X 28 0.08 0.00 0.00 0.25 weak 0.37 0.30

Yellow rust * average of individual trials where 0=no sig effect, 0.5= weak effect, 1 = strong effect ** for hits with at least 4 significant trials with 2 disease measurements For UK vs non-uk, large differences highlighted in pink NV - no variation in validation pops HIT by 2012/13 UK trials Non-UK Meta early/late R allele freq R allele freq 2014 trials* min FDR trials* 2012* trials 2012* analysis acting** Wagtail RL 2018 Validation 1 0.39 0.60 0.38 0.25 strong(2014) 0.31 0.56 2 0.17 0.90 0.25 0.00 strong(2014) 0.26 0.20 3 0.08 0.00 0.00 0.25 weak 0.05 0.00 4 0.97 0.55 1.00 1.00 strong(all) 6/6 late 0.12 0.13 5 0.89 0.80 0.88 0.92 strong(all) 3/6 late 0.28 0.56 6 0.47 0.15 0.56 0.50 weak 6/7 late 0.68 0.47 7 0.14 0.00 0.31 0.00 0.21 0.27 8 0.61 0.30 0.94 0.42 weak 6/6 late 0.24 0.16 9 0.08 0.30 0.06 0.00 weak 0.09 0.00 NV 10 0.00 0.00 0.00 0.00 weak 0.08 0.02 NV 11 0.39 0.30 0.31 0.58 weak 0.08 0.18 12 0.25 0.00 0.50 0.08 weak 0.48 0.40 X 13 0.17 0.00 0.13 0.00 weak 0.08 0.20 NV 14 0.06 0.10 0.00 0.17 0.05 0.02 NV 15 0.14 0.00 0.31 0.00 weak 0.61 0.87 X 16 0.61 0.20 0.63 0.75 weak 0.43 0.47 17 0.14 0.30 0.25 0.08 0.18 0.02 18 0.22 0.10 0.19 0.25 5/5 late 0.44 0.40 X 19 0.47 0.35 0.69 0.42 weak 4/5 early 0.34 0.04 X 20 0.08 0.10 0.13 0.08 0.05 0.00 NV 21 0.08 0.25 0.00 0.00 weak 2/4 0.41 0.53 X 22 0.31 0.10 0.38 0.42 weak 5/5 late 0.26 0.04 NV 23 0.47 0.00 0.69 0.42 weak 3/4 late 0.12 0.16 X 24 0.39 0.00 0.44 0.42 weak 2/4 0.23 0.07 X 25 0.39 0.00 0.44 0.42 weak 0.26 0.40 26 0.39 0.10 0.38 0.50 4/5 early 0.29 0.52 27 0.00 0.10 0.00 0.00 0.56 0.71 X 28 0.08 0.00 0.00 0.25 weak 0.37 0.30

Yellow rust * average of individual trials where 0=no sig effect, 0.5= weak effect, 1 = strong effect ** for hits with at least 4 significant trials with 2 disease measurements For UK vs non-uk, large differences highlighted in pink NV - no variation in validation pops HIT by 2012/13 UK trials Non-UK Meta early/late R allele freq R allele freq 2014 trials* min FDR trials* 2012* trials 2012* analysis acting** Wagtail RL 2018 Validation 1 0.39 0.60 0.38 0.25 strong(2014) 0.31 0.56 2 0.17 0.90 0.25 0.00 strong(2014) 0.26 0.20 3 0.08 0.00 0.00 0.25 weak 0.05 0.00 4 0.97 0.55 1.00 1.00 strong(all) 6/6 late 0.12 0.13 5 0.89 0.80 0.88 0.92 strong(all) 3/6 late 0.28 0.56 6 0.47 0.15 0.56 0.50 weak 6/7 late 0.68 0.47 7 0.14 0.00 0.31 0.00 0.21 0.27 8 0.61 0.30 0.94 0.42 weak 6/6 late 0.24 0.16 9 0.08 0.30 0.06 0.00 weak 0.09 0.00 NV 10 0.00 0.00 0.00 0.00 weak 0.08 0.02 NV 11 0.39 0.30 0.31 0.58 weak 0.08 0.18 12 0.25 0.00 0.50 0.08 weak 0.48 0.40 X 13 0.17 0.00 0.13 0.00 weak 0.08 0.20 NV 14 0.06 0.10 0.00 0.17 0.05 0.02 NV 15 0.14 0.00 0.31 0.00 weak 0.61 0.87 X 16 0.61 0.20 0.63 0.75 weak 0.43 0.47 17 0.14 0.30 0.25 0.08 0.18 0.02 18 0.22 0.10 0.19 0.25 5/5 late 0.44 0.40 X 19 0.47 0.35 0.69 0.42 weak 4/5 early 0.34 0.04 X 20 0.08 0.10 0.13 0.08 0.05 0.00 NV 21 0.08 0.25 0.00 0.00 weak 2/4 0.41 0.53 X 22 0.31 0.10 0.38 0.42 weak 5/5 late 0.26 0.04 NV 23 0.47 0.00 0.69 0.42 weak 3/4 late 0.12 0.16 X 24 0.39 0.00 0.44 0.42 weak 2/4 0.23 0.07 X 25 0.39 0.00 0.44 0.42 weak 0.26 0.40 26 0.39 0.10 0.38 0.50 4/5 early 0.29 0.52 27 0.00 0.10 0.00 0.00 0.56 0.71 X 28 0.08 0.00 0.00 0.25 weak 0.37 0.30

Yellow rust * average of individual trials where 0=no sig effect, 0.5= weak effect, 1 = strong effect ** for hits with at least 4 significant trials with 2 disease measurements For UK vs non-uk, large differences highlighted in pink NV - no variation in validation pops HIT by 2012/13 UK trials Non-UK Meta early/late R allele freq R allele freq 2014 trials* min FDR trials* 2012* trials 2012* analysis acting** Wagtail RL 2018 Validation 1 0.39 0.60 0.38 0.25 strong(2014) 0.31 0.56 2 0.17 0.90 0.25 0.00 strong(2014) 0.26 0.20 3 0.08 0.00 0.00 0.25 weak 0.05 0.00 4 0.97 0.55 1.00 1.00 strong(all) 6/6 late 0.12 0.13 5 0.89 0.80 0.88 0.92 strong(all) 3/6 late 0.28 0.56 6 0.47 0.15 0.56 0.50 weak 6/7 late 0.68 0.47 7 0.14 0.00 0.31 0.00 0.21 0.27 8 0.61 0.30 0.94 0.42 weak 6/6 late 0.24 0.16 9 0.08 0.30 0.06 0.00 weak 0.09 0.00 NV 10 0.00 0.00 0.00 0.00 weak 0.08 0.02 NV 11 0.39 0.30 0.31 0.58 weak 0.08 0.18 12 0.25 0.00 0.50 0.08 weak 0.48 0.40 X 13 0.17 0.00 0.13 0.00 weak 0.08 0.20 NV 14 0.06 0.10 0.00 0.17 0.05 0.02 NV 15 0.14 0.00 0.31 0.00 weak 0.61 0.87 X 16 0.61 0.20 0.63 0.75 weak 0.43 0.47 17 0.14 0.30 0.25 0.08 0.18 0.02 18 0.22 0.10 0.19 0.25 5/5 late 0.44 0.40 X 19 0.47 0.35 0.69 0.42 weak 4/5 early 0.34 0.04 X 20 0.08 0.10 0.13 0.08 0.05 0.00 NV 21 0.08 0.25 0.00 0.00 weak 2/4 0.41 0.53 X 22 0.31 0.10 0.38 0.42 weak 5/5 late 0.26 0.04 NV 23 0.47 0.00 0.69 0.42 weak 3/4 late 0.12 0.16 X 24 0.39 0.00 0.44 0.42 weak 2/4 0.23 0.07 X 25 0.39 0.00 0.44 0.42 weak 0.26 0.40 26 0.39 0.10 0.38 0.50 4/5 early 0.29 0.52 27 0.00 0.10 0.00 0.00 0.56 0.71 X 28 0.08 0.00 0.00 0.25 weak 0.37 0.30

Yellow rust Wagtail results summary Dramatic annual shift in effectiveness of hits pathogen changes Some hits effective across years key breeding targets Geographic and temporal variation UK/non-UK, late/early-acting Large allele frequency changes in last 10 years for some hits breeder selection for R alleles (f(r) ) or linked traits (f(r) ) Most hits unpublished/unnamed

Yellow rust in the NIAB MAGIC population Ad hoc data with natural infection from 2012, 2014 Laura Bouvet PhD multi-site, multi-year disease trials Single marker results: some shared QTL with Wagtail some distinctive to each population

Yellow rust pairwise interactions and allele stacking YR Hit 5, one trial only 14 RS - resistant allele at focal locus, susceptible allele at 2nd locus, etc.

Yellow rust pairwise interactions and allele stacking YR Hit 5, one trial only Rare suceptibles 14 RS - resistant allele at focal locus, susceptible allele at 2nd locus, etc.

Yellow rust pairwise interactions and allele stacking YR Hit 5, one trial only MAGIC hits not previously detected 14 MAGIC phenotype data collected by P. Howell, NIAB RS - resistant allele at focal locus, susceptible allele at 2nd locus, etc.

Yellow rust pairwise interactions and allele stacking YR Hit 5, one trial only 30% RL lines suboptimal MAGIC hits not previously detected 14 RS - resistant allele at focal locus, susceptible allele at 2nd locus, etc.

Yellow rust pairwise interactions and allele stacking Many different interactions patterns detected Additive Synergistic Redundancy Suppressors (often rare susceptible loci) Require different breeding approaches Some suppressors still present at a relatlively high frequency Some interactions with novel loci not found in single marker GWAS Some of these novel loci were found in NIAB MAGIC MAGIC and Wagtail in agreement when interactions considered 14

Yellow rust resistance future work Combine MAGIC, WAGTAIL results and resources Field test combinations of APR alleles MAGIC-derived Near-Isogenic Line (NIL) pairs Breeding company derived NILs New association mapping panel planted Revalidate previous hits New loci/combinations Includes more N European varieties New bi-parental populations made Old resistant lines lacking known resistance QTL New sources of resistance

Yellow rust resistance future work Detailed resistance characterisation (funding dependent): Microphenotyping Detailed disease progression studies Transcriptome differences

Acknowledgements NIAB Ian Mackay James Cockram Sarah Holdgate Alison Bentley Tobias Barber Richard Horsnell Phil Howell Gemma Rose Reading University Donal O Sullivan John Innes Centre James Brown DSV Matthew Kerton Elsoms Seeds Stephen Smith Lantmannen Tina Henriksson, Pernilla Vallenback Limagrain Simon Berry, Paul Fenwick,Ed Flatman KWS UK Nick Bird, Claire Freeman, Jacob Lage RAGT UK Ruth Bryant, Peter Jack Syngenta UK David Feuerhelm, Pauline Bansept-Basler Saaten Union Jörg Schondelmaier Sejet Linda Kærgaard Nielsen, Finn Borum