The coiled-coil NLR Rph1, confers leaf rust resistance in ...3 46 Introduction 47 Barley is the...

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The coiled-coil NLR Rph1, confers leaf rust resistance in barley 1

cultivar Sudan 2

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Peter Michael Dracatos 1*

, Jan Bartoš2, Huda Elmansour

1, Davinder Singh

1, Miroslava 4

Karafiátová2, Peng Zhang

1, Burkhard Steuernagel

3, Radim Svačina

2, Joanna Cobbin

4, Bethany 5

Clark1, Sami Hoxha

1, Mekhar S. Khatkar

5, Jaroslav Doležel

2, Brande B. Wulff

3, Robert F. Park

1 6

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1 Sydney Institute of Agriculture, Plant Breeding Institute, The University of Sydney, Private Bag 4011, 8

Narellan 2567, NSW, Australia. 9

2 Institute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, 10

Šlechtitelů 31, Olomouc CZ-78371, Czech Republic. 11

3 John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, United Kingdom. 12

4 School of Life and Environmental Sciences, Charles Perkins Centre, The University of Sydney, Sydney, NSW, Australia. 13

5 Faculty of Veterinary Science, The University of Sydney, 425 Werombi Road, Camden 2570, NSW, Australia. 14

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*Corresponding author [email protected] 16

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Short title: Rph1 confers barley leaf rust resistance 18

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Author contributions: PD, DS and RP designed the research; PD, BC, DS, SH, HE, JB, RS, PZ performed the 20

research; BW, JD, JB, BS, MK contributed new analytic, computational tools; BS, MSK, JCAC, HE, PD, JB 21

analyzed the data and PD wrote the paper with contributions from BW, PZ, JB, BS and DS 22

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One-sentence summary: Rph1-mediated resistance to leaf rust in cultivated barley cultivar Sudan is conferred 24

by a single member of a resistance gene cluster on the short arm of chromosome 2H. 25

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Plant Physiology Preview. Published on December 28, 2018, as DOI:10.1104/pp.18.01052

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon April 29, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

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http://www.plantphysiol.org

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Abstract 28

Unravelling and exploiting mechanisms of disease resistance in cereal crops is currently limited by their large 29

repeat-rich genomes and the lack of genetic recombination or cultivar-specific sequence information. We cloned 30

the first leaf rust resistance gene Rph1 (Rph1.a) from cultivated barley using ‘MutChromSeq’, a recently 31

developed molecular genomics tool for the rapid cloning of genes in plants. Marker-trait association in the CI 32

9214/Stirling doubled haploid population mapped Rph1 to the short arm of chromosome 2H in a physical region 33

of 1.3 Mb relative to the barley cultivar Morex reference assembly. A sodium azide mutant population in 34

cultivar Sudan was generated and 10 mutants were confirmed by progeny-testing. Flow-sorted 2H chromosomes 35

from Sudan (wild type) and six of the mutants were sequenced and compared to identify candidate genes for the 36

Rph1 locus. MutChromSeq identified a single gene candidate encoding a coiled-coil NLR receptor protein that 37

was altered in three different mutants. Further Sanger sequencing confirmed all three mutations and identified 38

an additional two independent mutations within the same candidate gene. Phylogenetic analysis determined that 39

Rph1 clustered separately from all previously cloned NLRs from Triticeae and displayed highest sequence 40

similarity (89%) with a homologue of the Arabidopis RPM1 protein in Triticum urartu. In this study we 41

determined the molecular basis for Rph1-mediated resistance in cultivated barley enabling varietal improvement 42

through diagnostic marker design, gene editing and gene stacking technologies. 43

Keywords: Resistance, barley, leaf rust, MutChomSeq, cloning, Rph1 44

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3

Introduction 46

Barley is the fourth most important cereal crop in the world and is mainly used for malt production, animal feed 47

and, in some regions, human consumption. The current agricultural practice of monoculture in addition to 48

climate change favours the emergence of new pathogen variants that can significantly reduce yield, posing a 49

serious threat to global food security. Since Biblical times, rust pathogens have plagued farmer’s fields causing 50

significant yield losses and, in severe cases, crop failure and famine (Kislev 1982). In particular, plant pathogens 51

of the Puccinia genus are some of the most feared and damaging diseases of cereal crops (Dean et al. 2012). 52

Although leaf rust caused by P. hordei is the most widespread and serious foliar disease of barley, it can be 53

controlled effectively by genetic resistance (Park et al., 2015). The leaf rust resistance (R) gene Rph1 was first 54

described in barley cultivars Oderbrucker, Speciale and Sudan by Roane and Starling (1967) and was mapped to 55

chromosome 2H using trisomic analysis (Tuleen and McDaniel 1971). Rph1-mediated resistance was later 56

designated Rph1.a to conform with recommended allele symbols for leaf rust resistance genes in barley 57

(Franckowiak et al., 1992). Despite the existence of virulence for most Rph genes in barley by prevailing P. 58

hordei variants, combining multiple genes conferring diverse resistance mechanisms, as demonstrated in wheat 59

(Park 2003; Koller et al., 2018), could provide a sustained method for broad spectrum disease control (Brun et 60

al., 2010) 61

The intense diversifying selection imposed on R genes has resulted in high accessional variation at R 62

gene loci including sequence polymorphisms and copy number variation (Noël et al., 1999; Kuang et al., 2005; 63

Chavan et al., 2015; Thind et al., 2018). In many cases, this has led to erosion of the orthogonal relationships 64

between R gene analogues belonging to different accessions of the same species (Noël et al., 1999; Kuang et al., 65

2005; Chavan et al., 2015; Thind et al., 2018). Most map-based R gene cloning projects therefore include the 66

generation of a high-quality physical sequence (e.g. a BAC tiling path) spanning the flanking markers delimiting 67

the R gene in the resistant accession. This is followed by identification of candidate R genes and experimental 68

validation by transformation of the candidate gene(s) into a susceptible accession (Periyannan et al., 2013; 69

Kawashima et al., 2016). Generating a physical tiling path is, however, expensive and time-consuming. 70

An alternative or complementary approach involves R gene identification by sequence-comparison of 71

mutants. A line containing the desired R gene in a background that is susceptible to the pathogen isolate of 72

interest is mutated and the progeny is screened for loss-of-resistance. If multiple, independently derived mutant 73

alleles are obtained and found to have mutations in the same gene, this then provides very strong evidence for 74

gene identification; the causal gene can be further substantiated by demonstrating genetic co-segregation 75

between the candidate gene and resistance. The size of cereal genomes, such as 16.03–16.58 Gb for wheat 76

(International Wheat Genome Sequencing Consortium 2018) and 4.88–5.04 Gb for barley (Mascher et al., 2017) 77

imposes a barrier, however, in terms of the cost of sequencing and computational analysis. This can be 78

overcome by sequencing only a selected fraction of the genome, an approach known as ‘genome complexity 79



4

reduction’. Because most R genes encode nucleotide binding site leucine-rich repeats (NLRs) (Kourelious and 80

van der Hoorn, 2017), NLR-exome capture and sequencing can be used to efficiently compare multiple mutant 81

alleles. This strategy was successfully used to clone Sr22, Sr45, Yr5, Yr7 and Pm21 from wheat or wheat-alien 82

introgression lines (Steuernagel et al., 2016; Xing et al., 2018; Marchal et al., 2018). More recently, NLR exome 83

capture on 151 genetically diverse individuals of the wild wheat D-genome progenitor Aegilops tauschii was 84

coupled to association genetics to rapidly clone Sr46 and SrTA1662 (Arora et al., 2018). 85

The very strength of NLR exome capture in providing a stringent complexity reduction is also its 86

weakness by excluding, perforce (i) NLRs with significant sequence divergence to the source sequences used in 87

bait design, (ii) NLRs with exotic integrated domains (Sarris et al., 2016), and (iii) R genes not conforming to 88

the canonical structure of an NLR (Krattinger et al., 2009; Fu et al., 2009; Moore et al., 2015). This bias can be 89

overcome by chromosome flow sorting, where only a prior knowledge of the chromosome on which the gene 90

resides is required (Gioergi et al., 2013; Steuernagel et al., 2017). Sánchez-Martín and colleagues flow sorted 91

and sequenced wheat chromosome 5D from six Pm2 mutants and the parental wild type. Subsequent sequence-92

comparison was sufficient to identify a single candidate gene which could then be confirmed by sequencing 93

additional mutants (Sánchez-Martín et al., 2016). A limitation of this approach is the high number of mutants 94

(~5 in barley, ~6 in wheat) necessary to identify a single candidate gene (Sánchez-Martín et al., 2016). This 95

requires the generation and screening of a large mutant population, typically numbering several thousand 96

individuals (Mago et al., 2017), in particular in barley (a diploid) where the tolerated mutation density is 97

approximately seven times less than that in hexaploid wheat (Uauy et al., 2017). The requirement for many 98

mutants for unambiguous gene identification can be mitigated if combining chromosome flow sorting with 99

positional mapping (Thind et al., 2017). A limitation of chromosome flow sorting is the generally low quality of 100

assemblies (N50 >2 kb; 75% genes assembled into contigs with 90% query coverage) obtained from flow 101

sorted and multiple displacement-amplified DNA (Sánchez-Martín et al., 2016). This can be vastly improved 102

with Chicago long-range linked-read sequencing and assembly to obtain N50 scaffold sizes of 9.76–22.39 Mb 103

(Thind et al., 2017; Xing et al., 2018), although at high cost. In this study, we combined MutChromSeq with 104

genetic mapping to rapidly clone Rph1 in barley cultivar (cv.) Sudan from a defined region on chromosome 2H. 105

We also report on developing a cost-effective wild-type sequence assembly with high contiguity (contig N50 106

>20.1 kb) and gene space representation (83% of genes with 90% query coverage). 107



5

Results 108

The availability of an array of P. hordei pathotypes with contrasting virulence for Rph1-mediated resistance 109

permitted a reliable phenotypic screen at the seedling stage of two barley populations segregating for the Rph1 110

locus, with the aim of confirming the previous map location reported by Tuleen and McDaniel (1971). The 111

barley cvs. CI 9214, Sudan and Berg were all postulated to carry Rph1 based on greenhouse tests with P. hordei 112

pathotypes with contrasting virulence/avirulence profiles (Table 1). Monogenic inheritance for Rph1-mediated 113

resistance was confirmed by the observed segregation in both barley mapping populations (CI 9214/Baudin and 114

CI 9214/Stirling) when inoculated at the primary leaf stage in the greenhouse with Rph1-avirulent P. hordei 115

pathotype 4610 P+ (Table 2, Fig. 1). 116

A total of 61 representative genotypes of the CI 9214/Stirling DH population from both resistant and 117

susceptible phenotypic classes were selected for genetic mapping of Rph1, and were subsequently genotyped 118

using 10,258 DArT-Seq marker loci. Further genome-wide marker-trait association (MTA) analysis 119

demonstrated that DArT sequences only on 2HS were significantly associated [−log10 (P-value) of 15] with 120

Rph1 phenotypic scores using Fischer’s exact test, LD-correlation coefficient and Chi squared analysis (Fig. 2, 121

Supplemental Fig. 1, Supplementary Table 1). Genetic mapping of Rph1 in the CI 9214/Baudin population 122

was also performed using a sub-set of 92 RILs from the mapping population. A 1.3-Mb physical region in the 123

Morex reference genome sequence known to harbour the Rph1 gene flanked by two DArT-Seq markers 124

(13,139,911 bp and 14,361,439 bp) from the CI 9214/Baudin mapping population was used to search for 125

candidate genes using a modified version of MutantHunter (Sánchez-Martín et al., 2016). The flanking markers 126

were identified based on the presence of two recombinants from the 92 RILs on either side of Rph1. 127

A conservative estimate of the genetic and physical interval known to harbour the Rph1 gene enabled a 128

second level of genome complexity reduction in addition to the chromosome sorting. A sodium azide mutant 129

population was produced for the Rph1 differential cv. Sudan and 2,100 M2 generation spikes were rust tested 130

with P. hordei pathotype 4610 P+ in the greenhouse for loss of function mutations in the Rph1 gene. We 131

identified 10 spikes that contained putative rph1 knockouts. At least two susceptible seedlings per M2 spike 132

were advanced and their progeny were rust tested in the M3 generation; nine families were phenotyped as 133

homozygous susceptible and one segregated. Of these, five homozygous susceptible families and one 134

heterozygous mutant family were processed for chromosome sorting for 2H and Illumina sequencing (Fig. 3). 135

Chromosomes were isolated according to Lysák et al. (1999), labelled in suspension with GAA microsatellite 136

using FISHIS following the protocol of Giorgi et al. (2013), stained with DAPI and analysed by a FASCAria II 137

SORP flow cytometer and sorter. The resulting bivariate flow karyotype with the 2H population highlighted is 138

shown in Supplementary Fig. 2. In total, 80,000 copies of chromosome 2H were flow sorted from Sudan wild 139

type and six Sudan-derived mutant lines. The purity of the sorted fractions determined by FISH was 86%. 140



6

Multiple displacement amplification (MDA) was only performed to amplify chromosomal DNA from the six 141

mutant lines, however in contrast to Sanchez-Martin et al. (2016), importantly MDA was not performed on 142

chromosomal DNA from the Sudan wild type. Illumina sequencing of amplified chromosomal DNA yielded 143

27.6–45.5 million of 250-bp paired-end (PE) reads for each of the six mutant chromosomes (representing 18–144

30x coverage). For the wild-type chromosome 2H of cv. Sudan, 222 million of 250-bp PE reads were obtained 145

(equivalent to 144x coverage) and assembled into 62,427 scaffolds with N50 = 8,032 and N50 length of 20.7 kb. 146

The total assembly length of 587.7 Mb represents 75% of the estimated chromosome size. 147

Illumina sequence reads of six mutant lines (M422, M483, M544, M761, M763 and M767) were 148

mapped to the wild-type Sudan chromosome 2H within the 1.3-kb region of interest to search for genes that 149

contain multiple independent mutations. A single full-length gene encoding an NLR (corresponding to 150

HORVU2Hr1G006480.6 in Morex) in scaffold 2850_1 from Sudan contained mutations in lines M422, M761, 151

M763 and M767. (Fig. 3; Supplementary Fig. 3; Table 3). No mutations were identified in lines M483 and 152

M544 using both Illumina or Sanger sequencing, suggesting either a cis regulatory mutation or a second-site 153

suppressor. Further examination of the Illumina reads for line M767 identified a heterozygous C/T mutation 154

changing a glycine to glutamic acid in the conserved GLPL motif. Rust testingin the M3 progeny of M767 155

determined that it segregated with Rph1-mediated resistance, whereas all other mutant lines were homozygous 156

susceptible. We PCR-amplified and Sanger sequenced the Rph1 gene for seven mutant lines (M199, M422, 157

M430, M727, M761, M763 and M767). We confirmed the MutChromSeq results and identified two additional 158

mutations in lines M199 and M430 in the NBS domain. Three mutant lines (M727, M761 and M763) shared the 159

same C/T mutation in the LRR domain (Gly to Asp), despite originating from different M2 spikes, therefore a 160

total of five independent mutations were confirmed in Rph1 (Table 3). 161

We also performed MutChromSeq on the entire chromosome 2H assembly to rule out the involvement 162

of additional gene/s outside the defined Rph1 region that show a concordance of multiple independent non-163

synonomous mutations. As part of this analysis we assessed if: (i) reported SNPs were induced by sodium azide 164

mutagenesis (i.e. G>A or C>T), (ii) whether the contig reported contains predicted high confidence (HC) coding 165

regions, and (iii) whether the reported mutations are located in a coding region of aligned genes. We identified 166

45 candidate contigs across the entire Sudan chromosome 2H containing mutations. Further examination 167

determined that 31 of the 45 contigs either carried no predicted coding genes or that the identified mutations 168

were not located in predicted genes. In a further five contigs where mutations were identified in genes, manual 169

checking determined they were not induced by Sodium Azide and were therefore considered false positives. The 170

remaining contigs carried only a single mutation within a candidate HC gene, however these mutations were 171

likely non-functional. Scaffold_2895 identified initially in the 1.3-kb region of interest remained the only 172

plausible Rph1 candidate based on the presence of multiple independent non-synonymous mutations. 173


https://apex.ipk-gatersleben.de/apex/f?p=284:45:::NO::P45_GENE_NAME:HORVU2Hr1G006480.6


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The Rph1 resistance gene in Sudan encoded for an NLR receptor protein (981 amino acid residues) with a 174

predicted Rx coiled-coil domain and carried a single intron in the nucleotide binding-site domain, which is 175

commonly found in NLRs in the Triticeae sub-tribe (Streuernagel et al., 2018) (Fig. 3). Phylogenetic analysis 176

comparing the full-length Sudan Rph1 protein sequence with that of previously cloned Triticeae NLRs 177

determined that Rph1 was more closely related to the MLA clade than other more divergent rust- and mildew-178

resistance NLRs, mainly from bread wheat (Fig. 4). The closest orthologue to Rph1 was an Arabidopsis RPM1 179

NLR homologue from T. urartu, which shared 89% amino acid identity. Further sequence comparison of the 180

Sudan resistance allele with three barley cultivars all lacking Rph1-mediated resistance and with available 181

genomic sequence (Morex, Bowman and Barke) identified seven amino acid substitutions that were common 182

amongst the susceptible accessions. 183

Rph1 barley differential lines Sudan and Berg are known to carry the same race specificity in response to 184

multiple Australian- and American-derived P. hordei pathotypes; however, the immune (Im) infection type 185

displayed by Berg when challenged with Rph1-avirulent isolates was different from the hypersensitive response 186

(HR) necrosis observed in Sudan. We therefore hypothesised that the R genes carried by Sudan and Berg might 187

be allelic at Rph1 or be different but carry closely linked genes. Rust tests using P. hordei pathotype 220 P+ 188

Rph13+ in a Sudan/Berg F3 population (n = 122) did not reveal any segregation (resistance vs susceptible); with 189

all families showing a non-segregating resistant pattern. The Chi-squared value (χ2

= 366) significantly 190

(p<0.0001) deviated from the segregation ratio expected for two independent genes (Table 2). No susceptible 191

individual was recovered amongst the entire progeny (n = 1,860 seedlings), indicating that the loci conferring 192

seedling resistance in both genotypes is most likely the same, i.e. allelic, or two physically proximal genes 193

linked in repulsion. The maximum recombination frequency between two alleles was estimated to be r = 1.2 at p 194

= 0.05. 195

We assessed the response of eight different barley lines (accessions and cultivars) postulated to carry 196

Rph1-mediated resistance with four P. hordei pathotypes with contrasting virulence to determine if they had the 197

Im or HR response characteristic of the resistance observed in Berg and Sudan, respectively (Table 1; 198

Supplementary Fig. 4). Tests indicated that five lines had the HR response and two lines (UWA Seln 8861 and 199

HOR15560) were Im as observed for Berg. We sequenced the Rph1 gene in these three Im lines (Berg, UWA 200

Seln 8861 and HOR15560) and three HR lines (CI 9214, ISR950.13 and CIho 119558) to confirm the haplotype 201

of resistant parent CI 9214 and to determine whether there was any molecular correlation between the 202

haplotypes of lines with the Berg (Im) vs. Sudan (HR) phenotypes. The results revealed that both different 203

phenotypes are not determined by their Rph1.a allele sequence. For example the CI 9214 (HR) and HOR15560 204

(Im) alleles were identical to that in Sudan (HR), in contrast Berg (Im), CIho 119558 (HR), ISR950.13 (HR) and 205

UWA seln 8861 (Im) all carried the susceptibility allele, suggesting their resistance is conferred by a different 206

gene (Table 1). 207



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9

Discussion 211

Understanding and exploiting the mechanisms that underpin important agronomic traits such as resistance to 212

biotic and abiotic stresses is only possible through identifying variants at the molecular level that define their 213

genetic control. Chromosome sorting and sequencing of wild type and multiple independent mutants, referred to 214

as MutChromSeq, provides a lossless complexity reduction method suitable for the cloning of any gene of 215

interest (Sánchez-Martín et al., 2016; Steuernagel et al., 2017). In this study, we used this approach to clone the 216

leaf rust resistance gene, Rph1, from cultivated barley. Rph1 was an attractive target due to the ability to reliably 217

phenotype mutants with ablated resistance. We determined that in both the CI 9214/Stirling and the CI 218

9214/Baudin mapping populations, Rph1 was inherited as a monogenic trait. Although there was no requirement 219

for recombination-based genetic mapping, we used MTA analysis (>10,000 DArT-Seq markers) and mapped 220

Rph1 to the short arm of chromosome 2H in the CI 9214/Stirling DH population, confirming previous trisomic 221

analysis by Tuleen and McDaniel (1971). The coupling of MutChromSeq with genetic mapping in this study 222

reduced the size of the genomic region interrogated and the number of mutants required. This is particularly 223

important for diploid organisms, such as barley, where generating multiple independent knock-outs in the same 224

gene requires more work (i.e. generating and screening of larger mutant populations) compared to that in a 225

polyploid organism, such as bread wheat. 226

The MutantHunter pipeline reported in Sánchez-Martín et al. (2016) was modified to search for 227

candidates within the 1.3-Mb region harbouring Rph1 on chromosome 2HS. We identified multiple independent 228

non-synonymous mutations within a gene on a single contig (Scaffold_2895). It was expected, however, that 229

other sodium azide-induced mutations would also be identified outside the regions of interest. Therefore, we 230

mapped the same mutant reads to the entire Sudan chromosome 2H assembly and identified the same Rph1 231

candidate on Scaffold_2895, thus validating our targeted approach and ruling out the involvement of other genes 232

outside the defined Rph1 region. Nevertheless, numerous contigs (45) were identified outside the target region 233

harbouring mutations that, following further examination, were ruled out as candidates due to either (i) the 234

absence of coding sequence, (ii) mutations not in coding genes, (iii) false positives or (iv) single non-function 235

mutations within genes. Due to the higher N50 of the present study (20.1 kb), this number is higher than that 236

reported in the study of Sanchez-Martin et al (2016) where the N50 was 1.4 kb. Taken together, we identified the 237

Rph1 resistance gene candidate on the short arm of chromosome 2H based on the sequence comparison of three 238

rph1 mutants with wild-type Sudan. All three mutations were confirmed by Sanger sequencing in addition to a 239

further two independent mutants derived from additional spikes tested at a later stage. Consequently, based on 240

the confirmation of five non-synonomous mutations, we now refer to this gene as Rph1. 241

Rph1 encodes for a predicted coiled-coil NLR receptor protein. Phylogenetic analysis in our study 242

suggested that Rph1 was located in a separate clade and is likely representative of a sub-family of NLRs that is 243

distinct from other recently cloned rust- and mildew-resistance NLR proteins from Triticeae. Recent cloning 244



10

studies in wheat have determined that stem rust (Sr33 and Sr50) and leaf rust (Lr22a) protein sequences show 245

marked similarity to previously characterised NLR families such as Mla from barley and RPM1 from 246

Arabidopsis, respectively (Periyannan et al., 2013; Mago et al., 2015; Thind et al., 2017). The closest known 247

orthologue to Rph1 was an RPM1-like NLR protein from Triticum urartu (89% sequence identity), suggesting 248

both shared a common ancestor; however, we show that Rph1 showed greater similarity to the Mla family 249

relative to that for Lr22a. Although Lr22a was located in a syntenic region on chromosome 2DS to Rph1, 250

bioinformatics analysis using the 2016 Morex genome browser suggests the true orthologue of Lr22a and RPM1 251

is located approximately 1 Mb downstream from the Rph1 gene. Interestingly, the predicted protein sequences 252

of Rph1 and TuRPM1 carried an Rx-like coil-coiled domain at the N-terminal that has been shown to be 253

essential for resistance against virus X in potato (Bendahmane et al., 2002). 254

The NB‐ARC domain of NB‐LRR proteins is known to act as a molecular switch that regulates their 255

activity. Previous characterization of loss‐of‐function mutants suggests that the GLPL motif functions as a 256

hinge, facilitating nucleotide‐dependent movement of the flanking helices, and that the ARC1 sub-domain 257

transmits these conformational changes to the other parts of the protein (Leipe et al., 2004). Dodds and 258

colleagues (2001) determined that a glycine to glutamic acid substitution in the highly conserved GLPL motif of 259

the P2 NLR protein from flax (Linum sativum) compromised resistance to flax rust (Melampsora lini). The HR 260

induced by transient expression of the Rx NLR from potato (Solanum tuberosum) was inhibited by the presence 261

of two mutations targeting the glycine and proline residues of the GLPL motif (Bendahmane et al., 2002). We 262

identified the same mutational variant as Dodds et al. (2001) in our study for Rph1 mutant M767. We also 263

identified a second mutation six amino acids downstream from the GLPL motif, suggesting that this conserved 264

region is critical for Rph1-mediated resistance. Interestingly, three mutant families derived from different M2 265

spikes shared the same mutation in the LRR domain that caused a glycine to change to an aspartic acid. It is 266

likely these M2 spikes were derived from the same meristem cell from a single M1 plant and hence carry the 267

same mutation that are therefore not independent. Sanger sequencing of the full-length coding sequence in our 268

study failed to detect mutations in M544 and M483, suggesting these families possibly either carry mutations 269

within the regulatory sequences of Rph1 or possibly in a secondary-site repressor. Previous studies in wheat 270

(Feuillet et al. 2003; McGrann et al., 2014), barley (Torp and Jørgensen 1986) and Arabidopsis (Tornero et al., 271

2002) indicated that second site or extragenic mutants during R gene loss-of-function screens was a common 272

occurrence. 273

Genes that confer pathogen defence are often clustered in plant genomes, evolving via duplication, 274

diversifying selection through mutation and transposon-insertion events. In barley, the best example of this is 275

the MLA locus, which is organised into three gene-rich islands separated by retro-transposable elements (Wei et 276

al., 2002). Such gene clusters in plants often comprise allelic series or represent closely related genes with 277

distinct recognition specificities. Rph1 was one of the four clustered NLRs in Morex; however, the 278



11

corresponding homologous 22-kb scaffold 2825_2 from Sudan carried two full-length NLRs from Morex 279

separated by only 2 kb relative to 80 kb in Morex (Supplementary Fig. 3). Taken together, Rph1 appears to be 280

part of a complex resistance locus (Supplementary Figure 4). In wheat, three closely linked stripe rust resistance 281

genes were recently cloned using MutRenSeq based on the presence of multiple independent mutants in each of 282

the three genes (Marchal et al., 2018). Yr5 and Yr7 were originally hypothesised to be allelic and closely linked 283

with YrSP (Zhang et al., 2009); however, molecular analysis performed on this complex locus on chromosome 284

2B determined that the Yr5- and Yr7-mediated resistance were each conferred by neighbouring paralogous NLR 285

genes (Marchal et al., 2018). In contrast to that for Yr5 and Yr7, Sudan and Berg in our study share the same 286

recognition specificity in response to all Australian and North American P. hordei isolates tested, but differ in 287

the infection type, with Berg displaying immunity and Sudan being characterised by HR necrosis. An allelism 288

test between Sudan and Berg determined phenotypically that no recombinants were found that gave rise to 289

susceptible individuals, indicating that the two genes are either closely linked in repulsion or allelic. Direct 290

comparison of the Rph1 protein sequence between Sudan and three sequenced barley genotypes lacking 291

functional Rph1 (Morex, Bowman and Barke) identified seven amino acid substitutions that are different 292

between the resistant and susceptible alleles. Sanger sequencing of the Rph1 gene using six barley accessions, 293

including CI 9214, Berg, HOR15560, UWA seln 8861, ISR950.13 and CIho 11958, revealed that both CI 9214 294

and HOR15560 Rph1 alleles were identical to that in Sudan (Rph1.a); however, Berg and the remaining three 295

accessions carried the same susceptible haplotype as that in Morex, Bowman and Barke with no correlation 296

between Rph1 haplotype and infection type. The observation that Berg has the Rph1 haplotype that is associated 297

with multiple susceptible lines suggests there may be another gene conferring resistance to P. hordei in Berg 298

that is epistatic to the susceptible Rph1 haplotype. It is therefore more likely that the Berg resistance gene is not 299

an allele of Rph1 as hypothesised but likely, as in the case for Yr5/Yr7, a closely linked or neighbouring NLR 300

gene. As we did not generate mutants for Berg, we can only speculate that the resistance present in Berg forms 301

part of the same NLR cluster as that for Rph1-mediated resistance. We further hypothesise that due to 302

overlapping specificity, possibly the resistance genes present in Sudan and Berg recognise the same avirulence 303

product in P. hordei. 304

The major bottleneck for gene cloning in cereal crops is the development of high-quality genomic 305

sequence from the genotype carrying the trait. We significantly improved the wild-type cv. Sudan assembly of 306

chromosome 2H and increased the N50 value by 15-fold, from 1.4 kb (Sánchez-Martín et al., 2016) to 20.1 kb. 307

We compared the quality of chromosome 2H assemblies for Sudan and Foma (Sánchez-Martín et al., 2016) 308

relative to that of the 2D Dovetail assembly reported by Thind et al. (2017) by performing a Benchmarking 309

Universal Single-Copy Orthologues (BUSCO) analysis (Simão et al., 2015) (http://busco.ezlab.org) and by 310

mapping all predicted high confidence (HC) genes to the respective chromosome two assemblies 311

(Supplementary Table 1A; Supplementary Table 1B). All forms of analysis indicated that not using MDA 312


http://busco.ezlab.org/


12

prior to Illumina sequencing and library construction improved the overall assembly quality in wild-type Sudan. 313

Sánchez-Martín and colleagues were able to successfully clone a gene from both wheat and barley with an 314

average N50 of 1.4 kb, meaning that 50% of the chromosome was assembled with contigs of 1.4 kb or longer. 315

The full-length Pm2 gene in wheat, however, is >4 kb, suggesting that the contig harbouring Pm2 was likely 316

derived from a rather small frequency of large sequence contigs. Methods such as MutChromSeq and the 317

recently developed TACCA are unique as they generate cultivar-specific sequence information which allows the 318

functional exploration of sequences not found in a reference genome (Steuernagel et al., 2016, Thind et al., 319

2017). Although our reported N50 is far from comparable to the recently developed Chicago long-range 320

sequencing technology, it permits a low-cost effective haplotype analysis of non-reference genomes. 321

Furthermore, our improved wild-type chromosome assembly provides increased confidence when cloning genes 322

with large introns using the MutChromSeq approach. 323

In conclusion, recently developed genomic methodologies such as MutChromSeq, TACCA, MutRenSeq 324

and AgRenSeq can now be used to mitigate the limitations of traditional map-based cloning approaches in crop 325

plants. We used MutChromSeq to clone Rph1, which confers leaf rust resistance in barley. Seven amino acid 326

changes were identified as diagnostic for resistance and susceptibility, enabling the prospect of enhanced 327

marker-assisted selection. Although virulence for Rph1-mediated resistance is present at varying frequencies in 328

global P. hordei pathogen populations, identifying the basis of resistance in a wide array of R genes from crops 329

will allow effective pyramiding of multiple resistances into elite crop varieties. The rapid introduction of 330

multiple favourable disease-resistance alleles in plants can also now be accelerated because of the emergence of 331

new breeding technologies such as gene editing coupled with speed breeding (Ghosh et al., 2018; Watson et al., 332

2018). Future work will also involve determining the effectiveness of Rph1-mediated resistance in response to 333

other diseases in crops such as wheat, maize and rice using a transgenic approach. 334

335

336

337



13

Materials and Methods 338

Plant and pathogen materials 339

The barley cultivar CI9214 was postulated to carry Rph1, whereas cultivars Baudin (Rph9.z) and Stirling 340

(Rph9.am) were known to lack Rph1 based on seedling response in multi-pathotype tests. Two barley mapping 341

populations were produced to map the Rph1 resistance gene, including a CI 9214/Stirling (258 lines) doubled 342

haploid (DH) population and a recombinant inbred line (RIL) population derived from the cross CI 9214/Baudin 343

(385 lines). Both populations were sourced from the Plant Breeding Institute–University of Sydney. For tests of 344

allelism, barley leaf rust differential genotypes cvs. Sudan with Berg were crossed to produce F1 seed. Each F1 345

plant was then selfed to produce F2 seed and 150 F2 seeds derived from a single F1 plant were randomly selected 346

and space planted, then selfed in the field in 2017 and 130 F3 families were harvested for rust testing. 347

The four pathotypes of P. hordei used in the study, along with their virulence/avirulence profiles, are 348

listed in Table 1. Both mapping populations and a collection of barley accessions postulated to carry Rph1 were 349

phenotypically assessed separately with the four P. hordei pathotypes, which have contrasting virulence. We 350

used two Rph1-avirulent [4610P+ and 220P+] and two Rph1-virulent [5457P+ and 253P-] pathotypes, 351

respectively, to rule out the involvement of known all-stage resistance genes in parental genotypes Stirling 352

(Rph9.am) and Baudin (Rph12). 353

Statistical analyses 354

The Chi-squared (χ2) test was used to determine the goodness-of-fit between the phenotypic data recorded from 355

disease infection types versus expected genetic ratios. 356

Inoculation procedure and disease assessment 357

Seedlings were inoculated as described by Dracatos et al. (2014) for both mapping and mutant populations. 358

Infection types were recorded 10 days post inoculation using the “0” to “4” scale (Park and Karakousis 2002). 359

Infection types of test lines of each population were compared with those displayed by the parents and barley 360

differential lines to assure accurate classification into resistant and susceptible classes. 361

Mapping Rph1 in the CI 9214/Stirling and CI 9214/Baudin mapping populations 362

Genomic DNA was extracted from the leaf tissues of a single plant from a subset of 61 CI 9214/Stirling DH 363

lines and 92 CI 9214/Baudin RILs from both mapping populations, using CTAB method as described by Fulton 364

et al. (1995). The DNA was prepared and shipped to DArT (Diversity Arrays Technology, Canberra, Australia) 365

for genotypic analysis as detailed on their website www.diversityarrays.com.au. 366

Marker-trait analysis of closely linked DArT markers at the Rph1 locus 367

The phenotypic data using P. hordei pathotype 4610 P+ was converted to binary data (susceptible 3+ = 0, 368

resistant ;1-CN = 1). Marker-trait analysis of each DArT-Seq marker with the Rph1 phenotype was conducted 369


http://www.diversityarrays.com.au/


14

by computing Fisher’s exact test on 2 X 2 count tables using R statistical software (www.r-project.org). The null 370

hypothesis was that the DArT-Seq marker genotypes were not associated with resistance to P. hordei; hence a 371

random distribution of genotypes in the resistant and susceptible phenotypic groups. The log10 of P values were 372

plotted against the positions on the physical Bowman genome assembly by means of chromosome-wise and 373

genome-wide ‘Manhattan’ plots. DArT-Seq markers associated with the Rph1 resistance gene are detailed in 374

Supplementary Table S3. 375

Generation of mutant population and phenotypic analysis 376

The mutagenesis procedure was performed according to that described in Chandler and Harding (2013) with 377

some modifications. Approximately 2,500 seeds of barley cultivar Sudan were immersed in water at 4°C 378

overnight. The imbibed seed were transferred to a 2-L measuring cylinder filled with water and aerated with 379

pressurised air for 8 h, with one change of water after 4 h. The water was drained. Seeds were incubated in a 380

shaker for 2 h in freshly prepared 1 mM sodium azide dissolved in 0.1 M sodium citrate buffer (pH 3.0), washed 381

extensively in running water for at least 2 h, and placed in a fume hood to dry overnight. Seeds were sown in 382

pots. After two weeks, pots were transferred to an outside standout area. After another two weeks, seedlings 383

were space transplanted to the field. Approximately 9,400 spikes were harvested from ~1,700 M1 plants, i.e. on 384

average 5–6 spikes/plant. Because each tiller is usually derived from independent (genetically distinct) meristem 385

cells in the seed embryo (Stadler 1928), the M2 seeds were threshed from single spikes. 386

The Sudan M2 spikes and M2-derived M3 families were phenotypically assessed using the Rph1-387

avirulent pathotype 4610 P+. In all cases at least two susceptible plants were transplanted for each candidate M2 388

family segregating for Rph1 knockouts for progeny testing. All sequence-confirmed mutants were progeny 389

tested at both the M3 and M4 generations and found to be homozygous susceptible. Sanger sequence 390

confirmation of all mutants was performed using sequence specific primers designed to capture both exon 391

regions of the Rph1 candidate gene. 392

Flow sorting and preparation of chromosomal DNA 393

Suspensions of intact mitotic chromosomes were prepared as described by Lysák et al. (1999). Briefly, root tip 394

meristem cells were synchronized using hydroxyurea, accumulated in metaphase using amiprophos-methyl and 395

mildly fixed by formaldehyde. Chromosome suspensions were prepared by mechanical homogenization of 50 396

root tips in 1 mL ice-cold LB01 buffer (Doležel et al., 1989). Chromosome analysis and sorting was done on a 397

FACSAria II SORP flow cytometer and sorter (Becton Dickinson Immunocytometry Systems, San José, USA). 398

Barley 2H chromosomes were sorted after bivariate analysis of DAPI fluorescence and fluorescence of GAA 399

microsatellites labelled with FITC using fluorescence in situ hybridization in suspension (FISHIS) (Giorgi et al., 400

2013). 401

Illumina library construction and sequencing 402



15

Flow-sorted chromosomes were treated with freshly prepared proteinase K and purified on Microcon YM-100 403

columns (Millipore Corporation, Bedford, USA). For 2H chromosomes from mutant lines, DNA was amplified 404

by multiple displacement amplification (MDA) using Illustra GenomiPhi V2 DNA Amplification Kit (GE 405

Healthcare, Giles, United Kingdom) as described by Šimková et al. (2008). Amplified DNA was then 406

fragmented by a Bioruptor sonication device (Diagenode, Liege, Belgium) and used to prepare sequencing 407

libraries with TruSeq DNA PCR-Free Library Prep kit (Illumina, San Diego, USA). For 2H chromosome of cv. 408

Sudan (wild type), non-amplified DNA (16 ng) was directly fragmented with a Bioruptor sonication device and 409

subsequently used to prepare a sequencing library with the NEBNext UltraII DNA library Prep Kit for Illumina 410

(New England Biolabs, Ipswich, USA). Pooled libraries of wild-type and five mutant chromosomes were 411

sequenced on an Illumina HiSeq in Rapid Run mode to gain 2 x 250-bp paired-end reads. Trimmomatic was 412

used to remove sequencing adaptors and trim raw reads (LEADING: 20 TRAILING: 20 SLIDINGWINDOW: 413

4:15 MINLEN: 100). The assembly of the wild-type chromosome sequence was performed with Meraculous 414

(Chapman et al., 2011) using k-mer size 111. 415

MutChromSeq 416

We extended the functionality of the MutChromSeq (Sánchez-Martín et al. 2016) pipeline by adding the 417

possibility to filter for a set of reference scaffolds. The updated pipeline is available at GitHub 418

(https://github.com/steuernb/MutChromSeq). In the specific case of Rph1, we used available mapping 419

information. In relation to the barley reference genome sequence of cultivar Morex (Mascher et al., 2017), this 420

was on chromosome 2H between nucleotide positions 13,139,911 bp and 14,361,439 bp. All genes that had 421

been annotated within that interval were aligned to scaffolds from our Sudan assembly of 2H. The list of 422

scaffolds with the best alignment for each gene were used as an additional filter for the updated MutChromSeq 423

pipeline. The Sudan 2H assembly was masked for repeats using RepeatMasker (http://repeatmasker.org) with 424

external repeat library TREP (http://wheat.pw.usda.gov/ITMI/Repeats) (Wicker et al., 2002). Raw data from 425

flow sorted chromosomes of wild type and mutants were quality trimmed using Trimmomatic (Bolger et al., 426

2014). Trimmed reads were aligned to repeat-masked reference using BWA (Li and Durbin 2009), version 427

0.7.12. Mappings were further processed using SAMtools (Li et al., 2009), version 0.1.19, and the following 428

sub-programs. Parameters diverging from default are mentioned below: samtools view -Shub -f 2 input.sam 429

output.bam; samtools sort; samtools rmdup; samtools index; samtools mpileup -B -Q 0 -f 430

Sudan_2H.masked.fasta. Pileup formatted files for wild type and mutants were converted to MutChromSeq 431

input with Pileup2XML.jar -c 5 -a 0.7. Finally, MutChromSeq.jar was executed with -n 2 -c 5 -a 0.1 -z 1. The 432

candidate contig was manually inspected using IGV 433

(http://software.broadinstitute.org/software/igv/book/export/html/6). 434

Phylogenetic analysis 435


https://github.com/steuernb/MutChromSeq

http://wheat.pw.usda.gov/ITMI/Repeats

http://software.broadinstitute.org/software/igv/book/export/html/6


16

The predicted Rph1 amino acid sequence was used as a query in GenBank using BlastP to identify closely 436

related sequences. The Rph1 amino acid sequence was then compared with that of related NLR sequences from 437

Triticeae including: Aegilops tauschii (Ata) (Lr21-AAP74647.1 and Sr33-AGQ17384.1) Secale cereale (Sc) 438

(Sr50-ALO61074.1), Triticum aestivum (Ta) (Lr22a-ARO38244.1, Sr22-CUM44212.1, Lr1-ABS29034.1, Sr45-439

CUM44213.1, Pm2-CZT14023.1, Pm3-ADH04488.1 and Pm8-AGY30894.1), T. urartu (Tu) (RPM1-like 440

EMS67965.1), Triticum monococcum subsp. monococcum (Tm) (Sr35-AGP75918.1 and MLA1-ADX06722.1), 441

Triticum dicoccoides (Td) (Lr10-ADM65840.1) and Hordeum vulgare (Hv) (MLA1-AAG37354.1, MLA6-442

CAC29242.1, MLA9-ACZ65487.1). An unrelated NLR from Arabidopsis, At5g45510-Q8VZC7.2, was 443

included as an out-group. A multiple sequence alignment was performed using ClustalW (Larkin et al., 2007), in 444

Geneious version 11.0.2 (https://www.geneious.com) with the BLOSUM scoring matrix, and settings of gap 445

creation at -10 cost, and gap extension at -0.1 cost per element. After removing all ambiguously aligned regions 446

using trimAl (Capella-Gutierrez et al., 2009) the final sequence alignment of length 1,026 amino acids (n=19) 447

was determined. A phylogenetic tree based on this alignment was then inferred using the Neighbor-Joining 448

method in the Geneious Tree Builder software, employing the JK genetic distance model. Bootstrap support for 449

individual nodes was generated using 1000 bootstrap replicates. 450

451

Supplemental Data 452

Supplemental Figure S1. Genome-wide marker-trait association analysis in the CI 9214/ Stirling doubled haploid population. 453

Supplemental Figure S2. Bi-parametric flow karyotype of barley cv. Sudan 454

Supplemental Figure S3. Sequence comparison at the Rph1 locus between the Morex reference and wild type resistance donor 455

cv. Sudan. 456

Supplemental Figure S4. Supplementary Figure S4- Infection response of seven barley accessions postulated to carry leaf rust 457

resistance gene Rph1 458

Supplemental Table S1. Assessment of sequence assembly quality for chromosome 2H in barley cultivars Foma (Sanchez-459

Martin et al. 2016) and Sudan and chromosome 2D in wheat cultivar Campala (Thind et al. 2017) using (A) BUSCO and (B) 460

mapping all predicted high confidence genes 461

Supplemental Table S2. Summary table of most closely associated DArT-Seq markers at the Rph1 locus on chromosome 2H 462

463

464

465

466

467

468

469

470


http://www.geneious.com/


17

Table 1. Infection response data of selected barley genotypes previously postulated to carry the Rph1 resistance gene tested 471

with four P. hordei pathotypes and their Rph1 sequence haplotype. 472

473

Accession 220P+1 5457P+

2 4610P+

3 253P-

4 Rph1 haplotype

CIho 11958 ;1-CN 3+ ;1-CN ;12C Susceptible

ISR950.13 ;1-CN 3+ ;1-CN 3+ Susceptible

Seln 8861 0;N 3+ ;N 3+ Susceptible

CI9214 ;1-CN 3+ ;1-CN 3+ Resistant

HOR 15560 0;N 3+ ;N 3+ Resistant

Sudan ;1-CN 3+ ;1-CN 3+ Resistant

Berg 0;N 3+ 0;N 3+ Susceptible

Bowman+Rph1 ;N 3+ ;N 3+ Resistant

Bowman5 3+ 3+ 3+ 3+ Susceptible

Stirling 3+ 3+ 3+ :1+C Susceptible

Baudin ;12-C 3+ 3+ ;12-C na

Gus5 3+ 3+ 3+ 3+ na

1 Pathotype 220P+ = avirulent on Rph1 and Rph12. 474

2 Pathotype 5457P+ = virulent on Rph1 and Rph12. 475

3 Pathotype 4610 P+ = avirulent on Rph1 and virulent on Rph12. 476

4 Pathotype 253 P- = virulent on Rph1 and avirulent on Rph12. 477

5 Susceptible controls. 478

6na = not applicable 479

480



18

Table 2. Segregation frequencies and genetic analysis of three mapping populations when inoculated with two barley leaf rust 481

pathotypes at seedling stage. 482

483

Population Generation Pathotype Number of

lines

Genetic

ratio

X2 P

Res Seg Sus

CI9214/Stirling DH 4610P+ 122 0 138 1:1A 0.99 >0.32

CI9214/Baudin RIL 4610P+ 168 0 194 1:1A 1.87 >0.17

Sudan/Berg F3 220P+ 122 0 0 7:8:1B 366.0 <0.0001

A = Res:Sus. 484

B = Res:Seg:Sus. 485

486



19

Table 3. Sodium azide induced mutations in the Rph1 candidate scaffold confirmed by Sanger sequencing. 487

488

bp position scaffold 2895_1 Mutational change Affected lines

Amino Acid Change

11, 416 G > A 763.2, 761.2, 727 Gly > Asp

12, 268 C > T 422 Gly > Asp

12, 298 C > T 767 Gly > Glu

12, 458 C > T 430.1 Ala > Pro

13, 365 G > A 199.2 Gly > Glu

489

490

491



20

Figure Legends 492

Figure 1 Monogenic inheritance for Rph1-mediated resistance in the CI 9214 x Stirling and CI 9214 x Baudin mapping 493

populations. 494

Seedling leaves of the infection types of (left to right): CI 9214 (C), Stirling (S), Baudin (B), C/S DH line (Rph1), C/S DH line 495

(rph1), C/B RIL (Rph1), C/B RIL (rph1) and susceptible control Gus inoculated with P. hordei pathotype 4610P+ (virulent on 496

Rph12 in Baudin, Rph9.am in Stirling and avirulent to Rph1 in CI 9214). 497

498

Figure 2 Marker trait association analysis in the CI 9214 x Stirling doubled haploid population maps Rph1 to the short 499

arm of chromosome 2H 500

Genome-wide Manhattan plot derived from marker-trait association (MTA) analysis using Fisher’s exact test on 2 X 2 count 501

table for seedling resistance to Puccinia hordei pathotype 4610P+ (binary scoring data) in the CI9214/Stirling doubled haploid 502

population using >10,000 DArT-Seq markers. The –log10 of P-values were plotted against the positions on the physical 503

Bowman genome assembly. The peaks above minimum threshold of 2 (P-value = 0.03) can be considered as significantly 504

associated. Vertical axis represents -log10 (P) values of the P-value of the marker-trait association. The colours blue and red 505

were used to differentiate between chromosomes (1H-7H, indicated by tick marks). 506

507

Figure 3 MutChromSeq and subsequent Sanger sequence confirmation of five susceptible rph1 knockout mutants 508

reveals that Rph1-mediated leaf rust resistance is conferred by a coil-coiled NLR gene on chromosome 2H. 509

Cloning of the barley Rph1 gene using MutChromSeq. A. Resistant Rph1 barley wild type donor cultivar Sudan, five sodium 510

azide-derived susceptible mutants (M199.2, M422, M430.1, M727 and M767) and the susceptible control Gus. B. Rph1 locus 511

showing intron–exon boundaries, protein domains and 5′ and 3′ untranslated regions (UTRs). Mutations identified by both 512

MutChromSeq and Sanger sequencing are indicated by red vertical lines, while mutations identified by Sanger sequencing of 513

additional mutants are indicated by black vertical lines. A number above the line indicates identical mutations occurring in 514

independent lines. CC, coiled-coil; NB-ARC, nucleotide-binding; LRR, leucine-rich repeat. 515

516

Figure 4 Phylogenetic analysis groups Rph1 in a separate cluster from other NLRs conferring rust resistance in cereal 517

crops 518

Neighbor-joining tree analysis of Rph1 from barley cultivar Sudan. The Rph1 amino acid sequence was then compared with 519

related NLR sequences from the Triticeae including: Aegilops tauschii (Ata) (Lr21-AAP74647.1 and Sr33-AGQ17384.1) 520

Secale cereale (Sc) (Sr50-ALO61074.1), Triticum aestivum (Ta) (Lr22a-ARO38244.1, Sr22-CUM44212.1, Lr1-ABS29034.1, 521

Sr45-CUM44213.1, Pm2-CZT14023.1, Pm3-ADH04488.1 and Pm8-AGY30894.1), T. urartu (Tu) (RPM1-like EMS67965.1), 522

Triticum monococcum subsp. monococcum (Tm) (Sr35-AGP75918.1 and MLA1-ADX06722.1), Triticum dicoccoides (Td) 523

(Lr10-ADM65840.1) and Hordeum vulgare (Hv) (MLA1-AAG37354.1, MLA6-CAC29242.1, MLA9-ACZ65487.1). 524



21

Statistical support for individual nodes was estimates from 1000 bootstrap replicates and values are represented as percentages 525

on the nodes (values of >70% are shown). The scale bar represented the proportion of site changes along each branch. 526

527



22

ACKNOWLEDGEMENTS 528

We thank Dr. Jan Vrána for chromosome sorting using flow cytometry and Ms. Zdeňka Dubská, Jitka Weiserová, Romana 529

Šperková and Helena Tvardíková for technical assistance. J.B., M.K., R.S and J.D. were supported by the Czech Ministry of 530

Education, Youth and Sports (award LO 1204 from the National Program of Sustainability I). BBHW and BS were supported 531

by the Biotechnology and Biological Sciences Research Council (BBSRC) Designing Future Wheat Cross-Institute Strategic 532

Programme (BB/P016855/1). PD, DS, HE, BC, SH and PZ were supported by the Grains Research and Development 533

Corporation and RFP by as the Judith & David Coffey chair of Sustainable Agriculture. 534

535



23

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https://www.ncbi.nlm.nih.gov/pubmed?term=Arora S%2C Steuernagel B%2C Chandramohan S%2C Long Y%2C Matny O%2C Johnson R%2C Enk J%2C Periyannan S%2C Hatta AM%2C Athiyannan N%2C Cheema J%2C Yu G%2C Kangara N%2C Ghosh S%2C Szabo LJ%2C Poland J%2C Bariana H%2C Jones JDG%2C Bentley AR%2C Ayliffe M%2C Olson E%2C Xu SS%2C Steffenson BJ%2C Lagudah E%2C Wulff BBH %282018%29 Resistance gene discovery and cloning by sequence capture and association genetics%2E BioRxiv&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Giorgi D%2C Farina A%2C Grosso V%2C Gennaro A%2C Ceoloni C%2C Lucretti S %282013%29 FISHIS%3A fluorescence in situ hybridization in suspension and chromosome flow sorting made easy%2E PLoS One 8%3A e&dopt=abstract

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https://scholar.google.com/scholar?as_q=FISHIS: fluorescence in situ hybridization in suspension and chromosome flow sorting made easy.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Giorgi&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=International Wheat Genome Sequencing Consortium %28IWGSC%29 %282018%29 Shifting the limits in wheat research and breeding using a fully annotated reference genome%2E Science&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Kislev ME %281982%29 Stem rust of wheat 3300 years old found in Israel%2E Science%2E 216%3A 993%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=van&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Krattinger SG%2C Lagudah ES%2C Spielmeyer W%2C Singh RP%2C Huerta%2DEspino J%2C McFadden H%2C Bossolini E%2C Selter LL%2C Keller B %282009%29 A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat%2E Science 323%3A 1360%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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https://www.ncbi.nlm.nih.gov/pubmed?term=Kuang H%2C Wei F%2C Marano MR%2C Wirtz U%2C Wang X%2C Liu J%2C Shum WP%2C Zaborsky J%2C Tallon LJ%2C Rensink W%2C Lobst S%2C Zhang P%2C Tornqvist CE%2C Tek A%2C Bamberg J%2C Helgeson J%2C Fry W%2C You F%2C Luo MC%2C Jiang J%2C Robin Buell C%2C Baker B %282005%29 The R1 resistance gene cluster contains three groups of independently evolving%2C type I R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum%2E Plant J 44%3A 37%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Li H%2C Handsaker B%2C Wysoker A%2C Fennell T%2C Ruan J%2C Homer N%2C Marth G%2C Abecasis G%2C Durbin R %282009%29 GPDPS%2E The Sequence Alignment%2FMap format and SAMtools%2E Bioinformatics%2E 25%3A 2078%26%23x&dopt=abstract

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https://scholar.google.com/scholar?as_q=Flow karyotyping and sorting of mitotic chromosomes of barley (Hordeum vulgare L.).&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lys�?¡k&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1

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Zhang P, McIntosh RA, Hoxha S, Dong C (2009) Wheat stripe rust resistance genes Yr5 and Yr7 are allelic. Theor App Genet 120: 25–29Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title


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