Colocalization of genetic regions that confer resistance/susceptibility against Puccinia species and association with Pyrenophora teres loci within the barley genome

Abstract

Cereal rust diseases, including leaf, stem, and stripe rust, are some of the most devastating and economically important diseases of barley. However, host–pathogen genetic interaction research for each pathosystem is typically conducted independently and in isolation. Examples of host resistance/susceptibility genes functioning sympathetically to multiple pathogens or antagonistically to additional pathogens have been reported. Therefore, consolidation of loci that have been reported in multiple studies and across pathosystems is useful for variety development to maximize resistance to multiple pathogens and avoid inadvertent incorporation of susceptibility loci that act antagonistically to other pathogens. This review summarizes loci reported in three key biotrophic pathosystems of barley, including leaf, stem, and stripe rust. In conjunction with previously consolidated net blotch loci, this review lays the foundation for a wider barley rust resistance/susceptibility atlas. This review aims to inform breeders and researchers in rapidly identifying accessions and loci that need further characterization and which loci would be most useful to introgress into elite varieties.

Introduction

Cereals are staple crops the world over, providing calories and protein to the growing global population (Hubbard et al., 2015; Kearney, 2010). Currently, barley ranks as the second most-produced temperate cereal in the world after wheat (Thiel et al., 2021). Barley is primarily used as animal feed yet is the key ingredient in brewing beer and distilling premium whiskey by providing the necessary nutrients and enzymes for alcohol production (Sayre-Chavez et al., 2022). Beer ranks third for the most consumed beverage worldwide behind water and tea (Salanță et al., 2020), and its consumption plays a major role in the social fabric in many parts of the world. Thus, a secure supply of malting quality barley is essential to support the multibillion-dollar added value industry. Barley is also reemerging as a food crop due to its human health benefits (Tosh and Bordenave, 2020), and efforts are underway to develop modern biofortified and heart-healthy hulless barley varieties.

A major constraint to barley yield and quality is disease outbreaks. Due to climate change, environmental conditions have led to more severe epidemics in important barley production regions, preventing the crops from reaching their full potential and requiring additional inputs for disease management and mitigation (Dean et al., 2012; Xie et al., 2018). Rusts have been a major bane of cereal production and a part of human history since the beginning of agriculture. The Romans performed sacrificial ceremonies of Robigalia to appease the god of cereal rust diseases, Robigus (Saunders et al., 2019). In addition, all rust species mentioned in this review are macrocyclic and heteroecious (Bolton et al., 2008; Jin et al., 2010; Leonard and Szabo, 2005). Thus, countries have performed extensive eradication programs of barberry, the alternative host to multiple rust species, in an attempt to prevent sexual recombination and stabilize rust populations to slow the evolution of new races of rust species (Saunders et al., 2019). Although not calculated for barley, the economic impact of rusts on wheat is estimated to be $4.3–5.0 billion, 3.5% of the $145 billion economic value of worldwide wheat (Figueroa et al., 2018).

Cereal rust species are members of the genus Puccinia from the basidiomycota division of fungi that are obligate biotrophs (Bolton et al., 2008; Jin et al., 2010; Jin and Steffenson, 1999; Leonard and Szabo, 2005). There are four primary species of rust known to infect barley (Table 1): Puccinia coronata var. hordei (Pch), the causal agent of crown rust; Puccinia hordei (Ph), the causal agent of the leaf (brown) rust; Puccinia striiformis f. sp. hordei (Psh), the causal agent of the stripe (yellow) rust; and Puccinia graminis f. sp. tritici (Pgt), the causal agent of the stem (black) rust, all showing close phylogenetic relationships with other cereal rusts (Brueggeman et al., 2020; Dracatos et al., 2019b; Park et al., 2015). The notion of formae speciales (ff. spp.) separating specialized forms of a species that infect specific host species was developed by Eriksson (1894). However, this specialization does not hold true for some formae speciales, as the wheat stem rust pathogen Pgt also infects barley. Depending on local fluctuations in pathogen virulence and the deployment of inadequate resistance loci, leaf, stem, and stripe rust of barley all have the potential to cause incredibly damaging epidemics (Dean et al., 2012; Kleinhofs et al., 2009). In comparison, crown rust does not cause significant yield loss (Jin et al., 1992; Jin and Steffenson, 1999), and therefore is relatively understudied.

Two types of resistance are described within cereal rust pathosystems: seedling/all-stage resistance (ASR) effective throughout the plant’s life cycle and adult plant resistance (APR) effective at the postseedling stage. ASR genes are often considered race-specific and associated with the hypersensitive response, whereas APR genes are often incomplete, providing additive resistance (Dracatos et al., 2015a), that can result in near-immunity when sufficiently stacked (Huerta-Espino et al., 2020). Some resistance/susceptibility genes are involved in interactions with multiple pathogens, whether as sympathetic resistance to multiple diseases or antagonistic relationships of resistance/susceptibility to biotrophic and necrotrophic pathogens. Therefore, the ability to report colocalization of newly reported loci currently requires intimate knowledge of respective pathosystems or an extensive and therefore time-consuming literature review. Previously, the Barley Genetics Newsletters provided an excellent resource for this purpose; however, with high-resolution mapping and the sheer abundance of loci reported in the current barley community, this easily becomes unmanageable. Similar consolidations have been achieved for various pathogens of wheat (Amo and Soriano, 2022; Jan et al., 2021; Pal et al., 2022; Peters Haugrud et al., 2022; Soriano and Royo, 2015; Yu et al., 2014; Zheng et al., 2021). This review consolidates resistance/susceptibility loci for the three highly devastating pathogens of barley leaf, stem, and stripe rust and the lesser pathogen crown rust against the Morex V3 reference genome (Mascher et al., 2021) to lay a foundation for a larger resistance/susceptibility atlas incorporating the net blotch consensus maps (Clare et al., 2020).

Genetics to crown rust

Crown rust was first identified in 1991 in the USA (Jin et al., 1992) and designated a variety of P. coronata in 1999 (Jin and Steffenson, 1999). Barley crown rust has currently only been documented in the USA, Hungary, and China (Tian et al., 2021). To date, only the Reaction to Puccinia coronata 1 (Rpc1) locus has been reported against Pch on chromosome 3H in HOR 2596 (Agrama et al., 2004). Rpc1 was reported to colocalize with Rph5, Rph6, and Rph7 (leaf rust); Rp1-D (stem rust); Run6 (loose smut); rym4 and rym5 (barley mild mosaic virus); and Ryd2 (barley yellow dwarf virus) at the time (Agrama et al., 2004; Jin and Steffenson, 2002). However, refinement of Rph5, Rph6, and Rph7 loci has shown that Rpc1 colocalizes with Rph10 (Martin et al., 2020). Candidate gene analysis for Rpc1 is limited due to the use of proprietary markers that encompass a large 314 Mb (175.45 to 489.01 Mb) genomic interval (Supplementary Table 1).

Genetics to leaf rust

Leaf rust is often reported as one of the most devastating barley diseases, with yield losses up to 62% and routinely contributing up to 30% yield loss under conditions conducive to epidemic formation (Cotterill et al., 1992; Griffey et al., 1994; King and Polley, 1976). Despite barley infections primarily being Ph, leaf rust can also be caused by P. triticina (Pt), the causal agent of wheat leaf rust (Kleinhofs et al., 2009). The genetics of leaf rust resistance have been studied since the 1920s (Fazlikhani et al., 2019), with at least 80 Leaf rust (Lr) (Prasad et al., 2020) and 28 Reaction to Puccinia hordei (Rph; Table 2) loci (Mehnaz et al., 2021a) identified within wheat and barley, respectively. Additionally, there are a series of Rphq partial resistance loci with minor effects (Marcel et al., 2007, 2008; Qi et al., 1998, 1999, 2000; Yeo et al., 2017), not to be confused with the set of RphQ loci (Ziems et al., 2014). Rphq1-10 and Rphq20-21 were first identified in L94 × Vada, Rphq11-13 in L94 × 116-5, Rphq14-15 and Rphq22-23 in Steptoe × Morex, and Rphq16-19 in Oregon Wolfe Barley (Marcel et al., 2007, 2008; Qi et al., 1998, 1999, 2000; Yeo et al., 2017).

Due to the number of reported loci, barley Rph loci appear complex; however, further research has revealed multiple Rph genes are allelic variants. In addition, Rphq loci are often elevated and reclassified into Rph loci. Therefore, the true number of Rph loci currently stands at 25 (Martin et al., 2020). The RphD locus is not assigned to any chromosome (Marcel et al., 2008). Additionally, two collections of diverse barley lines were found to carry uncharacterized leaf rust resistance (Mehnaz et al., 2021b; Verma et al., 2018). There are also three QTL detected within a population between Blenheim and E224/3, but marker intervals were not reported (Thomas et al., 1995).

Chromosome 1H

Rph4 was first mapped to the short arm of chromosome 1H (McDaniel and Hathcock, 1969; Qi et al., 1998; Tan, 1978). Additionally, Rph_MBR1012, when first mapped, was not suspected to be Rph4 (König et al., 2012). Further work delimited Rph_MBR1012 to a 500 kb interval (2.1–2.6 Mb) in close proximity to Rph4 (Fazlikhani et al., 2019). Subsequent work delimited Rph4 to a 97-kb interval (0.08–0.17 Mb), distal to Rph_MBR1012, and therefore is a distinct locus (Martin et al., 2020). Rph26 was identified in the wild bulbous barley line A17 (Yu et al., 2018), mapping to a 7.2-Mb interval (508.42–515.21 Mb) that was also mapped in previous studies (Gutiérrez et al., 2015; Hickey et al., 2011). Additional loci identified on chromosome 1H include RphQ1, RphQ3, and RphQ4 (Ziems et al., 2014); qGH_PBIC_3.91 (Dracatos et al., 2019b); Qlr.HeB-5-1H (Schnaithmann et al., 2014), Rphq14 (Yeo et al., 2017); Rphq21 (Marcel et al., 2008); and Rphq22 (Yeo et al., 2017).

Chromosome 2H

The Rph1 gene was first reported in the experimental line Minn. II 12.15 and cultivar Sudan (Roane and Starling, 1967; Watson and Butler, 1947) on chromosome 2H (Tuleen and McDaniel, 1971). Rph1 is highly likely to have been mapped as qField_PBIC_2016_3.14 (Dracatos et al., 2019b), QPh.2H-1 (Vatter et al., 2017), and QRph5 (Ziems et al., 2014). Rph1 encodes a coiled-coil (CC) nucleotide binding site leucine-rich repeat (NLR) receptor protein (Dracatos et al., 2019a). Phylogenetic classification of RPH1 places the NLR in the C9 clade, which includes the rice NLR Pik-2 that functions with the NLR Pik-1 (C12 clade) to confer resistance to Magnaporthe oryzae (Ashikawa et al., 2008; Bailey et al., 2018). Sequencing of rph1 mutants determined five mutants carry Rph1 mutations, whereas two mutants lacked mutations in Rph1 (Dracatos et al., 2019a). This observation supports the hypothesis that additional loci, such as a second NLR, are required for Rph1-mediated resistance. Rph8 was first described in Egypt 4 as an ASR locus (Tan, 1977), despite Egypt 4 previously being used as a susceptible check (Martin et al., 2020). The Rph8 locus remains elusive and understudied due to the lack of avirulent isolates on Rph8 (Jin et al., 1996). As Egypt 4 is the only known source of Rph8, introgression into Bowman delimited the locus to a 10.6-Mb (28.81–39.24 Mb) or 1.0-Mb (49.00–50.00 Mb) interval under the assumption that Rph8 is not allelic to Rph14/15/16/17 (Martin et al., 2020). This region is highly complex, with current mapping efforts delimiting Rph8, Rph14, Rph15, Rph16, and Rph17 to the same region (Derevnina et al., 2015; Martin et al., 2020). Rph14 was identified in barley accession PI584760 (Jin et al., 1996) and mapped to an 8.8-Mb interval (40.17–49.00 Mb) (Golegaonkar et al., 2009; Martin et al., 2020). In contrast, Rph15 was first identified in wild accession PI355447 (Chicaiza, 1996), and Rph16 in wild accessions HS078, HS084 (Ivandic et al., 1998), HS688 (Perovic et al., 2004), and potentially HS677 (Kopahnke et al., 2004), as well as landrace HOR1063 (Kicherer et al., 2000). Subsequently, Rph15 and Rph16 were confirmed to be allelic (Weerasena et al., 2004), whereas Rph14 was believed to be an independent locus based on segregation ratios (Derevnina et al., 2015). More recent studies dispute this, suggesting Rph14 may be allelic to Rph15/16 with the single susceptible individual separating Rph14 from Rph15/16 as a potential admixture (Derevnina et al., 2015). Therefore, Rph14, Rph15, and Rph16 are predicted to be an allelic series (Derevnina et al., 2015), of which Rph15/16 has already been validated as encoding a CC-NLR with an integrated zinc finger BED domain (Chen et al., 2021), located at 43.32–43.33 Mb. RPH15 is found in clade C24 within a subclade of related NLRs with N-terminal integrated zinc finger BED domains, including the resistance proteins Xa1, Xo1, Yr5, Yr7, and YrSP (Bailey et al., 2018; Marchal et al., 2018; Read et al., 2020; Yoshimura et al., 1998). These results suggest five potential alleles: Rph14.ab and Rph14.am (previously RphZhu4); Rph14.an (previously Rph1063) (Kicherer et al., 2000); and Rph15.ad and Rph15.ae (previously Rph16) (Derevnina et al., 2015; Martin et al., 2020). The allele designations.am and.an had already been applied to Rph9.am (Dracatos et al., 2014) and Rph24.an (Ziems et al., 2017) and therefore need to be addressed in the future. Rph17 is confirmed to be independent of Rph14/15/16 (Derevnina et al., 2015), mapping to a 22.4-Mb interval (11.23–33.61 Mb) using H. bulbosum × H. vulgare hybrids (Pickering et al., 1998). However, Rph17 currently encompasses Rph1 (Dracatos et al., 2019a) and the proximal end of Rph8 (Martin et al., 2020). Additionally, Rph17 is known to cosegregate with Mildew locus from Hordeum bulbosum (Mlhb), a powdery mildew resistance locus (Pickering et al., 1998). Lastly, RphQ7 maps in close proximity to this complex region (Ziems et al., 2014). Rph18 was also mapped using H. bulbosum × H. vulgare hybrids; however, it mapped to a 10.1-Mb interval (655.49–665.59 Mb) (Pickering et al., 2000), encompassing the validated Rph22 gene (Wang et al., 2019). Rph22 was originally mapped as Rphq2 (Qi et al., 1998) but was subsequently high-resolution mapped (Johnston et al., 2013) and identified as a lectin receptor-like kinase (Wang et al., 2019). Rph22 was also most likely mapped by association mapping studies as QPh.2H-2 (Vatter et al., 2017) and two unnamed QTL (Czembor et al., 2022; Gutiérrez et al., 2015). Both the wild bulbous barley and cultivated barley alleles confer stronger resistance responses to bulbous and cultivated barley leaf rust isolates, respectively (Wang et al., 2019). Additional loci mapping to chromosome 2H include Qlr.HeB-F23-2H (Schnaithmann et al., 2014); Rphq11 and Rphq12 (Qi et al., 2000; Yeo et al., 2017); QLr.S42-2H.a and QLr.S42-2H.b (von Korff et al., 2005); and two unnamed QTL (Amouzoune et al., 2022; Castro et al., 2012).

Chromosome 3H

Initially, the loci Rph5, Rph6, and Rph7 were believed to be dispersed along chromosome 3H (Zhong et al., 2003); however, Rph5 and Rph6 are currently hypothesized to be allelic variants, whereas Rph7 remains an independent locus. The Rph5/Rph6 and Rph7 loci are delimited to 4.5-Mb (1.05–5.50 Mb) and 134-kb intervals (5.98–6.12 Mb), respectively, using introgression mapping (Martin et al., 2020). Subsequently, Rph7 was identified as a NAC transcription factor at ~ 6.03 Mb (Chen et al., 2023). Four of eight mutants carried mutations in Rph7, indicating that additional loci are involved in Rph7-mediated resistance (Chen et al., 2023). Rph10 and Rph11 were originally mapped to chromosomes 3H and 6H within wild barley accessions Bar Giyyora 30 and Maalot 17, respectively (Feuerstein et al., 1990). Rph10 was subsequently mapped to an 18.1-Mb (442.26–510.34 Mb) interval (Martin et al., 2020). However, within the Rph10 backcross accession BW683, there is additional donor DNA in close proximity (~ 5.9 Mb) to Rph11 on chromosome 6H. Therefore, there is debate as to whether Rph10 was present in previous mapping studies due to the paucity of marker saturation at the time (Feuerstein et al., 1990) and that resistance may have been contributed by Rph11 (Martin et al., 2020).

Rph13 was identified in the experimental line PI531849, derived from a wild barley accession backcrossed to the British cultivar Berac (Martin et al., 2020). Rph13 was confirmed to be distinct from Rph1-12 (Jin et al., 1996) and mapped to a 1.1-Mb interval (591.73–592.81 Mb) (Jost et al., 2020). Additional loci mapping to chromosome 3H include qRphFra-3H (D., Singh et al., 2015), Qlr.HeB-F23-3H (Schnaithmann et al., 2014), qGH_PBIC_3.86 (Dracatos et al., 2019b), and three unnamed QTL (Czembor et al., 2022; Hickey et al., 2011). Lastly, several QTL map to chromosome 3H but have been unanchored, including Rphq17 and Rphq20 (Marcel et al., 2007); Rphq23 (Yeo et al., 2017); QLr.S42-3H.a (von Korff et al., 2005); and three unnamed QTL (Castro et al., 2012; Rossi et al., 2006; Thomas et al., 1995).

Chromosome 4H

Rph21 (RphRic) was identified in Ricardo (Sandhu et al., 2012), mapping to an 18.2-Mb interval (569.19–587.48 Mb). Unnamed QTL (Hickey et al., 2011) and QPh.4H-1 and QPh.4H-2 (Vatter et al., 2017) also map in close proximity to Rph21. Rph27 identified in cultivar Quinn provides limited value, only being effective against two pathotypes. In addition, due to the fact that DArTseq markers without sequence or positions were utilized, Rph27 was positioned using the gene HORVU.MOREX.r3.4HG0331680 and the full-length cDNA clone AK250035.1 (Rothwell et al., 2020) to a 350-kb interval between 1.40 and 1.76 Mb. As 20 DArTseq markers were determined to be in complete linkage with Rph27 (Rothwell et al., 2020), the Rph27 region is most likely larger, and further high-resolution mapping will be required before validation. Additional loci mapping to chromosome 4H include Qlr.HeB-5-4H and Qlr.HeB-F23-4H (Schnaithmann et al., 2014); Rphq10 (Qi et al., 1999); Rphq19 (Marcel et al., 2007); Rphq20 (Marcel et al., 2008); and QLr.S42-4H.a (von Korff et al., 2005). Lastly, two loci map to chromosome 4H but remain unanchored in Rphq5 (Qi et al., 1998) and Rphq8 (Ziems et al., 2014).

Chromosome 5H

Rph2 (RphQ) was first identified in Halycon, Kaputar, and Q21861 (Borovkova et al., 1997; Park et al., 2003) and is currently delimited to a large 278-Mb interval (34.07–312.74 Mb) (Martin et al., 2020). Currently, there are at least 12 allelic variants of the Rph2 locus present in at least 20 barley accessions (Table 2). However, as this locus is further refined, allelic variants may in fact be independent genes separating Rph2 into multiple loci due to the paucity of markers and small population size. Due to the large interval currently encompassing Rph2, it may also correspond to qField_PBIC_2018_rep1_11.79, qField_PBIC_2016_3.99, qField_PBIC_2018_rep2_17.45, and qGH_PBIC_9.67 (Dracatos et al., 2019b); RphQ9 (Ziems et al., 2014); and two unnamed QTL (Czembor et al., 2022; Schnaithmann et al., 2014).

The Rph9 locus identified in Ethiopian landrace HOR 2596 was designated after allelism tests with Rph1-8 donor accessions (Tan, 1977). The Rph12 locus was subsequently mapped to chromosome 5HL using Triumph and believed to be distinct from Rph9 based on both different reaction types and segregation with allelism tests with HOR 2596 (Rph9) (Jin et al., 1993). However, using a population of 3,858 F₂ lines of Triumph × HOR 2596, no segregation could be identified and determined Rph9 (Rph9.i) and Rph12 (Rph9.z) to be allelic (Borovkova et al., 1998). Rph12 has also been identified in Franklin and Tallon (Park et al., 2003). The cultivar Cantala was subsequently identified to have an additional allele of Rph9 (Rph9.am) (Dracatos et al., 2014). The Rph9/12 locus is delimited to a 7.5-Mb interval (532.57–540.07 Mb) using introgression mapping within Bowman (Martin et al., 2020).

Rph20 (qRphFlag) and Rph24 (qRphND) were simultaneously mapped (Dracatos et al., 2021; Hickey et al., 2011); however, since intervals were not reported, determining the localization is troublesome. In addition, the DArT markers mapping Rph20 do not have significant homology to chromosome 5H and align to chromosome 4H in all Morex assemblies (Mascher et al., 2017, 2021; Monat et al., 2019). However, using lower-quality BLAST hits, Rph20 could be anchored to a 74.7-Mb interval (477.71–552.46 Mb) on chromosome 5H. Rph20 is believed to have been sourced from H. laevigatum or Gull that is subsequently present in derived accession Vada (Golegaonkar et al., 2009; Hickey et al., 2011; Hickey et al., 2012) and previously mapped as Rphq4 (Liu et al., 2011; Qi et al., 1998). Diagnostic markers developed to track Rph20 (Dracatos et al., 2021), map to chromosome 4H in all Morex assemblies (Mascher et al., 2017, 2021; Monat et al., 2019), which also may explain the inability to locate markers used by Hickey et al. (2011). Whether this region is misassembled in all Morex versions or other phenomena have occurred, such as a translocation relative to Morex, should be investigated. Based on this current information, Rph20 may also correspond to QPh.5H-1 (Vatter et al., 2017), RphQ10 (Ziems et al., 2014), and an unnamed QTL (Gutiérrez et al., 2015).

Rph25 (RphFT) was identified in the Chinese cultivar Fong Tein and Australian cultivar Yagan (Kavanagh et al., 2017). However, due to the use of reporting cM positions within a population and lack of sequence availability, Rph25 cannot be anchored to the Morex assembly. Rph28 (RphHEB) identified in wild barley was the most recently designated locus (Mehnaz et al., 2021a), mapping to an ~ 100-kb interval (562.28–562.92 Mb). Rph28 was most likely previously identified as an unnamed QTL (Schnaithmann et al., 2014).

Chromosome 6H

Rph11 was mapped to a 9.7-Mb interval (542.55–552.27 Mb) using introgression mapping but may also be allelic to Rph10 currently assigned to chromosome 3H (Martin et al., 2020), which was previously discussed. Rph24 (qRPhND) was mapped to a large 351 Mb region (Hickey et al., 2011) and subsequently, a 7.9-Mb region (358.56–366.40 Mb) using DArT markers (Ziems et al., 2017). Rph24 was also previously mapped as Rphq3 (González et al., 2012); QPh.6H-2 and QPh.6H-3 (Vatter et al., 2017); RphQ11 (Ziems et al., 2014); qRphYer2-6H (D., Singh et al., 2015); and multiple unnamed QTL (Castro et al., 2012; Czembor et al., 2022; González et al., 2012; Gutiérrez et al., 2015; Hickey et al., 2011; Qi et al., 1998; Ziems et al., 2014). Diagnostic markers targeting indels were subsequently developed to track Rph24 (Dracatos et al., 2021) in close proximity to the distal flank of the 7.9 Mb region. However, the fact that three distinct loci, QPh.6H-2, QPh.6H-3, and QPh.6H-4 (Sallam et al., 2017), were identified within the previously 351 Mb Rph24 interval (Hickey et al., 2011), suggests there may be additional resistance loci along the chromosome. Further investigation will be required to determine the true number of resistance loci in the region. Additional loci mapping to chromosome 6H includes QLr.S42-5H.a (von Korff et al., 2005), Rphq16 (Yeo et al., 2017), QPh.6H-1 (Vatter et al., 2017), qRphYer1-6H (Singh et al., 2015), three unanchored QTL (Castro et al., 2012), and unanchored Rphq15 (Marcel et al., 2007).

Chromosome 7H

The Rph3 gene was first reported in the cultivar Aim and subsequently Estate (Henderson, 1945; Roane and Starling, 1967). Rph3 was mapped to chromosome 7HL (Jin et al., 1993) and cloned as a small, unique, avirulence-dependent inducible membrane protein, reminiscent of TALE-activated executor resistance genes (Dinh et al., 2022). Rph3 exhibits increased diversity in wild accessions compared to domesticated germplasm (Dinh et al., 2022), most likely due to Rph3 being sourced from a wild accession. Rph3 can confer a strong hypersensitive response or incomplete resistance in the cultivar Ribari and barley accession L94, respectively (Martin et al., 2020). Rph19 was first identified in cultivar Prior, exhibiting the same resistance specificity as Reka 1 and mapped to a 2.8-Mb interval (618.14–620.92 Mb) (Park and Karakousis, 2002). Rph23 (qRphYer-7H) was identified within the Australian cultivar Yerong and believed to have originated from Russian landrace LV-Taganrog (D., Singh et al., 2015), mapping to a 14.9-Mb interval (25.49–40.36 Mb). Additional loci mapping to chromosome 7H include Rphq1, Rphq8, Rphq9, Rphq13, and Rphx (Qi et al., 1998); RphP/RphQ15 (Park and Karakousis, 2002; Ziems et al., 2014); RphQ2, RphQ12, RphQ13, and RphQ14 (Ziems et al., 2014); QPh.7H-1, QPh.7H-2, and QPh.7H-3 (Vatter et al., 2017); Qlr.HeB-F23-7H (Schnaithmann et al., 2014); and QLr.S42-7H.a (von Korff et al., 2005). Furthermore, five unnamed QTL map to chromosome 7H (Czembor et al., 2022; Gutiérrez et al., 2015; Rossi et al., 2006; Thomas et al., 1995), and one unnamed QTL remains unanchored to chromosome 7H (Hickey et al., 2011).

Association mapping

There have been six association mapping studies identifying leaf rust loci. The first association mapping study was conducted on 360 elite barley lines from Australia. A total of 11 of the 15 reported QTL were previously identified loci and four deemed novel (Ziems et al., 2014). The second association mapping study was performed in the Halle Exotic Barley (HEB)-5 nested association mapping (NAM) panel (Schnaithmann et al., 2014). At the time, only one novel QTL was identified with remaining loci corresponding to previously characterized Rph loci (Schnaithmann et al., 2014). The third association mapping study was conducted in Latin American barley, identifying two novel QTL out of six loci detected (Gutiérrez et al., 2015). The fourth was conducted with the HEB-25 NAM panel, a significant expansion of the HEB-5 population, identifying a total of two novel loci out of 11 (Vatter et al., 2018). The fifth association mapping study identified six QTL (Czembor et al., 2022), with the most significant marker-trait association (MTA) mapping within 1.2 Mb of RphQ11 identified on chromosome 6H (Ziems et al., 2014) and therefore is unlikely to be novel. The last association mapping conducted ASR and APR, claiming 58 MTA, 32 of which were novel. However, based on the low LOD thresholds utilized, it could be argued that all but seven of the MTA detected should be considered significant. In addition, these seven MTA are within a 7-Mb interval, suggesting all markers may form a single locus (Amouzoune et al., 2022).

Genetics to stem rust

The stem rust pathogen Pgt contains the largest host range within Puccinia with 28 hosts and is the primary cause of barley and wheat stem rust (Dracatos et al., 2015b). Stem rust is unique in that a barley-specific ff. spp. has not been identified. In addition, other ff. spp. are known to infect barley, including Puccinia graminis f. sp. secalis (Pgs), Puccinia graminis f. sp. avenae (Pga) (Brueggeman et al., 2020; Dracatos et al., 2015b), and a Pgt × Pgs hybrid known as Scabrum rust arising on triticale (Park, 2007). Barley stem rust epidemics in North America during the 1920s–1930s resulted in yield losses between 15% and 20% (Steffenson, 1992); however, 100% yield loss has been reported in wheat to the Digalu (Pgt race TKTTF) lineage (Singh et al., 2015). Due to the widespread deployment of Rpg1, barley stem rust epidemics were largely controlled until the late 1980s when Pgt race QCCJB overcame Rpg1 (Sharma Poudel et al., 2018). In addition, the Ug99 (race TTKSK) lineage of Pgt isolates overcame Sr31 in wheat and is seen as a major threat to global food security with 80%–95% of worldwide acreage of wheat considered susceptible (Singh et al., 2015). In addition, over 95% of barley cultivars and wild accessions surveyed are considered susceptible (Hatta et al., 2021; Prins et al., 2020; Steffenson et al., 2017). Due to effective resistance gene deployment and adequate disease management over the past 75 years, stem rust was not considered a major threat despite its enormous potential to devastate barley and wheat crops (Singh et al., 2011). The first reported epidemics in over 60 years in the UK and the first in decades across Germany and Sicily have caused devastating damage (Edae and Rouse, 2020; Lewis et al., 2018). Reports have also found Pgt isolates becoming more aggressive at both warmer and cooler temperatures (Lewis et al., 2018). Alarmingly, the first isolates with virulence on Rpg1 and rpg4/Rpg5 when stacked together in barley line Q21861 were recently reported in the Pacific Northwestern region of North America (Upadhaya et al., 2021).

Genetic studies describing stem rust resistance have been reported since the 1930s (Powers and Hines, 1933). Over 60 Stem rust (Sr) resistance loci have been designated within wheat, with at least nine identified and validated (Chen et al., 2018; Hatta et al., 2021). Multiple wheat stem rust resistance genes can remain functional in a susceptible barley background to provide resistance against Pgt. For example, the wheat genes Sr22, Sr33, Sr35, and Sr45 all provide resistance to the Pgt race TTKSK when transformed into the susceptible barley background of Golden Promise (Hatta et al., 2021). In comparison, only nine Reaction to Puccinia graminis (Rpg, Table 3) loci have been identified within barley (Hatta et al., 2021). Rpg1-rpg4, rpg6-Rpg7, and RpgU were first identified against Pgt, whereas Rpg5 and rpgBH were identified against Pgs (Zhou et al., 2014). The RpgU locus was identified in Peatland, Husky, and Diamond (Fox and Harder, 1995) and potentially SB90585 (Harder and Legge, 2000); however, the locus was never mapped. Based on segregation ratios, RpgU is not Rpg1, and most likely not Rpg2 or Rpg3 (Fox and Harder, 1995). However, further investigation is required to determine the location of RpgU and whether RpgU is allelic to any other Rpg loci. The recessive locus rpgBH was identified in Black Hulless, effective against Pgs (Steffenson et al., 1984). As allelism tests or mapping experiments have not been conducted, it cannot be ruled out that rpgBH is not a different and/or less effective allele of previously mapped Rpg loci. Up to two other loci were reported in Purple Nudum and Skinless (Babriwala, 1954; Luig, 1957), but were not investigated further. A total of nine loci were identified against Pga (Rgpaq1-9); however, only Rpgaq7 and Rpgaq9 did not colocalize with previously reported Rpg loci and were considered novel (Dracatos et al., 2016a). Lastly, a total of 17 required for P. graminis resistance (rpr) mutants have been obtained using fast neutron irradiation of Morex (Rpr1-7) and Q21861 (Rpr8-17), three of which have been mapped as Rpr1, Rpr2, and Rpr9 (Gill et al., 2016; Solanki et al., 2019; Zhang et al., 2006).

Chromosome 1H

Currently, only association mapping studies have identified stem rust resistance loci on chromosome 1H. These include Rpgaq1 (Dracatos et al., 2016a), Rpg-qtl-1H-11_11277 and Rpg-qtl-1H-12_20613 (Case et al., 2018b), and 10 unnamed QTL (Czembor et al., 2022; Sallam et al., 2017; Turuspekov et al., 2016). Current evidence suggests the 10 unnamed QTL do not overlap and therefore chromosome 1H may harbor untapped potential for stem rust resistance.

Chromosome 2H

Rpg2 was first described in Heitpas-5 (Patterson et al., 1957) and mapped within a 21.9-Mb interval (533.27–555.12 Mb) (Case et al., 2018a); however, it remains largely under investigation due to the low level of resistance it provides (Kleinhofs et al., 2009). Additionally, a trans-eQTL regulator hotspot was identified that results in the suppression of hundreds of genes after Pgt inoculation and is colocalized with an enhancer of rpg4/Rpg5-mediated resistance to Pgt race TTKSK at the adult stage (Moscou et al., 2011). Both the enhancer and regulator are hypothesized to be the same gene, and therefore for this manuscript, this locus has been designated Rpg4-modifier element 2 (Rme2) and mapped to a 12.9-Mb interval (41.6–51.6 Mb). Additional loci mapping to chromosome 2H include Rpg-qtl-PH-PI38-2H (258.46–264.39 Mb) nested within Rpg-qtl-HH-Hie-2H.1 (221.89–26830 Mb) (Case et al., 2018a) that was also identified with association mapping (Hernandez et al., 2020a). Other loci include Rpg-qtl-HH-Hie-2H.2, Rpg-qtl-HH-Hie-2H.3, and Rpg-qtl-HH-Hie-2H.4 (Case et al., 2018a); Rpg-qtl-2H-12_11278 (Case et al., 2018b); Rpg-qtl-2H_SCRI_RS_115905 and Rpg-qtl-2H_SCRI_RS_109266 (Mamo, 2013); Rpgaq9 and unanchored Rpgaq2 (Dracatos et al., 2016a); and nine unnamed QTL (Czembor et al., 2022; Sallam et al., 2017).

Chromosome 3H

Rpg7 is the most recently designated Rpg locus identified in wild barley accessions WBDC094 and WBDC238, mapping to a 9.8-Mb interval (606.10–615.92 Mb) (Henningsen et al., 2021). Association mapping identified the MTA Rpg-qtl-3H_SCRI_RS_180847 approximately 0.98 Mb from the boundary of Rpg7 (Mamo, 2013). Rpr9, which was a gene identified by mutant analysis of line Q21861, is required for both Rpg1- and rpg4/Rpg5-mediated resistance, and mapped to a 770-kb interval (502.40–503.17 Mb) (Solanki et al., 2019). Rpr9 is hypothesized to function by facilitating ubiquitination and degradation of proteins required for resistance, based on previous research on Rpg1 (Solanki et al., 2019). In addition, rpr9 mutants resulted in a stunted root phenotype due to the hypothesis that Rpr9 is involved in hormone signaling (Solanki et al., 2019). Rpr9 appears to be encompassed by Rpg-qtl-HH-Hip-3H (Case et al., 2018a) and potentially mapped in association mapping (Czembor et al., 2022). Additional loci mapping to chromosome 3H include Rpg-qtl-PH-Hip-3H and Rpg-qtl-HH-Hip-3H (Case et al., 2018a); Rpg-qtl-3H-SCRI_RS_199887 (Case et al., 2018b); and qGH_PBIC_3.11 (Dracatos et al., 2019b). A total of 11 unnamed QTL have also been mapped to chromosome 3H (Hernandez et al., 2020a; Mamo et al., 2014; Sallam et al., 2017; Turuspekov et al., 2016), whereas Rpgaq6 remains unanchored (Dracatos et al., 2016a). Rpg-qtl-PH-Hip-3H and Rpg-qtl-HH-Hip-3H show partial overlap and encompass six MTA identified via association mapping (Czembor et al., 2022; Mamo et al., 2014; Sallam et al., 2017), suggesting less unique loci on chromosome 3H and will require further investigation.

Chromosome 4H

The Rpr1 locus was mapped to a 265.9-Mb interval (145.53–411.43 Mb) in the Morex V3 genome (Zhang et al., 2006). Rpr1 was identified as a suppressor of Rpg1 and therefore required for Rpg1-mediated resistance; however, Rpr1 is not involved in rpg4/Rpg5-mediated resistance (Zhang et al., 2006). Six MTA were reported within the Rpr1 region using association mapping (Sallam et al., 2017; Turuspekov et al., 2016); however, considering the size of the Rpr1 region, it may encompass different resistance loci. Additional loci mapped to chromosome 4H include Rpg-qtl-PH-PI38-4H, Rpg-qtl-HH-Hie-4H (Case et al., 2018a), Rpg-qtl-4H_12_30995 (Mamo, 2013), seven MTA that most likely form a single QTL based on cM positions (Sallam et al., 2017), and a further four unnamed QTL (Czembor et al., 2022; Turuspekov et al., 2016).

Chromosome 5H

Rpg3 was first reported in GAW-79 (Jedel et al., 1989) and mapped to chromosome 5H (Case et al., 2018a). Using markers reported to be significant, Rpg3 maps to a 323.5-Mb interval (94.22–417.72 Mb) using Morex V3. However, these significant markers are not present within the linkage map reported. Utilizing the genetic marker information of the map, Rpg3 maps to a 2.3-Mb interval (448.62–450.88 Mb) (Case et al., 2018a), outside of the original Rpg3 interval. Rpg3 is more likely to be located within the 2.3-Mb interval based on Rpg3 being localized to chromosome 5HL and the higher-quality genome assembly of Morex V3. However, as Rpg3 remains under investigated due to low-level resistance (Kleinhofs et al., 2009), this discrepancy should be addressed for both tracking Rpg3 for breeding purposes and future validation.

The rpg4 locus was first identified as providing resistance to Pgt isolates, whereas Rpg5 provided resistance to Pgs isolates and later Pga isolates (Dracatos et al., 2015b; Sun et al., 1996; Sun and Steffenson, 2005). The rpg4 gene was originally suspected as HvAdf2 (Brueggeman et al., 2009; Kleinhofs et al., 2009), whereas the Rpg5 gene was validated as HvRga2, encoding an NLR with an integrated protein kinase (functional haplotype) or protein phosphatase 2C domain (PP2C, nonfunctional haplotype) (Brueggeman et al., 2008). However, increasing evidence found that rpg4-mediated resistance was not a result of HvAdf2 and required Rpg5 (HvRga2) and two additional genes located at the locus, HvRga1 and HvAdf3, to be functional (Arora et al., 2013; Wang et al., 2013). The HvAdf3 gene within the locus was also deemed to be a candidate susceptibility gene (Moscou et al., 2011). Therefore, the rpg4/Rpg5 complex was renamed to the rpg4-Mediated Resistance Locus (RMRL) that includes RMRL1 containing HvRga1, Rpg5 (HvRga2), and HvAdf3; and RMRL2 containing the yet unidentified Rpg4-modifier element 1 (Rme1), which is required for rpg4-mediated wheat stem rust resistance but not required for Rpg5-mediated rye stem rust resistance (Wang et al., 2013). RPG5 (HvRGA2) and HvRGA1 belong to MIC1 (C16) and C7 clades, respectively (Bailey et al., 2018). NLRs in the MIC1 and C7 clades were found to be in head-to-head orientation in grasses such as the paired NLRs RGA5/RGA4 in rice that confer resistance to M. oryzae through recognition of the effectors AVR-Pia and AVR1-CO39 (Bailey et al., 2018; Cesari et al., 2013). The MIC1 clade is unique in the grasses, as NLRs in the clade have diverse C-terminal integrated domains with RGA5 carrying an integrated heavy metal-associated domain (Bailey et al., 2018; Cesari et al., 2013).

Using six highly diverse barley accessions, only one allele of rpg4/Rpg5 was identified, suggesting cultivated barley could be extremely vulnerable to a lack of diversity at rpg4/Rpg5 (Mamo et al., 2014). In addition, the rpg4/Rpg5 complex was found to be present in nearly every resistant landrace from Switzerland when assessing resistance to Pgt races TTKSK and QCCJB (Steffenson et al., 2016). Additional studies mapped rpg4/Rpg5 using association mapping, identifying a novel allele of rpg4/Rpg5 designated Rpg5Xx (Hernandez et al., 2019, 2020a). Previous work found that the region containing Rme1 is approximately 220 kb in size, proximal to RMRL1, containing a heat shock protein, a zinc finger SEC14 protein, and an actin depolymerization-like protein (HvAdf1) (Wang et al., 2013). Further investigation into the Morex V3 found that Rme1 encompasses 321 kb. Leaf-expressed candidate genes include those previously identified as well as a PP2C protein. Further work is needed to establish sequence and structural variation within the Rme1 region relative to diverse barley accessions.

The rpg4/Rpg5 locus was the only locus to provide resistance to Pgt race TTKSK in barley (Brueggeman et al., 2009); however, an additional locus, required for rpg4-mediated resistance 1 (Rrr1), is required to facilitate rpg4/Rpg5-mediated resistance when stacked with Rpg1 (Sharma Poudel et al., 2018). The Rrr1 locus was mapped to a 529-kb interval (560.96–561.49 Mb) on chromosome 5H (Sharma Poudel et al., 2018). Similar phenomena were observed with Rpr9 (required for Rpg1- and rpg4/Rpg5-mediated resistance) described earlier on chromosome 3H (Solanki et al., 2019), and the identification of two novel loci on chromosomes 5H (not Rrr1) and 7H that were additive to Rpg4/Rpg5 resistance, i.e., rpg4/Rpg5 is required for resistance but not sufficient (Hernandez et al., 2019). These complex interactions have made the introgression of rpg4/Rpg5-mediated resistance to elite cultivars more complicated than originally anticipated (Hernandez et al., 2019).

For further complexity, the recently released Woodies germplasm (Woody-1, DH160733 and Woody-2, DH160754) designed to systematically stack stripe and stem rust resistance have a null allele of Rpg5, yet remain highly resistant to stem rust (Hernandez et al., 2020a, b; Massman et al., 2024a). The high level of resistance present in the Woodies has been attributed to the QTL-SR locus, encompassing a 1.8-Mb region (469.6–470.4 Mb) in close vicinity to the rpg4/Rpg5 complex (Massman et al., 2024b). Candidate gene analysis of the Morex V3 region revealed 10 candidate genes within the region of interest, and a further three NLR genes within 10 Mb that may underlie QTL-SR due to structural rearrangements. Further comparative analysis revealed that large regions of Morex are absent from the Woody-1 genome assembly (Massman et al., 2024b). Therefore, instead, the Woodies may lack a susceptibility gene that is present in the susceptible barley accession Morex. The identification of this novel locus further complicates the resistance puzzle; however, Woody-2 has been identified to be highly amenable to transformation, which will aid in gene validation.

Additional loci mapping to chromosome 5H include Rpg-qtl-PH-PI38-5H (Case et al., 2018a), Rpg-qtl-5H-11_11355 (Case et al., 2018b; Zhou et al., 2014), Rpg-qtl-5H-SCRI_RS_10929 (Mamo, 2013), and three unnamed QTL (Czembor et al., 2022; Sallam et al., 2017). Multiple MTA are deemed to delimit Rpg-qtl-5H-11_11355 as a QTL due to linkage disequilibrium (Case et al., 2018b; Zhou et al., 2014) and were also mapped in earlier and subsequent association mapping studies (Hernandez et al., 2020a; Mamo, 2013). The boundary of Rpg-qtl-5H-11_11355 is approximately 14 Mb distal to Rpg3 and therefore is likely to be a distinct locus.

Chromosome 6H

The rpg6 locus is the only locus identified within H. bulbosum to stem rust, providing recessive resistance (Fetch et al., 2009) and located within a 25.5-Mb interval (0.08–25.55 Mb). The rpg6 locus has also been mapped in three association mapping studies (Czembor et al., 2022; Sallam et al., 2017; Turuspekov et al., 2016). Rpr2 mapped to a 43.3-Mb (68.28–111.54 Mb) interval and hypothesized to function as a stabilizer of Rpg1, as the RPG1 protein was degraded faster than that of highly resistant stem rust-resistant lines (Gill et al., 2016). An MTA embedded within the Rpr2 interval was also reported in association mapping (Czembor et al., 2022). Additional loci that map to chromosome 6H include a further eight unnamed QTL (Czembor et al., 2022; Sallam et al., 2017), eight MTA that most likely form a single QTL (Turuspekov et al., 2016), and unanchored Rpgaq3, Rpgaq7, and Rpgaq8 (Dracatos et al., 2016a).

Chromosome 7H

Rpg1 was the first Rpg locus identified and provided durable, broad-spectrum resistance to Pgt against all North American Pgt isolates for approximately 70 years (Roelfs et al., 1993). Rpg1 was first reported in 1933, with sources found in Peatland, Chevron, and Kindred (Powers and Hines, 1933; Shands, 1939; Steffenson, 1992). Cloning of Rpg1 identified a gene encoding a protein with two tandem serine/threonine protein kinase domains (Brueggeman et al., 2002, 2006) located at 3.74 Mb. Transcript analysis found that Rpg1 has the highest expression in leaf epidermal cells (Rostoks et al., 2004) and is predominantly located in the cytosol (Nirmala et al., 2006). Both protein kinase domains are required for resistance; however, the second kinase domain is required for autophosphorylation (Nirmala et al., 2006). In addition, two effectors are required for autophosphorylation with RIN4, and subsequent degradation of RPG1 is required for resistance (Chai et al., 2012; Gill et al., 2012; Horvath et al., 2003; Nirmala et al., 2007, 2010, 2011). Either Rrr1 or another locus designated required for Rpg1-mediated resistance 2 (Rrr2) is required for Rpg1-mediated resistance in the presence of rpg4/Rpg5 (Sharma Poudel et al., 2018). Rrr2 was mapped to a 673-kb interval (6.20–6.87 Mb) (Sharma Poudel et al., 2018), but is not the 7H locus reported by Hernandez et al. (2019). Additional loci mapping to chromosome 7H include Rpg-qtl-PH-PI38-7H and Rpg-qtl-HH-Hie-7H (Case et al., 2018a); qGH_BPIC_4.6 (Dracatos et al., 2019b); 19 unnamed QTL (Czembor et al., 2022; Hernandez et al., 2020a; Sallam et al., 2017; Zhou et al., 2014); and unanchored Rpgaq4 and Rpgaq5 (Dracatos et al., 2016a).

Association mapping

To date, there have been eight association mapping studies used to characterize stem rust resistance. The first identified up to 15 MTAs in wild barley, two of which were associated with rpg4/Rpg5 (Steffenson et al., 2007). The second association mapping study was conducted in US breeding material against Pgt race TTKSK effectively identifying two novel QTL on chromosomes 5H and 7H, respectively (Zhou et al., 2014). These were both mapped again in subsequent association mapping studies (Case et al., 2018b; Hernandez et al., 2020a). In the third association mapping study, 17 MTAs were reported using Kazakh spring barley in two environments (Turuspekov et al., 2016). However, one marker misassigned to chromosome 2H and four markers assigned to unknown chromosomal loci can be consolidated with other MTAs into a total of eight distinct loci. After consolidating these loci, only markers located at the proximal end of chromosome 6H colocalize with the previously identified locus rpg6 (Fetch et al., 2009). While the other loci can be deemed novel within stem rust, four colocalize with the leaf rust resistance loci Rph13, Rph20, Rph21, and Rph26. The fourth association mapping study was conducted in wild barley, identifying 45 MTAs, many of which were novel at the time (Sallam et al., 2017). The fifth association mapping study identified seven QTL from the barley core collection; one locus of notable interest was on chromosome 5H, as it provided APR not conferred by the rpg4/Rpg5 complex (Case et al., 2018b). The sixth and seventh association mapping studies were conducted on a double haploid population designed to increase resistance to stem rust race TTKSK (Hernandez et al., 2019, 2020a). These association mapping studies identified eight and six MTAs, respectively (Hernandez et al., 2019, 2020a), none of which were claimed to be novel; however, a new allele of rpg4/Rpg5 was identified as Rpg5Xx (Hernandez et al., 2020a). The last association mapping study identified 48 significant MTAs using European barley accessions (Czembor et al., 2022).

Genetics to stripe rust

Barley stripe rust is predominantly caused by Psh; however, barley can also be infected by P. striiformis f. sp. tritici (Pst), the causal agent of wheat stripe rust. Yield losses exceeding 70% have been reported but typically cause approximately 40% yield loss under environmental conditions conducive to disease in a susceptible variety (Marshall and Sutton, 1995). Psh is therefore potentially the most damaging rust, despite arguably being the most understudied of the three major barley rusts. Barley stripe rust was first described by European workers in the late 1800s, causing particular issues in winter barley in the UK and the Netherlands (Wellings, 2011). Subsequently, Psh was first reported in Columbia in 1975, spreading throughout South America by 1982 (Dubin and Stubbs, 1986), Mexico by 1987, and in the USA by 1991 (Chen et al., 1995; Marshall and Sutton, 1995). Due to stripe rust prevalence in colder, wetter climates, often at higher altitudes, stripe rust is often regarded as cold-temperature rust (Dracatos et al., 2019b). Around 88% of worldwide wheat production is susceptible to stripe rust (Beddow et al., 2015) and is considered a major pathogen of barley, with 60%–70% of Australian barley considered susceptible (Dracatos et al., 2019b; Gyawali et al., 2021).

The genetics of stripe rust resistance have been studied since the 1940s (Murty, 1942). To date, there are 78 Yellow rust (Yr) loci (Jamil et al., 2020) and at least 50 Resistance to Puccinia striiformis (Rps; Table 4) loci identified in wheat and barley, respectively (Bettgenhaeuser et al., 2021; Chełkowski et al., 2003; Chen and Line, 1999, 2001, 2003; Nover and Scholz, 1969; Pahalawatta and Chen, 2005). However, only 10 Rps loci have been formally designated within the barley-P. striiformis pathosystem (Clare et al., 2016), and even fewer have been mapped. Earlier mapping efforts made use of restriction fragment length polymorphisms, simple sequence repeats, amplified fragment length polymorphisms, and resistance gene analog polymorphisms, which make anchoring loci to the Morex V3 troublesome (Castro et al., 2002, 2003a, 2003b; Chen et al., 1994; Thomas et al., 1995; Toojinda et al., 1998, 2000; Vales et al., 2005).

Another caveat is that these loci are functional against P. striiformis sensu lato, meaning they can function against both or only Psh or Pst isolates. The first four Rps loci were originally designated Yr loci; however, Rps4 has only been associated with chromosome 1H, and rps3 was never mapped (Johnson, 1968; Nover and Scholz, 1969). In addition, Yr4 through Yr13 were identified in India but were not consistent with international nomenclature (Verma et al., 2018). There were also at least eight additional loci with Puccinia striiformis (Ps) nomenclature (Chen and Line, 1999; Luthra and Chopra, 1990). Many of the original Rps loci function under a recessive mode of inheritance, with only five out of 26 under a dominant mode of inheritance (Chełkowski et al., 2003; Chen and Line, 1999). The first loci identified to govern nonadapted resistance to Pst were RpstS1 and RpstS2 in Steptoe (Pahalawatta and Chen, 2005). More recently, nonadapted resistance to Pst has seen a renewed research focus with the mapping of Rps6 (Dawson et al., 2016; Li et al., 2016) and subsequent cloning of Rps7 and Rps8 (Bettgenhaeuser et al., 2021; Holden et al., 2022).

Chromosome 1H

Rps7 was the first Rps gene to be identified and validated within the barley-P. striiformis pathosystem (Bettgenhaeuser et al., 2021). Rps7 encodes an NLR that was previously identified as the barley immune receptor Mildew locus a (Mla), conferring resistance to Blumeria graminis f. sp. hordei, and M. oryzae (Brabham et al., 2023; Inukai et al., 2006), and susceptibility to Cochliobolus sativus (Leng et al., 2018). The authors warned that due to different haplotypes of Mla providing different specificities, often to different pathogens, breeders should be careful not to inadvertently remove resistance to nonadapted pathogens (Bettgenhaeuser et al., 2021). Rps7 was also mapped as QPsh-DP-2R-1.1 and QPsh-rM-6R-1.1 (Gyawali et al., 2021); qGH_WUR_rep1_3.26 and qGH_WUR_rep2_5.78 (Dracatos et al., 2019b); RPsh-1H (Belcher et al., 2018); and unnamed QTL (Hernandez et al., 2020a). The genetic mapping of Rps4 using protein and phenotypic markers placed the gene ~ 6.2 cM proximal to Mla (Johnson et al., 1969). Additional loci mapping to chromosome 1H include qField_Mex2015_3.30 and qGH_PBIC_5.29 (against Psph, Dracatos et al., 2019b); QPsh-r24-6R-1.1, QPsh-rQ-6R-1.2, QPsh-r24-6R-1.2, and QPsh-DP-2R-1.2 (Gyawali et al., 2021); QPs.1H-1 (Vatter et al., 2018); QPsh.FW6-1H (Belcher et al., 2018); and two unnamed QTL (Belcher et al., 2018; Dracatos et al., 2016b). Furthermore, eight unnamed unanchored MTA/QTL are present on chromosome 1H (Thomas et al., 1995; Visioni et al., 2018).

Chromosome 2H

The rps2 locus was originally identified as a recessive resistance locus against Psh in Abed Binder 12 (Nover and Scholz, 1969); however, it is currently only one of two Rps loci to be functional against Psh and Pst. Subsequent high-resolution mapping determined that rps2 was additive rather than completely recessive and localizing to a 3.4-Mb (658.7–662.1 Mb) interval (Dawson, 2015). Additional loci mapping to chromosome 2H include QPs.2H-1, QPs.2H-2, and QPs.2H-3 (Vatter et al., 2018); Qpsh.316A.2Ha and Qpsh.316A.2Hb (Esvelt Klos et al., 2020); QPsh-rQ-6R-2.1, QPsh-r7S0-2R-2.1, QPsh-DP-6R-2.1, QPsh-DP-6R-2.2, and QPsh-DP-2R-2.1 (Gyawali et al., 2021); qField_Mex2015_5.13, qField_Mex2015_5.30, and qField_Ecuad2017_3.97 (Dracatos et al., 2019b); and QPsh.FW6-2H.1 (Belcher et al., 2018). Furthermore, a total of four unnamed QTL from 10 MTA (Belcher et al., 2018) and three unnamed QTL (Dracatos et al., 2016b; Gutiérrez et al., 2015) were mapped to chromosome 2H, while 15 MTA/QTL remain unanchored (Rao et al., 2007; Rossi et al., 2006; Visioni et al., 2018).

Chromosome 3H

The recessive rps1 resistance locus was identified in Bigo and Abyssinian 14 and mapped in BBA2890 using resistance gene analog polymorphisms (RGAP); however, due to the use of these markers, an interval cannot be reported (Nover and Scholz, 1969; Yan and Chen, 2007a). One marker used to track rps1 places the causal gene in the vicinity of 578.33 Mb (Yan and Chen, 2007b). Loci with markers in close proximity to rps1 have included Qpsh.316A.3H (Esvelt Klos et al., 2020); RPsh-3H, QPsh.FW6-3H.2, and two unnamed QTL (Belcher et al., 2018); QPs.3H-2 and QPs.3H-3 (Vatter et al., 2018); and QPsh-rQ-6R-3.1 (Gyawali et al., 2021). Additional loci mapping to chromosome 3H include QPsh-rQ-2R-3.1, QPsh.FW6-3H.1, QPsh-r7S0-6R-3.1, QPsh-DP-6R-3.1, and QPsh-r57-2R-3.1 (Gyawali et al., 2021); QPs.3H-1 and QPs.3H-4 (Vatter et al., 2018); RpsHOR1428-3H, also mapped by association mapping (Clare, 2016; Gutiérrez et al., 2015); and qGH_PBIC_3.14 (Dracatos et al., 2019b). A further three unnamed QTL were mapped to chromosome 3H (Belcher et al., 2018; Gutiérrez et al., 2015), while 11 MTA/QTL remain unanchored (Rao et al., 2007; Rossi et al., 2006; Visioni et al., 2018).

Chromosome 4H

The rps5 (rpsGZ) locus identified in Grannenlose Zweizeilige was mapped to chromosome 4H using RGAPs (Yan and Chen, 2006) and subsequently to a 3.9-Mb interval (587.75–591.70 Mb) (Esvelt Klos et al., 2016). The nonadapted Rps8 resistance locus, functional against Pst, was the second validated Rps locus as a two-gene complex encoding a receptor kinase and an Exo70. Both the receptor kinase and Exo70 are required for resistance (Holden et al., 2022) and are located within a 170-kb interval (579.76–579.92 Mb). Due to the two-gene complex of Rps8, there are at least 27 unique alleles/haplotypes currently reported (Holden et al., 2022). Rps8 was first mapped by Bettgenhaeuser et al. (2021); however, it was also most likely mapped with association mapping as QPsh-rQ-2R-4.1 and QPsh-rM-6R-4.1 (Gyawali et al., 2021) and an unnamed MTA (Hernandez et al., 2020a). Additional loci mapping to chromosome 4H include QPsh-r57-6R-4.1, QPsh-r57-6R-4.2, QPsh-r57-6R-4.3 QPsh-rG-2R-4.1, QPsh-rG-2R-4.2, QPsh-DP-6R-4.1, QPsh-DP-6R-4.2, QPsh-r7S0-2R-4.1, QPsh-r7S0-6R-4.1, and QPsh-rG-2R-4.3 (Gyawali et al., 2021); Qpsh4Ha and Qpsh4Hb (Esvelt Klos et al., 2020); and qGH_WUR_rep1_3.86 and qGH_WUR_rep2_3.28 (Dracatos et al., 2019b). A further three unnamed QTL (Belcher et al., 2018; Dracatos et al., 2016b; Gutiérrez et al., 2015) and 10 unanchored MTA/QTL (Rao et al., 2007; Rossi et al., 2006; Visioni et al., 2018) are mapped to chromosome 4H.

Chromosome 5H

The final two most recently designated nonadapted resistance loci are Rps9 and Rps10. Rps9 was identified as the second locus functional against Psh and Pst, utilizing a backcrossing scheme to isolate the locus from HOR 1428 in a Manchuria background and delimited to an 11.5-Mb interval (533.16–544.07 Mb) (Clare et al., 2016). Rps9 has also been identified as QPs.5H-1 (Vatter et al., 2018), QPsh-r57-2R-5.1 (Gyawali et al., 2021), and an unnamed QTL (Gutiérrez et al., 2015). The same strategy was used to isolate Rps10, functional against Pst, from WBDC085. A marker in complete coupling with Rps10 was not found; however, using the two peak markers at the BC₂ and BC₂F₂ stages, Rps10 maps to a 16-Mb interval (554.80–570.84 Mb) (Clare, 2016). Rps10 was also mapped as QPsh-DP-2R-5.1 and QPsh-DP-2R-5.2 (Gyawali et al., 2021) and in close proximity to QPsh.FW6-5H.2 (Belcher et al., 2018) and QPsh-rM-6R-5.1 (Gyawali et al., 2021; Vatter et al., 2018) on the proximal flank and QPsh-r24-6R-5.2, QPsh-DP-2R-5.3, QPsh-rG-6R-5.2, and QPsh-rG-2R-5.1 (Gyawali et al., 2021) on the distal flank. Additional loci were mapped to chromosome 5H including the following: QPsh-rG-6R-5.1, QPsh-r24-6R-5.1, QPsh-r7S0-6R-5.1, QPsh-rM/Q-2R-5.1, QPsh-rM/Q-2R-5.2, QPsh-rM-2R-5.1, and QPsh-r24-2R-5.1 (Gyawali et al., 2021); QPsh.FW6-5H.1, QPsh.FW6-5H.3, six MTA most likely forming a single unnamed QTL, and another MTA (Belcher et al., 2018); one unnamed MTA (Hernandez et al., 2020a); qGH_PBIC_4.26 effective against Psph (Dracatos et al., 2019b); Qpsh.316A.5H (Esvelt Klos et al., 2020); five MTA that may form a single QTL (Dracatos et al., 2016b); and 14 unanchored MTA/QTL (Rao et al., 2007; Thomas et al., 1995; Visioni et al., 2018).

Chromosome 6H

Currently, only association mapping studies have identified stripe rust resistance loci on chromosome 6H. These include QPsh-rM-6R-6.1, QPsh-rM-6R-6.2, QPsh-rM-6R-6.3, QPsh.FW6-6H.4, QPsh-r57-6R-6.2, QPsh-DP-6R-6.1, QPsh-r7S0-6R-6.1, QPsh-r7S0-6R-6.2, QPsh-r7S0-6R-6.3, QPsh-r7S0-6R-6.4, QPsh-r24/57-6R-6.1, QPsh-rQ-6R-6.1 (Gyawali et al., 2021), QPsh.FW6-6H.1, QPsh.FW6-6H.2, QPsh.FW6-6H.3, one unnamed QTL (Belcher et al., 2018), Qpsh6H (Esvelt Klos et al., 2016), Qpsh.316A.6H (Esvelt Klos et al., 2020), and QPs.6H-1 (Vatter et al., 2018). Furthermore, seven MTA/QTL remain unanchored to chromosome 6H (Rao et al., 2007; Rossi et al., 2006; Visioni et al., 2018).

Chromosome 7H

Rps6 is functional only against Pst and was concurrently high-resolution mapped by two independent studies to a 267.6-kb (613.67–613.94 Mb) and 163.5-kb (613.77–613.93 Mb) interval (Dawson et al., 2016; Li et al., 2016). Rps6 was mapped in wild barley accessions and the German barley accession Abed Binder 12 (Dawson et al., 2016; Li et al., 2016) and potentially mapped in Franklin (Dracatos et al., 2016b). Rps6 was also identified using association mapping (Dracatos et al., 2016b; Gutiérrez et al., 2015). Rpsx was mapped to a 14.4-Mb (597.28–611.72 Mb) interval using CI10587 (Castro et al., 2003a). Rpsx has also been mapped as QPsh.FW6-7H (Belcher et al., 2018), two unnamed MTA forming a single QTL (Dracatos et al., 2016b), qGH_PBIC_4.51 against Psph (Dracatos et al., 2019b) and QPs.7H-1 (Vatter et al., 2018). Additional loci mapped to chromosome 7H include QPsh-r24/G-2R-7.1, QPsh-r24-2R-7.2, QPsh-rQ-6R-7.1, QPsh-r57-2R-7.1, QPsh-r7S0-2R-7.2, QPsh-rG-6R-7.1, and QPsh-rG-6R-7.2 (Gyawali et al., 2021); Rpsh-7H (Belcher et al., 2018); Qphs7H (Esvelt Klos et al., 2016); and Qpsh.316A.7H (Esvelt Klos et al., 2020). A single unnamed QTL also maps to chromosome 4H (Gutiérrez et al., 2015), whereas a further 10 MTA/QTL (Rao et al., 2007; Rossi et al., 2006; Visioni et al., 2018) remain unanchored to chromosome 4H.

Association mapping

To date, six association mapping studies have been used to characterize resistance to stripe rust in barley. The first used a Latin American barley population and identified a total of seven QTL, three of which were deemed novel (Gutiérrez et al., 2015). The second study, using the HEB-25 NAM panel, identified eight novel loci out of the 12 identified (Vatter et al., 2018). The third association study assessed Oregon and Minnesotan breeding material, identifying three ASR and 14 APR QTL, respectively, five of which were novel (Belcher et al., 2018). The fourth study assessed a global population of 261 barley accessions identifying 45 ASR and 18 APR QTL (Visioni et al., 2018); however, this cannot be verified as the DaRTseq markers could not be anchored to the Morex genome. The fifth study identified four QTL, none of which were novel; however, one locus was mapped for both stem and stripe rust (Hernandez et al., 2020a) in close proximity to Rph9. The last association mapping study assessed 336 ICARDA accessions with 42 ASR and 13 APR MTA identified, 33 of which were deemed novel (Gyawali et al., 2021).

Notable changes to net blotch consensus map

Marker positions for consolidated net blotch loci were identified using the Morex V3 genome assembly, further refining multiple loci after incorporating additional studies (Adhikari et al., 2020; Afanasenko et al., 2022; Alhashel et al., 2021, 2023; Clare et al., 2021; Czembor and Czembor, 2023; Esmail et al., 2023; Mazinani et al., 2020; Muria-Gonzalez et al., 2023; Skiba et al., 2022) and additional unanchored markers (Table 5; Supplementary Table 2). The total number of consensus loci for net blotch has been lowered from 73 to 72, despite the separation of SPN1 from Rpt5/Spt1, the identification of Rpt9 (Franckowiak and Platz, 2021), and the addition of two novel MTA (Czembor and Czembor, 2023). As noted, a major change in the net blotch consensus maps was the identification of Rpt9 (598.8–611.7 Mb), dividing Rpt4 (now 415.1–596.6 Mb) (Franckowiak and Platz, 2021) into two loci on the long arm of chromosome 7H. The Rpt4/Rpt9 region has been subsequently further characterized with two overlapping resistance loci identified at 592.2–602.0 Mb (Alhashel et al., 2021) and 587.1–598.8 Mb (Skiba et al., 2022), and therefore potentially mapping the same underlying gene of either Rpt4 or Rpt9. However, within this interval, a susceptibility locus was identified and high-resolution mapped (592.6–593.0 Mb) with the proposed name of Sptm1 (Alhashel et al., 2023). Whether Sptm1 is Rpt4, Rpt9, or a separate locus is currently unknown and requires further investigation. This is further supported by association mapping that identified two significant markers within the region (596.7 and 611.7 Mb) separated by multiple insignificant SNPs (Clare et al., 2021). Further work will be required to tease apart the true number of loci present in the Rpt4/Rpt9/Sptm1 region.

The most broad and effective resistance gene, Rpt5, against Pyrenophora teres f. teres (Ptt) has been validated as a RLP at 364.7 Mb, whereas Spt1 remains under investigation (Effertz, 2023; Effertz et al., 2024). Due to the centromeric location of Rpt5/Spt1, the majority of markers identified on chromosome 5H are most likely in linkage disequilibrium currently spanning from 111.9 to 466.6 Mb. However, this separates the SPN1 locus originally delimited to 46.0–90.3 Mb (Liu et al., 2015). Additionally, further work will be required to determine if any additional loci are present within the large linkage block that currently delimits Rpt5/Spt1. Unfortunately, Rpt5 has been broken by Canadian (Akhavan et al., 2016), French (Arabi et al., 1992), Turkish (Çelik Oğuz and Karakaya, 2017), and Moroccan isolates (Li et al., 2023; Richards et al., 2024). Interestingly, an association mapping study into Egyptian germplasm did not identify Rpt5, instead identified seven significant markers on 3H (Esmail et al., 2023). These are reported as seven separate MTA; however, NB-2, NB-3, NB-4 colocalize with Rpt3H-4 (Afanasenko et al., 2022; Clare et al., 2021; Daba et al., 2019; Islamovic et al., 2017; König et al., 2014; Lehmensiek et al., 2007; Novakazi et al., 2019; Richards et al., 2017; Tamang et al., 2015, 2021; Wonneberger et al., 2017; Yun et al., 2005), and NB-5, NB-6, NB-7, and NB-8 colocalize with QRpts3La (Burlakoti et al., 2017; Cakir et al., 2011; Daba et al., 2019; Lehmensiek et al., 2007; Raman et al., 2003; Richards et al., 2017; Tamang et al., 2015, 2019; Vatter et al., 2017; Wonneberger et al., 2017).

Lastly, multiple susceptibility loci have been identified in the barley-P. teres f. maculata (Ptm) pathosystem, including Sptm1, described earlier. Firstly, Spt2 was been high-resolution mapped to a single pentatricopeptide repeat-containing protein candidate gene on chromosome 5H in two independent mapping populations that share CI5791 as a common parent (Clare et al., 2024). The Spt2 locus is unique in that all parents are considered resistance to the Ptm isolate 13IM8.3; however, all F₁ individuals are considered hypersusceptible. This locus was previously mapped as resistance loci: NBP_QRptt5-1 (Wonneberger et al., 2017), QRpt-5H.2 (Clare et al., 2021), and potentially an unnamed QTL (Clare et al., 2020; Williams et al., 2003) raising interesting questions about whether the locus can function as a resistance and/or susceptibility target. Another locus designated Spm1 was identified within a 190-kb interval (9.12-9.31 Mb) on chromosome 1H (Muria-Gonzalez et al., 2023), that has previously been identified as resistance loci: QRptta-1H-4.11 (Amezrou et al., 2018), QRpta1H-2 (Mazinani et al., 2020), QNFNBAPR.Ar/F-1H (Lehmensiek et al., 2007) and a QTL identified between 19.4 and 25.7 cM (Martin et al., 2018). The Susceptibility to P. tritici-repentis 1 (Spr1) locus facilitates susceptibility to the pathogen P. tritici-repentis (Ptr), which primarily causes tan spots of wheat (Wei et al., 2020). The Spr1 locus to 9.4–12.0 Mb has also been included in the P. teres maps (Figure 1) and colocalizes with SFNB-2H-8-10 (Burlakoti et al., 2017), NBP_QRptt2-1 (Wonneberger et al., 2017), QRptts-2H-7.44 (Amezrou et al., 2018), QRptts-2H-9.00, QRptts-2H-161.70 (Adhikari et al., 2019), and unnamed QTL (Liu et al., 2015; Skiba et al., 2022; Tamang et al., 2015, 2019).

Figure 1

A trend of identifying susceptibility loci within the barley-P. teres pathosystem appears to be common after the initial identification of the Spt1 susceptibility locus (Richards et al., 2016), followed by Spt2 (Clare, 2022; Clare et al., 2024), Sptm1 (Alhashel et al., 2023), Spm1 (Muria-Gonzalez et al., 2023), and resistant accessions contributing susceptibility alleles at QRptm-3H-45-52, QRptm-5H-12-21, QRptm-5H-81-88, and QRptm-6H-60-64 (Alhashel et al., 2021). Loci nomenclature needs to be addressed urgently, considering multiple loci are identified to be effective against Ptt and Ptm. Despite recent research suggesting incipient speciation between Ptt and Ptm (Yuzon et al., 2023), there is considerable overlap (Clare et al., 2020) and the custom of utilizing three letters and numbers to designate barley loci (Bockelman et al., 1977). The designations Rpt and Spt provide no discrimination between Ptt and Ptm, unlike Sptm and Spm, which suggest these loci are only implicated within Ptm interactions, despite the fact these have been previously identified within the Ptt interaction but not formally designated. We therefore propose Sptm1 is renamed to Rpt4/Rpt9/Spt3 and Spm1 to Rpt11/Spt4. In addition, with the increased number of alleles being discovered at identified designated loci, e.g., Rph2 and Rps8 with 12 and 27 alleles, respectively, we also propose the removal of the current convention to designate alleles with a letter across all loci within the pathosystem and instead restart with each locus, i.e., Rpt2.b becomes Rpt2.a.

Genomic resources and locus colocalization

Currently, there are over 25 full pseudomolecule chromosome assemblies of barley to assess for allelic diversity, ranging from wild accessions, landraces, and cultivars (Jayakodi et al., 2020; Jiang et al., 2022; Mascher et al., 2021; Sakkour et al., 2022; Sato et al., 2021; Schreiber et al., 2020; Xu et al., 2021), that will no doubt expand with the ever-decreasing cost of long-read sequencing. These resources will allow for the rapid identification of new alleles once genes underlying resistance or susceptibility loci have been validated. In summary, chromosomes 6H and 5H contain the least and most amount of formally designated rust resistance genes, respectively (Figure 1; Table 6); however, this may not hold true as additional loci are added to the portfolio. A limitation of this atlas is that frequently raw data are not readily available to determine the nearest insignificant markers, to precisely delimit the MTA/QTL interval, and ultimately identify overlaps between loci. This is particularly a problem with association mapping studies and would therefore implore all marker data to be published in the future. With numerous studies remapping the same locus and the dearth of novel loci, research should focus on refining the genomic intervals underlying these intervals and gene validation.

A total of eight colocalizations of formally designated loci were identified, including Rps7 with Rpt11/Spt4; Spr1 with Rph1 or Rph17; rps2 with Rph18 or Rph22 and potentially Rpt3; Rps8 and Rph21; Rpt8 and rps5; Rph20 with Rph9/12 and Rps9; rpg4/Rpg5 with Rps10 and Rph28; and Rpt4/Rpt9/Spt3 with Rph3, Rph19, Rps6, and/or Rpsx on chromosomes 1H, 2H, 2H, 4H, 4H, 5H, 5H, and 7H, respectively (Figure 1). Rpg3 appears to colocalize with Rpt10/Spt2; however, the refined Spt2 region does not overlap with Rpg3, and therefore further investigation will be required to determine if Rpt10 colocalizes with Rpg3. The most notable colocalization is Rph28 and Rps10 with rpg4/Rpg5 on chromosome 5H. The Rph28 locus encompasses two of the three genes within the validated rpg4/Rpg5 complex, including the two NLRs of rpg4/Rpg5, Adf2, and two additional zinc fingers. In addition, Rps10 colocalizes with rpg4/Rpg5 and Rph28, although with a larger overlapping interval. Therefore, there is a high likelihood that the validated dual NLR genetic architecture of rpg4/Rpg5 and/or novel alleles of the rpg4/Rpg5 complex is functional against leaf, stripe, and stem rust. Both reports of Rph28 and Rps10 lack mention of the rpg4/Rpg5 complex, despite being validated over a decade ago and providing the most widespread resistance to stem rust, therefore showcasing the importance of high-resolution genetic mapping and developing a barley gene atlas.

Conclusion

This work was initiated due to the fact plant defense responses are highly coordinated and interconnected, with recent research showcasing sympathetic or antagonistic relationships of pathogen recognition mechanisms. Therefore, without a comprehensive resource collating all known resistance/susceptibility loci, identifying previously reported loci within additional accessions against different pathogens, or both, becomes burdensome. We therefore began the process of consolidating loci that confer resistance or susceptibility to three of the most important diseases of barley in leaf, stem, and stripe rust. In addition, previously reported net blotch loci were updated and included in the colocalization analysis. There is often difficulty determining which loci colocalize with each other due to asynchronous marker technologies and the larger mapping intervals of early mapping studies. However, researchers will be able to use this resource to quickly identify previously reported loci without intimate knowledge of these pathosystems, as we show with rpg4/Rpg5, Rph28, and Rps10 loci. Ideally, this atlas will be expanded to include additional fungal diseases as well as bacterial and viral diseases to identify conserved resistance mechanisms or pathogen-specific resistance to inform breeders in the development of highly resistant cultivars.

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