Next Article in Journal
Genetic Diversity of Circumsporozoite Surface Protein of Plasmodium vivax from the Central Highlands, Vietnam
Next Article in Special Issue
Genetic Diversity of Venturia inaequalis in Latvia Revealed by Microsatellite Markers
Previous Article in Journal
Efficacy of Repeated Applications of Bacteriophages on Salmonella enterica-Infected Alfalfa Sprouts during Germination
Previous Article in Special Issue
First Record of Alternaria pogostemonis: A Novel Species Causing Leaf Spots in Pogostemon cablin
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 11
Issue 10
10.3390/pathogens11101157
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Wheat Genes Associated with Different Types of Resistance against Stem Rust (Puccinia graminis Pers.)

by
Anatolii Karelov
1,2,*,
Natalia Kozub
1,2,
Oksana Sozinova
1,2,
Yaroslav Pirko
1,
Igor Sozinov
2,
Alla Yemets
1 and
Yaroslav Blume
1,*
1
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, 04123 Kyiv, Ukraine
2
Institute of Plant Protection, National Academy of Agrarian Sciences of Ukraine, 03022 Kyiv, Ukraine
*
Authors to whom correspondence should be addressed.
Pathogens 2022, 11(10), 1157; https://doi.org/10.3390/pathogens11101157
Submission received: 1 September 2022 / Revised: 25 September 2022 / Accepted: 5 October 2022 / Published: 7 October 2022
(This article belongs to the Special Issue Plant Pathogenic Fungi)
Review Reports Versions Notes

Abstract

:
Stem rust is one wheat’s most dangerous fungal diseases. Yield losses caused by stem rust have been significant enough to cause famine in the past. Some races of stem rust are considered to be a threat to food security even nowadays. Resistance genes are considered to be the most rational environment-friendly and widely used way to control the spread of stem rust and prevent yield losses. More than 60 genes conferring resistance against stem rust have been discovered so far (so-called Sr genes). The majority of the Sr genes discovered have lost their effectiveness due to the emergence of new races of stem rust. There are some known resistance genes that have been used for over 50 years and are still effective against most known races of stem rust. The goal of this article is to outline the different types of resistance against stem rust as well as the effective and noneffective genes, conferring each type of resistance with a brief overview of their origin and usage.

1. Introduction

Biotrophic phytopathogenic fungi are obligate parasites of plants that during evolution developed the ability to penetrate host cells without destruction for obtaining nutrients and energy [1]. Rust fungi of bread wheat (Triticum aestivum L.) cause diseases such as leaf rust (caused by Puccinia recondita Dietel and Holw), yellow rust (Puccinia striiformis var. striiformis Westend), and stem rust (Puccinia graminis Pers.), which may seriously affect wheat yield worldwide [2]. For instance, yield losses could be up to 100% for especially pathogenic races of stem rust [3]. Significant yield losses related to epiphytotics of stem rust were reported in Australia, the USA, Scandinavian countries, Central and South Europe, India, and Asia in the 20th century [4,5]. The situation became even more dramatic in the 21st century starting with stem rust epidemics in Africa. Furthermore, in the last decade there have been significant outbreaks of stem rust in Kenya due to the emergence of new Ug99 races [6], epidemics and devastating yield losses in Ethiopia in 2013 due to the TKTTF race [3], outbreaks in North Kazakhstan and Siberia in 2015–2017 [7,8], epidemics of stem rust in Germany in 2013 [9], the first cases of wheat stem rust infection in the United Kingdom in nearly 60 years [10], an outbreak of stem rust in Southern Italy in durum wheat [11], and further spread of stem rust in Europe [12].
Losses caused by the disease may be explained by the details of the life cycle and pathogenesis of P. graminis. The life cycle of the fungus involves five different spore stages during the asexual reproduction in wheat (the uredinial stage) and sexual reproduction, which starts at the teliospore stage and continues on an alternate host plant (barberry, Mahonia). Ascospores complete the P. graminis life cycle infecting cereals [13]. This process is associated with the formation of urediniospores positioned on the surface of a leaf sheath or a stem and further development of the complex system of penetration of the plant cell, which includes appresoria, a penetration peg, hyphae, haustoria, and a substomatal vesicle to provide nutrients to the parasite. In areas with mild winters and sufficiently wet springs, P. graminis can exist in the uredinial (asexual) state in winter cultivated and wild cereals [4,13]. In the case of significant stem rust infestation of plants, nutrient flow to kernels can be affected causing shriveled grain. Moreover, stems are weakened by the disease resulting in wheat lodging, which causes additional yield losses [13].
Another factor that makes stem rust an especially dangerous disease for wheat is its polymorphism and ability for mutagenesis of the causative agent and the rapid emergence of new P. graminis races, as it is a species with a high-evolutionary potential [14]. Regularly, shortly after the wide implementation of a gene conferring resistance to the disease, a race virulent to that gene emerges causing significant losses to agriculture in some countries [15,16]. Only a few stem rust genes have shown durable effectiveness in breeding history. One of these genes is the stem rust resistance gene on translocation 1BL/1RS from the Petkus rye (Secale cereale L.), which reliably provided stem rust resistance for about 40 years until the emergence of the first race of the Ug99 group, TTKSK, with virulence to Sr31 in Uganda in 1999, which turned out to be virulent to the majority of other widespread resistance genes [15]. Despite preventive measures to localize Ug99, it spread to the southern coast of Africa. In addition, the original race TTKSK has been reported in the Middle East [16]. Moreover, new types (probably mutants) of Ug99 have been detected, which have gained the status of races. In particular, especially virulent not only to Sr31 but also to other genes that, according to initial studies, conferred resistance to Ug99, are the races TTKST, TTTSK, TTKSP, PTKSK, PTKST, TTKSF+, TTKTT, TTKTK, TTHSK, TTHST, PTKTK, TTKTT+, and TTHTT discovered from 2005 to 2020 in Tanzania, Eritrea, Egypt, Rwanda, Kenya, Ethiopia, South Africa, Yemen, Mozambique, Zimbabwe, and Uganda [6,15,16,17,18,19,20,21]. In 2019, the race TTKTT was reported in Iraq [22]. The last decade is characterized by stem rust outbreaks in Europe, Asia, and African regions due to the emergence of new stem rust races with multiple virulences that are distinct from the Ug99 group [3,7,8,9,12,23,24,25,26]. The Digalu race (TKTTF) caused severe epidemics in southern Ethiopia in 2013–2014 when yield losses were up to 100% of the wheat cultivar ‘Digalu’ planted in large areas [3]. Among the currently prevalent European races are TTRTF, TKTTF, and TKKTF. The race TTRTF caused the outbreak of stem rust in Sicily in 2016 [27]. This race was first described in 2014 in Georgia [23] and became widespread in Europe [12]. TTRTF was also detected in 2016 in Eritrea [25] and 2019 in Ethiopia [24] and the south of Iran [25]. This race is avirulent to Sr31 but has virulence to many important genes providing resistance against Ug99 races such as Sr13b, Sr35, Sr37, and Sr50 [12,23]. Moreover, a number of novel stem rust races with virulence to Sr31 and other stem rust genes have been recently described including TKHBK [26] and 22 other races in Spain [12] and the race LTBSK in Western Siberia [12].
Genes conferring resistance against stem rust are referred to as Sr genes [5]. More than 60 genes have been identified to date. Some of them were detected in bread wheat (subsequently referred to as wheat own genes) and others were introgressed from related species. The majority of Sr genes are seedling (all-stage or juvenile) resistance genes. A small number of genes belong to race-nonspecific adult plants resistance genes (APRs). The goal of this article is to outline the different types of resistance against stem rust as well as the effective and noneffective genes, conferring each type of resistance with a brief overview of their origin and usage.

2. Own Resistance Genes in Bread Wheat

The majority of widespread own stem rust resistance genes of wheat are neither effective against races of stem rust that are currently common throughout the world, nor do they confer resistance against the especially dangerous races of the Ug99 group (Table 1) [5,16,17,18,19,20]. For instance, the resistance gene Sr5 on chromosome 6DS originated from the cultivar ‘Kanred’ and developed on the basis of the Ukrainian (Crimean) gene pool, is quite common among modern wheat cultivars [5,28]. Initially the gene conferred race-specific immunity-like resistance. However, cultivars with this gene had been cultivated in large areas so subsequently a number of P. graminis races were able to overcome Sr5 [29,30].
Another wheat own stem rust resistance gene, Sr6 on chromosome 2D, is also quite common. The gene was identified in the Canadian cultivar ‘McMurachy’ and most likely derives from the African wheat gene pool [5,21]. The level of resistance conferred by Sr6 depends on the environmental conditions [31]. Currently many stem rust races are virulent to the gene [29,30]. The Sr7 gene (with alleles a and b) is located on chromosome 4AL [32]. The allele a of the gene was first found in some cultivars from Kenya [28,32]. The resistance level conferred by Sr7 is also largely dependent on environmental conditions and genetic background [33,34] and there are stem rust races with virulence to the allele a of this gene [29,30]. The allele b of Sr7 was introduced into breeding from Australian wheat cultivars unintentionally in the 1920s and also originates from African bread wheat cultivars; the allele confers resistance to the stem rust races that are dominant in Australia [71] but not to Ug99 races [15], TTRTF [11], TKTTF, TKKTF, TKPTF, PKPTF, TKKTP [9] and some other races found in Europe [8,9,12] and Western Siberia [8]. The resistance conferred by the gene Sr8 on chromosome 6AS is associated with the alleles a and b [35,36,37]. The allele a is widely represented among modern cultivars while the allele b is rarely encountered [5,28]. Both alleles confer a moderate level of stem rust resistance (in case of the allele b, the resistance is temperature-dependent), which is overcome by stem rust races that are common worldwide (including by some races that had been reported to be avirulent to it) [29].
The Sr9 gene was localized on chromosome 2BL of wheat [49]. The alleles a and b of the gene originated from common wheat [39,49], but the allele c was transferred from Triticum timopheevii Zhuk. and further designated as Sr36, whereas the allele d was introgressed from T. turgidum subsp. dicoccum (Schrank) Schübl. [72] and g was from T. turgidum (L.) Thell. ssp. durum (Desf.) Husn. [5]. The bread wheat own allele h was initially designated as SrWeb as it derives from the Canadian cultivar Webster [41]. Moreover, it is one of few conferring resistance genes against most Ug99 races, except for TTKSF+ [21], but some other races of stem rust are virulent to this gene [41,72]. Other alleles of Sr9 are more or less sensitive to widespread races of stem rust [5]. Xwms47 is a molecular marker for the allele h of Sr9 [41].
Some of the stem rust resistance genes of wheat are more effective under certain temperature conditions [40,44]. For instance, Sr10, a bread wheat own gene located on chromosome 2B, which was first found in the Kenyan gene pool of bread wheat, is quite common among cultivars developed in different regions in different periods of time [40,42]. The gene is effective under lower temperatures and was characterized as an APR gene [42] but it was not considered to be effective against the currently widespread P. graminis races [73].
The stem rust resistance gene Sr15 was localized on chromosome 7AL, it is race-specific and not effective at temperatures higher than 26 °C [43,44]. Sr15 cosegregates with the leaf rust resistance gene Lr20 [45,46], the root lesion nematode resistance gene Rlnn1, and is closely linked to the powdery mildew resistance gene Pm1 [46]. It was first identified in cv. ‘Norka’ but afterwards was found in cultivars that were not related to it [28,45]. There are many races with virulence to Sr15 and the virulence level might be quite high [29,30]. Initially the gene was considered to confer no resistance against Ug99, but recent research has suggested otherwise [56]. The markers wri1–5, which were proposed to detect Rlnn1, might be also considered as diagnostic markers for Sr15 [46].
The common wheat own gene Sr16 was localized on chromosome 2BL [38,47]. The main source of Sr16 is considered to be cv. ‘Reliance’, and it probably inherited the gene from cv. ‘Kanred’ [5,28]. There are not many modern races of stem rust that are avirulent to this gene [30]. The Sr18 gene is also an ineffective own stem rust resistance gene; it is located on chromosome 1DL, and its origin is unknown [48,49]. The genes Sr19 and Sr20 originated from cv. ‘Marquiz’ and were localized on chromosome 2B [34]. None of them provide resistance against most races of P. graminis [29,73].
The Sr23 gene is effective only at high temperatures and with sufficient lighting [51]. The gene is located on chromosome 2BS and cosegregates with the leaf rust resistance gene Lr16 [51,52]. The sources of this gene are cv. ‘Selkirk’, ‘Exchange’, and ‘Warden’. The diagnostic markers for Lr16 might also be used to detect the Sr23 gene [28,52]. Sr23 is effective against old races of stem rust from the Australian collection but not against modern races with few exceptions [29,73].
Some wheat own stem rust resistance genes were tested with races of the Ug99 group and showed different levels of effectiveness. The Sr28 gene is located on chromosome 2BL and derives from cv ‘Kota’ [53]. Stem rust races that are virulent to this gene are quite common [29] and avirulent races mostly originate from Ethiopia and Nepal [30]. However, the result “moderate resistance–moderate sensitivity” was obtained while testing this gene against Ug99 in Njoro, Kenya in 2004–2005 [54]. In addition, according to literature, Sr28 might confer moderate APR to the stem rust races BCCBC, TTKSK, and TTKST (the latter two belong to the Ug99 group) [55]. The markers wPt-7004 and wmc332 are considered to be diagnostic markers for this gene [56,57].
Sr29 on chromosome 6D is a bread wheat own stem rust resistance gene of European origin [58,59]. The gene decreases the level of infection with some stem rust races, but races from Eastern Europe, Asia, Egypt, Ethiopia, and Turkey are virulent to it [29,30]. The source of the gene Sr30 on chromosome 5DL is Canadian cv. ‘Webster’, which could inherit it from the Russian gene pool [60,61]. The gene is considered to confer a high level of resistance (complete immunity in case of cv. ‘Webster’) against stem rust races that are common in Europe and North America, but some Australian races are virulent to this gene [29,30]. In addition, virulence to Sr30 was detected in races from Spain, Ethiopia, Turkey, Pakistan, and South America [30], namely, TTRTF [11], and Ug99 [15]. The Sr41 gene on chromosome 4D of cv ‘Waldron’ has not been widely employed in breeding programs [62,63]. The gene confers juvenile and adult resistance but not against Ug99 and other races of stem rust prevalent in the world [65].
The Sr42 gene was derived from cv. ‘Norin 40′ and mapped on chromosome 6DS [64]. At the same locus, the genes SrCad from cv. ‘Cadillac’ and SrTmp from cv. ‘Triumph 64′ were localized [41]. All three genes proved to confer resistance against the race TTKSK of the stem rust group Ug99 but among them only SrCad confers resistance against other deleterious races, as TTRTF and some others are virulent to SrTmp [11,20,41]. On the other hand, juvenile resistance conferred by SrCad is expressed on a sufficient level only in plants with the resistance allele of the Lr34/Yr18/Pm38/Bdv1/Sr57 gene [41,70]. Moreover, the SrCad gene is associated with the Bt10 gene conferring resistance to common bunt caused by Tilletia tritici (Bjerk.) G. Winter [41,69]. Among the genes, only for SrCad molecular markers for the resistance allele were developed [69,71].
The Sr48 gene on chromosome 2AL originated from cv. ‘Arina’ [66]. It was considered to confer moderate but stable juvenile resistance against Ug99 races as well as other stem rust races [17]. It was revealed that the gene is quite common among Australian wheat cultivars [66]. Although there are no open sources with molecular markers linked to it, the linkage of the gene with the yellow rust resistance gene Yr1 and microsatellite markers sun590 and sun592, being the closest ones, was reported [66,74].
The Sr49 gene was detected in cv. ‘Mahmaudi’ from Tanzania [66]. It confers resistance against all Australian stem rust races but not against Ug99 [17]. This gene is effective against the race TTRTF but new Spanish races with virulence to this gene have been recently found [12]. The Sr54 gene was localized on chromosome 2DL of cv. ‘Norin 40′ but was not studied due to its low effectiveness against Ug99 and other modern races of stem rust [68].
APR genes should be mentioned separately as they confer a moderate but stable level of resistance against one or several pathogens with low or moderate infection loads and can increase manifestation of other resistance genes [75] (Table 2). Another benefit of APR genes is their effectiveness over a long period of time and the fact that there are no races of the pathogens that completely overcome them [76]. One of the most studied is the Lr34/Yr18/Pm38/Bdv1/Sr57 gene on chromosome 7DS, which confers moderate resistance to all rust species, powdery mildew, and barley yellow dwarf virus [76]. In addition, the Lr34/Yr18/Pm38/Bdv1/Sr57 gene was shown to enhance expression of other known and unknown factors of resistance against stem rust [70], in particular, Ug99 [15,41]. The gene was sequenced and shown to code for a pleiotropic drug resistance-like (PDR-like) ATP-binding cassette (ABC) transporter involved in abscisic acid signaling [77,78]. Codominant and dominant markers cssfr5, SNP12, and ISBP1 for the resistance-associated allele have been proposed [77,79].
Another APR factor, the Lr67/Yr46/Sr55/Pm46/Ltn3 gene, is located on chromosome 4DL [80]. The gene was first identified in the common wheat line PI250413, and the line based on cv. ‘Thatcher’ with the gene was developed [41,80]. The gene was shown to confer moderate resistance against the stem rust races of the Ug99 group [81]. The sequencing of the Lr67/Yr46/Sr55/Pm46/Ltn3 gene revealed that it encodes a hexose transporter [86]. The Sr56 gene was discovered in cv. ‘Arina’ and localized on chromosome 5BL [82]. It confers APR that decreases stem rust infection by 12–15% [83]. Another APR gene, Lr46/Yr29/Pm39/Sr58, was localized on chromosome 1BL of cvs. ‘Pavon 76′ and ‘Lalbahadur’ [85,87].

3. Introgressed Stem Rust Resistance Genes

The diversity of Sr genes in the bread wheat gene pool was substantially enriched by the transfer of Sr genes from species belonging to its primary, secondary, as well as tertiary gene pools [88] (Table 3). The Sr11 gene was introgressed from cv. ‘Gaza’ of the tetraploid wheat T. turgidum ssp. durum [32]. The gene was localized on chromosome 6BL [62]. Stem rust races that are virulent to this gene may be encountered in Australia [89], South Africa [90], Canada [91], and the USA [92] but the gene is considered to confer resistance against the races common in Europe and India [29,30]. There were also reports about a low level of virulence to this gene in the races of P. graminis common in China and some regions of Africa [90].
The Sr12 gene was transferred to cv. ‘Marquillo’ and afterwards ‘Thatcher’ from cv. ‘Iumillo’ of T. turgidum ssp. durum [95]. The gene had been sufficiently effective until 1950 when the especially virulent stem rust race emerged [5]. However, there is evidence that the resistance level of Sr12 carriers significantly increases in the presence of other resistance genes, such as Sr9 [92].
The Sr13 gene was introgressed into common wheat cv ‘Khapstein’ from T. turgidum ssp. dicoccum cv ‘Khapli C.I.4013’ [95] to chromosome 6AL [36]. The gene is temperature-sensitive (the highest resistance level was observed at 20–28 °C) and confers moderate resistance against stem rust races that are common in Pakistan and India, but the races found in Europe and North America are highly virulent to this gene [29,30]. The Sr13 gene is considered to confer juvenile resistance against all the races of the Ug99 group [96]. A precise and convenient molecular marker for Sr13 was developed [132]. The cloned candidate gene encodes the CNL13 protein containing coiled-coil (CC), nucleotide-binding (NB), and leucine-rich repeat (LRR) domains, which are traditional for juvenile race-specific gene products. [96]. However, the authors indicated that the Sr13-mediated resistance is associated with the slower growth of the pathogen at high temperatures but not with the rapid cell death typical for the hypersensitivity response. In the later research, four different haplotypes of the gene, R1 (allele Sr13a), R2 (Sr13b), R3 (Sr13c), and R4 (Sr13d, susceptible to TTKSK and some other races tested) were discovered with use of more precise markers. The haplotypes provide different levels of resistance to some races of stem rust at different temperatures [133]. Sr13 alleles differ in reaction to the race TTRTF, which is virulent on Sr13b and avirulent on Sr13a [23].
The Sr14 gene was transferred from T. turgidum var. dicoccum cv. ‘Khapli’ to hexaploid cv. ‘Steinwedel’, and as a result cv. ‘Khapstein’ was obtained [44]. The gene was localized in the pericentromeric region of chromosome 1BL [134,135]. The resistance associated with Sr14 manifests at high temperatures and with good lighting [29,44]. The gene does not confer resistance to the races common in the USA [30]. The gene Sr17 on chromosome 7BL is one of the few recessive resistance genes and the only such gene that confers resistance to stem rust [136]. The gene originates from T. turgidum ssp. dicoccum cv. Yaroslav. It was introgressed into cv. ‘Hope’ and line ‘H-44′ together with other resistance genes [93]. The gene is effective at temperatures lower than 25 °C [136]. There are stem rust races worldwide that are virulent to this gene [29,30,73].
The Sr21 gene can be found in the samples of T. monococcum L. including line ‘Einkorn C.I.2433′, which is used as a differentiator [97,137]. This gene is more effective at higher temperatures (20–24 °C) than at lower temperatures (16 °C) [138]. Sr21 was localized on chromosome 2AL [138]. The races virulent to Sr21 are often met in North [73] and South America [30], there are also virulent mutants in Australia [74]. However, the gene confers resistance to most races of Ug99 [75,138]. To identify Sr21, the molecular markers FD527726 (0.15 cM distal), EX594406 (0.05 cM, proximal), and microsatellite Xgwm312 can be used [138]. The gene encodes a CC-NB-LRR protein (NLR) and accounts for the upregulation of multiple pathogenesis related genes at high temperatures [139].
The Sr22 gene was derived from T. monococcum ssp. boeoticum and localized on chromosome arm 7AL of bread wheat [140]. The gene is temperature-sensitive and effective at lower temperatures [5], and the Sr22b allele was recently identified [141]. Sr22 is effective against the Ug99 races but is linked with genes affecting agronomic traits of wheat [75,142]. The markers Xcfa2123, Xwmc633, XcsIH81-BM, and XcsIH81-AG were identified as closely linked to the gene, the latter is considered to be a diagnostic marker [142]. Sr22 was cloned and its product was shown to contain typical CC, NB, and LRR regions although the gene was shown to belong to a small gene family with three homologs [143]. Fourteen orthologs of the Sr22 gene were later reported both in T. boeoticum and other related species including T. aestivum although only one of them seemed to confer resistance to P. graminis [144].
The Sr24 gene was transferred to chromosome 3DL of bread wheat from the wild grass Thinopyrum ponticum (Podp.) Z.-W.Liu and R.-C.Wang (syn. Agropyron elongatum (Host) P. Beauv.) [100,145]. Although stem rust races with virulence to this gene were detected in South Africa [90], India [146], and Australia [5], the gene confers resistance against the majority of widespread P. graminis races [29,30], including the race TTRTF [11]. Moreover, Sr24 confers resistance against some of the Ug99 races [15,21]. The marker Sr24#12 is suggested to be completely linked to the gene [147]. Another gene conferring resistance against Ug99, is Sr25 cosegregating with Lr19 on the chromosomal fragment introgressed from Th. ponticum to chromosome 7DL [101,102]. The gene is not widely involved in breeding programs because it is linked with an undesired phenotypic trait, the yellow flour color [102,148]. The marker BF145935 was validated for the Sr25 gene [149]. Sr26 was also transferred from Th. ponticum [103]. The translocation is suggested to be full (6A/6Ag) but there is also evidence for a partial exchange with arms 6AL or 6AS [150]. The Sr26 gene confers resistance against the Ug99 races [15]. The translocation of the 6AS/6AL-6Ae#1L segment with the gene may cause a 9% decrease in yield [99]. Nevertheless, this gene is employed for improving stem rust resistance [151]. A codominant system to detect the gene was developed. The marker Xsr26#43 produces a 233-bp fragment in case of resistance, and marker XBE51879 produces a fragment of 328 bp if the gene is absent [152]. The Sr26 gene was cloned and found out to belong to the NLR family such as the majority of cloned wheat resistance genes [127].
The Sr27 gene originated from rye (S. cereale) cv. ‘Imperial’ and was localized on the 3A-3R translocation [104]. It is effective against Ug99 races [15,54] and virulence to this gene is quite rare as it can be found among greenhouse mutants of P. graminis, hybrids created in a laboratory, as well as African races including the ones from the Ug99 group [153]. Since the mid-1950s, the rye 1RS arm carrying the stem rust resistance gene Sr31 has been introgressed into many wheat cultivars [105,154]. The gene conferred resistance to all known races of stem rust at the time [155]. The SCAR markers for the translocation with the gene were developed [154]. However, TTKSK and other P. graminis races of the Ug99 group are able to infect plants with Sr31 [15]. Nevertheless, this gene proved to be effective against the race TTRTF. In 2022, a novel Spanish stem rust race TKHBK with virulence to Sr31 was reported [26]. Moreover, Patpour et al. [12] described 22 Spanish races with virulence to Sr31, of which 14 were found on bread wheat and the others on rye and Elymus repens, in areas of proximity to barberry, and one race with virulence to Sr31 (LTBSK) in Western Siberia.
The Sr32 gene was introgressed from Aegilops speltoides Tausch independently in several cases into all the group 2 chromosomes [106,156]. According to previous research in the USA, Canada, Mexico, and Southern Africa, no races virulent to the gene were discovered [136] until recently when a race with virulence to Sr32 was detected in Kazakhstan [7]. The gene was not widely used in breeding programs because of the trait adherent glume and other harmful traits [156]. The markers Xstm773 and Xbarc55 are considered to be diagnostic markers for this gene [106].
The Sr33 gene was first localized in Ae. tauschii Coss. and then transferred to chromosome 1DS of bread wheat [107,157]. The Sr33 gene is effective against Ug99 races of stem rust [15]. No race virulent to the Sr33 gene had been discovered during the field trials of wheat samples with the gene [30,54] until recently in Spain [26]. The gene was discovered to confer a significantly higher level of resistance when expressing in diploid plants (Ae. tauschii), while in T. aestivum the level of race-specific resistance was evaluated as moderate resistance—moderate susceptibility in the case of especially harmful races [54]. The study of expression of the gene revealed that it manifests itself as a common race-specific R-gene conferring resistance to biotrophic pathogens forcing hypersensitive cell death to prevent disease spread and feeding [158]. The first molecular markers that were considered to be effective for detection of the Sr33 gene were Xbarc152 and Xcfd15 [159]. The Sr33 gene and other closely linked genes AetRGA1a-d, AetRGA2a, and AetRGA3a were further cloned; the gene was found to contain six exons and the protein had the structure common for factors of juvenile resistance including a nucleotide binding site, an N-terminal CC, and a C-terminal LRR [160]. In further studies of the CC domain of SR33, additional similarity of its spatial structure to other proteins associated with race-specific resistance was discovered, and hypotheses of hypersensitive response triggered by this, and other proteins were confirmed [161]. Furthermore, the SR33 protein is homologous to MLA34 of barley conferring resistance against powdery mildew (Blumeria graminis f. sp. hordei) and TmMLA, an MLA-like protein of T. monococcum (the homology level in both cases is up to 86%), while the homology level for earlier discovered resistance associated proteins of wheat LR1, LR10 and LR21 was fairly low [160]. The SR33 protein, unlike proteins analogues, does not need chaperone proteins [161].
The Sr34 gene was transferred from the wild relative Ae. comosa Sibth. and Sm. to chromosome 2A (the 2A-2M translocation) and 2D (the 2D-2M translocation) together with the yellow rust resistance gene Yr8 [93]. Sr34 is considered to be more effective at lower temperatures. Avirulence to this gene is not common in Australia but more intrinsic for stem rust races from Southern Asia, China, Ethiopia, Kenya, and South America [29,30,152]. However, the gene does not confer resistance against Ug99 races [54].
The resistance gene Sr35 was transferred from T. monococcum to chromosome 3AL of common wheat [162] and confers resistance against the race TTKSK (Ug99) of stem rust and its variants TTKST and TTTSK [15,21,54]. The gene proved to confer resistance to moderate resistance under the infection background with a comparatively mild course of the disease during the field trials in Kenya in 2005–2006 [54]. Sr35 confers resistance to P. graminis races common in Australia and North America but there are races virulent to the gene in Ethiopia, Kenya, Malaysia, Nepal, Brazil, Chile, Argentina, and China [30]. The races TTRTF and TTKTF of clade IV-E2, which are currently found in Europe, are also virulent to this gene [12,23]. The markers XAK335187 and Xcfa2170 are considered to be closely linked with this gene [163]. Sr35 was sequenced and identified as identical to the CNL9 gene candidate having a 196 bp 5′UTR and a 1526 bp 3′UTR that includes three introns. Orthologs for the gene as well as for Sr13 were identified based of DNA sequences from related species [163].
The Sr36 gene was introgressed from T. timopheevi on chromosome 2BS and first designated as the allele Sr9c [109]. It confers resistance against the original Ug99 race of P. graminis but virulence of other races from the Ug99 group was reported [15,16,17,18,19,21]. Furthermore, cases of serious infestation with stem rust of cultivars with this gene in Australia and North America were reported, and other isolates virulent to Sr36 were also revealed [30]. Sr37 is another gene that is transferred from T. timopheevi [110]. The translocation with the gene and other potential resistance factors was localized on chromosome 4B but it has not gained major distribution [5]. According to the literature, races of stem rust virulent to the gene are quite common [29,30] and include TTRTF [23]. However, this gene is effective against Ug99 races [164].
The Sr38 gene was localized on a 2AS-2NS translocation from Ae. ventricosa Tausch together with the leaf rust resistance gene Lr37 and the yellow rust resistance gene Yr17 [111]. Virulence to Sr38 was first detected in 2000–2001 in South Africa and since then, in addition to the Ug99 group, it has been defeated by many stem rust races in European and Asian regions [12,165].
The Sr39 gene was localized on arm 2S introgressed into chromosome 2B of wheat from Ae. speltoides [112]. On the same arm at a distance of 3 cM, the leaf rust resistance gene Lr35 was localized [166]. The Sr39 gene confers juvenile and adult plant resistance at a level of resistance to moderate resistance to all races of stem rust known at the moment, including Ug99 [15,54]. RL6082 and other wheat lines obtained as a result of introgression showed a significant increase in flour water absorption and significant degradation of flour quality and other agronomic traits [112,163]. Therefore, attempts to decrease the size of the introgressed fragment keeping the Sr39 and Lr35 genes were made [167,168]. In particular, based on line RL5711 with the 2B-2S translocation, lines #220 and #247 were developed with the gene and the markers Sr39#50s and Sr39#22r for the Sr39 gene were developed [167]. Line #247 was used in breeding programs in Australia [167]. Other authors took RL6082 as a basis and with the use of the improved scheme for chromosome engineering obtained red wheat lines RWG1, RWG2, and RWG3 with reportedly small parts of the chromosome 2S. The authors proposed the markers Xrwgs27, Xrwgs28, and Xrwgs29 as more convenient for breeding [167]. Further validation of the markers for the Sr39 gene was carried out with use of a large amount of cultivars and lines. Based on this, Sr39#50s and Sr39#22r were considered precise and convenient but Xrwgs27, Xrwgs28 and Xrwgs29 were not precise enough or produced amplified fragments that were hard to distinguish with electrophoresis. Addtionally, the marker Xwmc474 was described and considered to be a diagnostic marker for the Sr39 gene [169].
The Sr40 gene was introduced from T. timopheevii subsp. armeniacum (Jakubz.) Slageren on translocation 2B-2G#2S [113]. The resulting line RL6088 was considered to be resistant against all the races of stem rust, including Ug99 [15,54]. However, a unique race with virulence on Sr32 and Sr40 was recently reported in Kazakhstan [7]. The line RL6088 was used to map the introgressed arm and the markers Xgwm319, Xwmc344, Xwmc474, Xwmc477, Xgwm374, and Xwmc661 were discovered to be linked to the gene of interest [114]. None of the markers were validated by other authors although it was claimed that the marker Xsr39#22r could detect the Sr40 gene in the breeding material that does not carry the Sr39 gene [169]. The fragment of the chromosome with the Sr40 gene also carries traits affecting flour quality and other agronomic traits [114].
The Sr43 gene was first discovered in Th. ponticum due to its effectiveness against stem rust and then successfully transferred to common wheat on the translocation 7DS-7el2L [115,170]. The gene has not gained major distribution because the translocated chromosome arm also carried factors affecting agricultural quality, in particular for yellow flour color [115]. The Sr44 gene derives from a partial amphyploid of wheat with the wild relative Thinopyrum intermedium (Host) Barkworth and D.R. Dewey (translocation 7DL-7J#1S) and confers resistance against all the biotypes of Ug99 [116]. However, Australian and European races of stem rust with virulence to this gene were discovered [12,116].
The Sr45 gene on chromosome 1DS was introgressed from Ae. tauschii [117,171]. It confers resistance against all the races of Ug99 and stem rust races that are common in India and Australia, but virulence to this gene was reported for races in Canada [117] and the novel Spanish race TKGLK [12]. The gene was cloned with use of the same technique as Sr22 and was also found to encode a CC-NB-LRR protein belonging to a family with 8–12 homologs [143]. The Sr46 gene was transferred from Ae. tauschii var. meyeri on chromosome 2DS. Virulence to this gene was discovered among stem rust races distributed over the world. Tests with Ug99 and wheat lines with Sr46 have been not carried out although the samples of Ae. tauschii with the gene showed juvenile resistance against the race TTKSK [118]. The gene was sequenced by conventional fine mapping in segregating diploid progenitor and wheat populations coupled with the sequencing of candidate genes in this region and was discovered to encode a CC-NB-LRR protein [172]. The Sr47 gene was introgressed from Ae. speltoides on the translocation 2BL-2SL 2SS [119,120]. During all the field trials it conferred total resistance against stem rust, but trials with Ug99 have not been carried out [120].
The Sr50 gene originates from rye cv. ‘Imperial’ (translocation 1DL.1DS-1R#3S-1DS) and confers resistance to Ug99 races but is sensitive to some other common races of P. graminis [121], in particular to TTRTF and the novel Spanish race KKGBM [12]. The gene was cloned and found out to be homologous to the barley Mla, encoding a CC-NB-LRR protein. The resistance conferred by it was discovered to be different from Sr31 and other genes on rye chromosome 1RS and molecular genetic markers for the gene were described [173]. The gene product was shown to interact with the pathogen in a way that has been described for CC-NB-LRR proteins and involved recognition of the corresponding AvrSr50 product. P. graminis races virulent to the gene were shown to express the protein with a substitution in a single surface-exposed residue or did not express it at all due to mutations in the gene [174].
The SrAmigo (Sr1RSAmigo) gene was introgressed as part of the 1AL/1RS translocation from the Argentinian rye cv. ‘Insave’ [131]. The first cultivar with the translocation was ‘Amigo’ registered in the USA in 1976, which obtained the translocation from the octoploid triticale cv. ‘Gaucho’ [175]. The presence of the translocation with the gene can be easily detected by electrophoresis of storage proteins. The SrAmigo gene confers moderate race-specific resistance against biotypes of Ug99 but is not effective against some other races of stem rust, in particular TRTTF [176] and TKKTP [9,173]. However, according to Patpour et al. [12], TKKTP is avirulent to this gene.
The Sr51 gene was transferred from Ae. searsii Feldman and Kislev ex K. Hammer on translocations 3AL-3SSS, 3BL-3SSS, and 3DL-3SSS and translocation recombination 3DS-3SSS/3SSL [122]. The gene confers total resistance against Ug99 and other races of stem rust it was trialed with, but the work to localize and introduce it on a smaller chromosome fragment is still in progress [122].
The Sr52 gene originates from the wild grass Dasypyrum villosum (L.) Borbas (translocation 6AL-6V.3L) [123]. It confers temperature-sensitive (effective within the temperature range 18–26 °C) resistance against the original race of Ug99 and other races of stem rust. In addition, possible coexpression with the increased level of resistance between this gene and others on the translocated arm or those of T. aestivum was reported [123]. However, it is ineffective against many currently prevalent European stem rust races [12].
The Sr53 gene was obtained from Ae. geniculata Roth by translocation of the chromosome 5M(g)L/5M(g)S part to arm 5DL [124]. The gene confers moderate juvenile as well as adult resistance against all the races of stem rust, including Ug99. The Sr59 gene was transferred from the rye S. cereale on the 2DS·2RL Robertsonian translocation, mapped, and proved to confer resistance against the Ug99 races of stem rust [125].
The Sr60 gene was transferred to common wheat from T. monococcum chromosome 5AmS. It is effective against the races QFCSC, QTHJC, and SCCSC but not the Ug99 group. The gene is closely linked to the markers CJ942731 and GH724575 and completely linked to LRRK123.1 [126]. Sr60 is 5008 bp in length with a complete coding sequence of 2175 bp; the predicted protein is 724 amino acids long and unlike most of the sequenced wheat resistance genes contains two putative protein kinase domains [126]. The Sr61 gene had been previously designated as SrB and was, such as Sr26, transferred from Th. ponticum. The gene proved to confer resistance to a set of races of stem rust other than Sr26 [127]. Similar to Sr26, it was also sequenced and found to be of the NLR type [127]. The Sr62 gene was introgressed into common wheat from Ae. sharonensis Eig on translocation 1SshS·1SshL-1BL/1SshS·1SshL-1DL [128,129]. The gene proved to confer resistance against some races of the Ug99 group. It was mapped, and KASP markers were developed [177].
Resistance conferred by the Sr63 gene was first described in T. turgidum cv. ‘Glossy Huguenot’ as an APR [178]. Recently the gene was mapped to chromosome 2AL, proved to confer resistance against all races of stem rust including Ug99, and closely linked molecular markers for its detection were developed [130]. Another gene conferring race nonspecific APR against stem rust and race-specific juvenile resistance against leaf rust as well as tolerance against powdery mildew is Sr2/Lr27/Pbc [93,94]. The gene was transferred from emmer wheat (T. turgidum ssp. dicoccum) cv. ‘Yaroslav’ in the 1920s and was reported by McFadden in 1930. As a result, cv. ‘Hope’ was obtained [93]. Further, it was discovered that APR in cv. ‘Hope’ was conferred by a single gene designated as Sr2 [179]. Resistance conferred by the Sr2 gene is associated with a decreased number of uredinia in infected plants. The gene was discovered to provide the highest level of resistance at the flowering stage [180]. The gene remains effective for more than 80 years and no stem rust race, including Ug99, is virulent against it [94,181]. In addition, the ability to enhance unknown factors of stem rust resistance was discovered for this gene, as with other APR genes [182]. Identification of resistance conferred by the gene in the field is complicated due to the moderate level of expression [183,184]. The main morphological trait of Sr2 is pseudo black chaff, which was reported to manifest itself unevenly in the field depending on other genes and temperature [184]. The juvenile leaf rust resistance gene Lr27, which was discovered to cosegregate with Sr2, needs resistance associated with the Lr31 gene to fully manifest itself [94].
The Sr2 gene was localized on the short arm of chromosome 3B [185]. On the first genetic map, the Lr27 and Sr2 genes were mapped at some genetic distance [183]. Gwm533 was the first molecular marker with a sufficient level of polymorphism, which was used in breeding for the resistance associated allele. It has three alleles: the 0 and 155 bp alleles are mostly associated with a lack of resistance and the 120 bp allele is mostly associated with resistance conferred by the gene [185]. Further, based on the marker sequence, STS markers stm598ctac and stm598gtag were developed; the markers have several alleles and only one for each marker (56~61 bp and 83~85 bp, respectively) was associated with resistance [186]. Additionally, based on the BAC library of wheat, a more detailed genetic map for chromosome 3B, including the Sr2 region, was developed and subsequently, more tightly linked markers were discovered: BE426676, BE401794, BE500189, CA640157, and BE591959. Among them, BE500189 and CA640157 showed the closest linkage, 0.14 cM and 0.07 cM, respectively [187]. Moreover, a number of SSR markers 3B028F08, 3B042G11, and 3B061C22 were developed based on the BAC map [188]. The SSR markers are close enough to the Sr2 gene, but they were found to have different alleles for the samples with the same allele of the Sr2 gene during trials with a number of lines and cultivars [169]. Recently, the SCAR marker csSr2 was identified based on the data from the BAC library of cv. ‘Hope’ 3B chromosome partial sequence. It was discovered that resistance and susceptibility-associated alleles differ by a single nucleotide polymorphism and in case of the resistance-associated allele there is a restriction site for enzyme BspHI; the marker is precise and does not segregate with the Sr2 gene (the estimated degree of accuracy is around 95%) [94]. More detailed mapping of the Sr2/Lr27/Pbc locus was carried out and the candidate genes that could confer Sr2-like resistance were proposed namely: TaGLP3_1/TaGLP3_2, TaGLP3_3/TaGLP3_4, TaGLP3_10, TaGLP3_6, TaGLP3_5, TaGLP3_8/TaGLP3_9. The location of the marker csSr2 was further revised and another marker was identified [118].

4. Conclusions

Numerous genes conferring resistance to stem rust have been discovered to date either in the gene pool of common wheat or in related species. Although many of them do not confer resistance to Ug99 races, some, such as Sr31, are still effective against other numerous modern and devastating races of P. graminis [11,23]. On the other hand, other genes that were considered to not be effective against modern races of stem rust appeared to have some value conferring resistance against Ug99 [56]. In accordance with recent discoveries, the Ug99 races of P. graminis should not be the only races considered as a threat to wheat production worldwide [3,9,12,25,26]. Introgressed R-genes, such as Sr33, seem to be the most effective at providing “strong” types of resistance against almost all the races of stem rust known to date [160] Such resistance is based on a gene-for-gene interaction with the pathogen and recognition of the pathogen’s effectors. However, as effectors are usually encoded by a single gene, mutations often cause an emergence of new races virulent to race-specific genes [1,6,7,174]. Resistance conferred by Sr2, as well as other APR genes, is based on more elaborate mechanisms of physiological responses to the pathogen invasion in general, therefore it seems to be far more promising on a long-term scale [76,189].
The studies of QTLs related to stem rust resistance in modern wheat cultivars mostly revealed the effectiveness and coexpression of known genes against the races used, but potential loci related to P. graminis resistance were discovered as well [181,190,191]. For instance, stem rust resistance of the spring wheat line ‘CI 14275′ to the races TTKSK, TRTTF, TPMKC, TTTTF, and RTQQC was shown to be conferred not only by the Sr12 gene but also by the unknown QTLs QSr.cdl-2BS.2 and QSr.cdl-6A [192]. Based on RIL populations from cv. ‘Baguette 13′, cv. ‘INIA Tero’, and line BR23//CEP19/PF85490′, QTLs on chromosomes 2B, 6A, and 7B were identified, of which the QTL on 2B was effective against Ug99 [59]. The QSr.umn-2B.2 QTL on chromosome 2B conferring APR against African and North American stem rust races (including the Ug99 race group) in four environments in the RB07/MN06113-8 population has been reported in the literature [166]. In addition, several minor QTLs on different chromosomes and major QTLs on chromosomes 1A and 1B were discovered [193].
To date stem rust resistance genes such as Sr13, Sr21, Sr22, Sr26, Sr33, Sr35, Sr45, Sr46, Sr50, Sr55, Sr57, Sr60, and Sr61 were sequenced [77,86,96,126,127,143,163,172,173,174]. Of them, only two (Sr55 and Sr57) are APRs and bread wheat own genes. Considering the importance of not only using stem rust resistance genes in breeding but also understanding the mechanisms of resistance, such studies are of prime value. New approaches such as “rapid cloning”, which was used for the Sr22 and Sr45 genes [143], and “sequence capture” which was used to clone Sr46 [172], might be considered as a way forward to sequence other stem rust resistance genes for studying special features of the expression of Sr genes in response to the pathogen and their involvement in plant immunity mechanisms.
Stem rust caused by P. graminis remains a constant threat to agriculture worldwide. New races have emerged that are virulent to the resistance genes which were considered to be effective even several decades ago. On the other hand, some Sr genes previously considered as ineffective have proved to be of use as they might provide resistance to new exotic races of stem rust. Moreover, when pyramided with other race-specific genes or genes conferring race-nonspecific moderate APR any resistance gene may take part in complex and durable stem rust resistance. The search for new Sr genes, especially APR genes, continues to be of primary importance. In this context, the report about the identification of the SrPan3161 gene on chromosome 4D in bread wheat cultivar PAN 3161, which accounts for 71.5% of the phenotypic variation for field resistance to the Ug99-group race PTKST, is very promising. This gene derives from the cultivar Tugela and may represent a novel APR [194].

Author Contributions

Conceptualization, Y.B. and I.S.; writing—original draft preparation, A.K., N.K. and O.S.; writing—review and editing, A.K., N.K., A.Y., Y.P. and Y.B.; supervision, Y.B. All authors have read and agreed to the published version of the manuscript.

Funding

This review was prepared and structured as a project of the National Research Foundation of Ukraine # 2224 “Creation of wheat gene pool to prevent Ug99 stem rust epiphytotics as a guarantee of food security in Ukraine“, however, financial support has been postponed due to the war against of Ukraine.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We acknowledge V. Kyrylenko (Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv) for giving suggestions aimed to improve the manuscript language.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 2005, 43, 205–227. [Google Scholar] [CrossRef]
  2. Simón, M.R.; Börner, A.; Struik, P.C. Editorial: Fungal wheat diseases: Etiology, breeding, and integrated management. Front. Plant Sci. 2021, 12, 671060. [Google Scholar] [CrossRef]
  3. Olivera, P.; Newcomb, M.; Szabo, L.J.; Rouse, M.; Johnson, J.; Gale, S.; Luster, D.G.; Hodson, D.; Cox, J.A.; Burgin, L.; et al. Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in Southern Ethiopia in 2013–2014. Phytopathology 2015, 105, 917–928. [Google Scholar] [CrossRef] [Green Version]
  4. Schumann, G.L.; Leonard, K.J. Stem rust of wheat (black rust). Plant Health Instr. 2000. [Google Scholar] [CrossRef]
  5. McIntosh, R.A.; Wellings, C.R.; Park, R.F. Wheat Rusts: An Atlas of Resistance Genes; CSIRO: Canberra, Australia, 1995; ISBN 978-94-010-4041-9. [Google Scholar]
  6. Newcomb, M.; Olivera, P.D.; Rouse, M.N.; Szabo, L.J.; Johnson, J.; Gale, S.; Luster, D.G.; Wanyera, R.; Macharia, G.; Bhavani, S.; et al. Kenyan isolates of Puccinia graminis f. sp. tritici from 2008 to 2014: Virulence to SrTmp in the Ug99 race group and implications for breeding programs. Phytopathology 2016, 106, 729–736. [Google Scholar] [CrossRef] [Green Version]
  7. Olivera Firpo, P.; Szabo, L.; Kokhmetova, A.; Morgunov, A.; Luster, D.G.; Jin, Y. Puccinia graminis f. sp. tritici population causing recent wheat stem rust epidemics in Kazakhstan is highly diverse and includes novel virulences. Phytopathology 2022. [Google Scholar] [CrossRef]
  8. Skolotneva, E.S.; Kosman, E.; Patpour, M.; Kelbin, V.N.; Morgounov, A.I.; Shamanin, V.P.; Salina, E.A. Virulence phenotypes of Siberian wheat stem rust population in 2017–2018. Front. Agron. 2020, 2, 6. [Google Scholar] [CrossRef]
  9. Olivera Firpo, P.D.; Newcomb, M.; Flath, K.; Sommerfeldt-Impe, N.; Szabo, L.J.; Carter, M.; Luster, D.G.; Jin, Y. Characterization of Puccinia graminis f. sp. tritici isolates derived from an unusual wheat stem rust outbreak in Germany in 2013. Plant Pathol. 2017, 66, 1258–1266. [Google Scholar] [CrossRef]
  10. Lewis, C.M.; Persoons, A.; Bebber, D.P.; Kigathi, R.N.; Maintz, J.; Findlay, K.; Bueno-Sancho, V.; Corredor-Moreno, P.; Harrington, S.A.; Kangara, N.; et al. Potential for re-emergence of wheat stem rust in the United Kingdom. Commun. Biol. 2018, 1, 13. [Google Scholar] [CrossRef] [Green Version]
  11. GRRC Report: Samples of Stem Rust Infected Wheat from ITALY. 01/2016 // Aarhus University, Department of Agroecology. 2016. Available online: https://agro.au.dk/fileadmin/Country_report_Sicily_-_November2016.pdf (accessed on 30 August 2022).
  12. Patpour, M.; Hovmøller, M.S.; Rodriguez-Algaba, J.; Randazzo, B.; Villegas, D.; Shamanin, V.P.; Berlin, A.; Flath, K.; Czembor, P.; Hanzalova, A.; et al. Wheat stem rust back in Europe: Diversity, prevalence and impact on host resistance. Front Plant Sci. 2022, 13, 882440. [Google Scholar] [CrossRef]
  13. Leonard, K.J.; Szabo, L.J. Pathogen profile: Stem rust of small grains and grasses caused by Puccinia graminis. Mol. Plant Pathol. 2005, 6, 99–111. [Google Scholar] [CrossRef]
  14. McDonald, B.A.; Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 2002, 40, 349–379. [Google Scholar] [CrossRef] [Green Version]
  15. Pretorius, Z.A.; Singh, R.P.; Wagoire, W.W.; Payne, T.S. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis. 2000, 84, 203. [Google Scholar] [CrossRef]
  16. Singh, R.P.; Hodson, D.P.; Huerta-Espino, J.; Jin, Y.; Bhavani, S.; Njau, P.; Herrera-Foessel, S.; Singh, P.K.; Singh, S.; Govindan, V. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 2011, 49, 465–481. [Google Scholar] [CrossRef] [Green Version]
  17. Singh, R.P.; Hodson, D.P.; Jin, Y.; Lagudah, E.S.; Ayliffe, M.A.; Bhavani, S.; Rouse, M.N.; Pretorius, Z.A.; Szabo, L.J.; Huerta-Espino, J.; et al. Emergence and spread of new races of wheat stem rust fungus: Continued threat to food security and prospects of genetic control. Phytopathology 2015, 105, 872–884. [Google Scholar] [CrossRef] [Green Version]
  18. Pretorius, Z.A.; Szabo, L.J.; Boshoff, W.H.P. First report of a new TTKSF race of wheat stem rust (Puccinia graminis f. sp. tritici) in South Africa and Zimbabwe. Plant Dis. 2012, 96, 590. [Google Scholar] [CrossRef]
  19. Fetch, T.; Zegeye, T.; Park, R.F.; Hodson, D.; Wanyera, R. Detection of wheat stem rust races TTHSK and PTKTK in the Ug99 race group in Kenya in 2014. Plant Dis. 2016, 100, 1495. [Google Scholar] [CrossRef]
  20. Patpour, M.; Hovmøller, M.S.; Justesen, A.F.; Newcomb, M.; Olivera, P.; Jin, Y.; Szabo, L.J.; Hodson, D.; Shahin, A.A.; Wanyera, R.; et al. Emergence of virulence to SrTmp in the Ug99 race group of wheat stem rust, Puccinia graminis f. sp. tritici, in Africa. Plant Dis. 2016, 100, 522–552. [Google Scholar] [CrossRef]
  21. RustTracker.org. Pathotype Tracker—Where Is Ug99? 2021. Available online: https://rusttracker.cimmyt.org/?page_id=22 (accessed on 21 August 2022).
  22. Nazari, K.; Al-Maaroof, E.; Kurtulus, E.; Kavaz, H.; Hodson, D.; Ozseven, I. First report of Ug99 race TTKTT of wheat stem rust (Puccinia graminis f. sp. tritici) in Iraq. Plant Dis. 2021, 105, 2719. [Google Scholar] [CrossRef]
  23. Olivera, P.D.; Sikharulidze, Z.; Dumbadze, R.; Szabo, L.J.; Newcomb, M.; Natsarishvili, K.; Rouse, M.N.; Luster, D.G.; Jin, Y. Presence of a sexual population of Puccinia graminis f. sp. tritici in Georgia provides a hotspot for genotypic and phenotypic diversity. Phytopathology 2019, 109, 2152–2160. [Google Scholar] [CrossRef]
  24. Tesfaye, T.; Chala, A.; Shikur, E.; Hodson, D.P.; Szabo, L.J. First report of TTRTF race of wheat stem rust, Puccinia graminis f. sp. tritici in Ethiopia. Plant Dis. 2019, 104, 293. [Google Scholar] [CrossRef]
  25. Patpour, M.; Justesen, A.F.; Tecle, A.W.; Yazdani, M.; Yasaie, M.; Hovmøller, M.S. First report of race TTRTF of wheat stem rust (Puccinia graminis f. sp. tritici) in Eritrea. Plant Dis. 2020, 104, 973. [Google Scholar] [CrossRef]
  26. Olivera, P.D.; Villegas, D.; Cantero-Martínez, C.; Szabo, L.J.; Rouse, M.N.; Luster, D.G.; Bartaula, R.; Lopes, M.S.; Jin, Y. A unique race of the wheat stem rust pathogen with virulence on Sr31 identified in Spain and reaction of wheat and durum cultivars to this race. Plant Pathol. 2022, 71, 873–889. [Google Scholar] [CrossRef]
  27. Bhattacharya, S. Deadly new wheat disease threatens Europe’s crops. Nature 2017, 542, 145–146. [Google Scholar] [CrossRef]
  28. RIS—Genetic Resources Information System for Wheat and Triticale: Database, International Maize and Wheat Improvement Ceter, El Batan, Mexico. Available online: http://wheatpedigree.net (accessed on 28 August 2022).
  29. Luig, N.H. A Survey of Virulence Genes in Wheat Stem Rust, Puccinia graminis f. sp. tritici (Adv. in Plant Breed); Verlag Paul Parney: Berlin/Humburg, Germany, 1983; pp. 5–198. [Google Scholar]
  30. Huerta-Espino, J. Analysis of Wheat Leaf and Stem Rust Virulence on a Worldwide Basis. Ph.D. Thesis, University of Minnesota, Minneapolis, MN, USA, 1992. [Google Scholar]
  31. Watson, I.A.; Luig, N.H. Progressive increase in virulence in Puccinia graminis var. tritici. Phytopathology 1968, 5, 70–73. [Google Scholar]
  32. Knott, D.R.; Anderson, R.G. The inheritance of rust resistance. I. The inheritance of stem rust resistance in ten varieties of common wheat. Can. J. Agric. Sci. 1956, 36, 174–195. [Google Scholar]
  33. Knott, D.R. The inheritance of rust resistance. IV. Monosomic analysis of rust resistance and some other characters in six varieties of wheat including Gabo and Kenya Farmer. Can. J. Plant Sci. 1959, 39, 215–228. [Google Scholar] [CrossRef] [Green Version]
  34. Loegering, W.Q.; Sears, E.R. Relationships among stem-rust genes on wheat chromosomes 2B, 4B and 6B. Crop Sci. 1966, 6, 157–160. [Google Scholar] [CrossRef]
  35. Sears, E.R.; Loegering, W.Q.; Rodenhiser, H.A. Identification of chromosomes carrying genes for stem rust resistance in four varieties of wheat. Agron. J. 1957, 49, 208–212. [Google Scholar] [CrossRef]
  36. McIntosh, R.A. Cytogenetical studies in wheat VI. Chromosome location and linkage studies involving Sr13 and Sr8 for reaction to Puccinia graminis f. sp. tritici. Aust. J. Biol. Sci. 1972, 25, 765–773. [Google Scholar] [CrossRef] [Green Version]
  37. Singh, R.P.; McIntosh, R.A. Cytogenetical studies in wheat XIV. Sr8b for resistance to Puccinia graminis tritici. Can. J. Genet. Cytol. 1986, 28, 189–197. [Google Scholar] [CrossRef]
  38. Sears, E.R.; Loegering, W.Q. Mapping of stem rust genes Sr9 and Sr16 of wheat. Crop Sci. 1968, 8, 371–373. [Google Scholar] [CrossRef]
  39. McIntosh, R.A.; Luig, N.H. Recombination between genes for reaction to P. graminis at or near the Sr9 locus. In Proceedings of the Fourth International Wheat Genetics Symposium, Agricultural Experiment Station, Columbia, MO, USA, 6–11 August 1973; Sears, E.R., Sears, L.M.S., Eds.; University of Missouri: Columbia, MO, USA, 1973; pp. 425–432. [Google Scholar]
  40. Green, G.J.; Knott, D.R.; Watson, I.A.; Pugsley, A.T. Seedling reactions to stem rust of lines of Marquis wheat with substituted genes for rust resistance. Can. J. Plant Sci. 1960, 40, 524–538. [Google Scholar] [CrossRef]
  41. Hiebert, C.W.; Thomas, J.B.; McCallum, B.D.; Humphreys, D.G.; DePauw, R.M.; Hayden, M.J.; Mago, R.; Schnippenkoetter, W.; Spielmeyer, W. An introgression on wheat chromosome 4DL in RL6077 (Thatcher*6/PI 250413) confers adult plant resistance to stripe rust and leaf rust (Lr67). Theor. Appl. Genet. 2010, 121, 1083–1091. [Google Scholar] [CrossRef]
  42. Green, G.J.; Knott, D.R. Adult plant reaction to stem rust of lines of Marquis wheat with substituted genes for resistance. Can. J. Plant Sci. 1962, 42, 163–168. [Google Scholar] [CrossRef]
  43. Sears, E.R.; Briggle, L.W. Mapping the gene Pm1 for resistance to Erysiphe graminis f. sp. tritici on chromosome 7A of wheat. Crop Sci. 1969, 9, 96–97. [Google Scholar] [CrossRef]
  44. Gousseau, H.D.M.; Deverall, B.J.; McIntosh, R.A. Temperature-sensitivity of the expression of resistance to Puccinia graminis conferred by the Sr15, Sr8b and Sr14 genes in wheat. Physiol. Plant Pathol. 1985, 27, 335–343. [Google Scholar] [CrossRef]
  45. Watson, I.A.; Luig, N.G. Sr15—A new gene for use in the classification of Puccina graminis var. tritici. Euphytica 1966, 15, 239–250. [Google Scholar] [CrossRef]
  46. Jayatilake, D.V.; Tucker, E.J.; Bariana, H.; Kuchel, H.; Edwards, J.; McKay, A.C.; Chalmers, K.; Mather, D.E. Genetic mapping and marker development for resistance of wheat against the root lesion nematode Pratylenchus neglectus. BMC Plant Biol. 2013, 13, 1–12. [Google Scholar] [CrossRef] [Green Version]
  47. McIntosh, R.A. Nature of Induced Mutations Affecting Disease Reaction in Wheat in “Induced Mutations against Plant Disease”; International Atomic Energy Agency: Vienna, Austria, 1997; pp. 551–565. [Google Scholar]
  48. Baker, E.P.; Sanghi, A.K.; McIntosh, R.A.; Luig, N.H. Cytogenetical studies in wheat III. Studies of a gene conditioning resistance to stem rust strains with unusual genes for avirulence. Aust. J. Biol. Sci. 1970, 23, 369–375. [Google Scholar] [CrossRef] [Green Version]
  49. Williams, N.D.; Maan, S.S. Telosomic mapping of genes for resistance to stem rust of wheat. In Proceedings of the Fourth International Wheat Genetics Symposium, Columbia, MO, USA, 6–11 August 1973; Sears, E.R., Sears, L.M.S., Eds.; University of Missouri: Columbia, MO, USA, 1973; pp. 765–770. [Google Scholar]
  50. Anderson, M.K.; Williams, S.S.; Maan, S.S. Monosomic analyses of genes for resistance derived from Marquis and Reliance wheat. Crop Sci. 1971, 11, 556–558. [Google Scholar] [CrossRef]
  51. McIntosh, R.A.; Luig, N.H. Linkage of genes for reaction to Puccinia graminis f. sp. tritici and P. recondita in Selkirk wheat and related cultivars. Aust. J. Biol. Sci. 1973, 26, 1145–1152. [Google Scholar] [CrossRef]
  52. Kassa, M.T.; You, F.M.; Hiebert, C.W.; Pozniak, C.J.; Fobert, P.R.; Sharpe, A.G.; Menzies, J.G.; Humphreys, D.G.; Rezac, H.N.; Fellers, J.P.; et al. Highly predictive SNP markers for efficient selection of the wheat leaf rust resistance gene Lr16. BMC Plant Biol. 2017, 17, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. McIntosh, R.A. Cytogenetical studies in wheat X. Monosomic analysis and linkage studies involving genes for resistance to Puccinia graminis f. sp. tritici in cultivar Kota. Heredity 1978, 41, 71–82. [Google Scholar] [CrossRef] [Green Version]
  54. Jin, Y.; Singh, R.P.; Ward, R.W.; Wanyera, R.; Kinyua, M.; Njau, P.; Fetch, T.; Pretorius, Z.A.; Yahyaoui, A. Characterization of seedling infection types and adult plant infection responses of monogenic Sr gene lines to race TTKS of Puccinia graminis f. sp. tritici. Plant Dis. 2007, 91, 1096–1099. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Rouse, M.N.; Wanyera, R.; Njau, P.; Jin, Y. Sources of resistance to stem rust race Ug99 in spring wheat germplasm. Plant Dis. 2011, 95, 762–766. [Google Scholar] [CrossRef] [Green Version]
  56. Babiker, E.M.; Gordon, T.C.; Chao, S.; Newcomb, M.; Rouse, M.N.; Jin, Y.; Wanyera, R.; Acevedo, M.; Brown-Guedira, G.; Williamson, S.; et al. Mapping resistance to the Ug99 race group of the stem rust pathogen in a spring wheat landrace. Theor. Appl. Genet. 2015, 128, 605–612. [Google Scholar] [CrossRef] [PubMed]
  57. Babiker, E.M.; Gordon, T.C.; Chao, S.; Rouse, M.N.; Wanyera, R.; Acevedo, M.; Brown-Guedira, G.; Bonman, J.M. Molecular mapping of stem rust resistance loci effective against the Ug99 race group of the stem rust pathogen and validation of a single nucleotide polymorphism marker linked to stem rust resistance gene Sr28. Phytopathology 2017, 107, 208–215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Dyck, P.L.; Kerber, E.R. Chromosome location of gene Sr29 for reaction to stem rust. Can. J. Genet. Cytol. 1977, 19, 371–373. [Google Scholar] [CrossRef]
  59. Baraibar, S.; García, R.; Silva, P.; Lado, B.; Castro, A.; Gutiérrez, L.; Kavanová, M.; Quincke, M.; Bhavani, S.; Randhawa, M.S.; et al. QTL mapping of resistance to Ug99 and other stem rust pathogen races in bread wheat. Mol. Breed. 2020, 40, 1–6. [Google Scholar] [CrossRef]
  60. Zeller, F.J.; Oppitz, K. Monosomic analysis for localizing the gene SrEC for resistance to stem rust in the wheat cv. ‘Etoile de Choisy’. Z. Für Pflanz. 1977, 78, 79–82. [Google Scholar]
  61. Knott, D.R.; McIntosh, R.A. The inheritance of stem rust resistance in the common wheat cultivar Webster. Crop Sci. 1978, 17, 365–369. [Google Scholar] [CrossRef]
  62. Sears, E.R. Chromosome mapping with the aid of telocentrics. In Proceedings of the Second International Wheat Genetics Symposium, Lund, Sweden, 18–24 August 1963; pp. 370–381. [Google Scholar]
  63. Riede, C.R.; Williams, N.D.; Miller, J.D.; Joppa, L.R. Chromosomal location of genes for stem rust resistance derived from ‘Waldron’ wheat. Theor. Appl. Genet. 1995, 90, 1158–1163. [Google Scholar] [CrossRef]
  64. Ghazvini, H.; Hiebert, C.W.; Zegeye, T.; Liu, S.; Dilawari, M.; Tsilo, T.; Anderson, J.A.; Rouse, M.N.; Jin, Y.; Fetch, T. Inheritance of resistance to Ug99 stem rust in wheat cultivar Norin 40 and genetic mapping of Sr42. Theor. Appl. Genet. 2012, 125, 817–824. [Google Scholar] [CrossRef]
  65. Prins, R.; Dreisigacker, S.; Pretorius, Z. Stem rust resistance in a geographically diverse collection of spring wheat lines collected from across Africa. Front. Plant Sci. 2016, 7, 973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Bansal, U.K.; Hayden, M.J.; Keller, B.; Wellings, C.R.; Park, R.F.; Bariana, H.S. Relationship between wheat rust resistance genes Yr1 and Sr48 and a microsatellite marker. Plant Pathol. 2009, 58, 1039–1043. [Google Scholar] [CrossRef]
  67. Bansal, U.K.; Muhammad, S.; Forrest, K.L.; Hayden, M.J.; Bariana, H.S. Mapping of a new stem rust resistance gene Sr49 in chromosome 5B of wheat. Theor. Appl. Genet. 2015, 128, 2113–2119. [Google Scholar] [CrossRef] [PubMed]
  68. Ghazvini, H.; Hiebert, C.W.; Thomas, J.B.; Fetch, T. Development of a multiple bulked segregant analysis (MBSA) method used to locate a new stem rust resistance gene (Sr54) in the winter wheat cultivar Norin 40. Theor. Appl. Genet. 2013, 126, 443–449. [Google Scholar] [CrossRef] [PubMed]
  69. Laroche, A.; Demeke, T.; Gaudet, D.A.; Puchalski, B.; Frick, M.; McKenzie, R. Development of a PCR marker for rapid identification of the Bt-10 gene for common bunt resistance in wheat. Genome 2000, 43, 217–223. [Google Scholar] [CrossRef]
  70. German, S.E.; Kolmer, J.A. Effect of the gene Lr34 in the enhancement of resistance to leaf rust of wheat. Theor. Appl. Genet. 1992, 84, 97–105. [Google Scholar] [CrossRef] [PubMed]
  71. Kassa, M.T.; You, F.M.; Fetch, F.M.; Fobert, P.; Sharpe, A.; Pozniak, C.J.; Menzies, J.G.; Jordan, M.C.; Humphreys, G.; Zhu, T.; et al. Genetic mapping of SrCad and SNP marker development for marker-assisted selection of Ug99 stem rust resistance in wheat. Theor. Appl. Genet. 2016, 129, 1373–1382. [Google Scholar] [CrossRef]
  72. Park, R.F.; Welling, C.R. Pathogenic specialisation of wheat rusts in Australia and New Zealand in 1988 and 1989. Australas. Plant Pathol. 1992, 21, 61–69. [Google Scholar] [CrossRef]
  73. Roelfs, A.P.; McVey, D.V. Low infection types produced by Puccinia graminis f.sp. tritici and wheat lines with designated genes for resistance. Phytopathology 1979, 69, 722–730. [Google Scholar] [CrossRef]
  74. Nsabiyera, V.; Bariana, H.; Zhang, P.; Hayden, M.J.; Bansal, U. Closely linked markers for stem rust resistance gene Sr48 in wheat. In Proceedings of the Resilience Emerging from Scarcity and Abundance, Phoenix, AZ, USA, 6–9 November 2016; pp. 6–9. [Google Scholar]
  75. Aktar-Uz-Zaman, M.; Tuhina-Khatun, M.; Musa Hanafi, M.; Sahebi, M. Genetic analysis of rust resistance genes in global wheat cultivars: An overview. Biotechnol. Biotechnol. Equip. 2017, 31, 431–445. [Google Scholar] [CrossRef] [Green Version]
  76. Keller, B.; Lagudah, E.S.; Selter, L.L.; Risk, J.M.; Harsh, C.; Krattinger, S.G. How has Lr34/Yr18 conferred effective rust resistance in wheat for so long? In Proceedings of the Borlaug Global Rust Initiative Technical Workshop 2012, Beijing, China, 1–4 September 2012; Institute of Plant Biology, University of Zurich: Zürich, Switzerland, 2012. [Google Scholar]
  77. Krattinger, S.G.; Lagudah, E.S.; Spielmeyer, W.; Singh, R.P.; Huerta-Espino, J.; McFadden, H.; Bossolini, E.; Selter, L.L.; Keller, B. A Putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 2009, 323, 1360–1363. [Google Scholar] [CrossRef] [Green Version]
  78. Krattinger, S.G.; Kang, J.; Bräunlich, S.; Boni, R.; Chauhan, H.; Selter, L.L.; Robinson, M.D.; Schmid, M.W.; Wiederhold, E.; Hensel, G.; et al. Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34. New Phytol. 2019, 223, 853–866. [Google Scholar] [CrossRef] [Green Version]
  79. Lagudah, E.S.; Krattinger, S.G.; Herrera-Foessel, S.; Singh, R.P.; Huerta-Espino, J.; Spielmeyer, W.; Brown-Guedira, G.; Selter, L.L.; Keller, B. Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor. Appl. Genet. 2009, 119, 889–898. [Google Scholar] [CrossRef] [Green Version]
  80. Dyck, P.L.; Samborski, D.J. Adult-plant leaf rust resistance in PI 250413, an introduction of common wheat. Can. J. Plant Sci. 1979, 59, 329–332. [Google Scholar] [CrossRef]
  81. Herrera-Foessel, S.A.; Singh, R.P.; Lillemo, M.; Huerta-Espino, J.; Bhavani, S.; Singh, S.; Lan, C.; Calvo-Salazar, V.; Lagudah, E.S. Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theor. Appl. Genet. 2014, 127, 781–789. [Google Scholar] [CrossRef] [PubMed]
  82. Bansal, U.K.; Bossolini, E.; Miah, H.; Keller, B.; Park, R.F.; Barianam, H.S. Genetic mapping of seedling and adult plant stem rust resistance in two European winter wheat cultivars. Euphytica 2008, 164, 821–828. [Google Scholar] [CrossRef]
  83. Bansal, U.K.; Bariana, H.; Wong, D.; Randhawa, M.; Wicker, T.; Hayden, M.; Keller, B. Molecular mapping of an adult plant stem rust resistance gene Sr56 in winter wheat cultivar Arina. Theor. Appl. Genet. 2014, 127, 1441–1448. [Google Scholar] [CrossRef] [PubMed]
  84. Dakouri, A.; McCallum, B.D.; Walichnowski, A.Z.; Cloutier, S. Fine-mapping of the leaf rust Lr34 locus in Triticum aestivum (L.) and characterization of large germplasm collections support the ABC transporter as essential for gene function. Theor. Appl. Genet. 2010, 121, 373–384. [Google Scholar] [CrossRef] [PubMed]
  85. Martinez, F.; Niks, R.E.; Singh, R.P.; Rubiales, D. Characterization of Lr46, a gene conferring partial resistance to wheat leaf rust. Hereditas 2001, 135, 111–114. [Google Scholar] [CrossRef]
  86. Moore, J.; Herrera-Foessel, S.; Lan, C.; Schnippenkoetter, W.; Ayliffe, M.; Huerta-Espino, J.; Lillemo, M.; Viccars, L.; Milne, R.; Periyannan, S.; et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 2015, 47, 1494–1498. [Google Scholar] [CrossRef] [PubMed]
  87. William, M.; Singh, R.P.; Huerta-Espino, J.; Islas, S.O.; Hoisington, D. Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat. Phytopathology 2003, 93, 153–159. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  88. Qi, L.; Friebe, B.; Zhang, P.; Gill, B.S. Homoeologous recombination, chromosome engineering and crop improvement. Chromosome Res. 2007, 15, 3–19. [Google Scholar] [CrossRef] [PubMed]
  89. Zwer, P.K.; Park, R.F.; McIntosh, R.A. Wheat stem rust in Australia –1969-1985. Aust. J. Agric. Res. 1992, 43, 399–431. [Google Scholar] [CrossRef]
  90. Roux, J.L.; Rijkenberg, F.H.L. Occurrence and pathogenicity of Puccinia graminis f.sp. tritici in South Africa during the period 1981-1985. Phytophylactica 1987, 19, 456–472. [Google Scholar]
  91. Harder, D.E.; Dunsmore, K.M. Incidence and virulence of Puccinia graminis f.sp. tritici on wheat and barley in Canada in 1989. Can. J. Plant Pathol. 1990, 12, 424–427. [Google Scholar] [CrossRef]
  92. Roelfs, A.P.; Casper, D.H.; Long, D.L.; Roberts, J.J. Races of Puccinia graminis in the United States in 1989. Plant Dis. 1991, 75, 1127–1130. [Google Scholar] [CrossRef]
  93. McFadden, E.S. A successful transfer of emmer characters to vulgare wheat. J. Am. Soc. Agron. 1930, 22, 1020–1034. [Google Scholar] [CrossRef] [Green Version]
  94. Mago, R.; Tabe, L.; McIntosh, R.A.; Kota, R.; Paux, E.; Wicker, T.; Breen, J.; Lagudah, E.S.; Ellis, J.G.; Spielmeyer, W. A multiple resistance locus on chromosome arm 3BS in wheat confers resistance to stem rust (Sr2), leaf rust (Lr27) and powdery mildew. Theor. Appl. Genet. 2011, 123, 615–623. [Google Scholar] [CrossRef] [PubMed]
  95. Knott, D.R. The inheritance of rust resistance. IX. The inheritance of resistance to races 15B and 56 of stem rust in the wheat variety Khapstein. Can. J. Plant Sci. 1962, 42, 415–419. [Google Scholar] [CrossRef]
  96. Zhang, W.; Chen, S.; Abate, Z.; Nirmala, J.; Rouse, M.N.; Dubcovsky, J. Identification and characterization of Sr13, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proc. Natl. Acad. Sci. USA 2017, 114, 9483–9492. [Google Scholar] [CrossRef] [PubMed]
  97. The, T.T. Chromosome location of genes conditioning stem rust resistance transferred from diploid to hexaploid wheat. Nature New Biol. 1973, 241, 256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  98. The, T.T.; McIntosh, R.A.; Bennett, F.G.A. Cytogenetical studies in wheat IX. Monosomic analyses, telocentric mapping and linkage relationships of genes Sr21, Pm4, and Mle. Aust. J. Biol. Sci. 1979, 32, 115–125. [Google Scholar] [CrossRef]
  99. The, T.T.; Latter, B.D.H.; McIntosh, R.A.; Ellison, F.W.; Brennan, P.S.; Fisher, J.; Hollamby, G.J.; Rathjen, A.J.; Wilson, R.E. Grain yields of near isogenic lines with added genes for stem rust resistance. In Proceedings of the Seventh International Wheat Genetics Symposium, Cambridge, UK, 13–19 July 1988; Miller, T.E., Koebner, R.M.D., Eds.; Institute of Plant Sciences: Cambridge, UK, 1988; pp. 901–909. [Google Scholar]
  100. McIntosh, R.A.; Dyck, P.L.; Green, G.J. Inheritance of leaf rust and stem rust resistances in wheat cultivars Agent and Agatha. Aust. J. Agric. Res. 1976, 28, 37–45. [Google Scholar] [CrossRef]
  101. Friebe, B.; Jiang, J.; Knott, D.R.; Gill, B.S. Compensation indexes of radiation-induced wheat Agropyron elongatum translocations conferring resistance to leaf rust and stem rust. Crop Sci. 1994, 34, 400–404. [Google Scholar] [CrossRef]
  102. Zhang, W.; Lukaszewski, A.J.; Kolmer, J.; Soria, M.A.; Goyal, S.; Dubcovsky, J. Molecular characterization of durum and common wheat recombinant lines carrying leaf rust resistance (Lr19) and yellow pigment (Y) genes from Lophopyrum ponticum. Theor. Appl. Genet. 2005, 111, 573–582. [Google Scholar] [CrossRef] [Green Version]
  103. Knott, D.R. The inheritance of rust resistance. VI. The transfer of stem rust resistance from Agropyron elongatum to common wheat. Can. J. Plant Sci. 1961, 41, 109–123. [Google Scholar] [CrossRef]
  104. Acosta, A.C. The transfer of stem rust resistance from rye to wheat. Diss. Abstr. 1962, 23, 34–35. [Google Scholar]
  105. Mettin, D.; Bluthner, W.D.; Schlegel, G. Additional evidence on spontaneous 1B.1R wheat-rye substitutions and translocations. In Proceedings of the Fourth International Wheat Genetics Symposium, Columbia, MO, USA, 6–11 August 1973; pp. 179–184. [Google Scholar]
  106. Mago, R.; Verlin, D.; Zhang, P.; Bansal, U.; Bariana, H.; Jin, Y.; Ellis, J.; Hoxha, S.; Dundas, I. Development of wheat–Aegilops speltoides recombinants and simple PCR-based markers for Sr32 and a new stem rust resistance gene on the 2S#1 chromosome. Theor. Appl. Genet. 2013, 126, 2943–2955. [Google Scholar] [CrossRef] [PubMed]
  107. Jones, S.S.; Dvorak, J.; Knott, D.R.; Qualset, C.O. Use of double-ditelosomic and normal chromosome 1D recombinant substitution lines to map Sr33 on chromosome arm 1DS in wheat. Genome 1991, 34, 505–508. [Google Scholar] [CrossRef]
  108. McIntosh, R.A.; Miller, T.E.; Chapman, V. Cytogenetical studies in wheat XII. Lr28 for resistance to Puccinia recondita and Sr34 for resistance to P. graminis tritici. Z. Für Pflanz. 1982, 89, 295–306. [Google Scholar]
  109. McIntosh, R.A.; Gyarfas, J. Triticum timopheevi as a source of resistance to wheat stem rust. Z. Fur Pflanzenzucht. 1971, 66, 240–248. [Google Scholar]
  110. Gyarfas, J. Transference of Disease Resistance from Triticum timopheevii to Triticum aestivum. Master’s Thesis, University of Sydney, Camperdown, Australia, 1978. [Google Scholar]
  111. Bariana, H.S.; McIntosh, R.A. Cytogenetic studies in wheat XIV. Location of rust resistance genes in VPM1 and their genetic linkage with other disease resistance genes in chromosome 2A. Genome 1993, 36, 476–482. [Google Scholar] [CrossRef] [PubMed]
  112. Kerber, E.R.; Dyck, P.L. Transfer to hexaploid wheat of linked genes for adult-plant leaf rust and seedling stem rust resistance from amphiploid of Aegiolops speltoides x Triticum monoccum. Genome 1990, 33, 530–537. [Google Scholar] [CrossRef]
  113. Dyck, P.L. Transfer of a gene for stem rust resistance from Triticum araraticum to hexaploid wheat. Genome 1992, 35, 788–792. [Google Scholar] [CrossRef]
  114. Wua, S.; Pumphrey, M.; Bai, G. Molecular mapping of stem-rust-resistance gene Sr40 in wheat. Crop Sci. 2008, 49, 1681–1686. [Google Scholar] [CrossRef] [Green Version]
  115. Kibiridge-Sebunya, I.; Knott, D.R. Transfer of stem rust resistance to wheat from an Agropyron chromosome having a gametocidal effect. Canad. J. Genet. Cytol. 1983, 25, 215–221. [Google Scholar] [CrossRef]
  116. Liu, W.; Danilova, T.V.; Rouse, M.N.; Bowden, R.L.; Friebe, B.; Gill, B.S.; Pumphrey, M.O. Development and characterization of a compensating wheat-Thinopyrum intermedium Robertsonian translocation with Sr44 resistance to stem rust (Ug99). Theor. Appl. Genet. 2013, 126, 1167–1177. [Google Scholar] [CrossRef] [Green Version]
  117. Marais, G.F.; Potgieter, G.F.; Roux, H.S.; Roux, J. An assessment of the variation for stem rust resistance in the progeny of a cross involving the Triticum species aestivum, turgidum and tauschii. S. Afr. J. Plant. Soil. 1994, 11, 15–19. [Google Scholar] [CrossRef] [Green Version]
  118. Rouse, M.N.; Olson, E.L.; Gill, B.S.; Pumphrey, M.O.; Jin, Y. Stem rust resistance in Aegilops tauschii germplasm. Crop Sci. 2011, 51, 2074–2078. [Google Scholar] [CrossRef]
  119. Faris, J.D.; Xu, S.S.; Cai, X.; Friesen, T.L.; Jin, Y. Molecular and cytogenetic characterization of a durum wheat-Aegilops speltoides chromosome translocation conferring resistance to stem rust. Chromosome Res. 2008, 16, 1097–1105. [Google Scholar] [CrossRef]
  120. Klindworth, D.L.; Niu, Z.; Chao, S.; Friesen, T.L.; Jin, Y.; Faris, J.D.; Cai, X.; Xu, S.S. Introgression and characterization of a goatgrass gene for a high level of resistance to Ug99 stem rust in tetraploid wheat. G3 (Bethesda) 2012, 2, 665–673. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  121. Anugrahwati, D.R.; Shepherd, K.W.; Verlin, D.C.; Zhang, P.; Mirzaghaderi, G.; Walker, E.; Francki, M.G.; Dundas, I.S. Isolation of wheat–rye 1RS recombinants that break the linkage between the stem rust resistance gene SrR and secalin. Genome 2008, 51, 341–349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  122. Liu, W.; Jin, Y.; Rouse, M.; Friebe, B.; Gill, B.; Pumphrey, M.O. Development and characterization of wheat-Ae. searsii Robertsonian translocations and a recombinant chromosome conferring resistance to stem rust. Theor. Appl. Genet. 2011, 122, 1537–1545. [Google Scholar] [CrossRef] [PubMed]
  123. Qi, L.L.; Pumphrey, M.O.; Friebe, B.; Zhang, P.; Qian, C.; Bowden, R.L.; Rouse, M.N.; Jin, Y.; Gill, B.S. A novel Robertsonian translocation event leads to transfer of a stem rust resistance gene (Sr52) effective against race Ug99 from Dasypyrum villosum into bread wheat. Theor. Appl. Genet. 2011, 123, 159–167. [Google Scholar] [CrossRef] [PubMed]
  124. Liu, W.; Rouse, M.; Friebe, B. Discovery and molecular mapping of a new gene conferring resistance to stem rust, Sr53, derived from Aegilops geniculata and characterization of spontaneous translocation stocks with reduced alien chromatin. Chromosome Res. 2011, 19, 669–682. [Google Scholar] [CrossRef] [PubMed]
  125. Rahmatov, M.; Rouse, M.N.; Nirmala, J.; Danilova, T.; Friebe, B.; Steffenson, B.J.; Johansson, E. A new 2DS·2RL Robertsonian translocation transfers stem rust resistance gene Sr59 into wheat. Theor. Appl. Genet. 2016, 129, 1383–1392. [Google Scholar] [CrossRef] [PubMed]
  126. Chen, S.; Rouse, M.N.; Zhang, W.; Zhang, X.; Guo, Y.; Briggs, J.; Dubcovsky, J. Wheat gene Sr60 encodes a protein with two putative kinase domains that confers resistance to stem rust. New Phytol. 2020, 225, 948–959. [Google Scholar] [CrossRef] [Green Version]
  127. Zhang, J.; Hewitt, T.C.; Boshoff, W.; Dundas, I.; Upadhyaya, N.; Li, J.; Patpour, M.; Chandramohan, S.; Pretorius, Z.A.; Hovmøller, M.; et al. A recombined Sr26 and Sr61 disease resistance gene stack in wheat encodes unrelated NLR genes. Nat. Commun. 2021, 12, 3378. [Google Scholar] [CrossRef] [PubMed]
  128. Millet, E.; Steffenson, B.J.; Prins, R.; Sela, H.; Przewieslik-Allen, A.M.; Pretorius, Z.A. Genome targeted introgression of resistance to African stem rust from Aegilops sharonensis into bread wheat. Plant Genome 2017, 10, 1–11. [Google Scholar] [CrossRef] [Green Version]
  129. Yu, G.; Champouret, N.; Steuernagel, B.; Olivera, P.D.; Simmons, J.; Williams, C.; Johnson, R.; Moscou, M.J.; Hernández-Pinzón, I.; Green, P.; et al. Discovery and characterization of two new stem rust resistance genes in Aegilops sharonensis. Theor. Appl. Genet. 2017, 130, 1207–1222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  130. Mago, R.; Chen, C.; Xia, X.; Whan, A.; Forrest, K.; Basnet, B.R.; Perera, G.; Chandramohan, S.; Randhawa, M.; Hayden, M. Adult plant stem rust resistance in durum wheat Glossy Huguenot: Mapping, marker development and validation. Theor. Appl. Genet. 2022, 135, 1541–1550. [Google Scholar] [CrossRef] [PubMed]
  131. Rabinovich, S.V. Importance of wheat-rye translocations for breeding modern cultivars of Triticum aestivum L. Euphytica 1998, 100, 323–340. [Google Scholar] [CrossRef]
  132. Periyannan, S.K.; Qamar, Z.U.; Bansal, U.K.; Bariana, H.S. Development and validation of molecular markers linked with stem rust resistance gene Sr13 in durum wheat. Crop. Pasture Sci. 2014, 65, 74–79. [Google Scholar] [CrossRef]
  133. Gill, B.K.; Klindworth, D.L.; Rouse, M.N.; Zhang, J.; Zhang, Q.; Sharma, J.S.; Chu, C.; Long, Y.; Chao, S.; Olivera, P.D.; et al. Function and evolution of allelic variations of Sr13 conferring resistance to stem rust in tetraploid wheat (Triticum turgidum L.). Plant J. 2021, 106, 1674–1691. [Google Scholar] [CrossRef]
  134. Baker, E.P.; McIntosh, R.A. Utilization of marked telocentric chromosomes in more efficient genetic analysis. In Proceedings of the Fourth International Wheat Genetics Symposium, Agricultural Experiment Station, University of Missouri, Columbia, MO, USA, 6–11 August 1973; pp. 635–636. [Google Scholar]
  135. McIntosh, R.A. Chromosome location and linkage studies involving the wheat stem rust resistance gene Sr14. Cereal Res. Commun. 1980, 8, 315–320. [Google Scholar]
  136. McIntosh, R.A.; Luig, N.H.; Baker, E.P. Genetic and cytogenetic studies of stem rust, leaf rust and powdery midew resistances in Hope and related wheat cultivars. Aust. J. Biol. Sci. 1967, 20, 1181–1192. [Google Scholar] [CrossRef] [Green Version]
  137. Stakman, E.C.; Stewart, D.M.; Loegering, W.Q. Identification of Physiologic Races of Puccinia graminis var. tritici. Agricultural Research Service E617; United States Department of Agriculture: Washington, DC, USA, 1962. [Google Scholar]
  138. Chen, S.; Rouse, M.N.; Zhang, W.; Jin, Y.; Akhunov, E.; Wei, Y.; Dubcovsky, J. Fine mapping and characterization of Sr21, a temperature-sensitive diploid wheat resistance gene effective against the Puccinia graminis f. sp. tritici Ug99 race group. Theor. Appl. Genet. 2015, 128, 645–656. [Google Scholar] [CrossRef] [Green Version]
  139. Chen, S.; Zhang, W.; Bolus, S.; Rouse, M.N.; Dubcovsky, J. Identification and characterization of wheat stem rust resistance gene Sr21 effective against the Ug99 race group at high temperature. PLoS Genet. 2018, 14, e1007287. [Google Scholar] [CrossRef] [Green Version]
  140. Kerber, E.R.; Dyck, P.L. Inheritance of stem rust resistance transferred from diploid wheat (Triticum monococcum) to tetraploid and hexaploid wheat and chromosome location of the gene involved. Canad. J. Genet. Cytol. 1973, 15, 397–409. [Google Scholar] [CrossRef]
  141. Luo, J.; Rouse, M.N.; Hua, L.; Li, H.; Li, B.; Li, T.; Zhang, W.; Gao, C.; Wang, Y.; Dubcovsky, J.; et al. Identification and characterization of Sr22b, a new allele of the wheat stem rust resistance gene Sr22 effective against the Ug99 race group. Plant Biotechnol. J. 2022, 20, 554–563. [Google Scholar] [CrossRef] [PubMed]
  142. Olson, E.L.; Brown-Guedira, G.; Marshall, D.; Stack, E.; Bowden, R.L.; Jin, Y.; Rouse, M.; Pumphrey, M.O. Development of wheat lines having a small introgressed segment carrying stem rust resistance gene Sr22. Crop Sci. 2010, 50, 1823–1830. [Google Scholar] [CrossRef]
  143. Steuernagel, B.; Periyannan, S.; Hernández-Pinzón, I.; Witek, K.; Rouse, M.N.; Yu, G.; Hatta, A.; Ayliffe, M.; Bariana, H.; Jones, J.D.; et al. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nat. Biotechnol. 2016, 34, 652–655. [Google Scholar] [CrossRef]
  144. Hatta, M.A.M.; Ghosh, S.; Athiyannan, N.; Richardson, T.; Steuernagel, B.; Yu, G.; Rouse, M.N.; Ayliffe, M.; Lagudah, E.S.; Radhakrishnan, G.V.; et al. Extensive genetic variation at the Sr22 wheat stem rust resistance gene locus in the grasses revealed through evolutionary genomics and functional analyses. Mol. Plant Microbe Interact. 2020, 33, 1286–1298. [Google Scholar] [CrossRef] [PubMed]
  145. Hart, G.E.; McMillin, D.E.; Sears, E.R. Determination of the chromosomal location of a glutamate oxaloacetate transaminase structural gene using Triticum-Agropyron translocations. Genetics 1976, 83, 49–61. [Google Scholar] [CrossRef]
  146. Bhardwaj, S.C.; Nyar, S.K.; Prashar, M.; Kumar, J.; Menon, M.K.; Singh, S.B. A pathotype of Puccinia graminis f. sp. tritici on Sr24 in India. Cereal Rusts Powdery Mildews Bull. 1990, 18, 35–38. [Google Scholar]
  147. Mago, R.; Bariana, H.S.; Dundas, I.S.; Spielmeyer, W.; Lawrence, G.J.; Pryor, A.J.; Ellis, J.G. Development of PCR markers for the selection of wheat stem Gousseau rust resistance genes Sr24 and Sr26 in diverse wheat germplasm. Theor. Appl. Genet. 2005, 111, 496–504. [Google Scholar] [CrossRef]
  148. Dvorak, J.; Knott, D.R. Homoeologous chromatin exchange in a radiation-induced gene transfer. Canad. J. Genet. Cytol. 1977, 19, 125–131. [Google Scholar] [CrossRef]
  149. Liu, S.; Yu, L.X.; Singh, R.P.; Jin, Y.; Sorrells, M.E.; Anderson, J.A. Diagnostic and co-dominant PCR markers for wheat stem rust resistance genes Sr25 and Sr26. Theor. Appl. Genet. 2010, 120, 691–697. [Google Scholar] [CrossRef]
  150. Dundas, I.S.; Anugrahwati, D.R.; Verlin, D.C.; Park, R.F.; Bariana, H.S.; Mago, R.; Islam, A.K.M.R. New sources of rust resistance from alien species: Meliorating linked defects and discovery. Aust. J. Agric. Res. 2007, 58, 545–549. [Google Scholar] [CrossRef]
  151. Randhawa, M.S.; Bains, N.S.; Sohu, V.S.; Chhuneja, P.; Trethowan, R.M.; Bariana, H.S.; Bansal, U. Marker Assisted Transfer of Stripe Rust and Stem Rust Resistance Genes into Four Wheat Cultivars. Agronomy 2019, 9, 497. [Google Scholar] [CrossRef] [Green Version]
  152. Wu, X.X.; Lin, Q.J.; Ni, X.Y.; Sun, Q.; Chen, R.Z.; Xu, X.F.; Qiu, Y.C.; Li, T.Y. Characterization of wheat monogenic lines with known Sr genes and wheat lines with resistance to the Ug99 race Ggroup for resistance to prevalent races of Puccinia graminis f. sp. tritici in China. Plant Dis. 2020, 104, 1939–1943. [Google Scholar] [CrossRef]
  153. Upadhyaya, N.M.; Mago, R.; Panwar, V.; Hewitt, T.; Luo, M.; Chen, J.; Sperschneider, J.; Nguyen-Phuc, H.; Wang, A.; Ortiz, D.; et al. Genomics accelerated isolation of a new stem rust avirulence gene-wheat resistance gene pair. Nat. Plants 2021, 7, 1220–1228. [Google Scholar] [CrossRef]
  154. Das, B.K.; Sainti, A.; Bhagwat, S.G.; Jawali, N. Development of SCAR markers for identification of stem rust resistance gene Sr31. Plant Breed. 2006, 125, 544–549. [Google Scholar] [CrossRef]
  155. Tomar, S.M.S.; Menon, M.K. Genes for Resistance to Rusts and Powdery Mildew in Wheat; Indian Agricultural Research Institute: New Delhi, India, 2001; p. 152. [Google Scholar]
  156. Friebe, B.; Jiang, J.; Raupp, W.J.; McIntosh, R.A.; Gill, B.S. Characterization of wheat-alien translocations conferring resistance to diseases and pests: Current status. Euphytica 1996, 91, 59–87. [Google Scholar] [CrossRef]
  157. Kerber, E.R. Resistance to leaf rust in hexaploid wheat: Lr32 a third gene derived from Triticum tauschii. Crop Sci. 1987, 27, 204–206. [Google Scholar] [CrossRef]
  158. Cesaria, S.; Moorea, J.; Chen, C.; Webb, D.; Periyannan, S.; Mago, R.; Bernoux, M.; Lagudah, E.S.; Dodds, P.N. Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC–NLR proteins. Stella Cesari 2016, 113, 10204–10209. [Google Scholar] [CrossRef] [Green Version]
  159. Sambasivam, P.K.; Bansal, U.K.; Hayden, M.J.; Lagudah, E.S.; Bariana, H.S. Identification of markers linked with stem rust resistance genes Sr33 and Sr45. In Proceedings of the 11th International Wheat Genetics Symposium, Brisbane, Australia, 24–29 August 2008; Russell, R.A., Lagudah, E.E., Langridge, P., Lynne, M.M., Eds.; Sydney University Press: Sydney, Australia, 2008. 3p. [Google Scholar]
  160. Periyannan, S.; Moore, J.; Ayliffe, M.; Bansal, U.; Wang, X.; Huang, L.; Deal, K.; Luo, M.; Kong, X.; Bariana, H.; et al. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 2013, 341, 786–788. [Google Scholar] [CrossRef]
  161. Casey, L.W.; Lavrencic, P.; Bentham, A.R.; Cesari, S.; Ericsson, D.J.; Croll, T.; Turk, D.; Anderson, P.A.; Mark, A.E.; Dodds, P.N.; et al. The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins. Proc. Natl. Acad. Sci. USA 2016, 113, 12856–12861. [Google Scholar] [CrossRef] [Green Version]
  162. McIntosh, R.A.; Dyck, P.L.; The, T.T. Cytogenetical studies in wheat. XIII. Sr35—A 3rd Gene from Triticum monococcum for resistance to Puccinia graminis tritici. Z. Für Pflazenzüchtung 1984, 92, 1–14. [Google Scholar]
  163. Saintenac, C.; Zhang, W.; Salcedo, A.; Rouse, M.N.; Trick, H.N.; Akhunov, E.; Dubcovsky, J. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science 2013, 341, 783–786. [Google Scholar] [CrossRef] [Green Version]
  164. Yu, L.X.; Barbier, H.; Rouse, M.N.; Singh, S.; Singh, R.P.; Bhavani, S.; Huerta-Espino, J.; Sorrells, M.E. A consensus map for Ug99 stem rust resistance loci in wheat. Theor. Appl. Genet. 2014, 127, 1561–1581. [Google Scholar] [CrossRef] [Green Version]
  165. Boshoff, W.H.P.; Pretorius, Z.A.; van Niekerk, B.D.; Komen, J.S. First report of virulence in Puccinia graminis f. sp. tritici to wheat stem rust resistance genes Sr8b and Sr38 in South Africa. Plant Dis. 2002, 86, 922. [Google Scholar] [CrossRef]
  166. Labuschagne, M.T.; Pretorius, Z.A.; Grobbelaar, B. The influence of leaf rust resistance genes Lr29, Lr34, Lr35 and Lr37 on bread making quality in wheat. Euphytica 2002, 124, 65–70. [Google Scholar] [CrossRef]
  167. Mago, R.; Zhang, P.; Bariana, H.S.; Verlin, D.C.; Bansal, U.K.; Ellis, J.G.; Dundas, I.S. Development of wheat lines carrying stem rust resistance gene Sr39 with reduced Aegilops speltoides chromatin and simple PCR markers for marker-assisted selection. Theor. Appl. Genet. 2009, 124, 65–70. [Google Scholar] [CrossRef]
  168. Niu, Z.; Klindworth, D.L.; Friesen, T.L.; Chao, S.; Jin, Y.; Cai, X.; Xu, S.S. Targeted introgression of a wheat stem rust resistance gene by DNA marker-assisted chromosome engineering. Genetics 2011, 187, 1011–1021. [Google Scholar] [CrossRef] [Green Version]
  169. Bernardo, A.N.; Bowden, R.L.; Rouse, M.N.; Newcomb, M.S.; Marshall, D.S.; Bai, G. Validation of molecular markers for new stem rust resistance genes in U.S. hard winter wheat. Crop Sci. 2013, 53, 755–764. [Google Scholar] [CrossRef]
  170. Knott, D.R.; Dvorak, J.; Nanda, J.S. The transfer to wheat and homoeology of an Agropyron elongatum chromosome carrying resistance to stem rust. Canad. J. Genet. Cytol. 1977, 19, 75–79. [Google Scholar] [CrossRef]
  171. Kerber, E.R.; Dyck, P.L. Inheritance in hexaploid wheat of leaf rust resistance and other characters derived from Aegilops squarrosa. Canad. J. Genet. Cytol. 1969, 11, 639–647. [Google Scholar] [CrossRef]
  172. Arora, S.; Steuernagel, B.; Gaurav, K.; Chandramohan, S.; Long, Y.; Matny, O.; Johnson, R.; Enk, J.; Periyannan, S.; Singh, N.; et al. Resistance gene cloning from a wild crop relative by sequence capture and association genetics. Nat. Biotechnol. 2019, 37, 139–143. [Google Scholar] [CrossRef]
  173. Mago, R.; Zhang, P.; Vautrin, S.; Šimková, H.; Bansal, U.; Luo, M.C.; Rouse, M.; Karaoglu, H.; Periyannan, S.; Kolmer, J.; et al. The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat. Plants 2015, 1, 15186. [Google Scholar] [CrossRef]
  174. Ortiz, D.; Chen, J.; Outram, M.A.; Saur, I.M.L.; Upadhyaya, N.M.; Mago, R.; Ericsson, D.J.; Cesari, S.; Chen, C.; Williams, S.J.; et al. The stem rust effector protein AvrSr50 escapes Sr50 recognition by a substitution in a single surface-exposed residue. New Phytol. 2022, 234, 592–606. [Google Scholar] [CrossRef]
  175. Sebesta, E.E.; Wood, E.A.; ·Porter, D.R.; Webster, J.A.; Smith, E.L. Registration of Gaucho greenbug-resistant triticale germplasm. Crop Sci. 1994, 34, 1428. [Google Scholar] [CrossRef]
  176. Olivera, P.D.; Jin, Y.; Rouse, M.; Badebo, A.; Fetch, T., Jr.; Singh, R.P.; Yahyaoui, A. Races of Puccinia graminis f. sp. tritici with combined virulence to Sr13 and Sr9e in a field stem rust screening nursery in Ethiopia. Plant Dis. 2012, 96, 623–628. [Google Scholar] [CrossRef] [Green Version]
  177. Yu, G.; Matny, O.; Champouret, N.; Steuernagel, B.; Moscou, M.J.; Hernández-Pinzón, I.; Green, P.; Hayta, S.; Smedley, M.; Harwood, W.; et al. Aegilops sharonensis genome-assisted identification of stem rust resistance gene Sr62. Nat. Commun. 2022, 13, 1607. [Google Scholar] [CrossRef]
  178. Hare, R.A. Characterization and inheritance of adult plant stem rust resistance in durum wheat. Crop Sci. 1997, 37, 1094–1098. [Google Scholar] [CrossRef]
  179. Hare, R.A.; McIntosh, R.A. Genetic and cytogenetic studies of durable adult-plant resistance in Hope and related cultivars to wheat rusts. Z. Pflanzenzuecht. 1979, 83, 350–367. [Google Scholar]
  180. Sunderwirth, S.D.; Roelfs, A.P. Greenhouse evaluation of the adult plant resistance of Sr2 to wheat stem rust. Phytopathology 1980, 70, 634–637. [Google Scholar] [CrossRef]
  181. Yu, L.X.; Morgounov, A.; Wanyera, R.; Keser, M.; Singh, S.K.; Sorrells, M. Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis. Theor. Appl. Genet. 2012, 125, 749–758. [Google Scholar] [CrossRef]
  182. Singh, S.; Singh, R.P.; Bhavani, S.; Huerta-Espino, J.; Eugenio, L.V. QTL mapping of slow-rusting, adult plant resistance to race Ug99 of stem rust fungus in PBW343/Muu RIL population. Theor. Appl. Genet. 2013, 126, 1367–1375. [Google Scholar] [CrossRef]
  183. Brown, G.N. The inheritance and expression of leaf chlorosis associated with gene Sr2 for adult plant resistance to wheat stem rust. Euphytica 1997, 95, 67–71. [Google Scholar] [CrossRef]
  184. Kota, R.; Spielmeyer, W.; McIntosh, R.A.; Lagudah, E.S. Fine genetic mapping fails to dissociate durable stem rust resistance gene Sr2 from pseudo-black chaff in common wheat (Triticum aestivum L.). Theor. Appl. Genet. 2006, 112, 492–499. [Google Scholar] [CrossRef]
  185. Spielmeyer, W.; Sharp, P.J.; Lagudah, E.S. Identification and validation of markers linked to broad-spectrum stem rust resistance gene Sr2 in wheat (Triticum aestivum L.). Crop Sci. 2003, 43, 333–336. [Google Scholar] [CrossRef]
  186. Hayden, M.J.; Kuchel, H.; Chalmers, K.J. Sequence tagged microsatellites for the Xgwm533 locus provide new diagnostic markers to select for the presence of stem rust resistance gene Sr2 in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 2004, 109, 1641–1647. [Google Scholar] [CrossRef]
  187. McNeil, M.D.; Kota, R.; Paux, E.; Dunn, D.; McLean, R.; Feuillet, C.; Li, D.; Kong, X.; Lagudah, E.; Zhang, J.; et al. BAC-derived markers for assaying the stem rust resistance gene, Sr2, in wheat breeding programs. Mol. Breed. 2008, 22, 15–24. [Google Scholar] [CrossRef]
  188. Mago, R.; Tabe, L.; Vautrin, S.; Šimková, H.; Kubaláková, M.; Upadhyaya, N.; Berges, H.; Kong, H.; Breen, J.; Doležel, J.; et al. Major haplotype divergence including multiple germin-like protein genes, at the wheat Sr2 adult plant stem rust resistance locus. BMC Plant Biol. 2014, 14, 379. [Google Scholar] [CrossRef] [Green Version]
  189. Lagudah, E.S. Molecular genetics of race non-specific rust resistance in wheat. Euphytica 2011, 179, 81–91. [Google Scholar] [CrossRef]
  190. Bokore, F.E.; Cuthbert, R.D.; Hiebert, C.W.; Fetch, T.W.; Pozniak, C.J.; N’Diaye, A.; Ruan, Y.; Meyer, B.; Knox, R.E. Mapping stem rust resistance loci effective in Kenya in Canadian spring wheat (Triticum aestivum L.) lines ‘AAC Prevail’ and ‘BW961’. Canad. J. Plant Pathol. 2021, 43 (Suppl. 2), S263–S274. [Google Scholar] [CrossRef]
  191. Bajgain, P.; Rouse, M.N.; Bhavani, S.; Anderson, J.A. QTL mapping of adult plant resistance to Ug99 stem rust in the spring wheat population RB07/MN06113-8. Mol. Breed. 2015, 35, 170. [Google Scholar] [CrossRef]
  192. Kosgey, Z.C.; Edae, E.A.; Dill-Macky, R.; Jin, Y.; Bulbula, W.D.; Gemechu, A.; Macharia, G.; Bhavani, S.; Randhawa, M.S.; Rouse, M.N. Mapping and validation of stem rust resistance loci in spring wheat line CI 14275. Front. Plant Sci. 2021, 11, 609659. [Google Scholar] [CrossRef]
  193. Shewabez, E.; Bekele, E.; Alemu, A.; Mugnai, L.; Tadesse, W. Genetic characterization and genome-wide association mapping for stem rust resistance in spring bread wheat. BMC Genom. Data 2022, 23, 11. [Google Scholar] [CrossRef] [PubMed]
  194. Chemonges, M.; Herselman, L.; Pretorius, Z.A.; Maré, A.; Boshoff, W.H.P. Characterisation of stem rust resistance in the South African winter wheat cultivar PAN 3161. Euphytica 2022, 218, 139. [Google Scholar] [CrossRef]
Table
Table 1. Own race-specific stem rust resistance genes in bread wheat.
Table 1. Own race-specific stem rust resistance genes in bread wheat.
GeneAlleleResistance Against Ug99Possible SourceChromosomeDNA Marker AvailableReferences
Sr5-NoKanred6DSNo[5,29,30]
Sr6-NoMcMurachy2DNo[5,31]
Sr7aNoCiano-674ALNo[32,33,34,35]
bNoSelkirk
Sr8aNoFrontana6ASNo[36,37]
bNoBezostaya 1
Sr9aNoTAM-1072BLYes[38,39]
bNoChinese spring
eNoArrivato
fNoChinese white
hYesWebster[40,41]
Sr10-NoMarquiz2BNo[40,42]
Sr15-MaybeNorka7ALYes[43,44,45,46]
Sr16-NoReliance2BLNo[38,47]
Sr18-NoGabo1DLNo[48,49]
Sr19-NoMarquiz2BNo[50]
Sr20-
Sr23-NoMyronovskaya 2642BSYes[51,52]
Sr28-ModerateKota2BLYes[53,54,55,56,57]
Sr29-NoAurora6DNo[58,59]
Sr30-NoWebster5DLNo[60,61]
Sr41-NoWaldron4DYes[62,63]
Sr42-NoNorin 406DSYes[64,65]
Sr48-ModerateArina2AL?[66]
Sr49-NoMahmoudi5BL?[67]
Sr54 NoNorin 402DL?[68]
SrCad-YesCadillac6DSYes[41,69,70,71]
SrTmp-YesTriumph 64Yes[41,71]
Table
Table 2. Own race-nonspecific stem rust APR genes of common wheat.
Table 2. Own race-nonspecific stem rust APR genes of common wheat.
GeneCosegregating Resistance FactorsResistance Against Ug99Possible SourceChromosomeDNA Marker AvailableReferences
Sr55Lr67/Yr46Pm46YesPI2504134DLYes[41,80,81]
Sr56-YesArina5BLYes[82,83]
Sr57Lr34/Yr18/Pm38/Bdv1YesBezostaya 17DSYes[77,79,84]
Sr58Lr46/Yr29/Pm39YesPavon 762DYes[85]
Table
Table 3. Introgressed stem rust resistance genes of bread wheat.
Table 3. Introgressed stem rust resistance genes of bread wheat.
GeneCosegregating
Resistance Genes, or Genes on the Same Arm		Resistance Against Ug99Source SpeciesPossible Source CultivarChromosomeDNA Marker AvailableReferences
Sr2Lr27ModerateT. turgidum ssp. dicoccum Hope3BSYes[93,94]
Sr9d-NoT. turgidum ssp. dicoccumNIL-LMPG-Sr9d-TR.DR2BLYes[93]
Sr9g-NoT. turgidum ssp. durum-2BLYes[39]
Sr11-NoT. turgidum ssp. durumGaza5BLYes[32,62]
Sr12-ModerateT. turgidum ssp. durumMarquillo3BSNo[92,95]
Sr13-YesT. turgidum ssp. dicoccumNIL-Marquis-Sr13,Sr14-Khapstein6ALYes[36,96]
Sr14-NoT. turgidum ssp. dicoccumNIL-Marquis-Sr13,Sr14-Khapstein1BLYes[44]
sr17-NoT. turgidum ssp. dicoccumSelkirk7BLNo[93]
Sr21-YesT. monococcumEinkorn C.I.24332ALYes[97,98]
Sr22-YesT. monococcum ssp. boeoticumSchomburgk 7ALYes[99]
Sr24-YesThinopyrum ponticum (Podp.) Z.-W.Liu and R.-C.WangNIL-LMPG-Sr243DLYes[100]
Sr25Lr19YesAg. elongatum Host. (Th. ponticum)NIL-LMPG-Sr257DLYes[101,102]
Sr26-YesAg. elongatum Host. (Th. ponticum)NIL-LMPG-Sr266A/6AgYes[103]
Sr27-YesS. cerealeNIL-LMPG-Sr273A/3RNo[104]
Sr31Lr26, Yr9NoS. cerealeKnyahynia Olha1BL/1RSYes[105]
Sr32-YesAegilops speltoides Tausch -2A, 2B, 2DYes[106]
Sr33Lr21YesAe. tauschii Coss.Lorikeet 1DSYes[107]
Sr34Yr8NoAe. comosa Sibth. and Sm.Marquillo2A/2M, 2D/2MYes[108]
Sr35-YesT. monococcumNIL-STEWART-Sr35-G-2919 3ALYes
Sr36-YesT. timopheeviSonglen2BSYes [109]
Sr37-YesT. timopheeviBoohai4BYes[110]
Sr38Lr37/Yr17NoAe. ventricosa TauschTrident2AS/2NSYes[111]
Sr39-YesAe. speltoides R.L.5344.RL-6082 2BYes[112]
Sr40-YesT. timopheevii subsp. armeniacum (Jakubz.)Maris-Fundin 2BSYes[113,114]
Sr43-YesAg. elongatum Host. (Th. ponticum)RWG-337DS/7el2LYes[115]
Sr44-YesTh. intermedium (Host) Barkworth and D.R. DeweyPayne7DL/7J#1SYes[116]
Sr45-YesAe. tauschiiThornbill1DSYes[117]
Sr46-?Ae. tauschii var. meyeriAUS-189132DSYes[118]
Sr47-?Ae. speltoides96–902BL/2SL·2SSYes[119,120]
Sr50-YesS. cereale cv. Imperial-1DL.1DS/1R#3S/1DSYes[121]
Sr51-YesAe. searsii Feldman and Kislev ex K.HammerTA-6555 3AL/3SSS, 3BL/3SSS 3DL/3SSSYes[122]
Sr52-YesD. villosum (L.) Borbas KS-12-WGGRC-57 6AL/6V.3LYes[123]
Sr53-YesAe. geniculata RothKS-12-WGGRC-58-T1 5M(g)L/5M(g)S / 5DLYes[124]
Sr59-YesS. cerealeTA5094T2DS·2RLYes[125]
Sr60-NoT. monococcum 5AmS [126]
Sr61-YesAg. elongatum Host.(Th. ponticum)W3757T6AS.6AL-6Ae#1Yes[127]
Sr62- Ae. sharonensis EigAS_16441SshS·1SshL-1BL/1SshS·1SshL-1DLYes[128,129]
Sr63 YesT. turgidum ssp. durumGlossy Huguenot2ALYes[130]
SrAmigo-YesS. cereale cv. InsaveAmigo1AL/1RSYes[131]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Karelov, A.; Kozub, N.; Sozinova, O.; Pirko, Y.; Sozinov, I.; Yemets, A.; Blume, Y. Wheat Genes Associated with Different Types of Resistance against Stem Rust (Puccinia graminis Pers.). Pathogens 2022, 11, 1157. https://doi.org/10.3390/pathogens11101157

AMA Style

Karelov A, Kozub N, Sozinova O, Pirko Y, Sozinov I, Yemets A, Blume Y. Wheat Genes Associated with Different Types of Resistance against Stem Rust (Puccinia graminis Pers.). Pathogens. 2022; 11(10):1157. https://doi.org/10.3390/pathogens11101157

Chicago/Turabian Style

Karelov, Anatolii, Natalia Kozub, Oksana Sozinova, Yaroslav Pirko, Igor Sozinov, Alla Yemets, and Yaroslav Blume. 2022. "Wheat Genes Associated with Different Types of Resistance against Stem Rust (Puccinia graminis Pers.)" Pathogens 11, no. 10: 1157. https://doi.org/10.3390/pathogens11101157

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop