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Karelov, A.;  Kozub, N.;  Sozinova, O.;  Pirko, Y.;  Sozinov, I.;  Yemets, A.;  Blume, Y. Own stem Rust Resistance Genes in Bread Wheat. Encyclopedia. Available online: https://encyclopedia.pub/entry/32138 (accessed on 27 July 2024).
Karelov A,  Kozub N,  Sozinova O,  Pirko Y,  Sozinov I,  Yemets A, et al. Own stem Rust Resistance Genes in Bread Wheat. Encyclopedia. Available at: https://encyclopedia.pub/entry/32138. Accessed July 27, 2024.
Karelov, Anatolii, Natalia Kozub, Oksana Sozinova, Yaroslav Pirko, Igor Sozinov, Alla Yemets, Yaroslav Blume. "Own stem Rust Resistance Genes in Bread Wheat" Encyclopedia, https://encyclopedia.pub/entry/32138 (accessed July 27, 2024).
Karelov, A.,  Kozub, N.,  Sozinova, O.,  Pirko, Y.,  Sozinov, I.,  Yemets, A., & Blume, Y. (2022, October 31). Own stem Rust Resistance Genes in Bread Wheat. In Encyclopedia. https://encyclopedia.pub/entry/32138
Karelov, Anatolii, et al. "Own stem Rust Resistance Genes in Bread Wheat." Encyclopedia. Web. 31 October, 2022.
Own stem Rust Resistance Genes in Bread Wheat
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This entry is adapted from the peer-reviewed paper 10.3390/pathogens11101157

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. 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-called Sr genes).

stem rust Puccinia graminis Pers. Ug99 wheat

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].

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].
Table 1. Own race-specific stem rust resistance genes in bread wheat.
Gene Allele Resistance Against Ug99 Possible Source Chromosome DNA Marker Available References
Sr5 - No Kanred 6DS No [5][29][30]
Sr6 - No McMurachy 2D No [5][31]
Sr7 a No Ciano-67 4AL No [32][33][34][35]
b No Selkirk
Sr8 a No Frontana 6AS No [36][37]
b No Bezostaya 1
Sr9 a No TAM-107 2BL Yes [38][39]
b No Chinese spring
e No Arrivato
f No Chinese white
h Yes Webster [40][41]
Sr10 - No Marquiz 2B No [40][42]
Sr15 - Maybe Norka 7AL Yes [43][44][45][46]
Sr16 - No Reliance 2BL No [38][47]
Sr18 - No Gabo 1DL No [48][49]
Sr19 - No Marquiz 2B No [50]
Sr20 -
Sr23 - No Myronovskaya 264 2BS Yes [51][52]
Sr28 - Moderate Kota 2BL Yes [53][54][55][56][57]
Sr29 - No Aurora 6D No [58][59]
Sr30 - No Webster 5DL No [60][61]
Sr41 - No Waldron 4D Yes [62][63]
Sr42 - No Norin 40 6DS Yes [64][65]
Sr48 - Moderate Arina 2AL ? [66]
Sr49 - No Mahmoudi 5BL ? [67]
Sr54   No Norin 40 2DL ? [68]
SrCad - Yes Cadillac 6DS Yes [41][69][70][71]
SrTmp - Yes Triumph 64 Yes [41][71]
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].
Table 2. Own race-nonspecific stem rust APR genes of common wheat.
Gene Cosegregating Resistance Factors Resistance Against Ug99 Possible Source Chromosome DNA Marker Available References
Sr55 Lr67/Yr46Pm46 Yes PI250413 4DL Yes [41][80][81]
Sr56 - Yes Arina 5BL Yes [82][83]
Sr57 Lr34/Yr18/Pm38/Bdv1 Yes Bezostaya 1 7DS Yes [77][79][84]
Sr58 Lr46/Yr29/Pm39 Yes Pavon 76 2D Yes [85]
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].

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Anatolii Karelov
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Natalia Kozub
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Oksana Sozinova
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Yaroslav Pirko
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Igor Sozinov
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Alla Yemets
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Yaroslav Blume
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