Plant Pathology

REVIEW

Progress in breeding for resistance to Ug99 and other races of the stem rust fungus in CIMMYT wheat germplasm

Sridhar BHAVANI (✉✉)1, David P. HODSON1, Julio HUERTA-ESPINO1,2, Mandeep S. RANDHAWA3, Ravi P. SINGH1

1 International Maize and Wheat Improvement Center, Texcoco 56237, Mexico 2 Campo Experimental Valle de México INIFAP, Chapingo 56230, Mexico

3 International Maize and Wheat Improvement Center, ICRAF Campus, Nairobi 00100, Kenya

Abstract Races belonging to the Ug99 (TTKSK) lineage of the wheat stem rust fungus, carrying complex virulence combinations, and their migration to countries in Africa, Middle East and Asia continue to pose a significant threat to global wheat production. The rapid spread of additional races, e.g., TKTTF or the Digalu lineage, in several countries causing localized epidemics reminds us of the vulnerability of wheat germplasm to stem rust disease, a formidable foe referenced as early as biblical times. A global rust monitoring system reflecting increased surveil- lance efforts has identified 13 races within the Ug99 lineage in 13 countries and unrelated lineages are emerging, spreading and posing serious threats to wheat production. Race TKTTF has caused localized epidemics in Ethiopia and its variants have been recently implicated in stem rust outbreaks in Europe. Concerted research efforts have resulted in the identification of several new resistance genes and gene combinations for use in breeding. Combining multiple adult plant resistance (APR) genes in high-yielding backgrounds and discovery of new quantitative trait loci conferring stem rust resistance has progressed in the recent years, enhancing the durability of resistance. Effective gene stewardship and new genera- tion breeding materials and cultivars that combine multiple race-specific or minor to intermediate effect APR genes, complemented by active surveillance and monitoring, have helped to limit major epidemics and increase grain yield potential in key target environments.

Keywords adult plant resistance, black rust, race-specific resistance, Triticum aestivum

1 Stem rust: “a formidable foe”

Wheat is one of the world’s most important staple cereal crops and a major constituent of daily calorie and protein intake in humans[1]. On a global scale, wheat is grown on over 240 Mha worldwide, which is a greater area than any other crop, and annual production is close to 750 Mt. Nearly 200 wheat diseases and pests have been documen- ted, 50 of which are considered sufficiently important to cause economic losses[2]. Potential grain yield losses due to diseases have been estimated at 18% and actual losses with current disease control practices stand at 13%[3]. Stem rust or black rust caused by Puccinia graminis f.

sp. tritici (Pgt) is a devastating disease of bread wheat (Triticum aestivum) and durum wheat (T. durum) in the major wheat-growing regions of the world. Wheat, barley (Hordeum vulgare) and barberry (Berberis vulgaris) have their origins in the Fertile Crescent, suggesting that the complex relationship of these species in the life cycle of stem rust has a very ancient history. Spores of stem rust discovered in archeological sites in Israel have been dated to 1300 BC[4]. The disease dates back to Biblical times, which describes epidemics of cereal rusts and smuts that were inflicted on the Israelites as divine punishment[5]. The Roman festival, Robigalia, as described by Numa Pompilius was held as early as 715–672 BCE to propitiate rust gods by prayer and sacrifice. Aristotle (384–322 BC) and Theophrastus attributed cereal rust epidemics to warm and wet weather conditions[5] and stem rust usually occurs in regions where warm and moist conditions prevail. Infection appears as large brick-red pustules carrying urediniospores on most aerial parts of the plant including stems, leaves, leaf sheath, glumes and awns of susceptible plants[6]. The disease can cause great damage to suscep- tible wheat cultivars over wide geographical regions and early infections can quickly escalate into devastating, widespread epidemics in a short interval of time owing to

Received March 27, 2019; accepted May 20, 2019

Correspondence: [email protected]

Front. Agr. Sci. Eng. 2019, 6(3): 210–224 https://doi.org/10.15302/J-FASE-2019268 Available online at http://journal.hep.com.cn/fase

© The Author(s) 2019. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)

favorable weather conditions, which can cause a heavy inoculum build up to be carried on wind currents, causing large-scale deployment to susceptible varieties. The severe infection of stems interrupts the translocation of nutrients to developing heads, resulting in poor grain fill, shriveled grain or no grain production. Heavy stem rust infection can turn stems brittle and cause lodging with a consequent total loss of grain[7]. Well-documented examples of stem rust epidemics occurred in Europe in 1932 and 1951, with yield losses of 5%–20% in Eastern and Central Europe and 9%– 33% in Scandinavia[8]. Sporadic stem rust epidemics were reported mainly for warmer areas through the mid-20th century, with occasionally severe yield losses[9,10]. Losses from stem rust have occurred in wheat in southern and north-western India, especially in years of unusually warm weather[11]. Severe epidemics were reported for wheat crops in northern China and Inner Mongolia in the early 1950s, under high temperatures and frequent rains that favored infection[12]. Widespread epidemics have also been observed in Australia[13] and Africa[14]. In North America, stem rust was limited to the Northern Great Plains, where more than half the yield of the 1935 spring wheat crop in North Dakota and Minnesota was lost to epidemics[15]. Although the rust epidemics in North America have been curtailed since 1974, the pathogen still poses a great threat under the current climate change scenario. When the role of barberry as an alternate host for stem

rust became clear, eradication programs for common barberry (Berberis vulgaris) in Europe and North America were successfully conducted in the early 1900s. To combat stem rust and reduce the frequency of epidemics, breeding programs in Australia, the USA, at CIMMYT (Interna- tional Maize and Wheat Improvement Center) and in other major wheat production regions developed and deployed resistant cultivars that for decades provided effective genetic control. With stem rust largely under control in several wheat-growing regions of the world due to cultivation of resistant cultivars, prediction models esti- mate that the annual global wheat grain losses would most likely be over 6.2 Mt in the absence of these resistant cultivars and if favorable conditions caused epidemics[16]. Stem rust has reemerged as a major threat in recent years

with the detection of a unique race called “Ug99”, identified in Uganda in 1998[17]. Designated TTKSK according to the North American stem rust nomenclature system[18], Ug99 is virulent to the important resistance genes Sr31 and Sr38, as well as several others present in cultivars of diverse origin. In large-scale field testing conducted in Kenya under natural stem rust infection, more than 80% of wheat germplasm from worldwide sources was either susceptible or lacked adequate resistance to Ug99[18,19] Subsequent to the identification of the Ug99 strain TTKSK, new variants of that lineage have appeared and overcome other resistance genes, including TTKST

with virulence to resistance gene Sr24 identified in 2006[20], TTTSK with virulence to Sr36 identified in 2007[21], and most recently races TTKTK and TTKTTwith virulence to SrTmp in 2014[22,23].

2 Status of Ug99 race group

In response to the resurgence of stem rust in eastern Africa and the threat of Ug99, in 2005 the international wheat research and development community, with support from key funding agencies, established the Global Rust Initiative––later renamed the Borlaug Global Rust Initi- ative––to significantly reduce the vulnerability of wheat crops worldwide to three rusts diseases[23]. Increased pathogen-monitoring activities as part of this initiative greatly improved tracking of the occurrence and spread of new and virulent variants in the Ug99 race group, as well as identification of other new stem rust races that are able to break down the resistance of widely grown wheat cultivars and cause severe local epidemics. Global surveillance and monitoring of wheat rusts has

been undertaken in a coordinated manner for over a decade, and it has been observed that the pathogen populations are evolving rapidly and wheat rusts are moving between regions/countries with increasing fre- quency. With such dynamic pathosystems and emerging threats to wheat production, sustained global surveillance and monitoring has become increasingly important. Through the dedicated efforts of global partners, the evolution and spread of important Pgt races have been successfully tracked[24]. A brief summary of the current status of key Pgt races is given here. Singh et al.[25] provided a recent and comprehensive

overview of the status of the Ug99 race group, describing the rapid evolution of new races and its geographical expansion, with eight races reported in 13 countries. New races have continued to emerge and, by 2019, 13 had been identified (Table 1), all within the same 13 countries. Similarly, in 2014, five new variants of Ug99 were detected in Kenya[23,26,27]. Two of these, TTKTK and TTKTT, were highly significant because they had acquired virulence to stem rust gene SrTmp, a key resistance gene in popular eastern African bread wheat cultivars such as cv. Robin in Kenya and cv. Digalu in Ethiopia. Race TTKTK was also detected in Egypt, Rwanda and Uganda in 2014[26], indicating its rapid and possibly widespread dispersal. No new Ug99 variants have been identified since 2015, However, Terefe et al.[28] reported the first occurrence of Ug99 race PTKSK in South Africa in 2017, that was previously identified in Ethiopia, Kenya and Yemen. It is not known if this represents a new incursion into southern Africa or if it is a locally occurring mutation. The current known distribution of the Ug99 race group is shown in Fig. 1.

Sridhar BHAVANI et al. Progress in breeding for stem rust resistance in wheat germplasm 211

3 Stem rust epidemics caused by races unrelated to Ug99 lineage

While the Ug99 race group continues to evolve in Africa, global monitoring has shown that new races genetically unrelated to Ug99 are also emerging, spreading and posing serious threats to wheat production. Genotyping of these isolates has detected two new lineages, or clades, that have shown rapid geographical expansion and causing dama- ging outbreaks of stem rust at scale. Clade IV, typified by race TKTTF and variants, is now detected across a wide geographical range[25]. Race TKTTF caused damaging, localized epidemics in Ethiopia in 2013 and 2014, owing to its virulence on SrTmp and the susceptibility of the widely grown cv. Digalu[29]. Evidence indicates that TKTTF was likely an incursion into eastern Africa from the Middle East[30]. In 2014, Clade IV races were also responsible for unusual outbreaks of stem rust in Germany[30] and the re-appearance of stem rust in the

UK[31]. Stem rust outbreaks in Sicily, Italy, in 2016[32]

were caused by another lineage, Clade III, typified by race TTRTF. First detected in Georgia in 2014, TTRTF and its variants are spreading rapidly, being reported in Egypt and Eritrea and spreading in Ethiopia and Kenya. The Clade III race RRTTF was also recently detected in Ecuador[33]. Races in Clades IVand III now predominate over the Ug99 race group (Clade I) in eastern Africa. Another significant development is the recent detection

of several populations of stem rust fungus with very strong signals of recombination through the completion of the sexual part of the life cycle. In northern Kazakhstan and western Siberia, large-scale stem rust epidemics recorded since 2015, have affected millions of hectares of wheat[34]. Sampling in these regions has revealed high race diversity, with hundreds of races identified. Similar high race diversity was reported from a localized stem rust outbreak in Sweden in 2017[35] and Georgia (USDA Cereals Disease Laboratory, unpublished data). In these cases,

Table 1 Puccinia graminis tritici races belonging to Ug99 lineage identified until 2019 in various countries with avirulence/virulence status on

discriminating resistance genes (updated from Singh et al.[25])

Race1 Common alias Resistance genes and avirulence (A) or virulence (V) status

Confirmed countries (year detected) Sr31 Sr21 Sr24 Sr36 Sr9h SrTmp

TTKSK Ug99 V V A A A A Uganda (1998), Kenya (2001), Ethiopia (2003), Sudan (2006), Yemen (2006), Iran (2007), Tanzania (2009), Eritrea (2012), Rwanda (2014), Egypt (2014)

TTKSF A V A A A A South Africa (2000), Zimbabwe (2009), Uganda (2012)

TTKST Ug99 + Sr24 V V V A A A Kenya (2006), Tanzania (2009), Eritrea (2010), Uganda (2012)

TTTSK Ug99 + Sr36 V V A V A A Kenya (2006), Tanzania (2009), Ethiopia (2010), Uganda (2012), Rwanda (2014), Egypt (2014)

TTKSP A V V A A A South Africa (2007)

PTKSK V A A A A A Kenya (2009), Ethiopia (2007), Yemen (2009), South Africa (2017)

PTKST V A V A A A Ethiopia (2007), Kenya (2008), South Africa (2009), Eritrea (2010), Mozambique (2010), Zimbabwe (2010)

TTKSF+ A V A A V A South Africa (2010), Zimbabwe (2010)

TTKTT Ug99 + Sr24 + SrTmp V V V A A V Kenya (2014)

TTKTK Ug99 + SrTmp V V A A A V Kenya (2014), Egypt (2014), Eritrea (2014), Rwanda (2014), Uganda (2014)

TTHSK V V A A A A Kenya (2014)

PTKTK V A A A A A Kenya (2014)

TTHST V V V A A A Kenya (2013)

Note: 1 Race designation follows the North American nomenclature system described by Jin et al.[20]. Race TTKSF+ is given a temporary name as it exceeds the current North American 20 differential gene set.

212 Front. Agr. Sci. Eng. 2019, 6(3): 210–224

Berberis spp. have been associated with the stem rust outbreaks and likely contributed to the observed race diversity.

4 Phenotyping platforms facilitating screening and breeding for stem rust resistance

A flagship objective of the Durable Rust Resistance in Wheat and Delivering Genetic Gains in Wheat (DGGW) projects during the last decade was to establish operational phenotyping platforms in Kenya and Ethiopia to screen and evaluate wheat accessions from all over the world at key hot-spot sites wherein maximum diversity of the pathogen exists. Testing was to be conducted at a quarantine facility and to facilitate breeding to identify and develop new resistant lines. Effective partner- ship between CIMMYT, Kenya Agriculture Livestock Research Organization and Ethiopian Institute of Agricul- ture Research under the DGGW project have had a crucial role in evaluating international wheat materials and identified new sources of resistance in breeding and pre-

breeding populations. This arrangement also supported Mexico-Kenya shuttle breeding by CIMMYT, pathogen surveys and surveillance, varietal releases in Kenya and other countries, and mapping of new sources of resistance and genomic selection studies. Over 650000 wheat and barley accessions that inc-

lude commercial cultivars, breeding materials, genetic resources and mapping populations from as many as 25 countries have been evaluated at Njoro, Kenya (Fig. 2) and over 100000 durum wheat accessions at Debre Zeit, Ethiopia. Over the decade of screening operations in Kenya and Ethiopia there has been a clear trend of increased resistance in both CIMMYT and national program breeding materials from wheat-growing countries with about 10%–20% entries showing promising levels of resistance and another 20% intermediate levels of resistance on average for all countries, compared to large proportion (as high as 90%) of susceptible materials when screening began in 2008 (unpublished data). Over 100 resistant or moderately resistant wheat cultivars have been released in different wheat-growing regions, clearly demonstrating the progress made in breeding for stem rust resistance globally.

Fig. 1 Detection and distribution of Puccinia graminis tritici races belonging to Ug99 race group in 2019. Updated from Singh et al.[25].

Sridhar BHAVANI et al. Progress in breeding for stem rust resistance in wheat germplasm 213

5 Resistance in wheat germplasm to current races

5.1 Race-specific resistance genes

Resistance to diseases can be broadly classified as race specific and race-nonspecific[36]. Race-specific genes (R- genes) have been traditionally preferred by plant breeders for their dominant, major-effect resistant phenotypes, which facilitated easy selection and deployment in breeding programs[37]. However, it has long been noted that the resistance of R-genes, particularly when deployed singly, breaks down quickly, in what has been often referred to as boom-bust cycles[38] and the use of one or more widely deployed R-genes favors the selection of new pathogen races with virulence to one or more widely deployed R-genes. The unique and broad virulence spectrum of the Ug99 race group has rendered not only several important R-genes ineffective but also several important wheat cultivars and breeding materials all over the world[39–41]. Even though some of the race-specific genes confer

resistance to the current races, they have limited use in breeding owing to negative linkage drag, unadapted backgrounds, and their secondary and tertiary gene pool origin necessitating considerable research efforts for utilization through breeding. About 20% of the CIMMYT current advanced breeding materials carry effective R- genes. Sr13, Sr22, Sr25, Sr26 and markers are routinely used to test for stem rust genes. Sr13, Sr22, Sr23, Sr25, Sr26, Sr32, Sr33, Sr35, Sr38, Sr42, Sr47, Sr50[42–54]

and temporarily designated genes SrHuw234, SrND643,

SrNing and SrYanac[55,56] (Table 2), along with multiple adult plant resistance (APR) genes including Sr2 in the background can be used in the breeders tool box for pyramiding using marker assisted selection. However, efficient gene stewardship measures need to be adopted to limit the occurrence of boom-bust cycles. Even though the wheat genome is large and complex, significant progress has been made in cloning six Ug99 resistance genes, including Sr13, Sr22, Sr33, Sr45, Sr35 and Sr50[57–61]. More resistance genes are necessary to diversify the combinations of resistance genes deployed as gene pyramids, or in transgenic cassettes, to provide durable resistance[25].

5.2 Race-nonspecific APR

Race-nonspecific APR is effective against multiple races of a pathogen species and/or effective against broad range of pathogens. Van der Plank[62] provided the theoretical basis of the concepts of resistance, which was widely used for breeding for stem rust resistance by Borlaug[63], for leaf rust resistance by Caldwell[64] and for yellow rust resistance by Johnson[65]. APR is generally quantitative, exhibiting partial or incomplete resistance typically triggered at later stages of development, so is therefore considered to be APR. These genes usually exhibit slower disease progress through an increased latency period, reduced infection points and lower spore production. The phenotypic effect of such genes is relatively minor to moderate, however, additive effects of multiple APR genes (4-5) in combinations can result in very high levels of resistance[66,67]. In contrast to most R-genes, some APR

Fig. 2 Wheat accessions phenotyped during 2005–2018 for Ug99 resistance at Njoro (Kenya) and participating countries, in partnership with Kenya Agriculture Livestock Research Organization, Kenya

214 Front. Agr. Sci. Eng. 2019, 6(3): 210–224

genes have proven to be highly durable, such as stem rust resistance gene Sr2, transferred to cvs Hope and H44-24a from Yaroslav emmer wheat by McFadden in the early 1920s, which has provided resistance to stem rust for over 100 years. This approach of breeding for slow development of the

three rusts has been integral to CIMMYT’s bread wheat improvement program for over 40 years, with a significant impact, averting major epidemics over the last few decades[68]. Significant progress has also been made in understanding the genetic basis and the mechanisms of such resistance and is being routinely applied in breeding at CIMMYT. Combinations of Sr2 with other unknown genes, commonly known as the Sr2-complex, have provided a basis of durable resistance to stem rust in germplasm from Australia, Canada, Mexico and the USA[69,70]. Sr2 is linked to a morphological marker called pseudo-black chaff phenotype and is known to confer modest levels of APR under high disease pressure[67–71], including infection by strains of the Ug99 race group[25,41,72]. Three pleiotropic APR genes in addition

to Sr2 (= Yr30) locus, viz. Sr55 (= Lr67/Yr46/Pm46), Sr57 (= Lr34/Yr18/Pm38/Sb1/Bdv1) and Sr58 (= Lr46/ Yr29/Pm39), conferring multi-pathogen resistance[73–76]

were identified in CIMMYT wheat germplasm and used in marker assisted selection (Table 3)[77–80]. These genes in combination with other APR genes confer enhanced APR to the three rusts[81]. Several mapping studies using CIMMYT semidwarf wheat cultivars showing high levels of resistance to the Ug99 race group indicated the presence of three to five quantitative trait loci conferring APR[82–84]. Notably, all studies indicated that Sr2 was the most important APR gene conditioning resistance to stem rust. Recent cloning of pleiotropic APR genes, Lr34

and Lr67, provided valuable insights into the mechanisms of race-nonspecific resistance. The two genes were found to respectively encode an ATP binding cassette transporter and a hexose transporter[85,86]. In addition to broad- spectrum multi-pathogen resistance, both genes express a leaf-tip necrosis phenotype, which is also observed in genotypes that carry the currently uncloned gene, Lr46. These phenotypic similarities suggest a common

Table 2 Molecular markers linked to stem rust resistance genes conferring seedling resistance and widely used in CIMMYT breeding program

Gene Reported linked marker Marker type Reference stock Reference

Sr13 barc104, dupw167, CD926040, BE471213 SSR Kofa, Kronos [42]

Sr22 wmc633, cfa2123 SSR Sr22Tb, Steinwedel [43]

Sr23 Xgwm210 SSR AC Domain [44]

Sr25 wMAS000032, wmc221 SSR Agatha, Misr#1 [45]

Sr26 Sr26#43, BE518379 STS WA1 [46]

Sr32 csSr32#1, csSr32#2 STS Angas, Aroona, Westonia [47]

Sr33 barc152, cfd15, BE405778, BE499711 SSR RL5288 [48,49]

Sr35 cfa2170, cfa2076, wmc169, wmc559 SSR G2919 [50]

Sr38 CIMwMAS0004, Ventriup/LN2 SNP, STS VPM1 [51]

Sr42 barc183, FSD_RSA SSR Norin 40 [52]

Sr47 Xrwgs38 SSR DAS15 [53]

Sr50 Sr50-5p-F3/R2 SSR Gabo1BL.1RS and Gabo1DL.1RS-DR.A [54]

Sr-6DS gpw5182, cfd49 SSR Niini, Coni, Blouk [55]

SrND643 Xgwm350, Xwmc219 SSR ND643 [56]

SrHuw234 wmc332 SSR Huwa [53]

SrYanac barc200 SSR Yaye [53]

Table 3 Molecular markers for pleotropic adult plant resistance (APR) genes used in CIMMYT wheat breeding program

Gene Reported linked marker Marker type Reference stock Reference

Lr34/Yr18/Pm38/Sr57 wMAS000003, wMAS000004 STS, SNP Parula, Thatcher, Glenlea, Jupateco R, Opata, Bezostaya, Chinese Spring.

[75]

Lr46/Yr29/Pm39/Sr58 csLV46, csLV46G22 CAPS Pavon 76, Parula, [76]

Lr67/Yr46/Pm46/Sr55 csSNP856 SNP RL6077 [77]

Sr2/Yr30 csSr2, wMAS000005 CAPS Pavon76 [78]

Sridhar BHAVANI et al. Progress in breeding for stem rust resistance in wheat germplasm 215

mechanism and their additive nature in interaction with other APR genes supports the value of their use in combinations to enhance the durability of resistance. Despite significant progress in characterizing new

sources of APR to stem rust over the last decade, mapping of APR genes can be tedious and challenging owing to their minor effects and their significant interaction with the environment. However, the additive nature of the gene interactions has enabled breeders at CIMMYT to select transgressive progenies that combine multiple minor genes, resulting in enhanced levels of resistance. High levels of APR to the Ug99 race group identified in some semi-dwarf lines was largely due to the selection environments at the phenotyping platforms in Kenya and Ethiopia, and this has allowed targeted breeding effort to build such genetically complex resistance within CIMMYT germplasm[27,40,72].

6 Breeding for stem rust resistance in CIMMYT’s international spring wheat germplasm

CIMMYT has been the largest provider of improved germplasm for most wheat producing countries. The germplasm is distributed in targeted yield trials, screening nurseries and trait-based nurseries, providing a rich source of diversity for various traits of interest to breeding programs. Selected lines from these trials and nurseries are either released directly as cultivars or used in breeding by several national breeding programs in Africa, Asia, Latin America, the Middle East and South Europe. The shuttle- breeding approach developed by Borlaug in the 1940s, originally with the idea of advancing two generations per year in two contrasting locations, shortened the breeding cycle by half. Furthermore by advancing segregating populations and other breeding materials twice each year at two distinct field sites, Ciudad Obregon and Toluca, in Mexico, the germplasm developed from CIMMYT became broadly adapted to various diverse wheat-growing regions and such an effort has continued to result in successful cultivars that are grown over large areas in many countries[87,88]. McFadden[89] developed wheat cv. Hope, derived from a

cross between the North American cv. Marquis and stem rust resistant tetraploid wheat cv. Yaraslav. A sister line derived from cv. Hope, H44-24a, became an important source of stem rust resistance for many wheat breeding programs because it has better agronomic characteristics than Hope. Further genetic characterization identified three resistance genes, Sr7b from Marquis, and Sr9b and Sr17 from Yaraslav[90–92]. Breeding for durable stem rust resistance in CIMMYT wheat breeding program started in the late 1940s when cv. Newthatch was introduced from North America that combined stem rust resistance from cvs Hope and Thatcher derived from tetraploid parents, emmer

cv. Yaraslav and durum cv. Iumillo, respectively[93]. Although several race-specific genes have been found in Hope and Thatcher, the most effective and durable component of the resistance in these two cultivars has been their APR. Cv. Hope and its derivative cv. Chris formed the

foundation of the high-yielding, semi-dwarf, stem rust resistant wheat cultivars in CIMMYT that were exten- sively used by Borlaug and led to the “Green Revolution” in the 1970s. Importantly the two Green Revolution cvs Sonalika and Siete Cerros, also possess adequate levels of resistance to the Ug99 race group in Kenya. The first stem rust resistant tall cultivar released in Mexico in the 1950s, cv. Yaqui 50, and other Sr2-carrying semi-dwarf cultivars largely controlled the stem rust problem in Mexico. Several other resistance genes, e.g., Sr11, Sr24, Sr31, Sr36 and Sr38, were widely used in various breeding programs to control stem rust in the early 1980s. However, gene Sr31 (1BL-1RS translocation) became widely used in many breeding programs including CIMMYT, which almost made stem rust non-existent for over 30 years until the detection of race Ug99 in Uganda. Another rust management strategy has been to rapidly replace suscep- tible cultivars with available resistant cultivars and continue breeding to incorporate diverse resistance genes and APR into high-yielding, adapted cultivars and new germplasm. Finally, a sustainable long-term control strategy is to identify, develop and deploy cultivars with high to adequate levels of durable APR to limit or delay the evolution and selection of new virulence. Testing of wheat lines from Australia, CIMMYT and the

USA at the phenotyping facility in Njoro, Kenya in 2005– 2006 identified a group of materials that conferred high levels of resistance to Ug99 due to the presence of resistance gene Sr24 located on a Thinopyrum elongatum translocation. The resistant Kenyan cv. KS Mwamba, released in 2001 and known to carry Sr24, was widely adopted by farmers, but Sr24 succumbed to stem rust race TTKST, initially detected in low frequency in 2006 but which caused a large-scale epidemic in 2007[20]. As an ongoing effort to mitigate the threat of Ug99, seven cultivars resistant to Ug99 races were released in 2009, 2010 and 2012 in Kenya. Among these, cv. Kenya Robin, released in 2009, became widespread due to higher yield potential and resistance (postulated to carry gene SrTmp). Severe stem rust infections were observed on cv. Kenya Robin in 2013 and two SrTmp variants, TTKTT and TTKTK, within Ug99 lineage detected. In Ethiopia in the same year, the unrelated race TKTTF overcame SrTmp in the widely-grown cv. Digalu, causing a severe but localized stem rust outbreak. Race analysis of samples from Kenya in 2014 and 2015 confirmed the migration of TKTTF to Kenya. This race had been previously reported in Turkey[94,95], Lebanon and Iran[25] and was introduced by wind dispersal[31]. Knowing the consequences of dependence on single,

216 Front. Agr. Sci. Eng. 2019, 6(3): 210–224

race-specific genes for controlling stem rust, CIMMYT undertook breeding for durable APR based on minor additive genes early on. The gene Sr2, which slows rust development, provides only modest levels of resistance by itself, as evidenced by large-scale testing in Kenya where genotypes with pseudo-black chaff expression showed varying degrees of stem rust severity compared to highly susceptible materials. These observations indicated that although Sr2 continues to confer at least some resistance, the gene alone was insufficient to provide adequate resistance under high disease pressure in Kenya. Sr2 was detected in several highly-resistant old, tall Kenyan cultivars, including cv. Kenya Plume[55] and CIMMYT- derived semi-dwarf wheat cvs Kingbird, Parula, Kiritati, Huirivis#1, Juchi, Muu and Pavon 76, which showed high- to-adequate levels of APR to Ug99 races. Wide testing of improved wheat germplasm has also helped in identifying additional sources of APR since the initial screening about a decade ago. These sources are being used at CIMMYT to incorporate durable APR into high-yielding, widely adapted wheat cultivars. In addition to Sr2, pleiotropic genes Sr55, Sr57 and Sr58 conditioning multi-pathogen resistance identified in CIMMYT germplasm are being used to build high levels of APR. Using the similar strategy of accumulating multiple

minor genes as demonstrated for leaf rust and yellow rust[93], breeding efforts were initiated to reconstitute high levels of APR to stem rust in wheat germplasm. A targeted breeding approach began in 2006 to develop lines that combine stem rust resistance in high-yielding spring wheat germplasm (Table 4). This was accomplished by extending the shuttle-breeding scheme to Kenya and maintaining two crop seasons per year in both Mexico and Kenya. Breeding populations in F3 (from simple crosses) and F4 (from BC1 and three-way crosses) generations are introduced to Kenya from Mexico, selected in the off-season and then in the main-season, and then returned to Mexico for final selection. A selected-bulk scheme[96] to advance segregat- ing population is used in successfully combining multiple minor genes and high yield[25]. This breeding strategy has resulted in the identification of rare transgressive segre- gants that combine yield and stem rust resistance. More- over, resistance derived from old, tall Kenyan cvs Kenya Swara and Kenya Fahari has been introgressed into new elite lines such as cv. Kasuko, identified for release in Kenya. Even though breeding for APR to stem rust only started just over a decade ago, there has been significant progress in identifying, characterizing and deploying complex resistance in high-yielding elite germplasm.

7 New technologies to improve stem rust resistance in wheat germplasm

Breeding for rust resistance is the major resource-intense activity next to yield in most breeding programs including

those undertaken by CIMMYT. Several new tools such as marker-assisted selection (MAS), genome-wide associa- tion study (GWAS) and genomic selection (GS) are routinely used at CIMMYT to complement (or) as alternatives for combining high-yielding wheat with adequate levels of polygenic APR[97,98]. Diagnostic markers can be assayed for the presence of resistance gene without the cost of greenhouse or field evaluations thereby reducing the number of plots for evaluation[97]. MAS is a promising strategy for improving the efficiency and accuracy of selection for major effect qualitative genes and can be used to pyramid genes and confirm the presence of genes and gene combinations in released cultivars. MAS would greatly facilitate effective “gene stewardship” measures to develop and deploy varieties that carry multiple resistance genes in combination and diversity for resistance within breeding materials. MAS can be successfully used in rapid introgression strategies, or forward selection approaches to ensure developed lines remain competitive. However, lack of diagnostic markers and the cost associated with developing reliable markers, limit most breeding programs to rely on phenotypic selection. The other limitation in using the pyramiding approach is the need to reconstruct the stack every time a new cross is made, as the genes tend to segregate unless reliable markers are used in tandem to select lines with multiple gene combinations. One of the intrinsic problem of MAS is in improving complex traits controlled by multiple minor effect genes[99]. Besides, the number of molecular markers linked to resistance genes remain insufficient to conduct marker-assisted selection. There- fore, GWAS and GS are promising alternatives for identifying and accumulating favorable alleles for rust resistance traits[99]. Rapid advancement in high-throughput genotyping

technologies in recent years have greatly reduced the cost of genotyping and have made a large number of markers routinely available that enables the use GWAS and GS to overcome the limitations of MAS[100]. GWAS enables the detection of QTL or causal genes for a target trait without using bi-parental segregating populations[99]

and on the other hand uses training populations to calibrate prediction models and enabling the selection of superior individuals based on genomic estimated breeding values (GEBV), which take into account the effects of multiple genes controlling a target trait[98]. At CIMMYT, cross-validation studies have been

performed to evaluate the potential of GS for APR to stem rust[100,101] and results suggested that GS could lead to increased genetic gain compared to MAS and phenotypic selection[98,102]. However, recent studies con- cluded that by implementing both genomic and phenotypic selection strategies in parallel for quantitative stem rust resistance[102] under similar selection intensities, genetic gains from genomic and phenotypic selection were equal. Although the power and resolution of GWAS and the

Sridhar BHAVANI et al. Progress in breeding for stem rust resistance in wheat germplasm 217

Table 4 CIMMYT wheat germplam combining high yield and stem rust resistance (R, APR categories) in international nurseries (based on highest

disease severity recorded in four seasons of field-testing at KALRO, Njoro, Kenya and seedling tests)

Germplasm identifi- cation no.

Cross name/Pedigree Selection history Stem rust severity/%

Resistance genes/ Category1

8237333 BECARD/ND643/2*WBLL1/3/SWSR22T.B./ 2*BLOUK #1//WBLL1*2/KURUKU

CMSS13Y00149S-099Y-099M-099NJ- 099NJ-8Y-0WGY

5 Sr22/SrND643

8234886 MISR 1/3/SWSR22T.B./2*BLOUK #1//WBLL1*2/ KURUKU

CMSS13B00039S-099M-099NJ-099NJ- 10Y-0WGY

15 Sr25/Sr22

8235073 ND643/2*WBLL1/4/WHEAR/KUKUNA/3/C80.1/ 3*BATAVIA//2*WBLL1/5/BORL14

CMSS13B00139S-099M-099NJ-099NJ- 50Y-0WGY

5 Sr25/SrND643

8235528 WBLL1*2/BRAMBLING*2//BAVIS/3/SWSR22T.B./ 2*BLOUK #1//WBLL1*2/KURUKU

CMSS13B00381S-099M-099NJ-099NJ- 5Y-0WGY

5 Sr22/Sr13

8235657 KRONSTAD F2004/KENYA SUNBIRD//WHEAR/ KRONSTAD F2004/3/WBLL1*2/BRAMBLING*2//

BAVIS

CMSS13B00453S-099M-099NJ-099NJ- 25Y-0WGY

10 Sr13/SrND643

8236725 DANPHE #1*2/SHORTENED SR26 TRANSLOCA- TION/3/SWSR22T.B./2*BLOUK #1//WBLL1*2/

KURUKU/4/SWSR22T.B./2*BLOUK #1//WBLL1*2/ KURUKU

CMSS13B01575T-099TOPY-099M- 099NJ-099NJ-2Y-0WGY

10 Sr22/Sr26

8236942 MUTUS*2//ND643/2*WBLL1/3/2*SWSR22T.B./ KACHU//2*KACHU

CMSS13B01701T-099TOPY-099M- 099NJ-099NJ-29Y-0WGY

1 Sr22/SrND643

8236956 WHEAR/KUKUNA/3/C80.1/3*BATAVIA// 2*WBLL1*2/4/NIINI #1*2/5/SWSR22T.B./

2*BLOUK #1//WBLL1*2/KURUKU

CMSS13B01707T-099TOPY-099M- 099NJ-099NJ-14Y-0WGY

5 SrNini/Sr22

8236960 SWSR22T.B./FRANCOLIN #1//2*FRNCLN/5/ WHEAR/KUKUNA/3/C80.1/3*BATAVIA//

2*WBLL1*2/4/NIINI #1/6/BORL14

CMSS13B01709T-099TOPY-099M- 099NJ-099NJ-11Y-0WGY

5 Sr22/SrNini

8248316 WBLL1*2/BRAMBLING//TAM200/TUI/3/VILLA JUAREZ F2009/4/2*BORL14

CMSS13B01705T-099TOPY-099M- 099NJ-099NJ-9Y-0RGY

5 Sr1A.1R

8249245 BABAX/LR42//BABAX/3/ER2000/4/BAVIS/5/ SWSR22T.B./2*BLOUK #1//WBLL1*2/KURUKU

CMSS14Y00716S-099Y-099M-0SY-19M- 0RGY

10 Sr13/Sr22

8238251 KFA/2*KACHU/3/2*ATTILA*2/PBW65*2// MURGA

CMSS13Y01093T-099TOPM-099Y- 099M-099NJ-099NJ-18Y-0WGY

5 APR_NIR

8238893 TOB/ERA//TOB/CNO67/3/PLO/4/VEE#5/5/KAUZ/ 6/FRET2/7/PASTOR//MILAN/KAUZ/3/BAV92/8/

ATTILA*2/PBW65*2//TNMU/9/ATTILA*2/ PBW65*2//MURGA

CMSS13Y01437T-099TOPM-099Y- 099M-099NJ-099NJ-32Y-0WGY

5 APR_NIR

8239063 CORRELL/3/PBW343*2/KUKUNA//TECUE #1/4/ PBW343*2/KUKUNA*2//FRTL/PIFED

CMSS13Y01496T-099TOPM-099Y- 099M-099NJ-099NJ-19Y-0WGY

10 APR_R

8234995 KACHU/DANPHE//KFA/2*KACHU CMSS13B00105S-099M-099NJ-099NJ- 41Y-0WGY

10 APR_R

8235423 KACHU//KIRITATI/2*TRCH/3/KFA/2*KACHU CMSS13B00118S-099M-099NJ-099NJ- 8Y-0WGY

5 APR_NIR

8235262 SUP152/2*DANPHE #1//BORL14 CMSS13B00270S-099M-099NJ-099NJ- 6Y-0WGY

10 APR_R

8235936 BECARD//ND643/2*WBLL1/3/KACHU/DANPHE CMSS13B00700S-099M-099NJ-099NJ- 5Y-0WGY

5 APR_NIR

8236909 WHEAR/KUKUNA/3/C80.1/3*BATAVIA// 2*WBLL1/4/PAURAQUE #1/5/WHEAR/KUKUNA/

3/C80.1/3*BATAVIA//2*WBLL1/6/2*KACHU/ DANPHE

CMSS13B01680T-099TOPY-099M- 099NJ-099NJ-14Y-0WGY

5 APR_NIR

8236918 CHYAK1/VILLA JUAREZ F2009//WBLL1*2/ BRAMBLING/7/PRL/2*PASTOR/4/CHOIX/STAR/ 3/HE1/3*CNO79//2*SERI/5/KIRITATI/2*TRCH/6/ PRL/2*PASTOR/4/CHOIX/STAR/3/HE1/3*CNO79//

2*SERI/8/KACHU/DANPHE

CMSS13B01683T-099TOPY-099M- 099NJ-099NJ-10Y-0WGY

10 APR_R

218 Front. Agr. Sci. Eng. 2019, 6(3): 210–224

accuracy of GS can be generally improved by large data sets; for quantitative disease resistance, greater selection intensities under GS and better prediction models may be needed to surpass phenotypic selection. Combining GWAS and GS with MAS will accelerate breeding cycles[103] and rationalize the design of breeding programs. Irrespective of whatever molecular techniques are used, there is a strong need to maintain the greenhouse and field phenotyping facility to verify that the desired level of resistance is expressed in the selected lines. Cloning of some wheat rust resistance genes in the

recent years offers scope to pyramid multiple genes as Cis-gene cassettes for enhancing resistance durability[25]. These gene stacks or cassettes developed on a single construct would be inherited as a single locus, thus facilitating rapid transfer into different genetic back- grounds without the fear of losing stacks due to segregation, hence making it easier to retain multiple gene combinations. Designing cassettes carrying combina- tions of both R and APR genes in high yielding lines by transformation in addition to other useful traits which are difficult to combine through conventional breeding can be accomplished through this process and offering scope of adding or replacing genes to generate new gene stacks. Although this technology is promising, the feasibility of developing varieties is limited by regulatory and consumer acceptance issues as transgenic wheat cultivars are not grown currently anywhere in the world. Genome editing technology in the recent years has

shown great potential to overcome the limitations of conventional resistance breeding. This technology offers the advantage of modifying specific target genes in elite varieties, thus bypassing the whole process of crossing.

Genome editing being site-specific avoids the potential problems of linkage drag and does not require genetic crosses and selection in segregating generations that can accelerate breeding for disease resistance and breeders can focus on more critical issues such as increasing yield potential. Genome editing was found to be effective in improving powdery mildew resistance in wheat[104] and can be used for modifying targets for a range of traits within polyploid genomes. To become a routine procedure, however, sequences of the resistance genes for editing need to be known, but these remain limited in wheat.

8 Future of rust resistance breeding

Stem rust is still one of the major threats to wheat production because of the extreme level of damage the disease causes to susceptible varieties. Although it is under control in the world’s major production areas, serious genetic vulnerability exists and active steps are being taken to incorporate new effective resistance into most wheat breeding programs. However, evolution and faster spread of more virulent pathogen races and selection for fungicide resistance due to excessive use necessitate reinforcing breeding strategies to develop adequate durable resistance to multiple diseases for enhancing wheat productivity, while simultaneously reducing the cultivation of suscep- tible varieties in disease prone regions. Cultivars carrying single race specific genes for

resistance have resulted in boom and bust cycles and breeding programs should ensure multiple gene combina- tions through MAS to enhance the resistance durability. On the other hand APR genes like Sr2 and Sr55, Sr57 and

(Continued)

Germplasm identifi- cation no.

Cross name/Pedigree Selection history Stem rust severity/%

Resistance genes/ Category1

8236943 SUP152*2/TINKIO #1/4/FRET2*2/SHAMA//KIRI- TATI/2*TRCH/3/BAJ #1/5/SUP152*2/TINKIO #1

CMSS13B01703T-099TOPY-099M- 099NJ-099NJ-15Y-0WGY

5 APR_NIR

8244588 KACHU/SAUAL/3/TACUPETO F2001/BRAM- BLING//KIRITATI/4/COPIO

CMSS14Y00648S-099Y-099M-0SY-13M- 0WGY

5 APR_NIR

8245010 KACHU/DANPHE*2//BORL14 CMSS14Y01482T-099TOPM-099Y- 099M-0SY-24M-0WGY

15 APR_R-MR

8245012 KACHU/DANPHE*2//BORL14 CMSS14Y01482T-099TOPM-099Y- 099M-0SY-34M-0WGY

5 APR_NIR

8241262 KACHU/BECARD//WBLL1*2/BRAMBLING*2/5/ ATTILA/3*BCN*2//BAV92/3/KIRITATI/WBLL1/4/

DANPHE

CMSS14B01373T-099TOPY-099M-0SY- 37M-0WGY

10 APR_R

8248604 CHIPAK*2//TRCH/HUIRIVIS #1 CMSS13Y01097T-099TOPM-099Y- 099M-099NJ-099NJ-6Y-0RGY

5 APR_NIR

8249240 NGL/4/PFAU/MILAN/3/BABAX/LR42//BABAX/5/ KFA/2*KACHU

CMSS14Y00712S-099Y-099M-0SY-5M- 0RGY

5 APR_NIR

Note: 1 Resistance categories for adult plant resistance (APR) are: NIR = near-immune resistant, R = resistant, and R-MR = resistant-moderately resistant.

Sridhar BHAVANI et al. Progress in breeding for stem rust resistance in wheat germplasm 219

Sr58 can be combined with other R or APR genes (due to their multi-pathogen and additive effects) resulting in higher levels of resistance. Even though only a few APR genes have been characterized in the past, with newer tools many such genes with broad-spectrum resistance should become available for use in breeding. Maintaining diversity for stem rust resistance within

breeding germplasm and identifying and characterizing new genes in the breeder’s toolbox will greatly reduce the vulnerability of cultivars and provide options for immedi- ate replacement. Active survey and surveillance in under- standing the variation in pathogen populations, their evolution and migration can help in pre-emptive breeding and coupled with forecasting models can help in reducing the disease impacts in many wheat-growing regions. Breeding strategies such as GWAS and GS will greatly enhance identification and selection of superior individuals based on GEBV, which take into account the effects of multiple genes controlling a target trait. Promising new technologies such as Cis-gene cassettes, gene editing, GM technology and additional genetic analysis will provide the tools for understanding and developing durable rust resistance. Finally, breeders and farmers should discourage growing stem rust susceptible varieties thereby reducing the inoculum build up, evolution of new virulences and spread to other wheat growing regions. This strategy can largely contain the disease, preventing it from developing into devastating epidemics.

9 Concluding remarks

The rapid evolution and spread of both the Ug99 and Digalu race groups of stem rust fungus over a decade in several countries of Africa, Middle East and Europe, causing localized epidemics, reconfirms the famous observation of Borlaug that “rust never sleeps”. Research to mitigate the threat of stem rust started with the launch of the Borlaug Global Rust Initiative in 2005. Major achievements include surveillance, including understand- ing pathogen diversity and its spread, evolution and migration, as well as the establishment of phenotyping platforms to facilitate the testing of global wheat germplasm and the identification and characterization of new sources of race-specific and APR genes. All of this has led to the development of rust-resistant cultivars and their rapid deployment in target countries. CIMMYT breeding over the last decade has provided improved high-yielding wheat germplasm carrying high to adequate resistance to the currently predominant races in Africa and the Middle East. More than 100 Ug99 resistant cultivars have been deployed both in primary and secondary risk regions, mitigating the potential threat even in countries where Ug99 is not yet present. However, emerging concerns of

new race groups migrating into Europe and across several countries in Africa highlights the importance of breeding and continuous deployment of resistant germplasm in target environments to limit future epidemics.

Acknowledgements We gratefully acknowledge the support of partnering institutions and financial support particularly from the DGGW Project managed by Cornell University and funded by the Bill and Melinda Gates Foundation and the UK Department for International Development, as well as the Indian Council of Agricultural Research, USAID, USDA-ARS and GRDC-Australia. We also thank Greg Grahek (Vice President of Publishing, The American Phytopathological Society) for Phytopathology’s permission (Ref. 25).

Compliance with ethics guidelines Sridhar Bhavani, David P. Hodson, Julio Huerta-Espino, Mandeep S. Randhawa, and Ravi P. Singh declare that they have no conflicts of interest or financial conflicts to disclose.

This article is a review and does not contain any studies with human or animal subjects performed by any of the authors.

References

1. Curtis B C. Wheat in the world. In: Curtis B C, Rajaram S,

Macpherson H G, eds. Bread wheat improvement and production.

FAO Plant Production and Protection Series. Rome: FAO, 2002, 1–

19

2. Wiese M V. Compendium of wheat diseases. 2nd ed. St. Paul,

USA: American Phytopathological Society Press, 1987, 112

3. Oerke E C. Crop losses to pests. Journal of Agricultural Sciences,

2005, 144(1): 31–43

4. Kislev M E. Stem rust of wheat 3300 years old found in Israel.

Science, 1982, 216(4549): 993–994

5. Chester K S. The nature and prevention of the cereal rusts as

exemplified in the leaf rust of wheat. Waltham, MA, USA:

Chronica Botanica, 1946, 538

6. Kolmer J A, Long D L, Hughes M E. Physiological specialization

of Puccinia triticina on wheat in the United States in 2004. Plant

Disease, 2006, 90(9): 1219–1224

7. Roelfs A P, Huerta-Espino J, Marshall D. Barley stripe rust in

Texas. Plant Disease, 1992, 76(5): 538

8. Zadoks J C. Epidemiology of wheat rust in Europe. FAO Plant

Protection Bulletin, 1963, 13: 97–108

9. Rees R G. Uredospore movement and observations on the

epidemiology of wheat rusts in north-eastern Australia. Australian

Journal of Agricultural Research, 1972, 23(2): 215–223

10. Watson I A. Wheat and its rust parasites in Australia. In: Evans L T,

Peacock W J, eds. Wheat science—today and tomorrow. Cam-

bridge, UK: Cambridge University Press, 1981, 129–147

11. Joshi L M, Palmer L T. Epidemiology of stem, leaf and stripe rusts

of wheat in northern India. Plant Disease Reporter, 1973, 57: 8–12

12. Roelfs A P. Foliar fungal diseases of wheat in the People’s

Republic of China. Plant Disease Reporter, 1977, 61: 836–841

13. Luig N H. Epidemiology in Australia and New Zealand. In: Roelfs

A P, Bushnell W R, eds. The cereal rusts, vol. 2, diseases,

distribution, epidemiology, and control. Orlando, FL, USA:

Academic Press, 1985, 301–328

220 Front. Agr. Sci. Eng. 2019, 6(3): 210–224

14. Saari E E, Prescott J M. World distribution in relation to economic

losses. In: Roelfs A P, Bushnell W R, eds. The cereal rusts, vol. 2,

diseases, distribution, epidemiology, and control, Orlando, FL,

USA: Academic Press, 1985, 259–298

15. Leonard K J. Stem rust-future enemy? In: Peterson P, ed. Stem rust

of wheat: from ancient enemy to modern foe. St. Paul, USA:

American Phytopathological Society Press, 2001, 119–146

16. Pardey P G, Beddow J M, Kriticos D J, Hurley T M, Park R F,

Duveiller E, Sutherst R W, Burdon J J, Hodson D. Right-sizing

stem rust research. Science, 2013, 340(6129): 147–148

17. 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 Disease, 2000, 84(2): 203

18. 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

Disease, 2007, 91(9): 1096–1099

19. Jin Y, Singh R P. Resistance in U.S. wheat to recent eastern

African isolates of Puccinia graminis f. sp. tritici with virulence to

resistance gene Sr31. Plant Disease, 2006, 90(4): 476–480

20. Jin Y, Szabo L J, Pretorius Z A, Singh R P, Ward R, Fetch T Jr.

Detection of virulence to resistance gene Sr24 within race TTKS of

Puccinia graminis f. sp. tritici. Plant Disease, 2008, 92(6): 923–

926

21. Jin Y, Szabo L J, Rouse M N, Fetch T Jr, Pretorius Z A, Wanyera

R, Njau P. Detection of virulence to resistance gene Sr36 within the

TTKS race lineage of Puccinia graminis f. sp. tritici. Plant

Disease, 2009, 93(4): 367–370

22. Patpour M, Hovmøller M S, Justesen A F, Newcomb M, Olivera P,

Jin Y, Szabo J, Hodson D, Shahin A, Wanyera R, Habarurema I,

Wobibi S. Emergence of virulence to SrTmp in the Ug99 race

group of wheat stem rust, Puccinia graminis f. sp. tritici, in Africa.

Plant Disease, 2016, 100(2): 522

23. Newcomb M, Olivera P D, Rouse M N, Szabo L J, Johnson J, Gale

S, Luster D G, Wanyera R, Macharia G, Bhavani S, Hodson D,

Patpour M, Hovmøller M S, Fetch T G Jr, Jin Y. Kenyan isolates of

Puccinia graminins f. sp. tritici from 2008 to 2014: virulence to

SrTmp in the Ug99 race group and implications for breeding

programs. Phytopathology, 2016, 106(7): 729–736

24. Hodson D P, Hansen J G, Lassen P, Alemayehu Y, Arista J, Sonder

K, Kosina P, Moncada P, Nazari K, Park R F, Pretorius Z A, Szabo

L J, Fetch T, Jin Y. Tracking the wheat rust pathogen. In:

Proceedings of the 2012 Borlaug Global Rust Initiative Technical

Workshop, Beijing, 2012

25. 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, Basnet B

R, Lan C, Hovmøller M S. Emergence and spread of new races of

wheat stem rust fungus: continued threat to food security and

prospects of genetic control. Phytopathology, 2015, 105(7): 872–

884

26. Patpour M, Hovmøller M S, Shahin A, Newcomb M, Olivera P, Jin

Y, Hodson D, Nazari K, Azab M. First report of the Ug99 race

group of wheat stem rust, Puccinia graminis f. sp. tritici, in Egypt

in 2014. Plant Disease, 2016, 100(4): 863

27. 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 Disease, 2016, 100(7): 1495

28. Terefe T, Pretorius Z A, Visser B, Boshoff W H B. First report of

Puccinia graminis f. sp. tritici race PTKSK, a variant of wheat

stem rust race Ug99 in South Africa. Plant Disease, 2019.

[Published online] doi:10.1094/PDIS-11-18-1911-PDN

29. Olivera P, Newcomb M, Szabo L J, Rouse M, Johnson J, Gale S,

Luster D G, Hodson D, Cox J A, Burgin L, Hort M, Gilligan C A,

Patpour M, Justesen A F, Hovmøller M S, Woldeab G, Hailu E,

Hundie B, Tadesse K, Pumphrey M, Singh R P, Jin Y. Phenotypic

and genotypic characterization of race TKTTF of Puccinia

graminis f. sp. tritici that caused a wheat stem rust epidemic in

southern Ethiopia in 2013–14. Phytopathology, 2015, 105(7):

917–928

30. 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 Pathology,

2017, 66(8): 1258–1266

31. Meyer M, Cox J A, Hitchings M D T, Burgin L, Hort M C, Hodson

D P, Gilligan C A. Quantifying airborne dispersal routes of

pathogens over continents to safeguard global wheat supply.

Nature Plants, 2017, 3(10): 780–786

32. Bhattacharya S. Deadly new wheat disease threatens Europe’s

crops. Nature, 2017, 542(7640): 145–146

33. Barnes C W, Ordóñez M E, Hambleton S, Dadej K, Szabo L J,

Fetch T G. Detection of wheat stem rust race RRTTF in Ecuador in

2016. Plant Disease, 2018, 102(2): 448

34. Shamanin V, Salina E, Wanyera R, Zelenskiy Y, Olivera P,

Morgounov A. Genetic diversity of spring wheat from Kazakhstan

and Russia for resistance to stem rust Ug99. Euphytica, 2016, 212

(2): 287–296

35. Berlin A. Stem rust attacks in Sweden heralds the return of a

previously vanquished foe. Available at SLU website on

September 1, 2017

36. Vander Plank J E. Disease resistance in plants. New York:

Academic Press, 1968

37. Boyd L A, Ridout C, O’Sullivan D M, Leach J E, Leung H. Plant-

pathogen interactions: disease resistance in modern agriculture.

Trends in Genetics, 2013, 29(4): 233–240

38. Johnson T. Man-guided evolution in plant rusts: through his

modification of the host plants of the cereal rusts, man is also

modifying the rusts. Science, 1961, 133(3450): 357–362

39. Singh R P, Huerta-Espino J, William H M. Genetics and breeding

for durable resistance to leaf and stripe rusts in wheat. Turkish

Journal of Agriculture and Forestry, 2005, 29: 121–127

40. Singh R P, Hodson D P, Huerta-Espino J, Jin Y, Njau P, Wanyera

R, Herrera-Foessel S A, Ward R W. Will stem rust destroy the

world’s wheat crop? Advances in Agronomy, 2008, 98: 271–309

41. 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. Annual Review of Phytopathology, 2011,

49(1): 465–481

42. Simons K, Abate Z, Chao S, Zhang W, Rouse M, Jin Y, Elias E,

Dubcovsky J. Genetic mapping of stem rust resistance gene Sr13 in

Sridhar BHAVANI et al. Progress in breeding for stem rust resistance in wheat germplasm 221

tetraploid wheat (Triticum turgidum ssp. durum L.). Theoretical

and Applied Genetics, 2011, 122(3): 649–658

43. Olson E L, Brown-Guedira G, Marshall D, Stack E, Bowden R L,

Jin Y, Rouse M N, Pumphrey M O. Development of wheat lines

having a small introgressed segment carrying stem rust resistance

gene Sr22. Crop Science, 2010, 50(5): 1823–1830

44. McCartney C A, Somers D J, McCallum B D, Thomas J,

Humphreys D G, Menzies J G, Brown P D. Microsatellite tagging

of the leaf rust resistance gene Lr16 on wheat chromosome 2BS.

Molecular Breeding, 2005, 15(4): 329–337

45. Zhang W, Dubcovsky J. Association between allelic variation at

the Phytoene synthase 1 gene and yellow pigment content in the

wheat grain. Theoretical and Applied Genetics, 2008, 116(5): 635–

645

46. 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. Theoretical

and Applied Genetics, 2013, 126(12): 2943–2955

47. 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 rust resistance genes Sr24 and Sr26 in diverse wheat

germplasm. Theoretical and Applied Genetics, 2005, 111(3): 496–

504

48. Sambasivam P K, Bansal U K, Hayden M J, Dvorak 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,

August 24–29, 2008

49. Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L,

Deal K, Luo M, Kong X, Bariana H, Mago R, McIntosh R, Dodds

P, Dvorak J, Lagudah E. The gene Sr33, an ortholog of barley Mla

genes, encodes resistance to wheat stem rust race Ug99. Science,

2013, 341(6147): 786–788

50. Zhang W, Olson E, Saintenac C, Rouse M, Abate Z, Jin Y,

Akhunov E, Pumphrey M, Dubcovsky J. Genetic maps of stem rust

resistance gene Sr35 in diploid and hexaploid wheat. Crop Science,

2010, 50(6): 2464–2474

51. Helguera M, Khan I A, Kolmer J, Lijavetzky D, Zhong-qi L,

Dubcovsky J. PCR assays for the Lr37-Yr17-Sr38 cluster of red

resistance genes and their use to develop isogenic hard red spring

wheat lines. Crop Science, 2003, 43(5): 1839–1847

52. 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. Theoretical and Applied Genetics, 2012, 125(4): 817–824

53. Yu G, Klindworth D L, Friesen T L, Faris J D, Zhong S,

Rasmussen J B, Xu S S. Development of a diagnostic co-dominant

marker for stem rust resistance gene Sr47 introgressed from

Aegilops speltoides into durum wheat. Theoretical and Applied

Genetics, 2015, 128(12): 2367–2374

54. Mago R, Zhang P, Vautrin S, Šimková H, Bansal U, Luo M C, Rouse M, Karaoglu H, Periyannan S, Kolmer J, Jin Y, Ayliffe M A,

Bariana H, Park R F, McIntosh R, Doležel J, Bergès H, Spielmeyer W, Lagudah E S, Ellis J G, Dodds P N. The wheat Sr50 gene

reveals rich diversity at a cereal disease resistance locus. Nature

Plants, 2015, 1(12): 15186

55. Lopez-Vera E E, Nelson S, Singh R P, Basnet B R, Haley S D,

Bhavani S, Huerta-Espino J, Xoconostle-Cazares B G, Ruiz-

Medrano R, Rouse M N, Singh S. Resistance to stem rust Ug99 in

six bread wheat cultivars maps to chromosome 6DS. Theoretical

and Applied Genetics, 2014, 127(1): 231–239

56. Basnet B R, Singh S, Lopez-Vera E E, Huerta-Espino J, Bhavani S,

Jin Y, Rouse M N, Singh R P. Molecular mapping and validation

of SrND643: a new wheat gene for resistance to the stem rust

pathogen Ug99 race group. Phytopathology, 2015, 105(4): 470–

476

57. 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.

Proceedings of the National Academy of Sciences of the United

States of America, 2017, 114(45): E9483–E9492

58. Steuernagel B, Periyannan S K, Hernández-Pinzón I, Witek K,

Rouse M N, Yu G, Hatta A, Ayliffe M, Bariana H, Jones J D,

Lagudah E S, Wulff B B. Rapid cloning of disease-resistance genes

in plants using mutagenesis and sequence capture. Nature

Biotechnology, 2016, 34(6): 652–655

59. Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L,

Deal K, Luo M, Kong X, Bariana H, Mago R, McIntosh R, Dodds

P, Dvorak J, Lagudah E. The gene Sr33, an ortholog of barley Mla

genes, encodes resistance to wheat stem rust race Ug99. Science,

2013, 341(6147): 786–788

60. 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

(6147): 783–786

61. Mago R, Zhang P, Vautrin S, Šimková H, Bansal U, Luo M C, Rouse M, Karaoglu H, Periyannan S, Kolmer J, Jin Y, Ayliffe M A,

Bariana H, Park R F, McIntosh R, Doležel J, Bergès H, Spielmeyer W, Lagudah E S, Ellis J G, Dodds P N. The wheat Sr50 gene

reveals rich diversity at a cereal disease resistance locus. Nature

Plants, 2015, 1(12): 15186

62. Van der Plank J E. Plant disease: epidemic and control. New York:

Academic Press, 1963

63. Borlaug N E. A cereal breeder and ex-forester’s evaluation of the

progress and problems involved in breeding rust resistant forest

trees: “Moderator’s Summary”. Biology of rust resistance in forest

trees. In: Proceedings of a NATO-IUFRO Advanced Study

Institute. August 17–24, 1969. USDA Forest Service Misc.

Publication, 1972, 1221: 615–642

64. Caldwell R M. Breeding for general and/or specific plant disease

resistance. In: Finlay KW Shepherd KW, eds. Third International

Wheat Genetics Symposium. Sydney, Australia: Butterworth,

1968, 263–274

65. Johnson R. Durable resistance to yellow (stripe) rust in wheat and

its implications in plant breeding. In: Simmonds N W, Rajaram S,

eds. Breeding strategies for resistance to the rusts of wheat. D.F.,

Mexico: CIMMYT, 1988, 63–75

66. Knott D R. Multigenic inheritance f stem rust resistance in wheat.

Crop Science, 1982, 22(2): 393–399

67. Knott D R. Using polygenic resistance to breed for stem rust

resistance in wheat. In: Simmonds N W, Rajaram S, eds. Breeding

222 Front. Agr. Sci. Eng. 2019, 6(3): 210–224

strategies for resistance to the rusts of wheat. D.F., Mexico:

CIMMYT, 1988, 39–47

68. Marasas C N, Smale M, Singh R P. The economic impact in

developing countries of leaf rust resistance breeding in CIMMYT

related spring bread wheat. D.F., Mexico: CIMMYT, 2004

69. McIntosh R A. The role of specific genes in breeding for durable

stem rust resistance in wheat and triticale. In: Simmonds N W,

Rajaram S, eds. Breeding strategies for resistance to the rusts of

wheat. D.F., Mexico: CIMMYT, 1988, 1–9

70. Rajaram S, Singh R P, Torres E. Current CIMMYT approaches in

breeding for leaf rust resistance. In: Simmonds N W, Rajaram S,

eds. Breeding strategies for resistance to the rusts of wheat. D.F.,

Mexico: CIMMYT, 1988, 101–118

71. Hare R A, McIntosh R A. Genetic and cytogenetic studies of

durable adult-plant resistances in ‘Hope’ and related cultivars to

wheat rusts. Z. Pflanzenzucht, 1979, 83: 350–36

72. Njau P N, Jin Y, Huerta-Espino J, Keller B, Singh R P.

Identification and evaluation of sources of resistance to stem rust

race Ug99 in wheat. Plant Disease, 2010, 94(4): 413–419

73. 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. Theoretical and Applied Genetics,

2014, 127(7): 1561–1581

74. 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. Theoretical and Applied Genetics, 2014, 127(4):

781–789

75. Singh R P, Herrera-Foessel S A, Huerta-Espino J, Bariana H,

Bansal U, McCallum B, Hiebert C W, Bhavani S, Singh S, Lan C,

Lagudah E S. Lr34/Yr18/Sr57/Pm38/Bdv1/Ltn1 confers slow

rusting, adult plant resistance to Puccinia graminis tritici. In:

Proceedings of the 13th International Cereal Rusts and Powdery

Mildews Conference, Chen W-Q, ed. Beijing, 2012

76. Singh R P, Herrera-Foessel S A, Huerta-Espino J, Lan C X, Basnet

B R, Bhavani S. Pleiotropic gene Lr46/Yr29/Pm39/Ltn2 confers

slow rusting, adult plant resistance to wheat stem rust fungus. In:

Proceedings of the 2013 Borlaug Global Rust Initiative Technical

Workshop, New Delhi, 2013

77. 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.

Theoretical and Applied Genetics, 2009, 119(5): 889–898

78. Kolmer J A, Lagudah E S, Lillemo M, Lin M, Bai G. The Lr46

gene conditions partial adult-plant resistance to stripe rust, stem

rust, and powdery mildew in Thatcher wheat. Crop Science, 2015,

55(6): 2557–2565

79. Forrest K, Pujol V, Bulli P, Pumphrey M, Wellings C, Herrera-

Foessel S, Huerta-Espino J, Singh R, Lagudah E, Hayden M,

Spielmeyer W. Development of a SNP marker assay for the Lr67

gene of wheat using a genotyping by sequencing approach.

Molecular Breeding, 2014, 34(4): 2109–2118

80. Mago R, Brown-Guedira G, Dreisigacker S, Breen J, Jin Y, Singh

R, Appels R, Lagudah E S, Ellis J, Spielmeyer W. An accurate

DNA marker assay for stem rust resistance gene Sr2 in wheat.

Theoretical and Applied Genetics, 2011, 122(4): 735–744

81. Randhawa M S, Lan C, Basnet B R, Bhavani S, Huerta-Espino J,

ForrestK L, Hayden M J, Singh R P. Interactions among genes Sr2/

Yr30, Lr34/Yr18/Sr57 and Lr68 confer enhanced adult plant

resistance to rust diseases in common wheat (Triticum aestivum L.)

line ‘Arula’. Australian Journal of Crop Science, 2018, 12(6):

1023–1033

82. Bhavani S, Singh R P, Argillier O, Huerta-Espino J, Singh S, Njau

P, Brun S, Lacam S, Desmouceaux N. Mapping durable adult plant

stem rust resistance to the race Ug99 group in six CIMMYT

wheats. In: Proceedings of Borlaug Global Rust Initiative

Technical Workshop. Saint Paul, Minnesota, USA, 43–53, 2011

83. Njau P N, Bhavani S, Huerta-Espino J, Keller B, Singh R P.

Identification of QTL associated with durable adult plant resistance

to stem rust race Ug99 in wheat cultivar ‘Pavon 76’. Euphytica,

2013, 190(1): 33–44

84. Singh A, Knox R E, DePauw R M, Singh A K, Cuthbert R D,

Campbell H L, Singh D, Bhavani S, Fetch T, Clarke F.

Identification and mapping in spring wheat of genetic factors

controlling stem rust resistance and the study of their epistatic

interactions across multiple environments. Theoretical and Applied

Genetics, 2013, 126(8): 1951–1964

85. 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(5919): 1360–1363

86. Moore J W, Herrera-Foessel S, Lan C, Schnippenkoetter W,

Ayliffe M, Huerta-Espino J, Lillemo M, Viccars L, Milne R,

Periyannan S, Kong X, Spielmeyer W, Talbot M, Bariana H,

Patrick J W, Dodds P, Singh R, Lagudah E. A recently evolved

hexose transporter variant confers resistance to multiple pathogens

in wheat. Nature Genetics, 2015, 47(12): 1494–1498

87. Lantican M A, Dubin H J, Morris M L. Impacts of international

wheat breeding research in the developing world, 1988–2002.

D.F.,Mexico: CIMMYT, 2005

88. Lantican M A, Braun H J, Payne T S, Singh R P, Sonder K, Baum

M, Van Ginkel M, Erenstein O. Impacts of International Wheat

Improvement Research, 1994–2014. D.F., Mexico: CIMMYT,

2016

89. McFadden E S. A successful transfer of emmer characters to

vulgare wheat. American Society of Agronomy, 1930, 22(12):

1020–1034

90. Mcintosh R, Luig N, Baker E. Genetic and cytogenetic studies of

stem rust, leaf rust, and powdery mildew resistances in Hope and

related wheat cultivars. Australian Journal of Biological Sciences,

1967, 20(6): 1181–1192

91. Knott D. The inheritance of resistance to stem rust races 56 and

15B–1L (Can.) in the wheat varieties Hope and H-44. Canadian

Journal of Genetics and Cytology, 1968, 10(2): 311–320

92. Knott D. Genes for stem rust resistance in wheat varieties Hope and

H-44. Canadian Journal of Genetics and Cytology, 1971, 13(2):

186–188

93. Stakman E, Rodenhiser H. Race 15B of wheat stem rust—what it is

and what it means. Advances in Agronomy, 1959, 10: 143–165

94. Mert Z, Karakaya A, Dusuncelı F, Akan K, Cetın L. Determination of Puccinia graminis f. sp. tritici races of wheat in Turkey. Turkish

Sridhar BHAVANI et al. Progress in breeding for stem rust resistance in wheat germplasm 223

Journal of Agriculture and Forestry, 2012, 36: 107–120

95. Newcomb M, Acevedo M, Bockelman H E, Brown-Guedira G,

Goates B J, Jackson E W, Jin Y, Njau P, Rouse M N, Singh D,

Wanyera R, Bonman J M. Field resistance to the Ug99 race group

of the stem rust pathogen in spring wheat landraces. Plant Disease,

2013, 97(7): 882–890

96. Singh R P, William H M, Huerta-Espino J, Rosewarne G. Wheat

rust in Asia: meeting the challenges with old and new technologies.

In: Proceedings of the 4th International Crop Science Congress,

New Directions for a Diverse Planet. Fisher T, Turner N, Angus J,

McIntyre L, Robertson M, Borrell A, Lloyd D, eds., 2004

97. Heffner E L, Jannink J L, Sorrells M E. Genomic selection

accuracy using multifamily prediction models in a wheat-breeding

program. Plant Genome, 2011, 4(1): 65–75

98. Mago R, Simkova H, Brown-Guedira G, Dreisigacker S, Breen J,

Jin Y, Singh R, Appels R, Lagudah E S, Ellis J, Dolezel J,

Spielmeyer W. An accurate DNA marker assay for stem rust

resistance gene Sr2 in wheat. Theoretical and Applied Genetics,

2011, 122(4): 735–744

99. Lorenz A J, Chao S, Asoro F G, Heffner E L, Hayashi T, Iwata H,

Smith K P, Sorrells M E, Jannink J L. Genomic selection in plant

breeding: knowledge and prospects. Advances in Agronomy, 2011,

110: 77–123

100. Rutkoski J, Poland J A, Singh R P, Huerta-Espino J, Bhavani S,

Barbier H, Rouse M N, Jannink J L, Sorrells M E. Genomic

selection for quantitative adult plant stem rust resistance in wheat.

Plant Genome, 2014, 7(3): 1–10

101. Ornella L, Singh S, Perez P, Perez P, Burgueño J, Singh R, Tapia E,

Bhavani S, Dreisigacker S, Braun H-J, Mathews K, Crossa J.

Genomic prediction of genetic values for resistance to wheat rusts.

Plant Genome, 2012, 5(3): 136–148

102. Khan M A, Korban S S. Association mapping in forest trees and

fruit crops. Journal of Experimental Botany, 2012, 63(11): 4045–

4060

103. Rutkoski J, Singh R P, Huerta-Espino J, Bhavani S, Poland J,

Jannink J L, Sorrells M E. Genetic gain from phenotypic and

genomic selection for quantitative resistance to stem rust of wheat.

Plant Genome, 2015, 8(2): 2–10

104. Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu J L.

Simultaneous editing of three homoeoalleles in hexaploid bread

wheat confers heritable resistance to powdery mildew. Nature

Biotechnology, 2014, 32(9): 947–951

105. Singh R P, Hodson D P, Jin Y, Huerta-Espino J, Kinyua M G,

Wanyera R, Njau P, Ward R W. Current status, likely migration

and strategies to mitigate the threat to wheat production from race

Ug99 (TTKS) of stem rust pathogen. Perspectives in Agriculture,

Veterinary Science, Nutrition and Natural Resources, 2006, 1

(054): 1–13

106. Meyer M, Burgin L, Hort M C, Hodson D P, Gilligan C A. Large-

scale atmospheric dispersal simulations identify likely airborne

incursion routes of wheat stem rust into Ethiopia. Phytopathology,

2017, 107(10): 1175–1186

107. 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, Berlin A, García R, Germán S E, Hanzalová A,

Hodson D P, Hovmøller M S, Huerta-Espino J, Imtiaz M, Mirza J

I, Justesen A F, Niks R E, Omrani A, Patpour M, Pretorius Z A,

Roohparvar R, Sela H, Singh R P, Steffenson B, Visser B, Fenwick

P M, Thomas J, Wulff B B H, Saunders D G O. Potential for re-

emergence of wheat stem rust in the United Kingdom. Commu-

nications Biology, 2018, 1(1): 13

108. Singh R P, McIntosh R A. Genetics of resistance to Puccinia

graminis tritici and Puccinia recondita tritici in Kenya Plume

wheat. Euphytica, 1986, 35(1): 245–256

109. Singh R P, McIntosh R A. Genetics of resistance to Puccinia

graminis tritici and Puccinia recondite tritici in four South African

wheats. Theoretical and Applied Genetics, 1990, 79(3): 401–

410

110. Singh R P, Huerta-Espino J, Rajaram S. Achieving near-immunity

to leaf and stripe rusts in wheat by combining slow rusting

resistance genes. Acta Phytopathologica et Entomologica Hungar-

ica, 2000, 35: 133–139

224 Front. Agr. Sci. Eng. 2019, 6(3): 210–224