The Crop Journal 10 (2022) 490–497Contents lists available at ScienceDirect
The Crop Journal
journal homepage: www.keaipubl ishing.com/en/ journals / the-crop- journal /Three co-located resistance genes confer resistance to leaf rust and stripe
rust in wheat variety Borlaug 100⇑ Corresponding author.
E-mail address: cxlan@mail.hzau.edu.cn (C. Lan).
https://doi.org/10.1016/j.cj.2021.07.004
2214-5141/
 2021 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. on behalf of KeAi Communications
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).Bowei Ye a, Ravi P. Singh b, Chan Yuan a, Demei Liu c, Mandeep S. Randhawa b, Julio Huerta-Espino d,
Sridhar Bhavani b, Evans Lagudah e, Caixia Lan a,⇑
aCollege of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, China
b International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, 06600 Mexico D.F., Mexico
cQinghai Provincial Key Laboratory of Crop Molecular Breeding, Northwest Institute of Plateau Biology, Chinese Academy of Science, Xining 810008, Qinghai, China
dCampo Experimental Valle de México INIFAP, Apdo. Postal 10, 56230, Chapingo, Edo. de Mexico, Mexico
eCSIRO Agriculture & Food, GPO Box 1600, Canberra, ACT 2601, Australia
a r t i c l e i n f o a b s t r a c tArticle history:
Received 21 December 2020
Revised 20 April 2021
Accepted 26 July 2021
Available online 17 August 2021
Keywords:
Co-located resistance loci
Common wheat
Gene interaction
Puccinia triticina
Puccinia striiformis
Triticum aestivumLeaf rust (LR) and stripe rust (YR) are important diseases in wheat producing areas worldwide and cause
severe yield losses under favorable environmental conditions when susceptible varieties are grown. We
determined the genetic basis of resistance to LR and YR in variety Borlaug 100 by developing and pheno-
typing a population of 198 F6 recombinant inbred lines derived from a cross with the susceptible parent
Apav#1. LR and YR phenotyping were conducted for 4 and 3 seasons, respectively, at CIMMYT research
stations in Mexico under artificial epidemics. Mendelian segregation analyses indicated that 3–5 LR and 2
YR genes conferred resistance in Borlaug 100. Lr46/Yr29 (1BL), Yr17 (2AS) and Yr30 (3BS) were present in
the resistant parent and segregated in the RIL population based on characterization by molecular markers
linked to these genes. When present alone, Lr46/Yr29 caused average 13% and 16% reductions in LR and
YR severities, respectively, in RILs. Similarly, Yr17 and Yr30 reduced YR severities by 57% and 11%, respec-
tively. The Yr30 and the Yr17 translocation were also associated with 27% and 14% reductions, respec-
tively, in LR severity, indicating that the 3BS and 2AS chromosomal regions likely carry new slow
rusting LR resistance genes, temporarily designated as LrB1 and LrB2, respectively. Additive effects of
Yr30*Yr17, Yr29*Yr17 and Yr29*Yr30 on YR and LR were significant and reduced YR severities by 56%,
55%, and 45%, respectively, and LR severities by 34%, 40%, and 45%, respectively. Furthermore, interaction
between the three genes was also significant, with mean reductions of 70% for YR and 54% for LR sever-
ities. Borlaug 100, or any one of the 21 lines with variable agronomic traits but carrying all three co-
located resistance loci, can be used as resistance sources in wheat breeding programs.

 2021 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by
Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC BY-NC-
ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).1. Introduction
Leaf rust (LR) and stripe rust (YR) are fungal wheat diseases
caused by Puccinia triticina (Pt) and P. striiformis f. sp. tritici (Pst),
respectively. Rusts are known to occur more frequently than other
wheat diseases and pose a serious threat to wheat production
worldwide. Beddow et al. [1] estimated that about 88% of world
wheat production could be affected by YR due to favorable climatic
conditions with expected annual production losses estimated
around 5.4 million tons. LR is the most widespread and common
disease of wheat and can cause yield losses of up to 70% in suscep-tible varieties [2]. Therefore, improving rust resistance is an impor-
tant objective for wheat breeding programs worldwide because
growing resistant varieties is the most economical, effective, and
environmentally friendly strategy to manage these diseases.
Resistance to rusts in wheat can be grouped in two broad cate-
gories based on the phenotypic expression at different stages of
growth. Seedling or all stage resistance is often differentially
expressed and is commonly referred as race specific resistance
[3]. This type of resistance usually exhibits various degrees of
hypersensitivity. Race specific resistance often fails within 3–
5 years of deployment due to selection of virulent variants [4].
Another type of resistance, often called as adult plant resistance
(APR) is effective at post-seedling or adult plant stages and is usu-
ally manifested by a slow disease progression (slow rusting)Co., Ltd.
B. Ye, R.P. Singh, C. Yuan et al. The Crop Journal 10 (2022) 490–497despite a susceptible host reaction. However, some race specific
adult plant resistance genes are also known. Effective levels of
the slow rusting type of resistance are more commonly controlled
by a small number of minor genes with additive effects [5,6] and
some have pleiotropic effects in conferring resistance to other dis-
eases [7,8]. However, the number of such resistance genes identi-
fied to date is limited, and the interactions among them are
inadequately studied. Therefore, it is important to identify new
APR genes and to elucidate their gene interactions for optimal uti-
lization in wheat breeding programs aimed at developing varieties
with durable resistance.
At present, about 100 LR resistance genes have been character-
ized in wheat [9]. Most of them are seedling resistance genes, how-
ever three pleiotropic genes Yr18/Lr34/Sr57/Pm38/Ltn1 [10], Yr29/
Lr46/Sr58/Pm39/Ltn2 [11] and Yr46/Lr67/Sr55/Pm46/Ltn3 [12], as
well as Lr68 [13], Lr74 [14], Lr75 [15], Lr77 [16], and Lr78 [17] con-
fer APR to LR. Likewise, 83 YR resistance genes have been formally
cataloged and some of them show slow-rusting APR, such as Yr16,
Yr30, Yr36, Yr39, Yr52, Yr59, Yr62, Yr68, Yr71, Yr75, Yr77, Yr78, Yr79,
Yr80, and Yr82 [18–22]. Closely linked or gene specific markers for
Lr34/Yr18, Lr46/Yr29, Lr67/Yr46, Yr30, and Lr68 have been devel-
oped, such as csLv34/cssfr1-cssfr5 [23,24], csLv46G22/csLv46 [25],
TM4/TM10 [26], csSr2/Xgwm533 [27,28] and cs7BLNRR/csGS [13],
respectively, that are commonly used in marker-assisted selection.
Wheat varieties may have improved resistance when they carry
multiple resistance genes. Singh et al. [29] found the complemen-
tary genes interaction between Lr27 and Lr31, indicating that resis-
tance was only expressed when seedling resistance genes Lr27 and
Lr31 appeared simultaneously in wheat such as in the chromosome
substitution line ‘‘Chinese Spring (Hope 3B)” and Australian wheat
cultivar Gatcher. Klymiuk et al. [30] reported that Pst race DK92/02
was virulent on Avocet + Yr15 (IT = 5–7), and AU85569 was viru-
lent on Avocet + Yr5 (IT = 7), while pyramiding Yr15 with Yr5 in
four different backgrounds (YecoraRojoYr5Yr15, PatwinYr5Yr15,
SummitYr5Yr15, and DirkwinYr5Yr15) showed full protection
against both virulent isolates. Zheng et al. [31] revealed that com-
binations of Yr17 + Yr26 and Yr9 + Yr18 conferring significant resis-
tance to Pst the field trails. Singh et al. [32,33] found that varieties
with resistance gene Lr34/Yr18 in combination with 2 to 4 addi-
tional minor effect genes displayed reduced LR and YR severities
under high inoculum pressure. Silva et al. [34] found that the
Lr34 + Lr68 + Sr2 gene combination significantly reduced the area
under the disease progress curve (AUDPC) for LR by 70% in the
genetic background of Parula. Ponce-Molina et al. [35] reported
that interaction between Lr46/Yr29 and Lr67/Yr46 reduced disease
severity by 11% for and 5% for YR. Liu et al. [36] reported significant
additive effects between gene combinations Yr26 + Yr48,
Yr30 + Yr64 and Yr30 + Yr48. Therefore, the interaction of resistance
genes in different combinations is not only important for enhanced
resistance but also maintains genetic diversity in achieving stable,
long-term resistance in wheat varieties.
The objectives of the present study were to: i) understand the
genetic basis of LR and YR resistance in a Apav#1 
 Borlaug 100
mapping population; ii) identify known and possible unknown
resistance genes in Borlaug 100 that contribute to high levels of
adult plant resistance to LR and YR; and iii) explore interaction
effects among the identified resistance genes.2. Materials and methods
2.1. Plant materials
We developed 198 recombinant inbred lines (RILs) from a cross
between Apav#1 (CIMMYT GID 1854090, pedigree: Avocet-YrA/
Pavon) and Borlaug 100 (CIMMYT name: Reedling#1, GID4917806808, pedigree: Rolf 07/4/Bow/Nkt//Cbrd/3/Cbrd/5/Fret2/Tuku
ru//Fret2). Apav#1 is susceptible to LR and YR at both the seedling
and adult plant stages. In contrast, Borlaug 100 showed high levels
of resistance to both diseases at the adult plant stage, but suscep-
tible and intermediate host reactions, respectively, at the seedling
stage. Borlaug 100 showed 9% higher grain yield than other widely
grown varieties, including its parent Roelfs F2007, good bread
quality, heat and drought tolerance, and expressed good resistance
to wheat blast when tested in Bolivia and Bangladesh. Because of
these attributes it was also released in Australia, Bangladesh, Boli-
via, and Nepal under the names Borlaug 100, WMRI#3, INIAF Trop-
ical, and Borlaug 2020, respectively.
2.2. Field trials
The RIL population and the parents were grown and pheno-
typed for LR and YR response at CIMMYT research stations at Ciu-
dad Obregon in the Yaqui Valley, and Toluca and El Batan in the
Central Mexican highlands. Specifically, the population was evalu-
ated for APR to YR at El Batan during the 2016 growing season
(YR2016B) and at Toluca during the 2016 and 2017 seasons
(YR2016T and YR2017T). LR assessments were made at Obregon
during 2015–2016 and 2016–2017 (LR2016Y and 2017Y) and El
Batan during the 2016 and 2017 (LR2016B and LR2017B) growing
seasons. The high yielding, irrigated environment in Obregon,
located at 28N latitude, 39 m above sea level, is appropriate for
LR phenotyping due to cool nights with good dews and warm days.
The Toluca research station is located at 18N latitude and 2640 m
above sea level, receives about 800 mm of rain during the crop sea-
son and experiences cool nights that together provide a good envi-
ronment for YR development. Similarly, El Batan is situated at 18N
latitude and 2200 m above sea level with about 400 mm rainfall
and has conducive temperatures for LR development; however,
YR can also occur if the cooler temperatures prevail for extended
periods during the tillering to heading stages.
2.3. Field trials and inoculation methods
The parents and RILs were planted in 0.7 m paired rows on
80 cm wide raised beds at about 60 seeds in each plot. In the LR
field experiment, spreaders of susceptible line Avocet + Yr24/Yr26
was sown on one side of each plot as clumps in the middle of
the 0.3 m pathways and around the experimental block. Equal pro-
portions of the urediniospores of Pt races MBJ/SP and MCJ/SP were
suspended in lightweight mineral oil (Soltrol 170R) and was
sprayed on the spreaders about 6 weeks after sowing; and the
same procedure was repeated over three consecutive days. The
avirulence/virulence formula of MBJ/SP and MCJ/SP was described
by Herrera-Foessel et al. [13]. A similar field design was used for YR
testing. A mixture of six susceptible wheat lines derived from the
Avocet/Attila, Morocco, and near-isogenic line Avocet + Yr31 were
used as YR spreaders. Pst race Mex08.13 was sprayed on the YR
spreaders within and around the test areas about 4 weeks after
sowing and repeated thrice. The avirulence/virulence formula for
Mex08.13 is given in Lan et al. [37].
2.4. Disease evaluation
The disease evaluations on flag leaves were carried out visually
and included disease severity (DS) based on the modified Cobb
Scale [38] and host reaction. The first disease data were recorded
when the susceptible parent Apav#1 displayed around 80% sever-
ity, whereas second scores were made one week later. The final DS
was used in all analysis. The host reactions followed the descrip-
tion given in Roelfs et al. [39], where ‘R’ = highly resistant, or
hypersensitive necrotic areas with no or small uredinia/
B. Ye, R.P. Singh, C. Yuan et al. The Crop Journal 10 (2022) 490–497sporulation; ‘MR’ = moderately resistant, or necrotic areas with
medium sized uredinia/moderate sporulation; ‘MS’ = moderately
susceptible, medium sized uredinia/moderate sporulation without
chlorosis/necrosis; ‘S’ = susceptible, large size uredinia/profusely
sporulating areas without chlorosis/necrosis; and various combi-
nations of the above.
2.5. Molecular marker analysis
DNA from parents and 198 RILs were extracted using the CTAB
method [25]. Functional/closely-linked molecular markers for 8
leaf rust (Lr1, Lr9, Lr10, Lr16, Lr19, Lr21, Lr26, and Lr46) and 11
stripe rust (Yr5, Yr9, Yr10, Yr15, Yr17, Yr18, Yr26, YrSP, Yr29, Yr30,
and Yr46) resistance genes (Table S1), were used for parental
screening. Three polymorphic markers, csLV46G22, gwm533, and
VENTRIUP/LN2, were then used for genotyping of the entire RIL
population. A standard polymerase chain reaction (PCR) was per-
formed following Dreisigacker et al. [25]. A 10 lL system was used
for PCR amplification, including 5 lL 2
 Taq PCR Mix, 2 lL 1 lmol
L1 primer and 3 lL DNA. The PCR amplification procedure was as
follows: pre-denaturation at 94 C for 5 min; denaturing at 94 C
for 1 min; annealing at 50–66 C for 1 min (the temperature deter-
mined by each primer); extension at 72 C for 2 min, a total of 30–
35 cycles; finally, extension for 10 min at 72 C and preservation at
4 C. Amplified products were detected by 1.5%–3% agarose gel
electrophoresis. Cleaved amplified polymorphism (CAP) was used
with csLV46G22, and amplification products were digested with
BspeI endonuclease (37 C, 1 h) before detection by electrophoresis.
KASP markers were assayed by RT-PCR.
2.6. Genetic and statistical analysis
The SAS PROC CORR program was used to calculate Pearson’s
correlation coefficients between final disease severities in tested
environments. The number of resistance genes was estimated
using the F6 phenotypic segregation ratio by the Mendelian segre-
gation [40]. The 198 RILs were grouped into three phenotypic cat-
egories based on DS and host reaction, including homozygous
parental type resistant (HPTR) that showed a similar or lower phe-
notype compared to the resistant parent, homozygous parental
type susceptible (HPTS), that showed a similar or higher phenotype
compared to the susceptible parent, and the remaining RILs formed
the ‘‘Others” category [40]. These results were then compared with
the expected frequencies from Mendelian segregation to deter-
mine the number of resistance genes. The v2 analysis was per-
formed using the ‘‘CHITEST” function in Microsoft Excel. The SAS
PROC GLM program was used to test the interaction between LR
and YR resistance loci.3. Results
3.1. Phenotypic analysis
The final LR severity (FDS) and reaction of the susceptible par-
ent Apav#1 were 90%–100% S across four environments whereas
resistant parent Borlaug 100 displayed 0–1% MS (Fig. S1A) in all
test environments. The mean LR severities of the population ran-
ged from 20.9% to 37.7% (Fig. S1A). The DS of RILs showed a contin-
uous distribution (Fig. S1A) across four environments, indicating
quantitative inheritance for LR.
The FDS and host reaction of Borlaug 100 were 1%–20% MS over
three YR test environments, whereas Apav#1 showed 90%–100% S.
The average DS for the entire population was 33.9% to 44.7%
(Fig. S1B). FDS for YR was also continuously distributed indicating
the presence of multiple resistance genes.492The correlation coefficients between disease severities of RILs
across the four LR environments ranged from 0.78 to 0.86 (Table 1),
and from 0.70 to 0.91 for the three YR environments (Table 1).
There were significant correlations ranging from 0.37 to 0.81
between LR and YR severities (Table 1). These relatively high corre-
lation coefficients between LR and YR severities indicated the pres-
ence of segregating pleiotropic resistance genes in the population.
3.2. Estimation of gene numbers
The Mendelian genetic analyses comparing the observed and
expected frequencies of RILs in the three phenotypic categories
suggested the segregation of 3 to 5 LR resistance genes with addi-
tive effects in the four environments (Table 2). For YR, the observed
frequencies of RILs in the three phenotypic categories conformed
to an expected segregation of two resistance genes showing addi-
tive effects in all three environments (Table 2).
3.3. Known resistance gene analysis
The closely linked molecular marker csLV46G22 confirmed the
presence of the pleiotropic resistance gene Lr46/Yr29 in Borlaug
100 and permitted classification of RILs for the presence and
absence of this gene. The LR severity of RILs ranged from 10%
to 90% when Lr46 was absent, whereas severity ranged from 1%
to 70% when present (Fig. 1A). The mean final LR severity of RILs
containing Lr46 was significantly reduced by an average of 17%
compared to the non-Lr46 RILs (Table 3). LR severity was 1%–
80% for RILs carrying the Yr30 gene from Borlaug 100 based on
molecular marker gwm533, and 5%–90% in RILs without the gene
(Fig. 1B). For the introgressed segment containing Yr17, also
derived from Borlaug 100, the LR severity of RILs with and with-
out the 2NS segment was 1%–70% and 5%–90%, respectively
(Fig. 1C). The significant reductions in LR severities in RILs due
to the presence of Yr30 and Yr17 were 17.2% and 18.3%, respec-
tively, indicating that these genes or gene regions, conferred slow
rusting resistance to LR (Table 3). We therefore provisionally des-
ignated the respective slow rusting leaf rust resistance genes as
LrB1 and LrB2.
For YR, the closely linked molecular markers for resistance
genes Yr29, Yr30 and Yr17 identified their presence in Borlaug
100 and RILs were also characterized for their presence or
absence. Single marker analysis showed a significant correlation
between these genes and YR severity reductions (Table 3). YR
FDS was 1% to 90% and 10% to 90% for RILs containing and lacking
Yr29, respectively (Fig. 1D). On average, RILs carrying only Yr29
showed significantly lower disease severity than RILs without it
(Table 3). For the APR gene Yr30, the mean YR severity of RILs car-
rying this gene was 15.4% less than the RILs without it (Table 3;
Fig. 1E). RILs with gene Yr17, showed mean FDS ranging from 1%
to 80% whereas those without it displayed 10%–90% FDS (Fig. 1F).
The disease severity for RILs carrying the introgressed Yr17 seg-
ment was significantly reduced by 32.7% compared with the RILs
without it (Table 3).
3.4. Interaction between detected resistance genes
The mean severities of RILs carrying combinations of at least
two resistance genes were significantly lower than the mean sever-
ities of RILs carrying only one of them. Based on combined data, the
gene combinations Yr30*Yr17, Yr29*Yr17 and Yr29*Yr30 had a sig-
nificant effect on YR response with reductions in YR severity by
56%, 55%, and 45%, respectively (Table 4). However, no significant
interaction on YR was detected among three resistance genes com-
pared with the two genes combinations (Table S2). The mean YR
FDS of RILs pyramided with all three genes was reduced to 5.7%,
B. Ye, R.P. Singh, C. Yuan et al. The Crop Journal 10 (2022) 490–497
Table 1
Phenotypic correlations between leaf rust (LR) and stripe rust (YR) disease severities in 4 leaf rust and 3 stripe rust environments in Apav#1 
 Borlaug 100 recombinant inbred
lines population.
Environments LR2016Y LR2016B LR2017Y LR2017B YR2016B YR2016T
LR2016B 0.78**
LR2017Y 0.84** 0.81**
LR2017B 0.80** 0.83** 0.86**
YR2016B 0.55** 0.37** 0.49** 0.52**
YR2016T 0.79** 0.75** 0.79** 0.81** 0.70**
YR2017T 0.73** 0.68** 0.74** 0.75** 0.70** 0.91**
LR2016Y, final leaf rust severity, Obregon 2015–2016; LR2016B, final leaf rust severity, Batan 2016; LR2017Y, final leaf rust severity, Obregon 2016–2017; LR2017B, final leaf
rust severity, Batan 2017; YR2016B, final stripe rust severity, Batan 2016; YR2016T, final stripe rust severity, Toluca 2016; YR2017T, final stripe rust severity, Toluca 2017. **,
P < 0.01
Table 2
The number of resistance genes that confer adult plant resistance to leaf rust and stripe rust calculated by Mendelian segregation ratios in Apav#1 
 Borlaug 100 recombinant
inbred lines population.
Category LR2016Y LR2016B LR2017Y LR2017B YR2016B YR2016T YR2017T
HPTR 14 7 19 22 34 42 43
HPTS 6 3 15 22 41 34 50
Others 178 187 161 151 121 116 102
Total 198 197 195 195 196 192 195
No. of genes 4 5 3 3 2 2 2
P-value 0.18* 0.39* 0.45* 0.79* 0.20* 0.32* 0.44*
LR2016Y, final leaf rust severity, Obregon 2015–2016; LR2016B, final leaf rust severity, Batan 2016; LR2017Y, final leaf rust severity, Obregon 2016–2017; LR2017B, final leaf
rust severity, Batan 2017; YR2016B, final stripe rust severity, Batan 2016; YR2016T, final stripe rust severity, Toluca 2016; YR2017T, final stripe rust severity, Toluca 2017;
HPTR, homozygous parental type resistant (RILs showing a similar phenotype as the resistant parent); HPTS, homozygous parental type susceptible (RILs showing a similar
phenotype as the susceptible parent); Others, RILs showing different responses from the above two categories; *, P < 0.05.
Fig. 1. Comparison for the mean leaf rust and stripe rust severities in the presence and absence of individual resistance genes in Apav#1 
 Borlaug 100 recombinant inbred
lines (RILs) population. (A) Leaf rust severities for RILs with and without Lr46. (B) Leaf rust severities for RILs with and without LrB1. (C) Leaf rust severities for RILs with and
without LrB2. (D) Stripe rust severities for RILs with and without Yr30. (E) Stripe rust severities for RILs with and without Yr29. (F) Stripe rust severities for RILs with and
without Yr17.i.e. approached a near-immune resistance level (Fig. 2). For LR,
highly significant interactions occurred between Yr30, or the provi-
sionally designated gene LrB1, and the other two genes as well as
among all three of them (Table S2). Similarly, the combination of
Yr30/LrB1*Yr17/LrB2, Lr46/Yr29*Yr17/LrB2 and Lr46/Yr29*Yr30/LrB1
reduced LR severity by 34%, 40%, and 45%, respectively (Table 4).
Once again, the mean LR FDS was <5% in 21 RILs that possessed
all three resistance genes (Fig. 2).4934. Discussion
YR and LR are devastating wheat diseases and occur worldwide.
They often weaken the growth and development of wheat plants
resulting in grain shriveling, and may lead to no harvest in serious
cases [41]. CIMMYT plays an important role in mitigating the
threat of these diseases by developing and sharing high yielding,
stress tolerant and disease resistant wheat germplasm with
B. Ye, R.P. Singh, C. Yuan et al. The Crop Journal 10 (2022) 490–497
Table 3
The final mean leaf rust and stripe rust severities for Apav#1 
 Borlaug 100 recombinant inbred lines (RILs) possessing and lacking resistance genes Lr46/Yr29, LrB1/Yr30 and LrB2/
Yr17 determined through respective molecular marker analysis and their comparison using t-tests.
Resistance gene Gene status No. of RILs Leaf rust severity (%) Stripe rust severity (%)
LR2016Y LR2016B LR2017Y LR2017B Mean YR2016B YR2016T YR2017T Mean
Lr46/Yr29 Absent 81 34.8 a# 20.3 a 50.3 a 41.2 a 36.6 a 25.2 a 44.0 a 48.9 a 39.2 a
Present 109 19.1 b 12.1 b 25.5 b 23.1 b 20.0 b 19.2 b 29.7 b 35.8 b 28.2 b
LrB1/Yr30 Absent 72 38.0 a 22.6 a 51.4 a 43.2 a 38.8 a 26.2 a 50.2 a 52.7 a 42.9 a
Present 110 18.6 b 12.0 b 27.7 b 23.8 b 20.5 b 19.1 b 27.9 b 35.6 b 27.5 b
LrB2/Yr17 Absent 105 33.8 a 21.3 a 44.2 a 40.9 a 35.1 a 31.1 a 54.1 a 58.6 a 47.9 a
Present 88 16.5 b 9.7 b 26.6 b 19.1 b 17.9 b 10.2 b 15.7 b 20.1 b 15.2 b
# a and b mean the significant difference between two values at P < 0.01; LR2016Y, final leaf rust severity, Obregon 2015–2016; LR2016B, final leaf rust severity, Batan
2016; LR2017Y, final leaf rust severity, Obregon 2016–2017; LR2017B, final leaf rust severity, Batan 2017; YR2016B, final stripe rust severity, Batan 2016; YR2016T, final
stripe rust severity, Toluca 2016; YR2017T, final stripe rust severity, Toluca 2017.
Table 4
Mean leaf rust and stripe rust severities of Apav#1 
 Borlaug 100 RILs with and without resistance genes Lr46/Yr29, LrB1/Yr30 and LrB2/Yr17 in the Apav#1/Borlaug 100
population.
Status of resistance gene No. of RILs Mean leaf rust severity (%) Mean stripe rust severity (%)
Lr46/Yr29 LrB1/Yr30 LrB2/Yr17
Absent Absent Absent 14 58.3 75.8
Absent Present Absent 21 31.7 65.3
Present Absent Absent 27 45.5 60.1
Present Present Absent 33 13.4 31.0
Present Absent Present 16 18.7 20.4
Absent Present Present 30 24.6 19.7
Absent Absent Present 10 44.9 19.1
Present Present Present 21 4.7 5.7
Fig. 2. Additive interaction between detected resistance gene Lr46/Yr29 (1BL), LrB1/Yr30 (3BS) and LrB2/Yr17 (2AS) and respective mean diseases severities in the
Apav#1 
 Borlaug 100 RIL population.partners worldwide. This improved germplasm is the major source
of new wheat varieties in Asia, Africa, and Latin America. Since the
1970s, CIMMYT has pioneered research on APR to rusts, and suc-
cessfully applied the strategy to build durable resistance in vari-
eties that has remained effective for over 50 years [42]. Borlaug
100, the variety used in this study, showed high levels of resistance
to LR and YR in field trials under Mexican environments despite
being susceptible to LR and showing only moderately resistant to
YR in the seedling stage. The distribution of Apav#1 
 Borlaug
100 RILs was continuous for both LR and YR severities in all trials.494Mendelian analyses of the observed phenotypic frequencies of RILs
in the three categories indicated that a minimum of three to five
genes with additive effects could be involved in LR resistance
and two genes conferred YR resistance. RILs were genotyped with
three polymorphic molecular markers known to be closely linked
to resistance genes Lr46/Yr29, Yr17 and Yr30 to determine their
contribution to resistance.
The pleiotropic, slow rusting resistance gene Lr46/Yr29 plays an
important role in wheat varieties with durable resistance to LR and
YR and has remained effective for over 40 years. This gene
B. Ye, R.P. Singh, C. Yuan et al. The Crop Journal 10 (2022) 490–497conferred resistance in various mapping populations and under
different experimental conditions [43–45]. For example, Lillemo
et al. [46] reported that Lr46/Yr29 reduced the severity of LR and
YR by 78% and 24%, respectively, and Lan et al. [47] found that
Lr46/Yr29 had similar effects on LR and YR responses with 40%
and 20% reductions in disease severity, when Lr46/Yr29 alone
was segregating in a population. The presence of Lr46/Yr29 in our
RIL population on reduced average LR and YR severities by 13%
and 16%, respectively.
Yr30 on chromosome 3BS is closely linked/pleiotropic to stem
rust (SR) resistance gene Sr2 and linked to LR gene Lr27. Crossa
et al. [48] reported that most CIMMYT spring wheat varieties car-
rying Sr2 showed moderate resistance to YR in multiple environ-
ments. In our population, Yr30 reduced mean YR severity by 7.2%
and LR severity by 17.2% indicating either that Yr30 had pleiotropic
effect on LR, or that a co-located slow rusting gene conferred LR
resistance. We provisionally designated the LR gene as LrB1. The
combination of LrB1 and Lr46 reduced disease severity by 45%,
indicating the importance of pyramiding them to achieve higher
resistance levels. Basnet et al. [49] also detected the same additive
effect in a segregating Avocet 
 Quaiu # 3 population. The comple-
mentary seedling resistance gene combination, Lr27 + Lr31, confers
LR resistance to avirulent races, but Pt races MBJ/SP and MCJ/SP
used in our study were virulent on plants with this gene combina-
tion in both seedling and adult plants. The Mexican cultivar Jupa-
teco 73S, known to possess Lr27 + Lr31, is highly susceptible to
these races in field trials. The susceptible seedling reaction of Bor-
laug 100 further demonstrates that the slow rusting resistance
attributed to Yr30 was not due to Lr27 + Lr31. Ingala et al. [50]
found an APR gene LrSV2, which is also located on chromosome
3BS, and is closely linked to SSR marker gwm533 [51]. In addition,
the high-resolution mapping of Lr27 and LrSV2 showed that both
genes were in adjacent intervals in chromosome 3BS [52]. There-
fore, it is necessary to perform allelism tests between Lr27, LrB1
and LrSV2 to confirm their relationship, however we postulate that
the slow rusting resistance to stem rust, YR and LR conferred by
Sr2, Yr30 and LrB1, respectively, is due to the same pleiotropic
resistance gene.
Yr17was reported as a seedling resistance gene to YR showing a
high level of resistance [53,54]. Milus et al. [55] suggested that the
expression of Yr17 resistance at the seedling or adult plant stage
varied with the genetic background and environmental conditions,
mainly affected by temperature and light intensity. Combining
Yr17 with other minor resistance genes can play an effective role
in imparting improved resistance levels. For example, the wheat
variety ‘Jagger’ has long-lasting resistance due to the combination
of Yr17 and the pleiotropic slow rusting resistance gene Yr18/Lr34
in North America [56]. Moreover, Yr17was the most effective resis-
tance genes in the Jagger mapping population explaining 80% of
the phenotypic variation. These results are consistent with our
finding where the combination of Yr17 and APR genes Yr29 and
Yr30 significantly improved the resistance levels to the Pst races
used. However, we have observed that the effect of Yr17 is lost to
Pst races that carry virulence to it (the infection type (IT) was ‘80
for Avocet + Yr17 near isogeneic line against Pst race Mex08.13
based on ‘0–9 Scale’).
Yr17 was identified in an introgressed segment of Aegilops ven-
tricosa chromosome 2 N in the wheat line VPM1. The translocation
also carried genes Lr37 and Sr38 [57]. The Pt races MBJ/SP and MCJ/
SP used in our study are virulent to the race-specific gene Lr37 (the
IT was 3 + against MBJ/SP and MCJ/SP, respectively, based on 0–4
Scale and the leaf rust severity of NIL-THATCHER-LR37-VPM was
80% against the both races in the adult plant stage in BV2014, El
Batan, Mexico), indicating the presence of a new slow rusting gene
for leaf rust, provisionally designated as LrB2. Although LrB2 had
only small effect in reducing LR severity when present alone, its495combination with Lr46 and LrB1 resulted in significant increase
in resistance (Table 4).
Our study again shows that pyramiding small to intermediate
effect APR genes is important for improving resistance to wheat
rusts. Lan et al. [58] found that Lr46/Yr29 and YrF had a significant
additive effect on reducing stripe rust disease severity and played
an important role in the resistance of wheat variety Francolin#1.
Herrera-Foessel et al. [59] reported that wheat line Lalbahadur
(Pavon 1B), which was one of the parents of Almop and possessed
both Lr46/Yr29 and Yr60 was a superior donor parent for breeding
because it displayed a much higher level of resistance in field trials
than lines carrying these genes independently. In addition, there is
compelling evidence that a high level of resistance or near-
immunity can be achieved through combining multiple minor/
intermediate effect APR genes [45,60,61]. The mean LR and YR
severities in field trials for the resistant parent Borlaug 100 in
our study were 1% and 10%, respectively; and the 21 RILs carrying
all three resistance genes showed mean severities of 4.7% for LR
and 5.7% for YR (Table 4). Borlaug 100, or selected RILs, can be used
as resistance sources for breeding.
CRediT authorship contribution statement
Bowei Ye: Formal analysis, Writing – original draft. Ravi P.
Singh: Funding acquisition, Project administration, Writing –
review & editing. Chan Yuan: Investigation, Writing - review &
editing. Demei Liu: Investigation. Mandeep S. Randhawa: Data
curation. Julio Huerta-Espino: Data curation. Sridhar Bhavani:
Data curation. Evans Lagudah: Resources. Caixia Lan: Conceptual-
ization, Data curation, Supervision, Writing - review & editing.
Declaration of competing interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared
to influence the work reported in this paper.
Acknowledgments
This work was supported by the International Cooperation and
Exchange of the National Natural Science Foundation of China
(31861143010), Huazhong Agricultural University Scientific &
Technological Self-innovation Foundation, Australian Grains
Research and Development Corporation (GRDC) with funding to
the Australian Cereal Rust Control Program (ACRCP), CGIAR
Research Program WHEAT (CRP-WHEAT), the Open Project of
Qinghai Provincial Key Laboratory of Crop Molecular Breeding
(2021-ZJ-Y05), and the Strategic Priority Research Program of the
Chinese Academy of Sciences (XDA24030102).
Appendix A. Supplementary data
Supplementary data for this article can be found online at
https://doi.org/10.1016/j.cj.2021.07.004.
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