977

Characterization of genetic loci conferring adult

plant resistance to leaf rust and stripe rust in
spring wheat
H.M. William, R.P. Singh, J. Huerta-Espino, G. Palacios, and K. Suenaga

Abstract: Leaf (brown) and stripe (yellow) rusts, caused by Puccinia triticina and Puccinia striiformis, respectively,
are fungal diseases of wheat (Triticum aestivum) that cause significant yield losses annually in many wheat-growing re-
gions of the world. The objectives of our study were to characterize genetic loci associated with resistance to leaf and
stripe rusts using molecular markers in a population derived from a cross between the rust-susceptible cultivar Avocet S
and the resistant cultivar Pavon76. Using bulked segregant analysis and partial linkage mapping with AFLPs, SSRs
and RFLPs, we identified 6 independent loci that contributed to slow rusting or adult plant resistance (APR) to the 2
rust diseases. Using marker information available from existing linkage maps, we have identified additional markers as-
sociated with resistance to these 2 diseases and established several linkage groups in the Avocet S Pavon76 popu-
lation. The putative loci identified on chromosomes 1BL, 4BL, and 6AL influenced resistance to both stripe and leaf
rust. The loci on chromosomes 3BS and 6BL had significant effects only on stripe rust, whereas another locus, charac-
terized by AFLP markers, had minor effects on leaf rust only. Data derived from Interval mapping indicated that the
loci identified explained 53% of the total phenotypic variation (R2) for stripe rust and 57% for leaf rust averaged
across 3 sets of field data. A single chromosome recombinant line population segregating for chromosome 1B was used
to map Lr46/Yr29 as a single Mendelian locus. Characterization of slow-rusting genes for leaf and stripe rust in im-
proved wheat germplasm would enable wheat breeders to combine these additional loci with known slow-rusting loci to
generate wheat cultivars with higher levels of slow-rusting resistance.

Key words: Puccinia triticina, Puccinia striiformis, Triticum aestivum, bulked segregant analysis, single chromosome
recombinant lines, linkage mapping, adult plant resistance. 990

Rsum : Les rouilles brunes et stries, causes respectivement par le Puccinia triticina et le P. striiformis, sont des
maladies fongiques du bl (Triticum aestivum) qui causent des pertes de rendement annuelles significatives dans plu-
sieurs rgions du monde. Les objectifs de cette tude taient de caractriser les locus gntiques associs la rsis-
tance ces rouilles en employant des marqueurs molculaires sur une population issue dun croisement entre la ligne
sensible Triticum aestivum Avocet S et le cultivar rsistant Triticum aestivum Pavon 76. En faisant appel lanalyse
des sgrgants en mlanges et la cartographie partielle au moyen de marqueurs AFLP, SSR et RFLP, les auteurs ont
identifi 6 locus indpendants qui contribuent une progression lente ou une rsistance ltat adulte (APR) aux 2
rouilles. laide dinformations dj disponibles grce dautres cartes gntiques, des marqueurs additionnels lis
la rsistance ces maladies et des groupes de liaison ont t produits au sein de cette population de cartographie. Les
locus putatifs identifis sur les chromosomes 1BL, 4BL et 6AL influencent la rsistance aux 2 rouilles. Les locus sur
les chromosomes 3BS et 6BL ont un effet significatif sur la rouille strie tandis quun autre locus identifi laide de
marqueurs AFLP exerce un effet mineur sur la rouille brune seulement. Les donnes de cartographie par intervalles ont
indiqu que les locus identifis expliquaient 53 % de la variation phnotypique (R2) pour la rouille strie et 57 % de la
variation pour la rouille brune suite trois essais au champ. Une population de lignes recombinantes pour le chromo-
some 1B a t employe pour tudier le locus Lr46/Yr29 comme locus mendlien. La caractrisation des gnes conf-
rant une progression lente des rouilles brune et strie au sein dun germoplasme de bl amlior pourrait permettre aux
slectionneurs de combiner ces locus avec dautres locus de rsistance afin de produire des cultivars prsentant une
plus grande rsistance la progression de la maladie.

Received 22 October 2005. Accepted 15 April 2006. Published on the NRC Research Press Web site at http://genome.nrc.ca on
30 September 2006.
Corresponding Editor: R. Appels.
H.M. William,1 R.P. Singh, and G. Palacios. International Maize and Wheat Improvement Center (CIMMYT), Apdo-Postal 6-641,
06600 Mexico; Molecular Plant Breeding Cooperative Research Centre, Melbourne, Australia.
J. Huerta-Espino. Campo Experimental Valle de Mexico-INIFAP, Apdo-Postal 10, 56230, Chapingo, Edo. De Mexico, Mexico.
K. Suenaga. Japan International Research Center for Agricultural Sciences (JIRCAS), 1-1 Ohwashi, Tsukuba, Ibaraki 305-8686, Japan.
1
Corresponding author (e-mail: m.william@cgiar.org).

Genome 49: 977990 (2006) doi:10.1139/G06-052 2006 NRC Canada

978
Mots cls : Puccinia triticina, Puccinia striiformis, Triticum aestivum, analyse des sgrgants en mlanges, lignes re-
combinantes pour un seul chromosome, cartographie gntique, rsistance ltat adulte.
[Traduit par la Rdaction]
Introduction William et al.
Wheat improvement efforts at the International Wheat and
Maize Improvement Centre (CIMMYT) during the last 3 de-
cades have resulted in a wide range of wheat cultivars with
adequate levels of resistance to important rust diseases.
Stripe (yellow) rust, caused by Puccinia striiformis Westend,
and leaf (brown) rust, caused by Puccinia triticina Eriks.,
are globally important wheat diseases that cause significant
yield losses under favorable conditions. Although a number
of race-specific genes that confer resistance to these diseases
are known in hexaploid wheat (Triticum aestivum L.) (McIntosh
et al. 2003), most of these genes are no longer effective, as
corresponding virulences have already been detected
(McIntosh et al. 1995). As CIMMYTs wheat-breeding ef-
forts are designed to develop cultivars that cover vast and
diverse agro-ecological regions, breeding efforts have empha-
sized the development and deployment of cultivars with
adult plant resistance of slow-rusting nature to these impor-
tant diseases. Although some race-specific resistance genes
such as Lr12, Lr22a, and Lr22b are expressed only in adult
plants, those involved in leaf rust resistance can be easily
distinguished from genes conferring slow-rusting resistance
based on infection type. Race-specific adult plant resistance
genes confer low infection type with an avirulent race,
whereas slow-rusting resistance genes are associated with
high infection type. It is often difficult to distinguish race-
specific and slow-rusting adult plant resistance to stripe rust
based on infection type because low disease severity is usu-
ally associated with some reduction in infection type owing
to the systemic nature of the fungus that induces chlorosis
and necrosis in stripes (Singh et al. 2001). Previous mapping
studies have also shown association between slow-rusting re-
sistance and reduction in adult plant stripe rust infection
type (Suenaga et al. 2003). Genes Lr34 and Yr18 that are ei-
ther linked or pleiotropic, contribute moderate levels of re-
sistance to both leaf and stripe rusts (Dyck 1977; Singh
1992), and have remained effective for more than 50 years;
they are thus regarded as examples of slow-rusting or adult
plant resistance. Another similar gene complex identified
more recently as Lr46/Yr29 (Singh et al. 1998; William et al.
2003) and present in Triticum aestivum Pavon76, has also
remained effective for almost 30 years.
Slow-rusting resistance is controlled by genetic factors
with moderately high heritability, and generally with addi-
tive gene action or interactions among additive genes
(Bjarko and Line 1988). Classical genetic studies have indi-
cated that CIMMYT-derived cultivars with higher levels of
slow-rusting and (or) adult plant resistance to leaf and stripe
rust often carry 34 minor genes with additive effects (Singh
and Rajaram 1994). Although genes such as Lr34/Yr18 and
Lr46/Yr29 have been effective for a considerable period of
time since their deployment, it is prudent to characterize and
deploy cultivars with additional slow-rusting genes to ensure
Genome Vol. 49, 2006
sustainable wheat production in vast areas of the developing
world where large-scale fungicide use is unfeasible.
Molecular markers can be effectively used for characteriz-
ing quantitative traits, for dissecting complex traits into
Mendelian factors or quantitative trait loci (QTLs), and for
establishing the genomic locations of such genetic loci. De-
veloping full linkage maps in wheat requires significant re-
sources given the size of the wheat genome, its 21 linkage
groups, and the well-known lack of polymorphism for mo-
lecular markers. Recent success in identifying microsatellite
markers in wheat has resulted in a significant increase in
their use in PCR-based assay systems. Previously published
wheat RFLP linkage maps have been supplemented with nu-
merous microsatellite markers (Sommers et al. 2004).
Microsatellite markers have given wheat researchers greater
opportunities to tag traits of importance enabling the devel-
opment of robust, large-scale marker assay systems for indi-
rect selection of traits. RFLP markers are still considered
useful research tools, particularly when developing anchor
markers to establish syntenic relationships with other cereal
species such as rice, where rapidly growing functional geno-
mics information can be used to characterize the wheat ge-
nome. Bulked segregant analysis (BSA) of the individuals at
the 2 extremes of the distribution of a particular trait segre-
gating in a population (Michelmore et al. 1991) has been ef-
fectively used for identifying molecular markers associated
with traits of importance in wheat (William et al. 1997; Shen
et al. 2003; Xu et al. 2005). BSA is especially advantageous
in the case of wheat, as full linkage map construction is dif-
ficult compared with other cultivated crop species. Linkage
mapping studies have also identified quantitative loci condi-
tioning resistance to leaf rust in the Opata Synthetic
(Nelson et al. 1997), Arina Forno (Schnurbusch et al.
2004), and Fukujokomugi Oligoculm (Suenaga et al.
2003) populations. Genetic characterization of adult plant re-
sistance to stripe rust resistance has also been reported
(Boukhatem et al. 2002), as has resistance to other important
diseases such as Fusarium head scab (Anderson et al. 2001)
and powdery mildew (Liu et al. 2001; Mingeot et al. 2002).
The aims of this study were to (i) characterize and estab-
lish genomic locations of loci that confer adult plant resis-
tance to leaf and stripe rust and (ii) identify closely linked
markers for their possible application in wheat improvement.
A recombinant inbred line (RIL) population segregating for leaf
rust and stripe rust resistance that was derived from a cross
between the susceptible wheat Avocet S and the resistant
Pavon76, and a set of F3 families of a single-chromosome
recombinant line population involving chromosome 1B of
Pavon76 were used. A previous report (William et al.
2003) established the genomic location of Lr46/Yr29. This
study further describes development of the linkage group as-
sociated with Lr46/Yr29 on chromosome 1BL, as well as
identifies additional regions associated with slow-rusting re-
sistance in Avocet S Pavon76 population.
2006 NRC Canada
William et al.
Materials and methods
Population development and phenotypic characterization
for leaf rust and stripe rust
The RIL population used in the study was derived from 2
individually harvested F1 plants of the cross Avocet S
Pavon76. Pavon76 is known to carry genes Lr46/Yr29 regation patterns of the F3 families confirmed the expected
and has moderately high levels of resistance to both leaf and
stripe rust (Singh et al. 1998). The population consisted of
146 individual F2-derived F5 and F6 lines that were obtained
by harvesting a random spike from each F3 line and a ran-
dom plant from each F4 and F5 line. Field evaluations were
conducted using the parents and the 146 F5 and F6 families
and the F6 population was used in the molecular analysis.
The F5 lines were evaluated for leaf and stripe rust in the
field for 1 season and the F6 lines were evaluated for both
diseases for 2 seasons at CIMMYTs research facilities in
Mexico. Field plots used in rust-screening experiments were
established on 75 cm wide raised beds and were arranged in
paired rows, 1 m in length and 20 cm between rows. The
leaf rust and stripe rust epidemics were initiated 46 weeks
after planting as described in William et al. (2003). Spreader
rows of the highly susceptible Triticum aestivum Morocco,
planted in hill plots on either side of the 1 m plots in the
0.5 m wide pathway, were sprayed with a suspension of
urediniospores in lightweight mineral oil Soltrol 170 (Phillips
66 Co., Bartlesville, Okla.). The Mexican Puccinia triticina
race MCJ/SP, nomenclature based on Singh (1991), used in
all leaf rust screening studies has the avirulence/virulence
formula Lr2a,2b,2c,3ka,9,16,19,21,24,25,28,29,30,32,33/1,
(3),3bg,10,11,12,13,14a,14b,15,17,18,20,22b,23,26,27 + 31.
The P. striiformis culture Mex96.11 used in all stripe rust
studies has the following avirulence/virulence formula:
Yr1,4,5,8,10,15,17,24,Sp/ 2,3,6,7,9,27,A. Fresh inoculum,
obtained by multiplying urediniospores on Morocco in the
greenhouse, was used for all inoculations. Field evaluation
was conducted on unreplicated plots. Earlier evaluation of
different segregating populations showed a high degree of
correlation among different years (Suenaga et al. 2003). The
adult plant severity measurements were based on the modi-
fied Cobb scale (Peterson et al. 1948). A scale of 09 de-
scribed by McNeal et al. (1971) was used to measure the
host response to stripe rust infection, which was recorded
only in 1999 on the F6 lines. Stripe rust severity was re-
corded at flowering and leaf rust severity was recorded at the
milk stage of grain development. Readings were usually
taken when the susceptible parent displayed severities be-
tween 80% and 100% on flag leaves. Visual estimates of
percent leaf area infected were recorded for both diseases. A
second reading was taken approximately 1215 d after the
first evaluation. By the time the second reading was taken,
the susceptible parent showed 100% infection severity.
Evaluation of single-chromosome recombinant lines
The slow-rusting gene Lr46 was located by Singh et al.
(1998) on chromosome 1B by field evaluating a single-
chromosome substitution series in the leaf rust susceptible
wheat Lalbahadur. A single chromosome recombinant line
population, derived from the cross between Lalbahadur
Lalbahadur (Pavon 1B) was developed that segregated for
979
chromosome 1B; F3 families were screened for leaf rust for
2 seasons (19981999 and 19992000) in CIMMYT experi-
mental station at Ciudad Obregon (27 N, 60 m above sea
level) with P. triticina race MCJ/SP. The F3 families were
classified into 3 categories: homozygous resistant (HR), seg-
regating (Seg), and homozygous susceptible (HS). The seg-
pattern of single gene segregation (William et al. 2003). We
used 16 F3 HR families and 16 HS families to further refine
the map distances between markers and Lr46/Yr29 locus, as
well as to establish the map location of these genes as a sin-
gle Mendelian locus.
Molecular mapping and identification of QTLs
The plant materials used in the study were grown in the
field during summer of 1998 and leaf tissue was harvested
after 6 weeks for DNA extraction. An alkyltrimethylammo-
nium bromide (CTAB) - based protocol was used for DNA
extraction (Hoisington et al. 1994). Two years of field data
for leaf rust and stripe rust were used in the Avocet S
Pavon76 population to identify entries for BSA. Initially,
entries showing resistance and susceptibility to both leaf and
stripe rust were considered to make the 2 bulks. Seven en-
tries with the highest levels of resistance to the 2 diseases
were selected in the resistant bulk and 11 entries with high
levels of susceptibility to both diseases were used to make
the susceptible bulk. After adjusting the concentration of
DNA to 0.3 g/L, equal amounts of DNA (100 L) from
each entry were mixed together to make the respective resis-
tant and susceptible bulks. The 2 bulks and both parents
were screened with 96 PstIMseI AFLP primer combina-
tions (Vos et al. 1995). The procedures used for AFLP anal-
ysis are described in William et al. (2003). When
polymorphisms observed between the 2 parents were present
in the bulks, these primer combinations were used to geno-
type the entire RIL population. One AFLP marker, found
earlier to be associated with the Lr46/Yr29 locus, was
mapped using the International Triticeae Mapping Initiative
(ITMI) population and the genomic location of the locus was
established on the distal end of chromosome 1BL (William
et al. 2003). Microsatellite (SSR) and RFLP markers identi-
fied from the 1BL linkage group of the ITMI linkage map
were genotyped across the entire RIL population to further
refine and associate more markers linked with Lr46/Yr29.
In addition to the BSA, the parents were screened with a
random set of wheat microsatellites selected from published
linkage maps to represent the wheat genome (Sommers et al.
2004; Graingenes Web site http://wheat.pw.usda.gov/
GG2/index.html). The AFLP genotyping described above
was combined with genotyping the entire population with
selected microsatellites to establish linkage groups for AFLP
markers associated with leaf and or stripe rust resistance.
Once chromosomal locations of the linkage groups were de-
termined in relation to published linkage maps (Sommers et
al. 2004), more SSRs from these linkage groups were
mapped to further saturate the identified linkage groups. A
limited number of RFLPs identified from linkage maps and
1 STS marker previously found to be associated with the
stem rust resistance gene Sr2 on chromosome 3BS (Sharp et
al. 2001) were also used for mapping. The procedures used
2006 NRC Canada
980 Genome Vol. 49, 2006

Fig. 1. Frequency distribution for (a) stripe rust severity, (b) leaf
rust severity, and (c) adult plant stripe rust infection type for the
Avocet S Pavon76 population. Three data sets are presented
for stripe rust and leaf rust severities, whereas 1 dataset is pre-
sented for stripe rust infection type.

for microsatellite assays and Southern hybridizations are de-

scribed in Hoisington et al. (1994) and Suenaga et al.
(2003).
Linkage analysis was conducted using MAPMAKER 3.0
(Lander et al. 1987). In some cases, ripple and place
commands were used to place markers identified in a link-
age group in the most appropriate order. Linkage group es-
tablishment and marker order assignments were done using
threshold LOD scores of 3.0 and recombination frequency
values of 0.4. Centimorgan (cM) values were computed ac-
cording to the Kosambi mapping function. Simple linear
regression was used to calculate the coefficient of determina-
tion (R2), a measure of the proportion of the total phenotypic
variation explained by each marker. Associations of markers
with resistance loci were determined by comparing the mean
leaf rust and stripe rust severities for the 2 genotypic classes
at each marker locus using single factor ANOVA and simple
interval mapping. These analyses were conducted using Q-
gene software (Nelson 1997) and composite interval map-
ping (CIM) software developed at CIMMYT (Jiang and
Zeng 1995). The final readings of the leaf rust and stripe
rust infection severities were used in all analyses of marker
trait associations and interval mapping.

Mapping of QTL associated with Lr46/Yr29 as a single

Mendelian trait
AFLP markers associated with genes Lr46/Yr29 in the
Avocet S Pavon76 population and microsatellites identi-
fied from the 1BL linkage group of the ITMI mapping popu-
lation were mapped using 32 F3 families (16 HR and 16 HS)
of the single-chromosome recombinant line population de-
scribed previously. Segregation of the Lr46/Yr29 gene com-
bination, identified as a major QTL in the Avocet S
Pavon 76 population, could be scored as a single Mende-
lian trait in the single-chromosome recombinant line popula-
tion.

Results
Phenotypic data and correlation
The resistant parent Pavon76 displayed a maximum in-
fection severity of 10% for leaf rust and 5%15% for stripe
rust, whereas the susceptible parent Avocet S showed maxi-
mum leaf and stripe rust severities of 90%100% in all 3 tri-
als. Stripe rust and leaf rust severities of the population
displayed a continuous pattern of distribution between the
severities of the 2 parents (Fig. 1). Based on the 09 scale,
adult plant stripe rust infection types were 56 for Pavon
76 and 8 for Avocet S. The F6 population also showed
variation in stripe rust infection type (Fig. 1). Pearsons cor-
relation coefficients for the 3 years of population severity
data for stripe rust ranged from 0.85 to 0.86. Among the
data sets for leaf rust severity, correlation coefficients ranged
from 0.76 to 0.86. These high correlation coefficient values

2006 NRC Canada

William et al.
among different years for stripe rust and leaf rust severity
demonstrate the reliability and reproducibility of field data
collected in unreplicated trials in test environments in Mex-
ico. The correlation coefficients among 3 years of stripe rust
data and 3 years of leaf rust data ranged from 0.68 to 0.85.
Adult plant stripe rust infection type readings and stripe rust
severity data also showed significant correlations ranging
from 0.65 to 0.70. These relatively high correlation coeffi-
cients suggest the possibility of presence of loci in the wheat
genome that influence resistance to both leaf and stripe rust
commonly.
Identification of loci associated with adult plant
resistance
BSA with 96 AFLP primer combinations identified sev-
eral polymorphic primer combinations between the 2 parents
and the bulks. These primer combinations were genotyped
across the entire population. Some primer combinations
identified clear presence and absence of amplified fragments
between the 2 bulks, whereas others identified clear intensity
differences between the 2 bulks under repeated conditions. A
total of 27 AFLP primer combinations were genotyped
across the entire population. The genotypic data for AFLPs
were combined with SSR, STS, and RFLP genotypic data.
The data set contained a total of 233 markers genotyped
among the 146 F6 families. In selecting putative loci with ef-
fects on leaf and stripe rust, markers with significant F val-
ues (p 0.01) for at least 2 out of the 3 years of data were
considered for further analysis. Because adult plant stripe
rust infection type readings were based on 1 year of field
data, only those markers with highly significant F values
(p < 0.001) were considered. In each linkage group found to
be associated with resistance, 1 marker with the highest sig-
nificance was selected (Table 1). The putative loci identified
by single-factor analysis of variance were further analyzed
by simple interval mapping (SIM). Because our goal was not
to develop a full linkage map, but to use BSA and partial
linkage mapping to characterize the slow-rusting loci, the re-
sulting comparatively small linkage groups were not used
for composite interval mapping. The QTL analysis of the
3 years of data for leaf and stripe rust were conducted indi-
vidually using Q-gene (Nelson 1997) and the CIM program
(Jiang and Zeng 1995). When slight shifts of the QTL peaks
during different years were observed during interval map-
ping analysis, the peak identified with the joint analysis was
considered to be the common peak associated with that QTL
using the CIM program.
Single-marker analysis
Single-marker analysis identified 5 markers associated
with putative loci on different chromosomes that had signifi-
cant effects on stripe rust severity (Table 1a). A locus with
highly significant effects for stripe rust severity was identi-
fied on chromosome 1BL by mapping an AFLP marker
found to be strongly associated with leaf and stripe rust se-
verity in the ITMI population (William et al. 2003). This lo-
cus was further characterized using markers from the ITMI
1BL linkage group to develop a linkage group in Avocet S type on chromosome 4BL was 13 cM distal to the marker
Pavon76 population. On average, the mean stripe rust se-
verity difference between the 2 marker allele classes for the
marker Xgwm259 was 29.6%. This marker explained 34.9%
981
of the total phenotypic variation (%R2) averaged over
3 years. The second locus with strong effects for stripe rust
was located on chromosome 6BL. The marker closest to the
locus had a mean difference in severity of 18.9% between
the 2 allele classes for the 3 years. The effect of the locus on
chromosome 3BS was somewhat lower and the average
mean difference for the 2 allele classes was 12.3%. The pu-
tative loci identified by markers on chromosomes 1BL, 6BL,
and 3BS were associated with the resistant parent
Pavon76. In addition, there were 2 other putative resis-
tance loci, 1 located on chromosome 4BL and another on
chromosome 6AL, which were associated with the suscepti-
ble parent Avocet S (Table 1a). The mean severity reduc-
tions associated with these 2 loci on chromosomes 4BL and
6AL were 15.4% and 16.6%, respectively. Chromosome 6AL
of Avocet S also carries a translocation from Agropyron
elongatum that is known to possess the race-specific stem
rust resistance gene Sr26 (Knott 1961).
The locus identified on chromosome 1BL also had a
highly significant effect on leaf rust. Two closely linked
AFLP markers identified in the linkage group of 1BL had
the highest association with leaf rust resistance in 2 of the
3 years. The highest significant F value for the remaining
year was associated with the marker Xgwm259, although the
AFLP markers also gave a very highly significant F value of
176.7. On average, these markers explained 50.7% of the to-
tal phenotypic variation for leaf rust and the mean severity
differences between the 2 allele classes for the most signifi-
cant marker was 45.6% (Table 1b). The markers identified
on chromosome 6BL that had significant effects on stripe
rust only had a marginal effect on leaf rust; they were statis-
tically significant in only 2 out of 3 years. The mean differ-
ence between the 2 marker allele classes was 12.9%
(Table 1b). In addition, the 2 loci on chromosomes 4BL and
6AL, where the contributing parent was Avocet S, also had
significant effects on leaf rust. The mean severity differences
associated with these 2 putative loci were 18.3% and 17.5%,
respectively (Table 1b). In addition, there was a small link-
age group of 4 AFLP markers with 1 marker showing statis-
tically significant but smaller effects for 2 of the 3 years.
The mean difference between the 2 marker allele classes for
the 2 years was 13.7%. Based on the single-factor analysis
of variance, it appears that the resistant parent contributed 3
genetic factors, 1 with major effects and the other 2 with
marginal effects on leaf rust. These loci are located on chro-
mosome 1BL and 6BL and the genomic location of the third
locus is unknown.
The adult plant stripe rust infection type had 4 highly sig-
nificant markers associated with resistance. The marker that
showed the highest significant effects with stripe rust resis-
tance on chromosome 1BL was also strongly associated with
adult plant stripe rust infection type, explaining 17.6% of the
total phenotypic variation (%R2). Similarly, the markers
identified on chromosomes 3BS and 6BL showed significant
effects, as did the linkage group on chromosome 4BL, con-
tributed by the susceptible parent Avocet S. The SSR
marker locus Xgwm513 with strongest effects on infection
with highest effects for stripe rust resistance based on sever-
ity (Table 1c; Figs. 2c, 3).
A total of 6 linkage groups were identified with either ef-
2006 NRC Canada
982 Genome Vol. 49, 2006

Table 1. Single factor analysis of variance for markers with potential linkage to loci with resistance of adult plant stripe rust, leaf rust,
and adult plant stripe rust infection type in Avocet S Pavon76 population.
(a) Stripe rust
Marker F value Probability R2 (%) Mean difference Effect from
Chromosome 1BL
F5, year 1 Xgwm259 69.71 0.0000 32.6 56.5123.75 Pavon76
F6, year 2 Xgwm259 83.94 0.0000 36.8 66.9836.20 Pavon76
F6, year 3 Xgwm259 77.73 0.0000 35.2 58.1032.87 Pavon76
Chromosome 3BS
F5, year 1 XPstAATMseCAC2 8.5 0.0042 6 45.8231.58 Pavon76
F6, year 2 XPstAATMseCAC2 6.52 0.0118 4.7 55.7544.73 Pavon76
F6, year 3 XPstAATMseCAC2 11.03 0.0012 7.7 50.3338.65 Pavon76
Chromosome 4BL
F5, year 1 Xgwm495 11.36 0.0010 7.4 27.9343.92 Avocet S
F6, year 2 Xgwm495 12.16 0.0007 7.9 40.1954.72 Avocet S
F6, year 3 Xgwm495 20.5 0.0000 12.7 34.2649.83 Avocet S
Chromosome 6AL
F5, year 1 Xgwm617 12.56 0.0005 8.1 22.7242.25 Avocet S
F6, year 2 Xgwm617 13.38 0.0004 8.6 35.6353.41 Avocet S
F6, year 3 Xgwm617 8.96 0.0033 5.9 34.2246.61 Avocet S
Chromosome 6BL
F5, year 1 XPstAGGMseCGA1 28.76 0.0000 17.6 50.6426.70 Pavon76
F6, year 2 XPstAGGMseCGA1 15.09 0.0002 10.1 57.8141.92 Pavon76
F6, year 3 XPstAGGMseCGA1 25.05 0.0000 15.8 52.8636.03 Pavon76

(b) Leaf rust

Chromosome Marker F value Probability R2 (%) Mean difference Effect from
Chromosome 1BL
F5, year 1 XPstAGAMseCAC1 & 2 131.4 0.0000 48.4 63.9326.96 Pavon76
F6, year 2 Xgwm259 181.7 0.0000 55.8 79.9227.28 Pavon76
F6, year 3 XPstAGAMseCAC1 & 2 117.2 0.0000 48.0 84.5837.38 Pavon76
Chromosome 4BL
F5, year 1 Xgwm368 11.9 0.0008 8.9 33.049.73 Avocet S
F6, year 2 Xgwm368 8.8 0.0036 6.4 37.5956.83 Avocet S
F6, year 3 Xgwm368 8 0.0056 6.4 45.9764.9 Avocet S
Chromosome 6AL
F5, year 1 Xgwm617 9.6 0.0023 6.3 30.5646.7 Avocet S
F6, year 2 Xgwm617 7.16 0.0083 4.8 35.6954.13 Avocet S
F6, year 3 Xgwm427 5.63 0.0191 4.2 43.8361.67 Avocet S
Chromosome 6BL
F5, year 1 XPstAGGMseCGA1 6.2 0.0143 4.37 48.8337.73 Pavon76
F6, year 2 XPstAGGMseCGA1 6.12 0.0146 4.34 57.7343.07 Pavon76
F6, year 3 XPstAGGMseCGA1 N.S.
Unknown chromosome
F5, year 1 XPstACGMseCAG1 7.52 0.0143 5.27 47.5535.81 Pavon76
F6, year 2 NS NS
F6, year 3 XPstACGMseCGT2 5.73 0.0185 5.13 63.1747.48 Pavon76

(c) Infection type

Chromosome Marker F value Probability R2 (%) Mean difference Effect from
1BL Xgwm259 30.78 0.0000 17.61 6.685.72 Pavon76
3BS XPstAATMseCAC2 17.96 0.0000 11.98 6.575.80 Pavon76

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William et al. 983

Table 1 (concluded).
Chromosome Marker F value Probability R2 (%) Mean difference Effect from
4BL Xgwm513 20.74 0.0000 13.2 5.556.43 Avocet S
6BL XPstAGGMseCAA1 12.65 0.0005 9.9 6.525.77 Pavon76
Note: Markers significant at p = 0.01 are identified along with the F values, the phenotypic variance (R2%), the mean difference between the 2 allele
classes for the most significant marker, and the contributing parent. NS, not significant.

Fig. 2. Partial linkage maps and the likelihood ratio curves of QTLs associated with adult plant stripe rust severity and leaf rust sever-
ity in the Avocet S Pavon76 population. The shaded arrowhead indicates the most likely positions of the QTLs in the QTL con-
tours, as well as in the linkage maps associated with resistance to stripe rust, whereas the clear arrowheads indicate the similar
positions for resistance to leaf rust. (a) Chromosome 1BL, (b) 3BS, (c) 4BL, (d) 6AL, (e) 6BL, (f) unknown linkage group.

fects on both stripe rust and leaf rust or on only 1 of the 2
diseases. The linkage group with a recombination distance
of 38.5 cM associated with chromosome 1B, representing
the distal region of wheat chromosome 1BL, carried a total
of 11 markers including 5 SSR markers, 1 RFLP marker,
and 5 AFLP markers. All 5 AFLP markers were identified
as a result of BSA, whereas the RFLP and SSR markers
were identified using markers from the ITMI linkage map of
chromosome 1BL (William et al. 2003). Another linkage
group of 18.8 cM that showed some association with stripe
rust severities and infection type was located on chromo-
some 3BS. This linkage group had 9 markers including
7 AFLP markers, 1 STS marker (Sharp et al. 2001), and
1 SSR marker. A third linkage group was identified on chro-
mosome 4BL with 7 markers with a total recombination
length of 37 cM. This linkage group was characterized by

2006 NRC Canada

984
Fig. 2 (continued).
5 SSR markers and 2 AFLP markers, all of which showed
distorted segregation towards the Pavon76 allele. The link-
age group associated with chromosome 6AL also had dis-
torted segregation toward the Pavon76 alleles and had
18 markers including 4 SSR markers with a total recombina-
tion distance of 52.5 cM. Distorted segregation in certain
wheat chromosomes, including chromosomes 4B and 6AL,
has been observed previously (Suenaga et al. 2005; Cadalen
et al. 1997). Most of the markers in these 2 linkage groups
showed highly significant (p = 0.001) distortion towards the
Pavon76 allele. Loci with distorted segregation may com-
promise the estimates of the recombination values and may
Genome Vol. 49, 2006
lead to spurious linkages (Kammholz et al. 2001). The
power of QTL detection may also be somewhat affected by
distorted loci (Suenaga et al. 2005). Clustering of distorted
loci might be associated with the presence of alien translo-
cations in one of the parents in mapping populations
(Kammholz et al. 2001). Given the tight clustering of markers
on chromosome 6AL, it is likely that this linkage group repre-
sents the translocation from Agropyron elongatum that Avo-
cet S is reported to carry on chromosome 6AL (McIntosh et
al. 1995). The linkage group associated with chromosome
6BL, which had significant effects on stripe rust and marginal
effects on leaf rust resistance, had a total of 7 markers with a
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William et al.
Fig. 2 (concluded).
total length of 55.1 cM. The chromosome assignments of the
mapped markers in the Avocet S Pavon76 population QTL was observed between the marker loci Xgwm140 and
was done by comparing the marker locations with the well-
established wheat linkage maps (Sommers et al. 2004). In ad-
dition to these linkage groups, we observed another small
linkage group associated with low levels of leaf rust resis-
tance, which was identified by 4 AFLP markers with a link-
age distance of 23.3 cM. The chromosomal location of this
linkage group is yet to be established. The 6 linkage groups
identified are presented in Fig. 2.
Interval mapping
Stripe rust
The 6 linkage groups associated with the 2 rust diseases
were further analyzed using interval analysis. A total of
5 putative loci contributing to stripe rust resistance were
identified. The locus identified in the long arm of chromo-
some 1BL had highly significant effects with LOD scores
985
ranging from 13.02 to 16.79 for the 3 years. The peak of the
Xgwm259 (Fig. 2a). This linkage group was first established
by BSA using AFLP markers. The 5 AFLP markers mapped
distinguished the bulks for both leaf rust and stripe rust. Al-
though QTL analysis seems to indicate the presence of 2
peaks, it is likely that this is a single locus with highly sig-
nificant effects. Joint analysis indicated that the QTL peak
had a highly significant LOD score of 17.1 (Table 2). Multi-
ple regression analysis indicated that the proportion of the
total phenotypic variation explained by this locus ranged be-
tween 33% and 40% over the 3 years (Table 2) with additive
effects ranging from 13.5 to 17.9. A second locus with
somewhat lesser, but highly significant, effects derived from
Pavon76 was identified on the 6BL linkage group. The
QTL contour peak for this linkage group was observed at 12
cM. The locus is flanked by the marker loci Xgwm58 and
XPstAGGMseCAA1 (Fig. 2e). Another SSR marker
Xgwm626 is linked to Xgwm58 at 6.3 cM. The LOD scores
2006 NRC Canada
986
Fig. 3. Likelihood ratio curves for QTLs associated with adult plant stripe rust infection type in the Avocet S
tion. The shaded arrows indicate the most likely positions of the QTLs.
associated with this locus ranged from 2.98 to 6.54 with the
joint analysis giving a LOD score of 7.64. The percentage of
the total phenotypic variation explained by the markers
ranged from 9.0% to 18.6% and the additive effects for the
3 years were 13.1, 8.0, and 8.5, respectively (Table 2). The
third locus with somewhat marginal effects on resistance de-
rived from the resistant parent Pavon76 was on chromo-
some 3BS (Fig. 2b). Although the effects were marginal,
this locus is likely to be located close to or within the region
associated with the stem rust resistance gene Sr2. Pavon76
is also known to carry the gene Sr2. The STS marker Xsun2,
developed from Xglk683 RFLP probe and another micro-
satellite marker Xgwm533 mapped in the linkage group are
reported to be associated with the Sr2 complex (Sharp et al.
2001; Spielmeyer et al. 2003). The probability values associ-
ated with F values in Table 1 and the relevant LOD scores
obtained with interval mapping (Table 2) were only margin-
ally significant. However, in other populations it has been
observed that the Sr2 region has some minor effect on stripe
rust resistance (Singh et al. 2001; Suenaga et al. 2003). Re-
cently, gene designation Yr30 was assigned to this stripe rust
resistance gene. Two additional loci, located on chromo-
somes 4BL (Fig. 2c) and 6AL (Fig. 2d) that showed dis-
torted segregation also were associated with resistance, with
Genome Vol. 49, 2006
Pavon76 popula-
contribution derived from the susceptible parent Avocet S.
In field trials, we have observed that Avocet S has some
level of resistance to stripe rust and leaf rust compared with
more susceptible cultivars such as Morocco. The linkage
group associated with chromosome 6AL had 18 markers,
mostly AFLPs. The QTL contours also indicated several
peaks (Fig. 2d). The QTL peaks associated with linkage
groups 4BL and 6AL, identified by joint analysis, were at 23
and 26 cM, respectively. Multiple regression analysis using
the CIM program indicated that the total phenotypic varia-
tion explained by the 5 loci identified ranged from 52.3% to
55.6%.
Leaf rust
The locus detected on chromosome 1BL derived from
Pavon76 gave the most-significant contribution to leaf rust
resistance. Although single factor analysis of variance iden-
tified 2 AFLP markers with highest F values at 12 cM
(Table 1b and Fig. 2a), joint analysis identified the peak of
the QTL at 34 cM. This position, similar to the QTL peak
associated with stripe rust resistance, is flanked by the 2
SSR markers Xgwm259 and Xgwm140 with close linkages to
several AFLP markers (Fig. 2a). The associated LOD scores
were highly significant ranging from 19.9 to 33.7 with the
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William et al. 987

Table 2. QTLs detected through simple interval mapping with effects on adult plant stripe rust, leaf rust and stripe rust infection type
in the Avocet S Pavon76 population.
(a) Stripe rust
Year 1 Year 2 Year 3
Position Additive Additive Additive Joint
Chromosome (cM) LOD effect R2 (%) LOD effect R2 (%) LOD effect R2 (%) LOD Effect from
1 BL 35 13.02 17.9 33.0 16.79 17.4 39.9 14.25 13.5 36.5 17.1 Pavon76
3BS 2 1.40 6.0 4.3 1.05 4.6 3.3 1.89 5.1 5.9 2.03 Pavon76
4BL 23 2.60 8.5 8.0 2.76 7.7 8.4 4.35 8.0 13.1 4.51 Avocet S
6AL 26 2.63 9.7 7.90 2.82 8.9 8.4 1.91 6.2 5.8 3.09 Avocet S
6BL 12 6.54 13.1 18.6 2.98 8 9 4.86 8.5 14.0 7.64 Pavon76
Total R2 (%) 53.3 52.3 55.6

(b) Leaf rust

Year 1 Year 2 Year 3
Position Additive Additive Additive Joint
Chromosome (cM) LOD effect R2 (%) LOD effect R2 (%) LOD effect R2 (%) LOD Effect from
1BL 34 19.9 20.1 49.7 33.7 31.4 61.6 21.64 25.7 50.9 33.9 Pavon76
4BL 24 2.05 8.8 6.1 0.81 6.2 2.9 1.60 8.2 5.5 2.80 Avocet S
6AL 17 2.02 8.0 4.4 1.34 8.6 2.9 0.93 6.8 2.4 2.35 Avocet S
6BL 15 1.06 5.3 3.3 1.38 8.0 3.8 0.77 5.6 2.7 1.56 Pavon76
Unknown 9 2.22 8.4 7.1 1.29 8.1 3.3 1.43 8.1 5.0 2.38 Pavon76
Total R2 (%) 55.20 63.7 53.7

(c) Infection type

Year 1 Year 2 Year 3
Position Additive Additive Additive Joint
Chromosome (cM) LOD effect R2 (%) LOD effect R2 (%) LOD effect R2 (%) LOD Effect from
1BL 37 6.3 0.49 18.5 Pavon76
3BS 2 2.7 0.33 8.3 Pavon76
4BL 11 4.7 0.48 12.9 Avocet S
6BL 14 2.5 0.32 7.9 Pavon76
Total R2 (%) 35.60

joint analysis indicating a LOD score of 33.9 (Table 2). The
additive effects ranged from 20.1 to 31.4, whereas the total
percentage phenotypic variation explained by the locus
ranged from 49.7% to 61.6% across the 3 seasons. The locus
associated with stripe rust resistance on chromosome 6BL
derived from Pavon76 had minor effects on leaf rust resis-
tance with LOD threshold values below those traditionally
accepted for QTL mapping. The short linkage group identi-
fied by the 4 AFLP markers had small effects on leaf rust re-
sistance as a contribution from Pavon76 (Table 2 and
Fig. 2f). The 2 loci contributed by Avocet S on chromo-
somes 4BL and 6AL for stripe rust also had some effect on
leaf rust resistance. However, the locations of the QTL peak
positions on chromosome 6AL linkage group for stripe rust
and leaf rust, indicated by the joint analysis, were somewhat
different (Table 2; Fig. 2d). The total phenotypic variation
explained by the 5 loci reported ranged from 53.7% to
63.7% for the 3 years (Table 2). The locus identified on
chromosome 3BS associated with stripe rust resistance did
not have a significant effect on leaf rust resistance.
Stripe rust infection type
Because we had only 1 data set from a single year for
stripe rust infection type, only the loci that had highly signif-
icant effects with LOD scores > 2.5 are reported. The 3 loci
on chromosomes 1BL, 3BS, and 6BL, derived from
Pavon76 and that influenced stripe rust severity, also had
significant effects on stripe rust infection type and explained
18.5%, 8.3%, and 7.9% of the total phenotypic variation, re-
spectively (Table 2). The locus associated with chromosome
4BL, contributed by Avocet S had a LOD score of 4.71
and explained 12.9% of the total phenotypic variation. There
was an additional locus on chromosome 6AL, contributed by
Avocet S, which had minor effects (not shown). The 4 loci
considered jointly explained 35.6% of the total phenotypic
variation (Table 2; Fig. 3).
Mapping Lr46/Yr29 as a single Mendelian trait
The QTL associated with genes Lr46/Yr29, was localized
on the distal end of chromosome 1BL (William et al. 2003).
We also used a single chromosome recombinant line (SCRL)
population, segregating for chromosome 1B, to map this im-
portant yet complex QTL (Fig. 2a) as a single Mendelian
trait. This population, developed using single chromosome
substitution lines, was previously utilized to locate Lr46 on
chromosome 1B of Pavon76 (Singh et al. 1998) and to as-

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Fig. 4. Linkage group associated with Lalbahadur Lalbahadur
(Pavon 1B) single chromosome recombinant line population.
sociate Lr46 with a gene conferring resistance to stripe rust
designated as Yr29 (William et al. 2003). We used 32 F3
families 16 homozygous resistant and 16 homozygous
susceptible to further characterize and identify markers
using the segregation of Lr46/Yr29 as a simple Mendelian
locus. When the Avocet S Pavon76 population was
used as a mapping population, the locus associated with
Lr46/Yr29 could be characterized only as one of several
QTLs segregating in the population. Furthermore, the QTL
contours associated with the locus was without a well de-
fined peak location. The single chromosome recombinant
line population enabled us to map this locus as a qualitative
trait; the homozygous resistant and homozygous susceptible
families could be used to characterize the families with pres-
ence and absence of the gene combination, which was not
possible using the Avocet S Pavon76 population. The
AFLP markers identified in the Avocet S Pavon76
population and microsatellite markers identified from
Sommers et al. (2004) consensus map were utilized for map-
ping. The linkage group developed from the SCRL popula-
tion has 9 markers with a total length of 42.8 cM (Fig. 4).
Although the exact map location of the Lr46/Yr29 can not be
guaranteed to be highly accurate because we used only 32
families for mapping, indications are that markers can be
identified flanking the Lr46/Yr29 locus.
Discussion
We have been able to characterize several loci associated
with durable resistance to stripe rust and leaf rust using BSA
and partial linkage mapping. This approach, although used
extensively for characterizing loci with qualitative effects,
can also be used to characterize and identify markers for
traits conditioned by loci with a continuous pattern of distri-
bution. The minimum number of genes that confer slow-
rusting response to leaf and stripe rust in Avocet S
Pavon76 have been estimated by studying the segregation
patterns of the F6 families to be 2 and 3, respectively (Wil-
liam et al. 2003). In wheat, where full linkage map construc-
tion is both time consuming and resource intensive, BSA
coupled with partial linkage mapping is a desirable alterna-
tive especially when multiple populations have to be evalu-
ated and mapped simultaneously.
The existence of genes with intermediate to minor effects
that confer durable or adult plant resistance to stripe and leaf
Genome Vol. 49, 2006
rusts is well known (Singh et al. 2000). The large-scale de-
ployment of cultivars containing adult plant resistant genes
Lr34/Yr18, Lr46/Yr29, and Sr2 underscores the importance
of such genes in stabilizing wheat production across vast
wheat-growing regions of the developing world where fun-
gicide use is minimal. Although a number of genes that con-
fer race-specific resistance to leaf, stripe, and stem rusts
have been identified, only a few slow-rusting genes have
hitherto been characterized (McIntosh et al. 2003). Use of
molecular markers to identify and characterize such genes
present in spring and winter wheats would facilitate their in-
creased use in cultivar development. The locus on the distal
region of chromosome 1BL with highly significant effects
on resistance to stripe and leaf rusts was also detected in
other mapping populations (Suenaga et al. 2003; Bariana et
al. 2001). The loci associated with stripe rust infection type
had considerable overlap with the QTLs detected for stripe
rust severity. Boukhatem et al. (2002) also detected 5 QTLs
associated with adult plant infection type in the ITMI map-
ping population. In our study, we detected 6 QTLs with sig-
nificant effects for the 2 diseases indicating the presence of
genetic variability for the loci controlling stripe and leaf rust
resistance. The markers associated with linkage groups on
chromosomes 4BL and 6AL showed significant distortion
towards the alleles contributed by Pavon76. The distortion
associated with chromosome 4B linkage group has also been
observed by other research reports (Suenaga et al. 2003;
Cadalen et al. 1997). Loci with distortion may result in spu-
rious linkages (Kammholz et al. 2001), which might also
have an effect on the power of QTL detection. However, we
have observed that in comparison to cultivars such as
Morocco with complete susceptibility to the rust diseases,
Avocet S and some other cultivars seem to possess some
genetic factors that contribute to slow rusting resistance
which results in significant delays in becoming completely
susceptible. It is our observation that to obtain sufficient lev-
els of protection under high disease pressure, wheat cultivars
require the presence of 4/5 slow rusting genes in combina-
tion. The presence of 1 or 2 slow rusting genes with minor
effects would not be sufficient to protect a cultivar from be-
coming almost completely susceptible under high disease
pressure, although such cultivars show significant delays in
becoming completely susceptible. For example even
Lalbahadur containing chromosome 1B of Pavon76 (with
Lr46/Yr29), would become as susceptible as Lalbahadur
with sufficient exposure to high inoculum pressure but it
takes a longer time. Suenaga et al. (2003) also detected a
QTL that had effect on stripe rust severity on chromosome
4BL. Our results also indicate that in addition to the stem
rust resistance gene Sr26 located on chromosome 6AS.6L
Ag. elongatum translocation, this translocation might also
have a minor effect in conferring slow rusting resistance.
The ability to map the complex QTLs identified with
genes Lr46/Yr29 as a single Mendelian locus further refines
that gene complex. The marker Xwmc44 was not polymor-
phic on Avocet S Pavon76 population, whereas Xbarc80
was not polymorphic on the parental lines of the SCRL pop-
ulation. Although the QTL results from the mapping popula-
tion did not define the precise location of the Lr46/Yr29
gene combination owing to the nature of the broad QTL
contours obtained, the results of this limited set of SCRLs
2006 NRC Canada
William et al.
indicate that there could be markers closely associated with
these genes. These markers will have to be validated in other
populations segregating for these genes in order to evaluate
their potential use in marker assisted selection applications. In
chromosome 1BL linkage group for Avocet S Pavon76 fects. Furthermore, characterization of these loci with multi-
population Xgwm259 and Xgwm140 are the closest SSR
markers for the QTL peak associated with both leaf and
stripe rust resistance. The distance between these 2 markers
are 13.7 cM (Fig. 2a). In mapping involving the F3 SCRL
population, the SSR marker Xwmc44 mapped closest to the
Lr46/Yr29 locus at a distance of 3.5 cM. In our hands, the
SSR Xwmc44 was an easier marker to work with compared
with Xgwm259. Sourdille et al. (2004) reported that in the
ITMI map the 2 markers Xgwm259 and Xwmc44 are very
close to each other. However, in combining several linkage
maps into a consensus map, Sommers et al. (2004) indicated
that there is some recombination distance between the 2
markers. Mateos-Hernandez et al. (2006), using a larger
number of F3 families of the Lalbahadur Lalbahadur
(Pavon1B) showed that the map distance between Lr46 and
Xwmc44 to be approximately 16 cM, whereas Rosewarne et
al. (2006) showed a map distance of 10.9 cM between the 2
loci using a set of F5 families of the same population. Com-
paring the QTL peak location in 1BL in our study with that
of Suenaga et al. (2003), also taking in to account the map-
ping in the SCRL populations in this study and that of
Rosewarne et al. (2006) and Mateos-Hernendez et al.
(2006), it is possible to speculate that Xwmc44, together
with other markers such as Xwmc367, and Xgwm140 can be
considered as potential flanking markers for manipulating
the Lr46/Yr29 gene combination in molecular breeding ef-
forts, at least until more reliable and closely linked markers
are made available.
In the Avocet S Pavon76 and other mapping popula-
tions, it appears that there are loci in the wheat genome that
have effects on multiple biotic stresses. In the case of the lo-
cus detected on chromosome 1BL, identified by genes
Lr46/Yr29, the effects on both leaf rust and stripe rust are
highly significant (Table 2, Fig. 2a). This is also the case
with the adult plant resistance locus detected on the short
arm of chromosome 7D, identified by the genes Lr34/Yr18
(Suenaga et al. 2003). Both of these genomic regions on
chromosomes 1BL and 7DS are also reported to be gene rich
regions (Erayman et al. 2004). On the other hand, the locus
detected on chromosome 3BS, known to be closely associ-
ated with the Sr2 region, had a minor effect on stripe rust re-
sistance but no detectable effect on leaf rust resistance. The
locus on chromosome 6BL had significant effects on stripe
rust but quite marginal effects on leaf rust. Although the
presence of loci with protective effects on multiple diseases
is possible, the loci on chromosome 3BS, 6BL, and the short
linkage group with only 4 AFLP markers indicate that there
also other loci with effects on only 1 of these 2 diseases. In
addition to the fact that some loci had effects on both stripe
and leaf rust, recent evidence also suggests close associa-
tions of the loci detected by markers on chromosome 1BL
and powdery mildew (Liu et al. 2001). Further, the regions
associated with the loci Lr34/Yr18 (Suenaga et al. 2003) also
seem to have effects on barley yellow dwarf tolerance
(Singh 1993), spot blotch resistance (Joshi et al. 2004) and
powdery mildew resistance (Spielmeyer et al. 2005). Other
989
regions of the wheat genome are also implicated in multiple
disease resistance (Boukhatem et al. 2002). It remains to be
confirmed if these multiple resistances are due to either the
presence of closely linked gene clusters or pleiotrophic ef-
ple resistance factors should help our understanding of the
nature of broad-spectrum disease resistance as well as en-
able manipulation of such gene complexes with molecular
markers in breeding populations.
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