Molecular mapping of adult-plant race-specific leaf rust resistance gene Lr12 in bread wheat

Abstract

Wheat (Triticum aestivum) gene Lr12 provides adult-plant race-specific resistance to leaf rust caused by Puccinia triticina. It is completely linked or identical to Lr31, which confers seedling resistance only when the complementary gene Lr27 is also present. F2 and F2-derived F3 families were developed from a cross between the susceptible variety Thatcher and TcLr12, an isoline carrying Lr12. Of 230 F3 families, 55 were homozygous resistant, 115 were segregating for resistance, and 60 were susceptible to P. triticina, fitting a monogenic 1:2:1 segregation ratio. Lr12 was mapped on chromosome arm 4BL and was flanked by markers Xgwm251 and Xgwm149 at distances of 0.9 and 1.9cM, respectively. Using linked markers and wheat deletion stocks, Lr12 was located in deletion bin 4BL-5, FL=0.86–1.0, comprising the terminal 14% of 4BL. The markers will be useful for following
Lr12/Lr31 in crosses and for further mapping studies.

Full text

Molecular mapping of adult-plant race-specific leaf rust
resistance gene Lr12 in bread wheat
S. Singh
•
Robert L. Bowden
Received: 5 October 2009 / Accepted: 17 May 2010
Ó US Government 2010
Abstract Wheat (Triticum aestivum) gene Lr12
provides adult-plant race-specific resistance to leaf rust
caused by Puccinia triticina. It is completely linked or
identical to Lr31, which confers seedling resistance only
when the complementary gene Lr27 is also present. F
2
and F
2
-derived F
3
families were developed from a cross
between the susceptible variety Thatcher and TcLr12,
an isoline carrying Lr12. Of 230 F
3
families, 55 were
homozygous resistant, 115 were segregating for resis-
tance, and 60 were susceptible to P. triticina, fitting a
monogenic 1:2:1 segregation ratio. Lr12 was mapped on
chromosome arm 4BL and was flanked by markers
Xgwm251 and Xgwm149 at distances of 0.9 and 1.9 cM,
respectively. Using linked markers and wheat deletion
stocks, Lr12 was located in deletion bin 4BL-5,
FL = 0.86–1.0, comprising the terminal 14% of 4BL.
The markers will be useful for following Lr12/Lr31 in
crosses and for further mapping studies.
Introduction
Leaf rust, caused by the fungus Puccinia triticina,is
one of the most important foliar diseases of wheat
(Triticum aestivum L.) worldwide (McIntosh et al.
1995; Nagarajan and Joshi 1975; Roelfs et al. 1992).
Yield losses vary from trace to 30% or more,
depending on the growth stage of initial infection,
environmental conditions, and leaf rust resistance
genes present in the cultivars (Kolmer et al. 2007).
More than 60 leaf rust resistance genes in wheat have
been named (McIntosh et al. 1995, 2008).
The majority of leaf rust resistance genes are
effective at all growth stages, from the seedling
through the adult-plant stage. This type of resistance
is variously known as seedling resistance, major-
gene, qualitative, race-specific, or hypersensitive
resistance. In many cases, seedling resistance genes
can provide very high levels of resistance. Unfortu-
nately, most of these seedling resistance genes have
not provided durable resistance when deployed in the
field (Kolmer et al. 2007; McIntosh et al. 1995).
Seedling resistance genes are exemplified by Lr10,
which was cloned and shown to be an NBS-LRR-type
resistance gene (Fueillet et al. 2003).
Another type of resistance is associated with adult-
plant resistance (APR), minor gene or quantitative
inheritance, race-nonspecificity, slow rusting, and
nonhypersensitive resistance reactions (Singh et al.
2005; William et al. 2006). APR is characterized by a
susceptible seedling infection type followed by
increasingly effective resistance in post-seedling
stages (Park and McIntosh 1994). Slow-rusting resis-
tance is characterized by fewer and smaller pustules,
longer latent periods, and smaller area under the
S. Singh  R. L. Bowden (&)
Department of Plant Pathology and USDA-ARS Hard
Winter Wheat Genetics Research Unit, 4007
Throckmorton Hall, Kansas State University,
Manhattan, KS 66506-5502, USA
e-mail: robert.bowden@ars.usda.gov
123
Mol Breeding
DOI 10.1007/s11032-010-9467-4

disease progress curve (Singh et al. 2005). Selection
for APR and/or slow rusting can be an effective
method of increasing levels of durable resistance
(Singh et al. 2005). Race-nonspecific APR genes are
best exemplified by Lr34, which was recently cloned
and shown to be a putative ABC transporter (Kratt-
inger et al. 2009).
Lr12 is a leaf rust resistance gene that does not fit
neatly into either of the previous categories. Lr12 is
race-specific and is associated with a qualitative,
hypersensitive resistance response, similar to seedling
resistance (McIntosh et al. 1995). However, Lr12 is
an APR gene, similar to race-nonspecific, slow-
rusting resistance genes. Furthermore, Singh et al.
(1999) summarized evidence that the race-specificity
pattern of Lr12 was the same as that of Lr31 and
showed that Lr12 is completely linked or identical to
Lr31. Lr31 confers race-specific seedling resistance,
but only when present with the complementary gene
Lr27 (Singh and McIntosh 1984; McIntosh et al.
1995). Singh et al. (1999) suggested that Lr27 is a
genetic modifier of Lr12 that allows expression at the
seedling stage. Cloning Lr12 could provide a unique
opportunity to study complementary gene action and
the molecular mechanisms of APR expression.
Lr12 was originally identified in the wheat culti-
vars Exchange and Chinese Spring (Dyck et al. 1966;
McIntosh and Baker 1966). Lr12 has subsequently
been reported in wheat cultivars from Australia,
China, North America, and South America (Kolmer
2003; McIntosh et al. 1995; Park and McIntosh 1994;
Wamishe and Milus 2004). Because Lr12 is an adult-
plant gene, gene postulation studies are laborious and
are rarely done (Wamishe and Milus 2004). Conse-
quently, the frequency of Lr12 in commercial wheat
cultivars is not clear. Developing diagnostic molec-
ular markers for Lr12 would facilitate gene postula-
tion studies for APR in commercial cultivars or
breeding lines (Wamishe and Milus 2004).
The literature on the chromosome location of Lr12
and Lr31 is confusing. Lr12
was reported on chro-
mosome 4A by Dyck and Kerber (1971) and McIn-
tosh and Baker (1966). Designations of chromosomes
4A and 4B were later switched (Naranjo et al. 1988).
Based on studies with aneuploid genetic stocks,
Singh and McIntosh (1984) reported that Lr31
resided on chromosome arm 4Ab, which corresponds
to chromosome arm 4BL under current nomenclature
(Endo et al. 1991). Roelfs et al. (1992) listed Lr12 on
4A; McIntosh et al. (1995) listed Lr12 on 4B and
listed Lr31 on 4BS; Nelson et al. (1997) mapped Lr31
on 4BL; Singh et al. (1999) listed both Lr12 and Lr31
on 4BS; and the Catalogue of Gene Symbols for
Wheat—2008 (McIntosh et al. 2008) listed Lr31 on
4BL, but the entry for the complementary gene Lr27
indicated that Lr31 is on 4BS.
The objective of this study was to confirm the
chromosome location of Lr12 and to identify closely
linked PCR-based DNA markers as a step toward
producing diagnostic markers and the eventual clon-
ing of Lr12.
Materials and methods
Plant material
TcLr12 (RL 6011, pedigree Exchange/6*Thatcher), a
near-isogenic line (NIL) that carries leaf-rust resis-
tance gene Lr12 (Dyck 1991), was crossed to its
recurrent susceptible parent, Thatcher. Two hundred
and thirty F
2
plants and F
2
-derived F
3
families were
used in this study.
Leaf rust resistance evaluation
Individual plants were grown in Metro-Mix 360 (Sun
Gro Horticulture, Bellevue, WA, USA) in 1-L pots in
the greenhouse at roughly 20 ± 3° C, with supple-
mental high-pressure sodium lights to provide a 15-h
photoperiod. At the anthesis growth stage, the
parents, F
1
,F
2
, and twenty plants from each F
3
family were uniformly inoculated with the P. triticina
isolate PRTUS25 (race MDBJG according to North
American race nomenclature (Kolmer et al. 2008))
suspended in Soltrol 170 light oil (Chevron Phillips
Chemical Company, The Woodlands, TX, USA).
PRTUS25 is avirulent to Lr12. Inoculation was done
in the evening, and the inoculated plants were then
incubated overnight in a mist chamber at 20 ± 3° C
with 100% relative humidity for 14 h. After the
incubation period, plants were removed from the mist
chamber and maintained in the greenhouse. Disease
reaction on flag leaves was recorded 12 days after
inoculation, using the 0–4 scale described by Roelfs
et al. (1992). Infection types of ;1 to 2? were
considered resistant whereas infection types of 3–4
were considered susceptible.
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Marker analysis
Freeze-dried leaf samples were ground in liquid nitro-
gen and total genomic DNA was extracted using the
CTAB-DNA method (Saghai-Maroof et al. 1984).
Polymorphism was assessed with PCR-based DNA
markers located on chromosome 4B of wheat including
Xgwm66, Xgwm107, Xgwm112, Xgwm165, Xgwm192,
Xgwm193, Xgwm368, Xgwm495, Xgwm513, Xgwm538,
Xgwm6, Xgwm149, and Xgwm251 from Ro
¨
der et al.
(1998); and Xwmc47 Xbarc25, Xbarc60, Xbarc109,
Xbarc124, Xbarc163, Xwmc238, Xwmc254, Xwmc89,
Xwmc16, Xwmc349, Xwmc657, Xwmc310, Xwmc413,
Xwmc491, Xwmc710, Xwmc546, and Xwmc754 from
the GrainGenes database (http://wheat.pw.usda.gov/
ggpages/SSR/WMC). The PCR assays were carried
out in 25-ll reactions as described by Ro
¨
der et al.
(1998), in an MJ Research PTC-200 thermocycler
(Watertown, Mass., USA). Products were separated on
2.3% Gene-Pure HiRes Agarose (ISC Bioexpress,
Kaysville, UT, USA). Gels were stained with ethidium
bromide and visualized with UV light.
Bulked segregant analysis
Genomic DNA of 20 homozygous resistant and 20
homozygous susceptible F
3
families were pooled in
equal proportions to make resistant and susceptible
bulks. To identify molecular markers closely linked to
the rust resistance gene, a total of 31 SSR primer pairs
were screened for polymorphism between the parents
and the resistant and the susceptible DNA bulks.
Genetic analysis
Goodness of fit of observed to expected segregation
ratios was tested using chi-square tests. Linkage
analysis was performed on the segregating F
3
popula-
tion (n = 230) for the Lr12 locus and the polymorphic
microsatellite markers identified by bulked segregant
analysis. Linkage between the Lr12 locus and the
markers was calculated using MAPMAKER version
3.0 (Lander et al. 1987), with an LOD threshold of 3.0.
Physical placement on wheat chromosome 4BL
Molecular markers flanking the resistance gene were
placed on the physical map of the wheat genome
using nullisomic–tetrasomic and ditelosomic lines.
The Chinese Spring (CS) and CS aneuploid lines used
in the study were obtained from the Wheat Genetic
and Genomic Resources Center at Kansas State
University. These included: nullisomic–tetrasomic
(N4BT4D) lines (Sears 1966); ditelosomic lines 4BS
(Dt4BS) (Sears and Sears 1979); and CS deletion lines
for the chromosome 4B long arm (4BL-1, FL = 0.71;
4BL-5, FL = 0.86) (Endo and Gill 1996).
Results
Genetics of Lr12
TcLr12 was resistant with an infection type of ;1 to 2
against isolate PRTUS25. Twenty-five F
1
(Thatcher
9 TcLr12) plants were tested for their reaction with
the pathogen and all were resistant, indicating
dominant inheritance of resistance in TcLr12.F
2
and F
3
phenotypic data were consistent with the
segregation of a single locus (Table 1).
Bulked segregant analysis
Five primer pairs (GWM149, GWM251, GWM375,
GWM495 and WMC657) generated polymorphic
fragments between the bulks. For example, primer
pair GWM251 amplified a 120-bp band in the
resistant parent TcLr12 and the resistant bulk and a
130-bp fragment in Thatcher and the susceptible
bulk.
Linkage analysis
All five polymorphic SSR markers were scored on
230 F
3
derived families from Thatcher 9 TcLr12. All
of these primers behaved as codominant markers
Table 1 Segregation of leaf rust resistance in a population
derived from cross Thatcher 9 TcLr12
Generation Number of F
2
plants and F
3
families
a
RHSv
2
P value
F
2
170 – 60 0.14 0.70
F
3
55 115 60 0.22 0.90
a
Expected segregation ratio for one gene postulation in F
2
is
3:1 and in F
3
is 1:2:1
.
R resistant, H heterozygous and S
susceptible
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123

(Fig. 1) and the resistance reaction was treated as a
sixth codominant character. The six loci were tightly
linked and spanned *15 cM (Fig. 2). Lr12 was
flanked by marker Xgwm251 at a distance of
0.9 cM and by Xgwm149 at a distance of 1.9 cM.
Assignment to chromosome bin
The markers Xgwm149 and Xgwm251 linked to
resistance gene Lr12 were placed on chromosome
4BL using CS deletion stocks. Fragments were
amplified from TcLr12 and CS using these markers
but did not amplify from N4BT4D, Dt4BS, 4BL-1,
and 4BL-5, thus placing both markers and the
resistance gene in the most distal 4BL bin, 4BL5,
FL = 0.86–1.00.
Discussion
The adult-plant race-specific resistance gene Lr12
was located on chromosome arm 4BL by linkage
analysis and chromosome bin-mapping. Our results
for Lr12 confirm the original location on 4BL
reported by Singh and McIntosh (1984) for Lr31.
Confusion in the literature about the chromosome
location can be explained by a series of unfortunate
events including switching of the assignment of
chromosomes 4A and 4B (Naranjo et al. 1988),
renaming of chromosome arm b to the long arm
(Endo et al. 1991), delayed appreciation of the
probable identity of Lr12 with Lr31, and bookkeeping
errors.
Lr12 was located in chromosome deletion bin
4BL-5 and was closely flanked by markers Xgwm149
and Xgwm251. Nelson et al. (1997) reported that a
quantitative trait locus (QTL) they identified as Lr31
was located in the region around RFLP marker
XksuG10. According to the Wheat Composite 2004
linkage map (GrainGenes 2.0, http://wheat.pw.usda.
gov/GG2/ index.shtml), XksuG10 is approximately
1 cM distal from Xgwm149. Thus our results for Lr12
agree with those of Nelson et al. (1997) for Lr31. The
flanking PCR-based markers were codominant, and
should be useful for marker-assisted selection or in
fine mapping studies. It remains to be tested whether
these markers have diagnostic value for the presence
of Lr12/Lr31 in uncharacterized wheat cultivars or
breeding lines.
Chromosome deletion bin 4BL-5, which com-
prises the terminal 14% of 4BL, accounts for most of
the recombination on 4BL and appears to be a hot
spot for gene duplication and evolution (See et al.
2006). Bansal et al. (2008) recently reported that
adult-plant race-specific leaf rust resistance gene
Lr49 is also located on 4BL. It was loosely flanked by
markers Xbarc163 and Xwmc349. This location lies
approximately 10 cM distal to the location of Lr12/
Lr31 according to the composite map. Lr49 has a
hypersensitive resistance response like Lr12, but
differs in race specificity (Saini et al. 2002). There
are no other named leaf rust resistance genes reported
on this arm (McIntosh et al. 2008). However, Naz
et al. (2008) mapped a possible new QTL for seedling
resistance to leaf rust on 4BL near Xwmc349 in a
cross of a winter wheat and a synthetic hexaploid.
The QTL is close to Lr49, but Lr49 is an APR gene.
The QTL could be Lr31, but this was deemed
unlikely because they could not detect the comple-
mentary gene, Lr27. Nevertheless, the Lr27 ? Lr31
gene combination has been reported in T. turgidum
Fig. 1 Electrophoretic pattern of DNA fragments generated
by primer pair GWM251 for F
3
lines of the cross
Thatcher 9 TcLr12. The 120-bp fragment is associated with
the rust-resistant allele and the 130-bp fragment is associated
with the rust-susceptible allele. A homozygous resistant, B
homozygous susceptible, H heterozygote
Fig. 2 Placement of Lr12 on genetic map of chromosome arm
4BL of wheat in the cross Thatcher 9 TcLr12. The centromere
is toward the top of the figure
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(Huerta-Espino et al. 2009) and could have been
present in the synthetic parent. William et al. (2006)
reported a new QTL for resistance to leaf rust in
Avocet S in the interval between markers Xgwm368
and Xgwm495, which is approximately 3–6 cM
proximal to Lr12/Lr31. They also reported a QTL
for stripe rust resistance in the same interval.
The agronomic value of Lr12/Lr31 has varied both
geographically and over time. When first described in
1966, Lr12 was effective against a wide range of
races of leaf rust in Canada (Dyck et al. 1966). Lr12
was once suggested to enhance the durable APR gene
complex (Roelfs 1988), but evidence of unconven-
tional resistance mechanisms was not found (Bender
et al. 2000). Singh and Gupta (1992) noted that Lr12
was ineffective to all wheat leaf rust pathotypes
tested in Mexico in 1988–1990. Kolmer (2003)
considered Lr12 to be an effective APR gene in the
southeastern USA, whereas Wamishe and Milus
(2004) considered Lr12 alone to be ineffective in
the same region. Kolmer et al. (2005) showed that
virulence to Lr12 occurred in a wide range of
virulence phenotypes in the USA. Park and McIntosh
(1994) described large temporal fluctuations in vir-
ulence frequency for Lr12/Lr31 in Australia and
suggested a gene deployment strategy using combi-
nations with seedling resistance genes. A recent
report of new virulence in durum isolates of P.
triticina to Lr27 ? Lr31 suggested that Lr27 ? Lr31
had hitherto been providing useful resistance in
Mexican durums (Huerta-Espino et al. 2009).
Clearly, Lr12/Lr31 has been repeatedly overcome by
new virulent pathotypes and its future agronomic value
is limited to deployment in combinations with other
genes. Nevertheless Lr12/Lr31 is one of the most
interesting race-specific genes due to its interaction with
Lr27. Final confirmation of theidentity of Lr12 and Lr31
and elucidation of the mechanisms of interaction with
Lr27 will be achieved by cloning the genes.
Acknowledgments This is contribution number 10-034-J
from the Kansas Agricultural Experiment Station. Portions of
this research work were supported by USDA-ARS CRIS
project 5430-21000-006-00D (Genetic Enhancement for
Resistance to Biotic and Abiotic Stresses in Hard Winter
Wheat), and by a grant from the Kansas Wheat Commission.
We thank the Wheat Genetics and Genomics Resources Center
at Kansas State University for providing the aneuploid stocks.
Mention of trade names or commercial products is solely for
the purpose of providing specific information and does not
imply recommendation or endorsement by the USDA.
References
Bansal UK, Hayden MJ, Venkata BP, Khanna R, Saini RG,
Bariana HS (2008) Genetic mapping of adult plant leaf
rust resistance genes Lr48 and Lr49 in common wheat.
Theor Appl Genet 117:307–312
Bender CM, Pretorius ZA, Kloppers FJ, Spies JJ (2000) His-
topathology of leaf rust infection and development in
wheat genotypes containing Lr12 and Lr13. J Phytopathol
148:65–76
Dyck PL (1991) Genetics of adult plant leaf rust resistance in
Chinese Spring and Sturdy wheats. Crop Sci 31:309–311
Dyck PL, Kerber ER (1971) Chromosome location of three
genes for leaf rust resistance in common wheat. Can J
Genet Cytol 13:480–483
Dyck PL, Samborski DJ, Anderson RG (1966) Inheritance of
adult-plant leaf rust resistance derived from the common
wheat varieties Exchange and Frontana. Can J Genet
Cytol 8:665–671
Endo TR, Gill BS (1996) The deletion stocks of common
wheat. J Hered 87:295–307
Endo TR, Mukai Y, Yamamoto M, Gill BS (1991) Physical
mapping of a male-fertility gene of common wheat. Jpn J
Genet 66:291–295
Fueillet C, Travella S, Stein N, Albart L, Nublat A, Keller B (2003)
Map-based isolation of the leaf rust disease resistance gene
Lr10 from the hexaploid wheat (Triticum aestivum L.) gen-
ome. Proc Natl Acad Sci USA 100:15253–15258
Huerta-Espino J, Singh RP, Herrera-Foessel SA, Pe
´
rez-Lo
´
pez
JB, Figueroa-Lo
´
pez P (2009) First detection of virulence
in Puccinia triticina to resistance genes Lr27 ? Lr31
present in durum wheat in Mexico. Plant Dis 93:110
Kolmer JA (2003) Postulation of leaf rust resistance genes in
selected soft red winter wheats. Crop Sci 43:1266–1274
Kolmer JA, Long DL, Hughes ME (2005) Physiologic spe-
cialization of Puccinia triticina on wheat in the United
States in 2003. Plant Dis 89:1201–1206
Kolmer JA, Jin Y, Long DL (2007) Wheat leaf and stem rust in
the United States. Aust J Agric Res 58:631–638
Kolmer JA, Long DL, Hughes ME (2008) Physiologic spe-
cialization of Puccinia triticina on wheat in the United
States in 2006. Plant Dis 92:1241–1246
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-
Espino J, McFadden H, Bossolini E, Selter LL, Keller B
(2009) A putative ABC transporter confers durable
resistance to multiple fungal pathogens in wheat. Science
323:1360–1363
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ,
Lincoln SE, Newberg L (1987) MAPMAKER: an inter-
active computer package for constructing primary genetic
linkage maps of experimental and natural populations.
Genomics 1:174–181
McIntosh RA, Baker EP (1966) Chromosome location of
mature plant leaf rust resistance in Chinese Spring wheat.
Aust J Biol Sci 19:943–944
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an
atlas of resistance genes. CSIRO Publishing, Colling-
wood, Australia
McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C,
Somers DJ, Appels R, Devos KM (2008) Catalogue of
Mol Breeding
123

Gene Symbols for Wheat (2008). http://www.shigen.nig.
ac.jp/wheat/komugi/genes/download.jsp. Accessed 11 Feb
2010
Nagarajan S, Joshi LM (1975) A historical account of wheat
rust epidemics in India and their significance. Cereal
Rusts Bull 3:29–33
Naranjo T, Roca A, Goicoechea PG, Giraldez R (1988)
Chromosome structure of common wheat: Genome reas-
signment of chromosomes 4A and 4B. In: Miller TC,
Koebner, RMD (eds) Proc 7th Int Wheat Genet Symp,
IPSR, Cambridge, UK,115–120 1988
Naz AA, Kunert A, Lind V, Pillen K, Le
´
on J (2008) AB-QTL
analysis in winter wheat: II Genetic analysis of seedling
and field resistance against leaf rust in a wheat advanced
backcross population. Theor Appl Genet 116:1095–1104
Nelson JC, Singh RP, Autrique JE, Sorrells ME (1997) Map-
ping genes conferring and suppressing leaf rust resistance
in wheat. Crop Sci 37:1928–1935
Park RF, McIntosh RA (1994) Adult plant resistances to
Puccinia recondita f.sp. tritici in wheat. N Z J Crop Hortic
Sci 22:151–158
Ro
¨
der MS, Korzun V, Wendehake K, Plaschke J, Tixier MH,
Leroy P, Ganal MW (1998) A microsatellite map of
wheat. Genetics 149:2007–2023
Roelfs AP (1988) Resistance to leaf and stem rusts in wheat.
In: Simmonds NW, Rajaram S (eds) Breeding strategies
for resistance to the rusts of wheat. CIMMYT, Mexico
D.F., pp 10–22
Roelfs AP, Singh RP, Saari EE (1992) Rust diseases of wheat:
concepts and methods of disease management. CIMMYT,
Mexico, DF
Saghai-Maroof MA, Biyashev RM, Yang GP, Zhang Q, Allard
RW (1984) Extraordinarily polymorphic microsatellites
DNA in barley species diversity, chromosome location
and population dynamics. Proc Natl Acad Sci USA
91:5466–5470
Saini RG, Kaur M, Singh B, Sharma S, Nanda GS, Nayar SK,
Gupta AK, Nagarajan S (2002) Genes Lr48 and Lr49 for
hypersensitive adult plant leaf rust resistance in wheat
(Triticum aestivum L.). Euphytica 124:365–370
Sears ER (1966) Nullisomic–tetrasomic combinations in
hexaploid wheat. In: Riley R, Lewis KR (eds) Chromo-
some manipulations and plant genetics. Oliver and Boyd,
Edinburgh, pp 29–45
Sears ER, Sears LMS (1979) The telocentric chromosomes of
common wheat. In: Ramanujan S (ed) Proceedings of the
5th International Wheat Genetics Symposium. Indian
Society of Genetics and Plant Breeding, New Delhi, 389–
407 1979
See DR, Brooks S, Nelson JC, Brown-Guedira G, Friebe B,
Gill BS (2006) Gene evolution at the ends of wheat
chromosomes. Proc Natl Acad Sci USA 103:4162–4167
Singh RP, Gupta AK (1992) Expression of wheat leaf rust
resistance gene Lr34 in seedlings and adult plants. Plant
Dis 76:489–491
Singh RP, McIntosh RA (1984) Complementary genes for
reaction to Puccinia recondita tritici in Triticum aestivum
II. Cytogenetic studies. Can J Genet Cytol 26:736–742
Singh D, Park RF, McIntosh RA (1999) Genetic relationship
between the adult plant resistance gene Lr12 and the
complementary gene Lr31 for seedling resistance to leaf
rust in common wheat. Plant Pathol 48:567–573
Singh RP, Huerta-Espino J, William HM (2005) Genetics and
breeding for durable resistance to leaf and stripe rusts in
wheat. Turk J Agric For 29:121–127
Wamishe YA, Milus EA (2004) Seedling resistance genes to
leaf rust in soft red winter wheat. Plant Dis 88:136–146
William HM, Singh RP, Huerta-Espino J, Palacios G, Suenaga
K (2006) Characterization of genetic loci conferring adult
plant resistance to leaf rust and stripe rust in spring wheat.
Genome 49:977–990
Mol Breeding
123