Theoretical and Applied Genetics

, Volume 123, Issue 4, pp 615–623 | Cite as

A multiple resistance locus on chromosome arm 3BS in wheat confers resistance to stem rust (Sr2), leaf rust (Lr27) and powdery mildew

  • R. Mago
  • L. Tabe
  • R. A. McIntosh
  • Z. Pretorius
  • R. Kota
  • E. Paux
  • T. Wicker
  • J. Breen
  • E. S. Lagudah
  • J. G. Ellis
  • W. Spielmeyer
Original Paper

Abstract

Sr2 is the only known durable, race non-specific adult plant stem rust resistance gene in wheat. The Sr2 gene was shown to be tightly linked to the leaf rust resistance gene Lr27 and to powdery mildew resistance. An analysis of recombinants and mutants suggests that a single gene on chromosome arm 3BS may be responsible for resistance to these three fungal pathogens. The resistance functions of the Sr2 locus are compared and contrasted with those of the adult plant resistance gene Lr34.

Introduction

The resistance gene Sr2 was transferred from tetraploid emmer wheat (Triticum turgidum ssp. dicoccon) into common wheat (Triticum aestivum L.) in the 1920s (McFadden 1930) and has since been effective against all known pathotypes of the wheat stem rust pathogen (Puccinia graminis f. sp. tritici). The Sr2 response is characterized by partial resistance, which restricts the number and size of uredinia and is expressed only in adult plants. The gene was mapped to chromosome arm 3BS by Hare and McIntosh (1979) and associated with a trait called pseudo-black chaff (PBC), which causes a variable and genotype-dependent pigmentation of stems and/or glumes (McFadden 1939; Hare and McIntosh 1979). In a fine mapping study, PBC could not be separated from Sr2 by genetic recombination (Kota et al. 2006).

The leaf rust (caused by P. triticina) resistance gene Lr27 was also mapped to chromosome arm 3BS and co-segregated with Sr2 in families consisting of 289 lines (Singh and McIntosh 1984a, b). In contrast to Sr2, Lr27 resistance is race specific and requires a complementary gene (Lr31) on chromosome 4B. Although seedling resistance conferred by Lr31 is dependent on the presence of Lr27, there is evidence that Lr31 may be identical to Lr12, which alone confers race-specific adult plant resistance (Singh et al. 1999). Lr27 may also be allelic to another adult plant leaf rust resistance gene (SV2) (M. Dieguez, pers. comm.).

In this study, we investigated the genetic relationship of Lr27 and Sr2 in more detail by mapping Sr2 and Lr27 in a high-resolution mapping family. We also isolated susceptible mutants for both genes to investigate the possibility that stem rust and leaf rust resistance may be conferred by the same gene. Furthermore, given the previous findings that the multiple rust resistance genes Lr34/Yr18 and Lr46/Yr29 provide partial resistance to powdery mildew (caused by Blumeria graminis f. sp. tritici) (Spielmeyer et al. 2005; Lillemo et al. 2008), we further investigated the likelihood that Sr2 confers resistance to powdery mildew.

Materials and methods

Plant material and mapping family

Sr2 was transferred to hexaploid wheat by crossing “Yaroslav” emmer with the susceptible “Marquis” (McFadden 1930). Stem rust-resistant variety “Hope”, which was one source of Sr2 in early breeding programs, was selected from progeny of the interspecific cross (McFadden 1930). Two accessions of “Yaroslav” used in this study were obtained from the Australian Winter cereal collection. They were differentiated from other emmer accessions and shown to be identical to Hope, but not to Marquis, with respect to Sr2-specific markers (Mago et al. 2011). An F2 mapping family was derived from a cross between cv. Chinese spring (CS) and the chromosome substitution line CS (Hope 3B), which carries Sr2. The high-resolution mapping family was generated by screening 1,340 F2 seeds (equivalent to 2,680 gametes) with flanking simple sequence repeat (SSR) markers gwm389 and gwm533 as described in Kota et al. (2006). The mapping family was reduced to 17 recombinants by placing Sr2 between wEST marker CA640157 and gwm533 (Kota et al. 2006).

Seedling leaf rust screen

To screen for leaf rust resistance gene Lr27, 1-week-old seedlings were inoculated in the glasshouse at the Plant Breeding Institute, Cobbitty, Australia with the leaf rust race 10-1,2,3 (culture accession no. 347) using the protocol described by McIntosh et al. (1995). Rust responses were scored 10–14 days post-infection according to the scale proposed by Stakman et al. (1962).

Adult plant stem rust test in the field

Stem rust resistance screening was done on adult plants in the field in 2009 with the rust races 98-1,2,3,5,6 (culture no. 279) and 34-1,2,7 + Sr38 (culture no. 565) using the protocol described by Kota et al. (2006). Lines were scored as resistant or susceptible based on the level of infection on parental lines.

Adult plant stem rust testing in glasshouse

For testing the stem rust response of adult plants in the glasshouse, entries CS(Hope3B) (resistant), 72-2 deletion mutant (susceptible), four M5 sister lines of mutant M39 (39-1, 39-2, 39-3, 39-4), four M5 sister lines of mutant M40 (40-1, 40-2, 40-3, 40-4) and four M5 sister lines of mutant M48 (48-1-1, 48-1-2, 48-2-1, 48-2-2) were grown in plastic cones in a glasshouse as described by Pretorius et al. (2007). Hartog (resistant) and two susceptible lines, entry 37 from the 2nd ISRTN 07 and Kariega, were included as controls. Two replications, arranged over two trays, were planted. Depending on the number of seeds available, the total number of plants tested ranged from two to eight per entry. When most entries were at anthesis (46 days after planting), plants were inoculated by spraying with a suspension of urediniospores of isolate UVPgt60 (race PTKST) in sterile, distilled water (1 mg/ml) containing Tween 20®. As much as 100 ml of suspension was applied as uniformly as possible per replication using a pressurized atomizer (Pretorius et al. 2007). Immediately after inoculation, plants were placed in a plastic tent (dew chamber) on a glasshouse bench flooded with water. The plants were removed from the dew chamber after 24 h and maintained in a greenhouse at 18–25°C. Stem rust severities and reaction types on the last internodes were scored 15 days after inoculation. The most common response for an entry over the two replications was recorded. A similar adult plant glasshouse assay was conducted in Canberra to test mutants M161 and M174 with the stem rust race 98-1, 2, 3, 5, 6.

Powdery mildew testing

A glasshouse isolate of powdery mildew, caused by B. graminis f. sp. tritici, was maintained on susceptible plants. Screening of test genotypes (generally four biological replicates per genotype) was conducted by growing test plants in a growth cabinet (25°C, 16 h day, 18°C, 8 h night). At approximately 5 weeks after sowing (late tillering), plants were transferred to the glasshouse and inoculated with mildew as follows. Test plants were randomized and laid on their sides on the glasshouse bench, and sporulating mildew spreader plants were shaken gently overhead. A fine mist of spores settled onto the test plants, which were then placed in shallow tubs and watered from below, without disturbance of the leaves. Phenotypes were recorded at approximately 11 days after inoculation.

Scoring pseudo-black chaff

PBC was scored as a qualitative trait based on the presence of dark pigmentation, which accumulates on stem internodes both in glasshouse and field-grown plants. As the plants matured, pigmentation was also scored on the glumes. From each mutant, approximately 20 individuals per M6 family were screened for PBC in the glasshouse.

Mutagenesis and mutant screens

Mutagenesis of the resistant line CS(Hope3B) was done using both γ-irradiation and ethylmethane sulfonate (EMS). A dosage of 20 krads was used for irradiation, which was chosen based on LD50 as described in Mago et al. (2004). For EMS treatment, the seeds were soaked for 24 h in water at room temperature after which EMS (0.4 or 1%) was added and treated for 12 h at 28°C with shaking. The solution was decanted and seeds washed under tap water for several hours to remove residual EMS and grown in the field to produce M1 heads. Field screening for stem rust mutants was done by sowing approximately 20 M2 seeds from single heads in 60 cm field rows. Over 10,000 M2 field rows derived from single heads (includes γ-irradiated and 0.4% EMS treated) were screened for loss of stem rust resistance in four field seasons at the University of Sydney Plant Breeding Institute, Cobbitty, Australia. In each season, field rows were scored at least twice at the adult plant stage before and after anthesis. Irrigation was used to maintain moist conditions during the infection process. The test plot area included susceptible infection rows, single spikes of which were inoculated by injecting 2–5 ml of a water-based P. graminis f. sp. tritici urediniospore suspension directly into a stem internode at 1–2 m intervals. For leaf rust mutant screening, M2 seeds (1% EMS treated) from single spikes were sown in large metal trays in the glasshouse and screened for Lr27 mutants at the seedling stage, as described above. Mutants were scored for leaf rust, stem rust and powdery mildew in the M5 and M7 generations.

PCR amplification of markers

PCR reactions were performed in 20 μl volumes with 2–4 μl (100 ng) DNA template, 0.2 mM dNTP, 10 pmol of each primer, 1.5 mM MgCl2, 1× GoTaq Flexi buffer and 0.5 U GoTaq Flexi Taq polymerase (Promega). The primer sequences and PCR conditions are shown in Table 1.
Table 1

Primer sequences and PCR conditions for the amplification of the markers co-segregating with Sr2

Marker

Primer sequence

PCR conditions

MSF_2

F-GAAAAGATATGTCCTTTGGTGG

R-GAAGATTCGCAACTTCTTCAGC

95°C—2 min (1 cycle)

30 cycles of

95°C—30 s

62°C—40 s

72°C—1 min

1 cycle

72°C—5 min

15°C—1 min

RKO_2

F-AAATCTAACCAAGGATAATCAATC

R-ACATCAAGCATCCTTTCCGTTTGC

95°C—2 min (1cycle)

30 cycles of

95°C—30 s

58°C—40 s

72°C—2 min

1 cycle

72°C—5 min

15°C—1 min

CA746621

F-GGGTGCACATCCATTGACTTT

R-TTCTCTCAAGAGCGGGTGCT

95°C—2 min (1cycle)

30 cycles of

95°C—30 s

58°C—40 s

72°C—50 s

1 cycle

72°C—5 min

15°C—1 min

CD882879

F-CCGTCCACCGGGAACAAGACC

R-GCTCCTCGCGATGACCCCAC

95°C—2 min (1cycle)

30 cycles of

95°C—30 s

58°C—40 s

72°C—50 s

1 cycle

72°C—5 min

15°C—1 min

BEX_2

F-TGCGGGTTCAAGAACGTCAAC

R-GTTCATGTCCGTGATGATCA

95°C—2 min (1cycle)

30 cycles of

95°C—30 s

58°C—40 s

72°C—50 s

1 cycle

72°C—5 min

15°C—1 min

Results

High-resolution map of Sr2

The stem rust resistance gene Sr2 was previously positioned between wEST marker CA640157 and SSR marker gwm533 on chromosome arm 3BS using a high-resolution mapping family generated from Chinese Spring (CS) × CS(Hope3B) (Fig. 1) (Kota et al. 2006). We used the tightly linked marker CA640157 to start a chromosome walk by screening a chromosome 3B-specific BAC library of CS (Šafář et al. 2004). The physical map of the Sr2 region was then completed by utilizing BAC contig information from the early stages of physical map construction of chromosome 3B (Paux et al. 2008). The Sr2 region was contained within contig 11 (1.2 Mb) of the 3B physical map, which was sequenced and annotated as part of a larger study of gene density and transposable elements (Choulet et al. 2010; Breen et al. 2010). The CS sequence was used to develop markers and define the Sr2 region in more detail (Fig. 1). EST-derived marker DOX_1 recombined with Sr2 on the distal side in RIL#7, and marker RKO_1 was separated by one recombination event from Sr2 on the proximal side through RIL#10 (Fig. 1). These two recombinants were among F2 progeny derived from 2,680 gametes; therefore, DOX_1 and RKO_1 delineate a genetic interval of approximately 0.07 cM, which represents approximately 570 kb in CS (Fig. 1). Five additional markers, BEX_2, CD882879, CA746621, RKO_2 and MSF_2, were developed from the intervening sequence and co-segregated with Sr2. All these markers were within features annotated on the Chinese Spring 3B physical map of Choulet et al. (2010), with the exception of CD882879 and CA746621. Wheat EST CD882879 has 92% identity with sequences at 469 kb in the 1.2 Mb CS sequence (Genbank accession FN645450), and CA746621 has 87% identity with sequences at 393 kb in the FN645450 sequence. No recombination event was detected in the approximate 450 kb sequence between markers BEX_2 and MSF_2. The marker csSr2 was previously published as the most useful marker to select for Sr2 in a wide range of genetic backgrounds (Mago et al. 2011).
Fig. 1

a High-resolution genetic map of the Sr2 region on chromosome arm 3BS and the corresponding physical map of the susceptible haplotype of Chinese Spring. The physical map and annotation are part of contig 11 (1.2 Mb) published by Choulet et al. 2010. Wheat ESTs CD882879 and CA746621 mapped to 469 kb and 393 kb, respectively, in the published contig 11 sequence. The contig 11 DNA sequence was previously submitted to GenBank under accession number FN645450. b A subset of seven critical recombinants from the mapping family CS × CS(Hope3B) was used for fine mapping of markers and genes (a genotype = Chinese Spring, b genotype = CS(Hope3B). These seven recombinants define the genetic interval in CS that corresponds to Sr2 region (highlighted by shading) and were selected from a set of 17 recombinants originally reported between CA640157 and gwm533 (Kota et al. 2006)

Leaf rust resistance and powdery mildew resistance co-locate with Sr2

The leaf rust response was evaluated in the parental lines and seven critical recombinants to estimate the genetic linkage between Lr27 and Sr2. The parental lines showed clear differences in response to leaf rust at the seedling stage with CS (Hope3B), which contains both Lr27 + Lr31, showing moderate resistance (infection type (IT); 12X), whereas CS (containing Lr31, but not Lr27) was susceptible (IT 33+). Hope (presumably containing only Lr27) and Marquis, presumably lacking both Lr27 and Lr31, were susceptible while Yaroslav emmer (donor of Sr2 and Lr27) was highly resistant probably due to the presence of additional gene(s) (Fig. 2). The infection types on recombinant lines were similar to the parental types (Table 2). Leaf rust resistance and Sr2 co-segregated in seven critical recombinant lines (Fig. 1) confirming that race-specific leaf rust resistance expressed in seedlings is tightly linked to Sr2 (Singh and McIntosh 1984a).
Fig. 2

Leaf rust infection types on first leaves of parental lines 14 days post-inoculation. The following genotypes are shown: Hope, Chinese Spring (Hope 3B) chromosome substitution line, Chinese Spring, Marquis and Yaroslav emmer

Table 2

Summary of known rust resistance genotypes of parental lines and stem rust, leaf rust and powdery mildew scores of parental and recombinant lines

Genotype

Sr2

Lr27

Lr31

Stem rust

Leaf rust

Powdery mildew

Parental

 Yaroslav emmer

+

+

?

R

R

R

 Marquis

S

S

S

 Hope

+

+

R

S

MR

 CS

+

S

S

S

 CS (Hope3B)

+

+

+

R

R

R

Recombinants

 RL#7

   

R

R

R

 RL#10

   

R

R

R

 RL#113

   

R

R

R

 RL#114

   

R

R

R

 RL#9

   

S

S

S

 RL#117

   

S

S

S

 RL#124

   

S

S

S

In the glasshouse when powdery mildew was allowed to proliferate, the level of mildew infection was noted to be lower on CS(Hope3B) than on CS. The initial observation was confirmed in repeated and replicated glasshouse experiments with plants at the late tillering stage (approximately 5 weeks after sowing), with consistent results (Fig. 3). The resistance response of CS(Hope3B) was accompanied by necrotic lesions, which may have contributed to limiting fungal growth. Although infected leaves of Hope showed some necrosis, there was more fungal growth on Hope than on CS(Hope3B). Marquis was susceptible and Yaroslav emmer highly resistant probably due to other effective resistance genes. When the seven recombinant lines were inoculated with powdery mildew, lines resistant to stem rust and leaf rust were also resistant to powdery mildew. Recombinants susceptible to both rusts were also susceptible to powdery mildew, indicating that the resistance to three different fungal pathogens was not separated by recombination (Table 2).
Fig. 3

Powdery mildew infection on leaves of 5-week-old plants (+11 days) grown in the glasshouse. The following genotypes are shown: Hope, Chinese Spring (Hope 3B) chromosome substitution line, Chinese Spring, Marquis and Yaroslav emmer

Five independent mutants lack resistance to stem rust, leaf rust and powdery mildew

Putative mutants lacking stem rust resistance and PBC were recovered from gamma-irradiated seed along with at least one of the resistant sibs from the same M2 family. Loss of the Sr2 phenotype in individual plants in the CS background was difficult to ascertain. Progeny tests of putative mutants were conducted in the following field season. A total of four homozygous mutants that lacked stem rust resistance and PBC were recovered. Markers flanking the Sr2 locus failed to amplify from these mutants indicating that loss of resistance in each case was the result of a large deletion. These mutants also lost resistance to leaf rust and powdery mildew.

Given the possibility that Sr2 and Lr27 resistance may be encoded by the same gene, we screened other M2 families from 1% EMS-treated seed for loss of seedling leaf rust resistance. Nineteen leaf rust-susceptible mutants were recovered among 4,000 M2 families with loss of flanking markers, suggesting that these lines also contained large deletions. Subsequent progeny testing of these mutants in the field showed they had also lost adult plant stem rust resistance and PBC. Testing of a subset of these mutants demonstrated that they had lost powdery mildew resistance under glasshouse conditions. Although EMS treatment is expected to induce point mutations or small deletions, it is possible that the high concentration of EMS (1%) used in the current study may have led to large deletions of the chromosome.

Five putative leaf rust-susceptible mutants, M39, M40, M48, M161 and M174, retained flanking markers, DOX_1 and RKO_1, and co-segregating markers, BEX_2, CD882879, CA746621, RKO_2 and MSF_2, suggesting that they may be point mutations or small deletions. Progeny testing of M5 and M7 families confirmed the loss of leaf rust resistance in these mutants (Table 3). M39, M40 and M48 were also grown in the field in 2009 to evaluate their response to stem rust. M39 and M40 were scored as homozygous susceptible to stem rust and lacked PBC, although 1 out of 20 plants in the family M39 may have retained small amounts of PBC in the field. Several M48 progeny displayed PBC and diminished stem rust infections, indicating either a partial knockout phenotype or segregation. Plants were individually harvested from field rows and progeny of four plants from each mutant were grown in the glasshouse. Progeny derived from M40 lacked PBC, indicating that this mutant was homozygous. In M39, two of the four families contained one or two plants with small amounts of PBC suggesting either a partial knockout phenotype, or that the line may still be segregating, although previously it appeared homozygous for loss of stem rust and leaf rust resistance. PBC was clearly visible on several plants in three of four M48 families, confirming the previous observations of partial loss of PBC and stem rust resistance in the field.
Table 3

Disease scores of CS(Hope3B), mutants and controls grown under field and glasshouse conditions

 

Powdery mildew

Leaf rust

Stem rust

   

Field

Glasshouse

Sister lines

Stem rust score

Classification

CS/Hope3B

R

R

R

 

10MS

R

72-2 del mutant

S

S

S

 

40S

S

Mutant 39

MRa

S

S

39-1

40MSS

S

    

39-2

40S

S

    

39-3

20MSS

MS

    

39-4

50MSS

S

Mutant 40

MSa

S

S

40-1

30S

S

    

40-2

40MSS

S

    

40-3

40S

S

    

40-4

20S

MS

Mutant 48

MRa

S

S

48-1-1

40S

S

    

48-1-2

40S

S

    

48-2-1

5MS

R

    

48-2-2

30MSS

S

Mutant 161

MRa

S

nt

 

MSb

S

Mutant 174

MSa

S

nt

 

MSb

S

Hartog (res control)

nt

nt

nt

 

5MS

R

Line 37 ISRTN 07

(sus control)

nt

nt

nt

 

50S

S

Kariega (sus control)

nt

nt

nt

 

30S

S

nt not tested

aCompared to CS(Hope3B)

bTested in Canberra

Three mutants (M39, M40 and M48) were also tested as adult plants for stem rust resistance under glasshouse conditions in the Republic of South Africa using a Ug99-related Pgt isolate that was virulent on the lines at the seedling stage. Although differences in rust responses were less pronounced than expected between resistant wild-type CS(Hope3B) and the susceptible deletion mutant 72-2 (Fig. 4), the levels of stem rusting on M5 progeny of these mutants were clearly higher than on the wild type with the exception of one family derived from M48, which was resistant (Table 3). These glasshouse results confirmed the more pronounced phenotypes of mutants M39 and M40 in comparison to M48. Mutants M161 and M174 also showed higher level of stem rust as compared to CS(Hope3B) in glasshouse tests conducted in Canberra.
Fig. 4

Stem rust infection on stems after anthesis on 1 CS(Hope3B), 2 72-2 deletion, 3 Hartog (resistant control) and 4 line 37 ISRTN 07 (susceptible control)

Mutants M39, M40, M48, M161 and M174 were tested for response to powdery mildew in the glasshouse and the infection phenotypes of all mutants were distinguishable from the resistant parent (Table 3). CS(Hope 3B) showed little or no proliferation of mildew and the development of necrotic patches on infected leaves by 11 days after inoculation. All plants (between 4 and 7 per genotype) of M39, M48 and M161 showed less necrosis and clearly more proliferation of mildew than CS(Hope 3B). M40 and M174 appeared to be susceptible with no large patches of necrosis.

Discussion

In this study, stem rust resistance gene Sr2, leaf rust resistance gene Lr27 and powdery mildew resistance could not be separated by recombination. Three independent mutants were isolated that lacked resistance to stem rust, leaf rust and powdery mildew. Loss of leaf rust resistance in these mutants could have resulted from mutations in the complementary gene Lr31 on chromosome 4B; however, there is no evidence that this gene is involved in stem rust and powdery mildew resistances determined at the Sr2 locus. The resistance response to powdery mildew was associated with necrosis of leaf cells. Because mutants retained markers that were flanking and co-segregating with the Sr2 locus, it is possible that mutants carry small deletions or point mutations that resulted in the loss or disruption of a single gene and loss of resistance to three fungal pathogens. However, there are reports that a small number of wheat genotypes express Lr27 specificity without conferring stem rust resistance (Singh and McIntosh 1984a, b and Singh pers. comm.) suggesting that Sr2 and Lr27 may recombine and are therefore encoded by separate genes. To our knowledge, no wheat line has been reported where the reciprocal is true, i.e., carrying Sr2 and lacking Lr27. A possible explanation of these observations is that Lr27 and Sr2 are encoded by the same gene, but the stem rust resistance conferred by Sr2 is not expressed or is difficult to detect in certain backgrounds. For example, the Australian cultivar “H45” was predicted to encode a functional Lr34 gene based on DNA data, although it is susceptible to stripe rust and leaf rust, indicating that the intact Lr34 gene is not sufficient for resistance in this background (Lagudah et al., unpublished). Because the physical map used in this study was derived from the susceptible haplotype Chinese Spring, it is also possible that these mutants harbor larger deletion events if the resistant haplotype in Hope has diverged significantly from CS. A final conclusion about the molecular basis of Sr2, Lr27 and Pm resistance must await the cloning of these genes.

There are notable similarities between the Sr2 locus and the recently cloned resistance gene Lr34 on chromosome 7DS. A single gene confers adult plant resistance to leaf rust (Lr34) and stripe rust (Yr18) and causes necrosis of the tips of the flag leaves, a trait commonly referred to as leaf tip necrosis (Krattinger et al. 2009). Lr34 was also linked to the powdery mildew resistance gene (Pm38) (Spielmeyer et al. 2005) and loss of function mutants were susceptible to powdery mildew, indicating that a single gene was effective against three fungal pathogens. In this study, we demonstrate that a multiple resistance locus on 3BS also confers resistance to two rusts and powdery mildew, which was associated with necrosis of leaf cells. In a previous study, Sr2 was also associated with leaf chlorosis under high-temperature conditions (Brown 1997).

There are also notable differences between Sr2 and Lr34. For example, the race non-specific, adult plant resistance gene Sr2 is associated with race-specific leaf rust resistance gene Lr27 that can be scored in the seedling stage. However, the expression of the resistance is dependent on the presence of Lr31. Both Lr34 and Yr18 are considered race non-specific genes that are effective only at the adult plant stage, although Lr34 resistance can be seen on seedlings under specific low-temperature conditions (Dyck 1977). From the analysis of mutants, it is possible that a single gene is responsible for both the Sr2 and Lr27 resistances. Similar observations were made with Lr34, which was associated with the expression of additional leaf rust and stem rust resistance that was not directly encoded by Lr34 (Dyck and Samborski 1982; German and Kolmer 1992; Spielmeyer et al. 2008; Kolmer et al. 2011; Hiebert et al. 2010). These interactions are particularly pronounced in Thatcher (Tc)-derived germplasm. Loss of function mutants for Lr34/Yr18/Pm38/Ltn1 also eliminated adult plant stem rust resistance in the Tc background confirming that Lr34 rather than tightly linked genes is responsible for the enhanced resistance effect (Krattinger et al. 2009). Components of stem rust resistance expressed in the presence of Lr34 were recently mapped to chromosomes 2BL and 6DS providing important insights into the genetic basis of stem resistance in Tc and Tc derivatives (Kolmer et al. 2011; Hiebert et al. 2010). The adult plant resistance gene Lr67/Yr46, which was recently mapped to chromosome 4DL, was also associated with adult plant stem rust resistance in the Tc background, suggesting positive interactions between race non-specific adult plant resistance and that unlinked rust resistance genes may occur rather frequently and such interactions may contribute to the durability of this class of resistance genes in wheat (Dyck 1987; Hiebert et al. 2011; Herrera-Foessel et al. 2011).

Notes

Acknowledgments

We thank Xiaodi Xia and Sutha Chandramohan for their excellent technical assistance. We acknowledge support from Grains Research Development Corporation (GRDC) which is co-funding rust research at CSIRO. We thank Dr Jaroslav Dolezel, Dr Hana Simkova and Dr Catherine Feuillet, who facilitated early access to the chromosome 3B-specific BAC library and 3B physical map information, and Prof Rudi Appels for coordinating the sequencing and annotation of the BAC clones.

References

  1. Breen J, Li D, Dunn DS, Bekes F, Kong X, Zhang J, Jia J, Wicker T, Mago R, Ma W, Bellgard M, Appels R (2010) Wheat beta-expansin (EXPB11) genes: Identification of the expressed gene on chromosome 3BS carrying a pollen allergen domain. BMC Plant Biol 10:99PubMedCrossRefGoogle Scholar
  2. Brown GN (1997) The inheritance and expression of leaf chlorosis associated with gene Sr2 for adult plant resistance to wheat stem rust. Euphytica 95:67–71CrossRefGoogle Scholar
  3. Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, Schlub S, Le Paslier MC, Magdelenat G, Gonthier C, Couloux A, Budak H, Breen J, Pumphrey M, Liu S, Kong X, Jia J, Gut M, Brunel D, Anderson JA, Gill BS, Appels R, Keller B, Feuillet C (2010) Megabase level sequencing reveals contrasted organisation and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22:1686–1701PubMedCrossRefGoogle Scholar
  4. Dyck PL (1977) Genetics of leaf rust reactions in three introductions of common wheat. Can J Genet Cytol 19:711–716Google Scholar
  5. Dyck PL (1987) The association of a gene for leaf rust resistance with the chromosome 7D suppressor of stem rust resistance in common wheat. Genome 29:467–469CrossRefGoogle Scholar
  6. Dyck PL, Samborski DJ (1982) The inheritance of resistance to Puccinia recondita in a group of common wheat cultivars. Can J Genet Cytol 24:273–283Google Scholar
  7. German SE, Kolmer JA (1992) Effect of gene Lr34 in the enhancement of resistance to leaf rust of wheat. Theor Appl Genet 84:97–105CrossRefGoogle Scholar
  8. Hare RA, McIntosh RA (1979) Genetic and cytogenetic studies of durable adult-plant resistances in Hope and related cultivars to wheat rusts. Z Planzenzücht 83:350–367Google Scholar
  9. Herrera-Foessel SA, Lagudah ES, Huerta-Espino J, Hayden MJ, Bariana HS, Singh D, Singh RP (2011) New slow-rusting leaf rust and stripe rust resistance genes Lr67 and Yr46 in wheat are pleiotropic or closely linked. Theor Appl Genet 122:239–249PubMedCrossRefGoogle Scholar
  10. Hiebert CW, Thomas JB, McCallum BD, Humphreys DG, DePauw RM, Hayden MJ, Mago R, Schnippenkoetter W, Spielmeyer W (2010) An introgression on wheat chromosome 4DL in RL6077 (Thatcher*6/PI250413) confers adult plant resistance to stripe rust and leaf rust (Lr67). Theor Appl Genet 121:1083–1091PubMedCrossRefGoogle Scholar
  11. Hiebert CW, Fetch TG, Zegeye T, Thomas JB, Somers DJ, Humphreys DG, McCallum BD, Cloutier S, Singh D, Knott DR (2011) Genetics and mapping of seedling resistance to Ug99 stem rust in Canadian wheat cultivars ‘Peace’ and ‘AC Cadillac’. Theor Appl Genet 122:143–149PubMedCrossRefGoogle Scholar
  12. Kolmer JA, Garvin DF, Jin Y (2011) Expression of a Thatcher wheat adult plant stem rust resistance QTL on chromosome 2BL is enhanced by Lr34. Crop Sci 51:526–533Google Scholar
  13. Kota R, Spielmeyer W, McIntosh RA, Lagudah ES (2006) Fine genetic mapping fails to dissociate durable stem rust resistance gene Sr2 from pseudo-black chaff in common wheat (Triticum aestivum L.). Theor Appl Genet 112:492–499PubMedCrossRefGoogle Scholar
  14. Krattinger SG, Lagudah ES, Spielmeyer W, Singh R, 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 323:1360–1363PubMedCrossRefGoogle Scholar
  15. Lillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM, He ZH, Bjornstad A (2008) The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theor Appl Genet 116:1155–1166PubMedCrossRefGoogle Scholar
  16. Mago R, Spielmeyer W, Lawrence GJ, Ellis JG, Pryor A (2004) Resistance genes for rye stem rust (SrR) and barley powdery mildew (Mla) are located in syntenic regions on short arm of chromosome 1. Genome 47:112–121PubMedCrossRefGoogle Scholar
  17. Mago R, Simkova H, Brown-Guedira G, Dreisigacker S, Breen J, Jin Y, Singh R, Appels R, Lagudah ES, Ellis J, Dolezel J, Spielmeyer W (2011) An accurate DNA marker assay for stem rust resistance gene Sr2 in wheat. Theor Appl Genet 122:735–744PubMedCrossRefGoogle Scholar
  18. McFadden ES (1930) A successful transfer of emmer characters to vulgare wheat. J Am Soc Agron 22:1020–1034Google Scholar
  19. McFadden ES (1939) Brown necrosis, a discolouration associated with rust infection in certain rust resistant wheats. J Agric Res 58:805–819Google Scholar
  20. McIntosh RA, Park RF, Wellings CR (1995) Wheat rusts: an atlas of resistance genes. CSIRO Publications, AustraliaGoogle Scholar
  21. Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Berges H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of 1 Gigabase bread wheat chromosome 3B. Science 322:101–104PubMedCrossRefGoogle Scholar
  22. Pretorius ZA, Pienaar L, Prins R (2007) Greenhouse and field assessment of adult plant resistance in wheat to Puccinia striiformis f. Sp. Tritici. Aust Plant Pathol 36:552–559CrossRefGoogle Scholar
  23. Šafář J, Bartoš J, Janda J, Bellec A, Kubaláková M, Valárik M, Pateyron S, Weiserová J, Tušková R, Číhalíková J, Vrána J, Šimková H, Faivre-Rampant P, Sourdille P, Caboche M, Bernard M, Doležel J, Chalhoub B (2004) Dissecting large and complex genomes: flow sorting and BAC cloning of individual chromosomes from bread wheat. Plant J 39:960–968PubMedCrossRefGoogle Scholar
  24. Singh RP, McIntosh RA (1984a) Complementary genes for reaction to Puccinia recondita tritici in Triticum aestivum I. Genetic and linkage studies. Can J Genet Cytol 26:723–735Google Scholar
  25. Singh RP, McIntosh RA (1984b) Complementary genes for reaction to Puccinia recondite tritici in Triticum aestivum II. Cytogenetic studies. Can J Genet Cytol 26:736–742Google Scholar
  26. 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 48:567–573CrossRefGoogle Scholar
  27. Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005) Powdery mildew resistance is associated with durable leaf rust and stripe rust resistance genes Lr34/Yr18 and maps to a single locus on the short arm of chromosome 7D of wheat. Theor Appl Genet 111:731–735PubMedCrossRefGoogle Scholar
  28. Spielmeyer W, Singh RP, McFadden H, Wellings CR, Huerta-Espino J, Kong X, Appels R, Lagudah ES (2008) Fine scale genetic and physical mapping using interstitial deletion mutants of Lr34/Yr18: a disease resistance locus effective against multiple pathogens in wheat. Theor Appl Genet 116:481–490PubMedCrossRefGoogle Scholar
  29. Stakman EC, Stewart DM, Loegring WQ (1962) Identification of physiologic races of Puccinia graminis var tritici. Agricultural Research Service E617 United States Department of Agriculture, WashingtonGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • R. Mago
    • 1
  • L. Tabe
    • 1
  • R. A. McIntosh
    • 2
  • Z. Pretorius
    • 5
  • R. Kota
    • 1
  • E. Paux
    • 4
  • T. Wicker
    • 3
  • J. Breen
    • 6
  • E. S. Lagudah
    • 1
  • J. G. Ellis
    • 1
  • W. Spielmeyer
    • 1
  1. 1.CSIRO Plant IndustryCanberraAustralia
  2. 2.University of Sydney Plant Breeding Institute CobbittyCamdenAustralia
  3. 3.Institute of Plant BiologyUniversity of ZurichZurichSwitzerland
  4. 4.Institut National de la Recherche Agronomique, Universite Blaise Pascal, Unite Mixte de Recherche 1095 Genetics Diversity and Ecophysiology of CerealsClermont-FerrandFrance
  5. 5.Department of Plant SciencesUniversity of the Free StateBloemfonteinSouth Africa
  6. 6.Centre for Comparative GenomicsMurdoch UniversityMurdochWestern Australia

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