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Molecular mapping of stripe rust resistance gene YrSN104 in Chinese wheat line Shaannong 104 Muhammad Azeem Asad1, Xianchun Xia1, Chengshe Wang2 and Zhonghu He1,3 Institute of Crop Science, National Wheat Improvement Center/The National Key Facility for Crop Gene Resources and Genetic Improvement, Chinese Academy of Agricultural Sciences (CAAS), Beijing, PR China 2 College of Agronomy, Northwest Sci-Tech University of Agriculture and Forestry, Yangling, Shaanxi, PR China 3 International Maize and Wheat Improvement Center (CIMMYT) China Office, c/o CAAS, Beijing, PR China 1
Asad, M. A., Xia, X.-C., Wang, C.-S. and He, Z.-H. 2012. Molecular mapping of stripe rust resistance gene YrSN104 in Chinese wheat line Shaannong 104. – Hereditas 149: 146–152. Lund, Sweden. eISSN 1601-5223. Received 7 February 2012. Accepted 26 June 2012. Stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a serious yield-limiting factor for wheat production worldwide. The objective of this study was to identify and map a stripe rust resistance gene in wheat line Shaannong 104 using SSR markers. F1, F2 and F3 populations from Shaannong 104/Mingxian 169 were inoculated with Chinese Pst race CYR32 in a greenhouse. Shaannong 104 carried a single dominant gene, YrSN104. Six potential polymorphic SSR markers identified in bulk segregant analysis were used to genotype F2 and F3 families. YrSN104 was closely linked with all six SSR markers on chromosome 1BS with genetic distances of 2.0 cM (Xgwm18, Xgwm273, Xbarc187), 2.6 cM (Xgwm11, Xbarc137) and 5.9 cM (Xbarc240). Pedigree analysis, pathogenicity tests using 26 Pst races, haplotyping of associated markers on isogenic lines carrying known stripe rust resistance genes, and associations with markers suggested that YrSN104 was a new resistance gene or an allele at the Yr24/Yr26 locus on chromosome 1BS. Deployment of YrSN104 singly or in combination to elite genotypes could play an effective role to lessen yield losses caused by stripe rust. Zhonghu He, Inst. of Crop Science, National Wheat Improvement Center/The National Key Facility for Crop Gene Resources and Genetic Improvement, Chinese Academy of Agricultural Sciences (CAAS), 12 Zhongguancun South Street, CN-100081 Beijing, PR China. E-mail:
[email protected]
Stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is an important fungal disease of wheat worldwide. It causes significant yield losses in areas with cool and high altitude climates (Roelf et al. 1992; Singh et al. 2000). China is the largest epidemiological region for stripe rust in the world (Stubbs 1988) extending across winter and spring growing areas (Chen et al. 2009). During the last decade, a total of 15.6 million ha was damaged by Pst races CYR32 and CYR33 (Kang et al. 2010). Stripe rust can be controlled by fungicides, but their use is expensive and potentially hazardous to human health and the environment. A more economic and environmentally friendly approach is to grow stripe rust resistant cultivars to control the disease and reduce yield losses. Many resistance genes have been identified in common wheat and its relatives such as Secale cereale and Dasypyrum villosum (McIntosh 1992; Cao et al. 2008). So far, 52 stripe rust resistance genes (Yr1Yr49) have been mapped and catalogued on different chromosomes in wheat ( www.shigen.nig.ac.jp/wheat/ komugi/genes/symbolClassList.jsp ). These resistance genes can be categorized into three groups; seedling resistance genes or major genes or all stage resistance genes (Yr1–10, Yr15, Yr17, Yr19–Yr28, Yr31–Yr35,
Yr37–38, Yr40–45, Yr47), adult plant resistance (APR) genes express at adult plant stage (Yr18, Yr29, Yr30, Yr46, Yr48, Yr49), and high temperature adult plant resistance genes (HTAP) express as plant grow older and weather becomes warmer (Yr11–Yr14, Yr16, Yr36, Yr39) (Chen 2005; Lin and Chen 2007, 2009). Despite the formally designated major resistance genes (Yr1–Yr49), 41 temporarily major stripe rust resistance genes have also been identified and mapped on different chromosomes of wheat ( www.shigen.nig.ac.jp/wheat/komugi/genes/ symbol ClassList.jsp ). Most of the seedling resistance genes are presently not effective in wheat due to evolution of new virulent pathogenic races (Kang et al. 2010), whereas, the adult plant resistance genes such as Yr18 and Yr29 are more durable and long lasting to sustain and combat new virulent races (Krattinger et al. 2009). Because of the transient effectiveness of race-specific resistance various strategies such as gene pyramiding (Watson and Singh 1952), multiline cultivars (Browning and Frey 1969; Borlaug 1981) and cultivar mixtures (Wolfe et al. 1981) were proposed as ways to prolong the period of effectiveness, or to buffer potential losses to new races (McIntosh and Lagudah 2000). Most stripe rust resistance genes are ineffective against currently
© 2012 The Authors. This is an Open Access article. DOI: 10.1111/j.1601-5223.2012.02261.x
Hereditas 149 (2012) predominant races in China (Kang et al. 2010). Ongoing identification and use of new resistance genes are needed to sustain resistance. Molecular markers made it easier to identify new resistance genes. During the last decade, stripe rust resistance genes have been mapped on various wheat chromosomes, including Yr18 (Suenaga et al. 2003), YrC591 (Li et al. 2009), Yr45 (Li et al. 2011), Yr46 (Herrera-Foessel et al. 2011) and Yr48 (Lowe et al. 2011). Molecular markers are economical and efficient in locating genes and potentially useful for gene pyra miding. Cox et al. (1993) successfully pyramided three leaf rust resistance genes Lr41, Lr42 and Lr43 into common wheat. Santra et al. (2006) pyramided two single dominant genes Yr5 and Yr15 against stripe rust races found in North America. Liu et al. (2000) pyramided three powdery mildew resistance gene combinations, Pm2 Pm4a, Pm2 Pm21, Pm4a Pm21 into an elite wheat cultivar Yang158. Revathi et al. (2010) pyramided two leaf rust (Lr24, Lr28) and one stripe rust resistance gene Yr15 in bread wheat variety HD2877. Currently, SSR markers are extensively used in mapping and tagging genes, marker assisted selection, and gene pyramiding in wheat. Shaannong 104, a high yielding winter wheat developed from Shaannong 757/Shaannong 229//1-5/1187 at Northwest Sci-Tech University of Agriculture and Forestry, is highly resistant to stripe rust at the seedling stage in the greenhouse and in the field with 0 to 0; infection type. The objectives of our study were to map potential stripe rust resistance genes in Shaannong 104 and to identify tightly linked SSR markers that can be used for marker assisted selection in breeding programs. MATERIAL AND METHODS Plant material For characterization of the resistance gene in wheat cultivar Shaannong 104, which was selected from Shaannong 757/Shaannong 229//1-5/1187, a mapping population developed by crossing it with the highly susceptible cultivar Mingxian 169. Seedling tests were conducted in a greenhouse. Shaannong 104, Mingxian 169, 15 F1 plants, 613 F2 plants and 55 F3 families were included in the study. Pst race CYR32 was provided by the College of Plant Protection, Northwest Sci-Tech University of Agriculture and Forestry, Yangling, Shaanxi. Fresh uredospores of CYR32 were multiplied by propagation on seedlings of Mingxian 169. Lines with known genes present in a common back ground are important to make a comparison with new identified genes for genetic tests. Near isogenic lines in Avocet S (Australian spring wheat Avocet selection, semi dwarf displays a degree
Molecular mapping of stripe rust resistance gene 147 of cold requirement, but is insensitive to day length) background carrying different stripe rust resistance genes Yr9, Yr10, Yr15, Yr24, Yr26 were used in the present genetic investigation. Seedling test with PST race CYR32 Seedlings of the parents, F1, F2 and F3 populations were grown in the greenhouse. Fifteen seeds, along with three seeds of Mingxian 169 as a check, were planted in each pot. Seedlings were inoculated with Pst when first leaves were fully emerged. After inoculation, the seedlings were placed in plastic covered boxes and incubated at 9–11°C and 100% RH for 24 h in darkness. Seedlings were then grown in a 16 h photoperiod (22 000 lux) at 13–17°C and 70% RH. Infection types (IT) were scored two weeks after inoculation when pustules were fully developed on the susceptible check. ITs on individual plants were recorded on a 0–4 scale (Bariana and McIntosh 1993), and were then categorized into two easily distinguished resistant and susceptible classes. Plants with ITs 0; to 2, and 3 to 4 were considered as resistant and susceptible, respectively. After disease scoring, the fresh second or third leaf was selected for DNA extraction. The 4–5 cm leaf of each F2 plant was put into 2 ml eppendorf tube separately. Small portion of leaf from 30 plants of each F3 family were cut together and put into 2 ml eppendorf tube for DNA extraction. SSR analysis Genomic DNA was extracted from newly developed second and third leaves after scoring of disease resistance using the CTAB protocol (Sharp et al. 1988). Each F2 plant was individually sampled for DNA extraction, whereas DNA from F3 families was extracted from bulked tissue from 30 plants. Extracted DNA was quantified on agarose gels. Resistant and susceptible bulks for bulked segregant analysis (Michelmore et al. 1991) comprised equal amounts of DNA from 10 resistant and 10 susceptible F2 plants, respectively. In total, 1528 pairs of wheat SSR primers including 382 pairs of BARC (Beltsville Agriculture Research Station) primers (Song et al. 2000), 240 pairs of GWM (Gatersleben Wheat Microsatellite) primers (Röder et al. 1998), 640 pairs of WMC (Wheat Microsatellite Consortium) primers (Gupta et al. 2003), 144 pairs of CFD (Clermont Ferrand D-genome) primers (Guyomarc’h et al. 2002), 64 pairs of GDM (Gatersleben D-genome Microsatellite) primers (Pestsova et al. 2000), and 58 pairs of CFA (Clermont Ferrand A-genome) primers (Sourdille et al. 2004) were screened on the parents, and bulks. PCR were conducted in volumes of 15 ml containing 1.0 U Taq DNA polymerase and 1.5 ml 10 Taq reaction buffer (50 mmol KCl, 10 mmol tris–HCl, 1.5 mM MgCl2, pH 8.3) (Beijing Huitian Dongfang Sci.
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and Tech. Co., Ltd.), 200 mM of each dNTP (Beijing Biodee Biotechnology Co., Ltd.), 6 pmol of each primer and 80 ng of template DNA. The DNA amplifications were carried out under the following conditions: denaturation at 94°C for 5 min, followed by 35 cycles of 94°C for 1 min, 55–61°C (depending on primers) for 1 min, 72°C for 1 min per cycle, and a final extension for 10 min at 72°C in a thermal cycler (Mycycler, Bio-RAD, USA). After amplification, PCR products were denatured by adding 3 ml of loading buffer (98% formamide, 10 mM EDTA, 0.25% bromophenol blue, 0.25% xylene cynol, pH 8.0) at 95°C for 5 min. PCR products were separated by electrophoresis in 6% denaturing polyacrylamide gels at 80W for approximately 90 min and bands were visualized by silver staining (Bassam et al. 1991). Statistical analysis and genetic linkage mapping The phenotypic and genotypic data were statistically analyzed by c2-tests for goodness of fit of observed to expected ratios. Linkage values determined using
Mapmaker 3.0 (Lincoln et al. 1992) were converted to map distances (cM) by the Kosambi function (Kosambi 1944) and LOD scores of 3.0 were used as thresholds for the declaration of linkage. The genetic linkage map was drawn with Mapdraw V2.1 (Liu and Meng 2003). RESULTS Pathogenicity of 26 Pst isolates or races on Shaannong 104 and lines with resistance genes on chromosome 1B Shaannong 104 was highly resistant to 26 Pst isolates or races, including the prevailing CYR32 (Li et al. 2006b, Table 1). Shaannong 104 (YrSN104) and Yr15/6 Avocet S (Yr15) were resistant to all 26 races whereas Yr24/3 Avocet S (Yr24) and Yr26/3 AvocetS (Yr26) showed the same seedling reactions except with isolate 75078 from Egypt (Table 1). YrSN104 was resistant (IT 0;), whereas Yr24 and Yr26 were moderately resistant or susceptible IT 2 and 2-3, respectively, against Pst isolate 75078.
Table 1. Infection types of wheat genotypes to 26 international and Chinese isolates or races of Puccinia striiformis f. sp. tritici.
Isolate 58893 59791 60105 61009 68009 72107 74187 75078 76088 76093 78028 78080 80551 82061 82517 85019 86036 86094 86106 86107 PE92 CYR 26 CYR 27 CYR 29 CYR 32 CYR-Su-1
Origina
Clement Yr9 Yrcle
Moro Yr10 YrMor
Yr15/6 Avocet S Yr15
Yr24/3 Avocet S Yr24
Netherlands Netherlands Germany Netherlands Netherlands Ecuador Egypt Afghanistan Pakistan Israel Mexico Netherlands Chile France Chile Bolivia Kenya Ethiopia Ethiopia Italy China China China China China
0 0; 0, 0; 0 0 0 0 0 0 0 0 0 4 4 0; 0; 0 3 0 4 0 0 0 4 4 0;
0, 0; 0 0 0 0 4 0 3, 4 0 0 0 0 0 0 0 0 0, 0; 0; 0 0, 0; 0; 0 0; 0 0 0
0 0 0 0; 0; 0 0 0 0 0 0 0 0 0; 0 0 0 0 0 0 0 0 0; 0 0, 0; 0
0; 0; 1 0; 0; 0; 0; , 1 0; 2 0 0; 1 0; 0; 0; 0; 0; 0; 0; 0; 1 0; 0; 0; 0 0; 0; 0; 0
information from our previous study (Li et al. 2006b). a
Yr26/3 Avocet S Yr26 0; 0, 1 0; 0; 0; 0; , 1 0; 2, 3 0; 0; 0; 0; 0; 0; 0; 0, 1 0; 0; 0; 0; 0; 0; 0; 0; 0; 0, 0;
Shaannong 104 YrSN104
Mingxian 169
0; 0, 0; 0; 0; 0; 0 0 0; 0 0 0 0; 0; 0 0 0; 0 0 0, 0; 0, 0; 0 0 0 0 0 0
4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4
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Molecular mapping of stripe rust resistance gene 149
Inheritance of stripe rust resistance in Shaannong 104 Shaannong 104 was resistant with IT 0; whereas Mingxian 169 was susceptible with IT 4. All 15 F1 plants were resistant with IT 0;-2. The F2 population segregated 449 plants resistant (IT 0;-2) and 164 susceptible (IT 3-4), a single gene ratio (c23:1 1.00, P1df 0.32). The F3 families segregated 19 homozygous resistant: 24 segregating: 12 homozygous susceptible confirming the single gene hypothesis (c21:2:1 2.67, P2df 0.26) (Table 2). The resistance gene in Shaannong 104 was designated as YrSN104. Linkage analysis and genetic map of YrSN104 A total of 1528 SSR primer pairs were screened on the resistant and susceptible parents; 187 were polymorphic. In bulked segregant analysis, six co-dominant markers, Xgwm11, Xgwm18, Xgwm273, Xbarc137, Xbarc187 and Xbarc240, located on chromosome 1B, were iden tified as potentially linked to the resistance locus as they have expressed the same bands for Shaannong 104 and resistant bulk, and Mingxian 169 and susceptible bulk. When these markers were tested on a sample of the segregating F2 population, most of the resistant and susceptible plants showed the same DNA fragments as the resistant and susceptible parents and bulks, respectively. All 613 F2 plants were then screened with the six markers. Based on linked markers, linkage analysis indicated that markers were 2.0 to 5.9 cM from the resistance locus (Fig. 1). Based on, phenotypic evaluation and subsequent genotyping of 55 F3 families with linked SSR markers, linkage analysis showed that YrSN104 was linked to six loci with genetic distance ranging from 2.0 to 5.9 cM. The closely linked markers were Xgwm18 and Xgwm273, and Xbarc187 with genetic distances 2.0 and 2.6 cM, respectively. Allelic comparison of YrSN104 with other genes on chromosome 1B The allelic comparison of YrSN104 (Shaannong 104) with other stripe rust resistance genes previously mapped Table 2. Segregation of stripe rust reactions to CYR 32 in F1, F2, and F3 progeny of Mingxian169/Shaannong104. Observed no. of plants/lines Plant material
Res.
0 Mingxian 169 P1 Shaannong 104 P1 15 F1 15 F2 449 F3 19
Seg. Sus. 0 0 0 – 24
15 0 0 164 12
Expected ratio
3:1 1:2:1
c2
P
1.00 0.32 2.67 0.26
Fig. 1. Linkage map of YrSN104 linked to six SSR markers on chromosome 1BS using F3 families. Loci names and corres ponding locations on the genetic map are indicated on the right side. Map distances are shown on the left side.
to the same chromosome was carried out with linked SSR markers Xgwm273 and Xgwm18 using near-isogenic lines (NILs) with Yr9 (Yr9/6 Avocet S), Yr10 (Yr10/6 Avocet S), Yr15 (Yr15/6 Avocet S), Yr24 (Yr24/3 Avocet S) and Yr26 (Yr26/3 Avocet S). Electrophoresis of PCR products in 6% polyacrylamide gels revealed that allele at YrSN104 is likely to be different from those in the NILs at the SSR markers (Fig. 2). DISCUSSION Stripe rust is a more serious threat than other diseases to wheat production in temperate regions of the world. Shaannong 104 is resistant to the predominant Chinese P. striiformis race CYR32. Genetic and molecular analyses showed that the resistance conferred by YrSN104 is located on chromosome 1B. Close linkage with markers Xgwm18 and Xgwm273 suggested that YrSN104 is present on the short arm based on locations of the markers provided in http://wheat.pw.usda.gov/cgi-bin/ graingenes . Several stripe rust resistance genes are already mapped on chromosome 1B, viz. Yr10, Yr15, Yr21, Yr24, Yr26, Yr29, YrH52, and YrCH42 (Lin and Chen 2008). Yr10, Yr15, Yr24, Yr26, YrH52, and YrCH42 are located on short arm, whereas Yr21 and Yr29 are on long arm. Cappelle-Desprez with Yr3a, Hybrid 46 with Yr3b, Vilmorin 23 with Yr3c, Clement and Lovrin 10 with Yr9,
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Fig. 2A–B. Electrophoresis of PCR products amplified with SSR markers GWM273 (A) and GWM18 (B) linked with the resistance gene YrSN104. The critical bands (as indicated by arrows) in Shannong 104 and the resistant bulk, were not present in Mingxian 169 and the susceptible bulk or any of the NILs. Arrows on the left side indicate the fragment sizes of ladders. M pUC18 DNA/Mspl, YrSN104 resistance gene in Shaannong 104, Ps susceptible parent, Br resistant bulk, Bs susceptible bulk, Near isogenic lines with Yr9, Yr10, Yr15, Yr24 and Yr26.
Lehmi with Yr21 and a Lalbahadur line with Yr29 are susceptible to race CYR32, whereas Yr29 confers nonrace specific adult plant resistance (William et al. 2003). Therefore, YrSN104 cannot be any of these genes. Resistance genes Yr10 (Wang et al. 2002), Yr15 and YrH52 (Peng et al. 1999, 2000), Yr24 (Liu et al. 2005) and Yr26 (Ma et al. 2001, Wang et al. 2008) are effective against CYR32 in China. Infection type studies on lines with Yr24 and Yr26 using 26 different Pst isolates showed that YrSN104 is resistant to all the isolates whereas Yr24 or Yr26 was moderately resistant or susceptible to isolate 75078 from Egypt (Table 1). Pedigree analysis indicated that Yr10 was derived from Triticum aestivum, Yr15 and YrH52 from T. dicoccoides, and Yr24, Yr26 and YrCH42 (Li et al. 2006a) from T. turgidum, respectively, whereas YrSN104 was derived from T. aestivum. Pedigree information suggested that the source of YrSN104 was different from previously mapped genes on chromosome 1B. Different alleles of markers Xgwm273 and Xgwm18 are present in Shaannong104 (YrSN104) compared with Avocet isogenic lines carrying Yr15, Yr24 and Yr26 (Fig. 2). This suggests that YrSN104 may be a different allele at the Yr24/Yr26 locus. Although the stripe rust resistance genes have been identified in wheat wild relatives, it is relatively difficult to incorporate these genes directly into other elite genotypes due to their inferior agronomic traits. In contrast, genes derived from common wheat are more convenient to transfer into new cultivars. YrSN104, derived from common wheat line Shaannong104 with good agronomic traits, can be used in wheat breeding programs
and identified linked molecular markers should expedite its use in targeting stripe rust resistance. The present study concludes that YrSN104, a single dominant gene located on chromosome 1BS against prevailing Pst race CYR32, may be a new seedling stripe rust resistance gene or allelic to Yr24/Yr26, and indentified linked molecular markers can be significant to exploit and utilize in marker assisted wheat breeding program for disease resistance. Further studies are needed to narrow down the genetic distance and identify additional mole cular markers distal to target gene such as RGA, EST or STS markers or by comparative genetic studies. Acknowledgements – This study was supported by the International Collaboration Project from the Ministry of Agriculture (2011-G3), National Science Foundation of China (30821140351 and 30671294), and China Agriculture Research System (CARS-3-1-3).
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