Euphytica 71 : 1 0 7-113,1993 .© 1993 Kluwer Academic Publishers . Printed in the Netherlands.

Inheritance of stripe rust (yellow rust) resistance in the wheat cultivarCarstens V

Xianming Chen & Roland F Line'Department of Plant Pathology, Washington State University and US . Department of Agriculture, AgriculturalResearch Service, Pullman, WA 99164-6430, USA;' PPNS 0148, College of Agriculture and Home EconomicsResearch Center, Project 3694, Washington State University, Pullman, WA 99164, USA

Received 13 April 1993 ; accepted 8 September 1993

Key words : Puccinia striiformis, resistance genes, stripe rust, Triticum aestivum, wheat, yellow rust

Summary

Carstens V, one of the wheat cultivars used to differentiate races of Puccinia striiformis (stripe rust or yellowrust) in Europe, was crossed with stripe rust susceptible cultivars and cultivars with genes for resistance to thedisease to determine the genetic basis of its stripe rust resistance . Seedlings of the parents and F,, F 2 , and F,progeny were evaluated for resistance to North American races of P striiformis. Based on those evaluations,Carstens V has three genes for resistance to North American race CDL-21, two genes for resistance to racesCDL-17, CDL-20, and CDL-29, and one gene for resistance to race CDL-27 . The genes that confer resistanceto race CDL-17 also confer resistance to race CDL-21 . The three genes were either dominant or recessivedepending upon the race used in the test and the cultivar used in the cross . None of the genes in Carstens V arethe same as the genes for resistance in Cappelle Desprez, Chinese 166, Clement, Compair, Heines Peko,Hybrid 46, Minister, Nord Desprez, Triticum spelta album, and Vilmorin 23 .

Introduction

The wheat cultivar Carstens V, which is used to dif-ferentiate races of Puccinia striiformis Westend. inEurope (Johnson et al ., 1972; Stubbs, 1985), is resist-ant to many European and North American racesof the stripe rust pathogen (Stubbs, 1985 ; de Valla-vieille-Pope & Line, 1990) . The genetic basis of re-sistance in Carstens V has not been studied . Under-standing the genetics of resistance should be helpfulfor exploiting the resistance in gene deployment,gene rotation, gene pyramiding, and multiline de-velopment, as well as in understanding the geneticbasis for virulence in stripe rust races . This studywas conducted to determine the number of genescontrolling the stripe rust resistance of Carstens V,

the mode of inheritance for the genes, and the rela-tionship of the genes in Carstens V to previouslyidentified genes in Cappelle Desprez, Chinese 166,Clement, Compair, Heines Peko, Hybrid 46, Minis-ter, Nord Desprez, Triticum spelta album, and Vil-morin 23 .

Materials and methods

Carstens V was crossed in a greenhouse with Cap-pelle Desprez, Chinese 166, Clement, Compair,Heines Peko, Hybrid 46, Minister, Nord Desprez,Triticum spelta album, and Vilmorin 23, wheat culti-vars with identified genes for stripe rust resistance,and with Michigan Amber (Table 1) . The F, seed

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and 105 F3 families from randomly selected FZ plantsfor Carstens V/Chinese 166 were obtained fromfield grown plants .

To test plants for resistance, seed of parents andF,, F2, and F 3 progeny were planted in plastic potsfilled with a potting mixture of peat, perlite, sand,Palouse silt loam soil, and vermiculite in a ratio of6 : 2 : 3 : 3 : 4. Lime, Osmocote 14-14-14, and ammo-nium nitrate were added at 1 .69, 3 .30, and 2 .20 g/L,respectively. About 10 seeds were planted in eachpot. The seedlings were grown in a rust-free green-house at a diurnal temperature cycle of 10-25° C .

When the plants were at the two-leaf stage, theywere uniformly inoculated with urediospores of aspecific test race, placed in a dew chamber at 10° Cfor 24 hours, and then placed in a greenhouse cham-ber at a diurnal temperature cycle that graduallychanged between 4° C at 2 a.m. to 20° C at 2 p.m . .The light period consisted of daylight supplement-ed with metal halide lights to extend the duration oflight to 16 hours . Seedlings of the parental cultivarsand F, and F2 progeny were tested with the samerace at the same time. For each cross, 8 to 20 paren-tal plants, 3 to 5 F, plants, and 236 to 609 F 2 plantswere evaluated depending upon the cross and race .

For each of the 105 F 3 families from Carstens V/Chi-nese 166,14 to 44 plants were evaluated dependingupon the individual families .

Five North American races (Table 1) that wereavirulent on Carstens V, virulent on Michigan Am-ber, and differed for virulence on the other cultivars(Line & Qayoum, 1991; de Vallavieille-Pope & Line,1990) were used to test the parents and progeny .Each race was originally purified by single sporeisolation or by transferring single pustules for sev-eral generations . Either freshly collected spores orspores that had been stored at 4° C for less than onemonth were used for all tests. To prevent mixing ofraces, the inoculum of each race was increased onplants within isolation booths, and when possible,maintained on cultivars that were susceptible tothat specific race but resistant to the other races .Races that were virulent on common cultivars wereincreased in separate facilities at different periodsof time. For each test of parents and progeny, the 13North American differential cultivars were also in-oculated to check the purity of the test race .

Infection types produced by the host-pathogeninteraction were recorded when uredia were fullydeveloped on the susceptible cultivars (18-21 days

Table 1. Stripe rust resistance genes in wheat cultivars used to study the genetics of resistance in Carstens V, and the reaction of Carstens Vand the cultivars to North American Cereal Disease Laboratory (CDL) races of Puccinia striiformis

CI = Crop Index number, PI = Plant Identification number, and WA = Washington State number .Yr genes designated by numbers have been previously named and Yr genes designated by letters are provisional gene designations

(Chen & Line, 1992a, 1992b, 1992c, 1993 ; Lupton & Macer,1962 ; McIntosh, 1983 ; Singh & Johnson, 1988) .R = resistant, I = intermediate, and S = susceptible. See Line & Qayoum (1991) and de Vallavieille-Pope & Line (1990) for differential

response to the races .

Identificationnumber'

Cultivar Genes forresistance'

Reaction to North American races`

CDL-17 CDL-20 CDL-21 CDL-27 CDL-29

PI 191311 Carstens V R R R R RPI 315203 Michigan Amber S S S S SCI 011765 Chinese 166 Yrl S R S R RPI 180620 Heines Peko Yr2,Yr6 R R R S RPI 262223 Cappelle Desprez Yr3a,Yr4a R R R R RPI 167419 Nord Desprez Yr3a,YrND R S R R RPI 201196 Minister Yr3c,YrMin R S R R RPI 125093 Vilmorin 23 Yr4a,YrV23 I S R I IPI 164755 Hybrid 46 Yr4b,YrH46 R R R R RWA 005768 Triticum spelta album Yr5 R R R R RPI 325842 Compair Yr8,YrCom R R R R RWA 007716 Clement Yr9,YrCle R R R R R

after inoculation) . Infection types 0, 1, 2, 3, 5, and 8were recorded using the 0-9 Infection type scaleand the concept of basic and expanded scales de-scribed by Line et al. (1970) . Infection types 0, 1, 2,and 3 were classified as resistant and infection type8 was classified as susceptible . Infection type 5 wasconsidered as resistant or susceptible dependingupon the cross . Chi-square tests were used to deter-mine the goodness of fit of the segregation ratios . F3data from Carstens V/Chinese 166 were analyzedseparately for resistance to races CDL-17 andCDL-21 and jointly to determine the relationship ofthe gene or genes for resistance to both raceCDL-17 and race CDL-21 .

Results and discussion

Number of stripe rust resistance genes . To determinethe number of resistance genes in Carstens V, prog-eny from Carstens V/Chinese 166 were tested withraces CDL-17 and CDL-21, Carstens V/MichiganAmber were tested with races CDL-17, CDL-20,CDL-21, CDL-27, and CDL-29, and Carstens V/Minister were tested with race CDL-20. The infec-tion types of parents and the F, progeny, the observ-ed and expected F2 ratios, and chi-square tests forgoodness of fit are shown in Table 2 .

Table 2. Infection types of Parents and F, progeny, observed and expected F2 segregation ratios, and chi-square tests for goodness of fit forF2 progeny from crosses of Carstens V with susceptible cultivars when inoculated with North American Cereal Disease Laboratory(CDL) races of Puccinia striiformis

Cross'

CDL race

Infection type

P, P, P, P, F,

The F2 segregation ratios for Carstens V/Michi-gan Amber indicate that there are three dominantgenes for resistance to race CDL-21, two comple-mentary recessive genes for resistance to racesCDL-17, CDL-20, and CDL-29, and one recessivegene for resistance to race CDL-27. The genes forresistance to races CDL-17, CDL-20, and CDL-29may be the same and possibly also the same as twoof the three genes conferring resistance to raceCDL-21. The F2 segregation ratios for Carstens V/Chinese 166 indicate that there are two dominantgenes and one recessive gene for resistance to raceCDL-21 and one dominant and one recessive genewith complementary interaction for resistance torace CDL-17 . The F Z segregation ratio from Car-stens V/Minister also indicates that Carstens V hastwo genes for resistance to race CDL-20 . The num-ber of genes detected from the crosses of CarstensV with Michigan Amber, Chinese 166 and Ministerare in agreement, but some of the ratios are differ-ent, which indicate that the gene expression can beinfluenced by genetic background .When F 3 families from Carstens V/Chinese 166

(Table 3) were tested with race CDL-17, the ratio ofresistant, segregating, and susceptible families bestfit a 1 : 8 : 7 ratio, which indicates that Carstens Vhas one dominant and one recessive gene that arecomplementary for resistance to race CDL-17, as

F2 R : S ratios'

x2

P`

Number ofgenes and

Observed

Theoretical

mode ofinheritances

P, = female parent and P2 = male parent, CV = Carstens V, C166 = Chinese 166, MA = Michigan Amber, MIN = Minister .' R =resistant and S = susceptible .P = probability of a greater value due to chance alone.

' D = dominant and R = recessive . Interpretations for some ratios can be found in Fasoulas (1981) .

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CV MA 21 1 8 1 410 : 50 57 : 7 0.00 0 .96 3DCV MA 17 2 8 8 36 :436 1 :15 1 .30 0 .25 2RCV MA 20 2-3 8 15 :378 1 :15 3 .97 0 .05 2RCV MA 29 2 8 8 27 : 300 1 :15 2 .25 0 .13 2RCV MA 27 2 8 100 : 265 1 : 3 0.99 0 .32 1 RCV C166 21 1 8 1 379 : 19 61 : 3 0.01 0 .94 2D, I RCV C166 17 2 8 8 80 : 350 3 : 13 0.01 0 .94 1 D,1 RCV MIN 20 2-3 8 8 153 : 117 9 : 7 0 .02 0 .89 2D

1 10

expected from F2 data. When the same F3 familieswere tested with race CDL-21, the ratio of resistant,segregating, and susceptible families best fit a 3726 : 1 ratio, which indicates that Carstens V has twodominant genes and one recessive gene for resist-ance to race CDL-21, as expected from F 2 data .When each of the 105 individual families were ana-lyzed (data not shown), the segregation ratios in-dicated that there are two genes for resistance torace CDL-17, but the number of plants used foreach family was too small to distinguish the expect-ed three genes segregating for resistance to raceCDL-21. When the F3 data for races CDL-17 andCDL-21 were analyzed jointly, the data best fit athree-gene model with different gene expressionsand interactions for races CDL-17 and CDL-21 .Thus, the F3 data on the number of genes for resist-ance to race CDL-17 and race CDL-21 agree withthe F2 results. The two genes for resistance to raceCDL-17 also conferred resistance to race CDL-21 .However, the expression of the genes in the F2 andF3 results (Table 2 and Table 3) varied dependingupon the race .

Table3 . Observed and expected number, expected ratio, and chi-square tests for goodness of fit of resistant, segregating and susceptibleF, families of the cross Carstens V with Chinese 166 tested with races CDL-17 and CDL-21 of Puccinia striiformis

Phenotype

Observed number

Theoretical number Theoretical ratio

Group CDL-17

CDL-21

P = probability of a greater value due to chance alone .

Relationship of Carstens V resistance genes to resist-ance genes in other cultivars . Susceptible plantswere obtained when F2 progeny from crosses ofCarstens V with Cappelle Desprez, Clement, Chi-nese 166, Compair, Heines Peko, Hybrid 46, Minis-ter, Nord Desprez, Triticum spelta album, and Vil-morin 23 were inoculated with races that were avi-rulent on both parents (Table 4 and Table 5) . Theseresults indicate that the genes in Carstens V are dif-ferent from those in the other cultivars in the cross-es .

The data from Carstens V/Hybrid 46 tested withrace CDL-21 (Table 4) indicate that there are fourgenes for resistance in the progeny. We previouslyreported that Hybrid 46 has one dominant gene forresistance to race CDL-21 (Chen & Line, 1993) . Da-ta from the present study confirmed those resultsand showed that there are three genes in Carstens Vfor resistance to race CDL-21 . The 249 : 7 ratioagrees with the 57 : 7 ratio for Carstens V/MichiganAmber tested with race CDL-21 (Table 2), whichindicates three dominant genes in Carstens V thatconfer resistance to race CDL-21 and susceptibility

x 2 P'

1 Resistant 6 6 .56 12 Segregating 49 52 .50 83 Susceptible 50 45.94 7

Total (for CDL-17) 105 105 .00 16 0 .64 0.73

1 Resistant 64 65 .02 372 Segregating 41 44 .28 263 Susceptible 0 1 .70 1

Total (for CDL-21) 105 105 .00 64 1 .96 0 .38

1 Resistant Resistant 6 6 .56 42 Segregating Resistant 32 32 .81 203 Susceptible Resistant 26 21 .33 134 Segregating Segregating 17 19.96 125 Susceptible Segregating 24 22 .97 146 Susceptible Susceptible 0 1 .64 1

Total 105 105 .00 64 3 .15 0 .68

`' P, = female parent and P, = male parent, CV = Carstens V, H46 = Hybrid 46, TSA = T spelta album, and C166 = Chinese 166 .R = resistant and S = susceptible .P = probability of a greater value due to chance alone .D = dominant and R = recessive. Interpretations for some ratios can be found in Fasoulas (1981) .

genes at two of the loci are epistatic . When the samecross was tested with race CDL-20 (Table 4), alsofour genes for resistance were detected . Since Hy-brid 46 has two genes for resistance to race CDL-20(Chen & Line, 1993), the other two genes are in Car-stens V.The FZ segregation ratio from Carstens V/Cap-

pelle Desprez tested with race CDL-20 (Table 4) in-dicates three recessive genes . We previously report-ed that Cappelle Desprez had one recessive genefor resistance to race CDL-20 (Chen & Line, 1993) .

Thus, these results indicate that Carstens V has tworecessive genes for resistance to that race, which isin agreement with the data from crosses of CarstensV with susceptible cultivars (Table 2) . However, thedata do not show the complementary interactionsas indicated in Table 2 . The results suggest thatthere are interactions between genes in Carstens Vand Cappelle Desprez .

The Fz segregation ratio from Carstens V/TT spel-ta album tested with race CDL-21 (Table 4) indi-cates that there are four dominant genes and the

Table 5. Infection types of parents and F, progeny and observed F, ratio from crosses of Carstens V with resistant cultivars when in-oculated with North American Cereal Disease Laboratory (CDL) race CDL-21 of Puccinia striiformis

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Table 4. Infection types of parents and F, progeny, observed and expected F 2 segregation ratios, and chi-square tests for goodness of fit forF 2 progeny from crosses of Carstens V with resistant cultivars when inoculated with North American Cereal Disease Laboratory (CDL)races of Puccinia striiformis

P, = female parent and P2 = male parent, CV = Carstens V, HP = Heines Peko, MIN = Minister, V23 = Vilmorin 23, CD = CappelleDesprez, COM = Compair, ND = Nord Desprez, and CLE = Clement . The other cultivars crossed with Carstens V have been reported tohave two genes for resistance to race CDL-21 (Chen & Line, 1990,1992) .n R = resistant and S = susceptible . There might be five genes in these crosses . But the number of plants were not adequate to detect fivegenes. Therefore the theoretical ratios were not tested . See the text for detail.

Cross' Infection type Observed F2 ratio'

P, P2 P, P2 F, R : s

C V HP 1 1 606 : 3CV MIN 1 0 1 486 :2C V V23 1 0 0 500 : 3CV CD 1 0 1 396 : 6CV COM 1 0 578 : 7CV ND 1 0 0 5(X) : 6CV CLE 1 0 0 499 : 8

Cross CDL race Infection type F2 R : S ratio' X2 P` Number ofgenes andmode ofinheritance'

P, P2 P, P 2 F, Observed Theoretical

CV H46 21 1 0 0 447 : 16 249 : 7 0.92 0.34 4DCV H46 20 2-3 1-2 8 53 : 214 49 :207 0.09 0.77 4RCV CD 20 2-3 2-3 160 : 122 37 : 27 0.13 0.71 3RCV TSA 21 1 0 0 338 : 9 249 : 7 0.03 0.87 4DCV TSA 29 2 0 203 : 33 55 : 9 0.00 0 .97 2R,1 DCV C166 27 2 1 8 85 : 175 5 : 11 0.25 0 .62 1D,IRCV C166 29 2 2 8 95 :218 19 : 45 0.86 0 .35 1D,2R

1 1 2

susceptibility alleles are epistatic at two of the loci .These results agree with our previous report that Tspelta album has one dominant gene (Yr5) for re-sistance to race CDL-21 (Chen & Line, 1992b) andwith data in Table 2 showing that Carstens V hasthree genes for resistance to that race . The 249 : 7ratio agrees with the results from other tests withthe same race. When tested with race CDL-29 (Ta-ble 4), the F2 segregation ratio indicates one dom-inant gene and two recessive genes. Since T speltaalbum has one dominant gene, Yr5, for resistance torace CDL-29 (Chen & Line, 1992b), the two reces-sive genes are in Carstens V.

For Carstens V/Chinese 166 (Table 4), the F 2 seg-regation ratios indicate one dominant gene and onerecessive gene for resistance to race CDL-27, andone dominant gene and two complementary reces-sive genes for resistance to race CDL-29 . Whentested with race CDL-27, the 5 : 11 ratio indicatesthat when the dominant resistance locus is hetero-zygous, resistance is ineffective. The F, data alsosupport that conclusion. Such gene interactions arealso indicated by the F2 ratio (19 : 45) and the F, in-fection type when the cross was tested with raceCDL-29. Since Chinese 166 has a dominant gene,Yrl, for resistance to races CDL-27 and CDL-29(Chen & Line, 1992a, 1992b, 1992c), Carstens V hasone gene for resistance to race CDL-27 and twogenes for resistance to race CDL-29 . These resultsagree in number of resistance genes with the F Z datafrom the Carstens V/Michigan Amber cross testedwith race CDL-27 and CDL-29. The gene for resist-ance to race CDL-27 was recessive in both CarstensV/Chinese 166 (Table 4) and Carstens V/MichiganAmber (Table 2). When tested with race CDL-29,two recessive genes were complementary, whichwas in agreement with the results of Carstens V/Mi-chigan Amber tested with the same race . The re-sults indicate that Yrl gene in the heterozygous con-dition is suppressed by a gene or genes in CarstensV.

We have previously reported that Heines Peko,Minister, Vilmorin 23, Cappelle Desprez, Compair,Nord Desprez, and Clement each have two genesfor resistance to race CDL-21 (Chen & Line, 1992a,1992b, 1992c, 1993) . Therefore, when tested withrace CDL-21, there should be five genes in the

crosses of Carstens V with these cultivars . The num-ber of plants used in each test (Table 5) were notadequate to confirm the existence of five genes . Theresults, however, do show that the genes in CarstensV are different from the genes in these cultivars .

We did not cross Carstens V with Lee, which hasYr7 and YrLee, and Moro, which has Yr10 and Yr-Mor (Chen & Line, 1992a, 1992b, 1992c; McIntosh,1983) . However, based on race-cultivar interactions(de Vallavieille-Pope & Line, 1990) and the pedi-grees (Zeven & Zeven-Hissink, 1976), we can con-clude that Carstens V does not have the genes forresistance that are in Lee and Moro . Consequently,the genes in Carstens V are different from previous-ly named Yr genes and those that have been previ-ously identified (Table 1) . We have provisionallydesignated those genes as YrCV1, YrCV2, andYrCV3. Since these genes are different from otherYr genes, they may be useful as gene sources inbreeding programs .

We can also use these results in combination withcultivar-race interactions on the differential culti-vars (de Vallavieille-Pope & Line, 1990 ; Line &Qayoum, 1991) to interpret what correspondinggenes for virulence may be in each of the races usedin this study. Race CDL-21 does not have virulencegenes corresponding to resistance genes YrCV1,YrCV2, and YrCV3 . Races CDL-17, CDL-20, andCDL-29 have a corresponding virulence gene forresistance gene YrCV1. Race CDL-27 has corre-sponding virulence genes for resistance genesYrCV1 and YrCV2 .

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