C10-12-0719.indd

2074 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, SEPTEMBER–OCTOBER 2011

RESEARCH

EGILOPS TAUSCHII Coss. is the donor of the D genome of hexa-

ploid wheat (Triticum aestivum L.; Kihara, 1944; McFadden

and Sears, 1946). The close relationship between A. tauschii and

T. aestivum has facilitated the rapid introgression of several agro-

nomically important disease traits from A. tauschii to T. ae stivum

including resistance to wheat stem rust (caused by Puccinia graminis

Pers.:Pers f. sp. tritici Eriks. & E. Henn.; Kerber and Dyck, 1979;

Gill and Raupp, 1987; Marais et al., 1998).

Recent epidemics of stem rust in eastern Africa have raised con-

cern about the resistance of currently grown wheat cultivars to new

races of P. graminis f. sp. tritici (Pgt) from Africa. In 1999, isolates of Pgt

from Uganda, reported under the race name Ug99, were found to

possess virulence to the majority of stem rust resistance genes used in

agriculture (Pretorius et al., 2000). Isolates of Ug99 as well as those

from Kenya were designated as race TTKSK based on the North

American stem rust nomenclature (Wanyera et al., 2006; Jin et al.,

2008). Race TTKSK and/or variants have spread throughout eastern

and southern Africa, Yemen, and Iran (Nazari et al., 2009; Pretorius

Stem Rust Resistance

in Aegilops tauschii Germplasm

Matthew N. Rouse, Eric L. Olson, Bikram S. Gill, Michael O. Pumphrey, and Yue Jin*

ABSTRACT

Aegilops tauschii Coss., the D genome donor of

hexaploid wheat, Triticum aestivum L., has been

used extensively for the transfer of agronomi-

cally important traits to wheat, including stem

rust resistance genes Sr33, Sr45, and Sr46. To

identify potentially new stem rust resistance

genes in A. tauschii germplasm, we evaluated

456 nonduplicated accessions deposited in the

USDA National Small Grains Collection (Aber-

deen, ID) and the Wheat Genetic and Genomic

Resources Center collection (Kansas State

University, Manhattan, KS), with races TTKSK

(Ug99), TRTTF, TTTTF, TPMKC, RKQQC, and

QTHJC of Puccinia graminis Pers.:Pers. f. sp.

tritici Eriks. & E. Henn. Ninety-eight acces-

sions (22%) were identi ed as resistant to race

TTKSK. A broad range of resistant infection

types (; to 2+) were found in reaction to race

TTKSK. Resistance was signi cantly associ-

ated among most of the races in pairwise com-

parisons. However, resistance was largely race

speci c. Only 12 of the accessions resistant to

race TTKSK were also resistant to the other  ve

races. Results from this germplasm screening

will facilitate further studies on the genetic char-

acterization of accessions with potentially novel

sources of resistance to race TTKSK.

M.N. Rouse and Y. Jin, USDA-ARS, Cereal Disease Lab., Dep. of

Plant Pathology, Univ. of Minnesota, St. Paul, MN 55108; E.L. Olson

and B. Gill, Dep. of Plant Pathology, Kansas State Univ., Manhattan,

KS 66506; M.O. Pumphrey, Dep. of Crop and Soil Sciences, Wash-

ington State Univ., Pullman, WA 99164. Mention of trade names or

commercial products in this article is solely for the purpose of providing

speci c information and does not imply recommendation or endorse-

ment by the U.S. Department of Agriculture. Received 21 Dec. 2010.

*Corresponding author (Yue.Jin@ars.usda.gov).

Abbreviations: ARS, Agricultural Research Service; IT, infection

type; Pgt, Puccinia graminis f. sp. tritici.

Published in Crop Sci. 51:2074–2078 (2011).

doi: 10.2135/cropsci2010.12.0719

Published online 6 July 2011.

form or by any means, electronic or mechanical, including photocopying, recording,

or any information storage and retrieval system, without permission in writing from

the publisher. Permission for printing and for reprinting the material contained herein

has been obtained by the publisher.

CROP SCIENCE, VOL. 51, SEPTEMBER–OCTOBER 2011 WWW.CROPS.ORG 2075

et al., 2010; Singh et al., 2006). Variants of race TTKSK

have been identi ed with additional virulence to resistance

genes Sr24 and Sr36 (Jin et al., 2008; Jin et al., 2009). These

variants (races TTKST and TTTSK, respectively) pose an

even greater threat to worldwide wheat production. Screen-

ing of currently grown cultivars and breeding germplasm

indicated that the majority of the germplasm from Asia, the

United States, and Canada are susceptible to TTKSK (Fetch

2007; Jin and Singh, 2006; Singh et al., 2008). Unfortu-

nately, much of the resistance to race TTKSK available in the

United States is conferred by Sr24 and Sr36 (this resistance is

not e ective to races TTKST and TTTSK). Of the available

sources of resistance to race TTKSK and variants described

to date, most of the resistance genes have been introgressed

from wild relatives of wheat (Singh et al., 2006; Jin et al.,

2007) and have not been utilized extensively in agriculture

because of linkage between these genes and deleterious fac-

tors (Singh et al., 2008).

Three stem rust resistance genes previously have been

transferred from A. tauschii to wheat: Sr33, Sr45, and Sr46

(Kerber and Dyck, 1979; Marais et al., 1998; E. Lagu-

dah, personal communication, 2010). These genes pro-

vide resistance to race TTKSK ( Jin et al., 2007; M. Rouse

and Y. Jin, unpublished data, 2010). Additional resistance

genes may be present in A. tauschii germplasm. The iden-

ti cation of new genes will provide breeders with diverse

genes for pyramiding to increase the durability of resis-

tance. Our objective was to screen the available accessions

of A. tauschii for resistance to race TTKSK to facilitate the

characterization and introgression of novel resistance.

MATERIALS AND METHODS

Aegilops tauschii accessions were obtained from the USDA-

Agricultural Research Service (ARS) National Small Grains

Collection (Aberdeen, ID; 118 accessions) and from the Wheat

Genetic and Genomic Resources Center (Manhattan, KS;

412 accessions). The accession names and sources were cross

checked to eliminate accessions that were redundant among or

within the two collections. We identi ed 456 nonredundant

accessions. The geographic origins of these accessions are dis-

played in Table 1.

Six to ten seedlings of the 456 accessions were inoculated

with six races of Pgt: TRTTF, TTKSK, TTTTF, QTHJC,

RKQQC, and TPMKC (Table 2). Screening with TRTTF,

TTKSK, and TTTTF was conducted at the USDA-ARS Cereal

Disease Laboratory (Saint Paul, MN). Screening with QTHJC,

RKQQC, and TPMKC was conducted at Kansas State Univer-

sity (Manhattan, KS). Accessions that have been used previously

to introgress stem rust resistance genes Sr33 and Sr45, RL5288

and RL5289, respectively, were obtained from Colin Heibert

(Agriculture and Agri-Food Canada, Winnipeg, MB). The dip-

loid A. tauschii source of Sr46 (AUS 18913) and genetic stocks of

Sr33 and Sr45 in hexaploid backgrounds, CSID 5404 and CSID

5406, respectively, were obtained from the Commonwealth Sci-

enti c and Industrial Research Organization (CSIRO) (Can-

berra, Australia). These stocks and susceptible ‘Chinese Spring’

(CI 14108) were inoculated with the six Pgt races. Urediniospores

of stem rust isolates in gelatin capsules stored at −80°C were heat

shocked at 45°C for 15 min and placed in a rehydration chamber

for 2 to 4 h maintained at 80% relative humidity by a KOH solu-

tion (Rowell, 1984). Procedures in inoculation, incubation, and

disease assessment were as described previously ( Jin et al., 2007).

Infection types (ITs) were classi ed as in Stakman et al. (1962).

Infection types with substantial necrosis or chlorosis were desig-

nated as “N” or “C,” respectively. Low infection frequency was

used to indicate notably low density of uredinia for a given leaf

area. Infection types 0 to 2++ were considered low ITs indicat-

ing host resistance whereas ITs 3= to 4 were considered high ITs

indicating host susceptibility. When low and high ITs were pres-

ent on the same leaf, the plant was considered resistant. Acces-

sions were classi ed as heterogeneous when both resistant and

susceptible plants were present.

Frequencies of resistant, susceptible, and heterogeneous

accessions were calculated for each of the six races. For each

accession, the reaction to the combined races was determined

as susceptible if the IT to any of the six races was high, resistant

if the ITs to all six races were low, and heterogeneous if the

reaction to one of the races was heterogeneous and the reaction

to the  ve other races was low or heterogeneous. To test for

associations of resistance, we calculated χ

values based on the

assumption of independence of resistance to each race for every

pairwise comparison of races. Percent of accessions resistant or

heterogeneous for each country of origin were calculated.

To measure the repeatability of visually scoring infection

types, a total of 37 randomly selected accessions were planted

a second time for screening with Pgt races TTTTF, TTKSK,

and TRTTF for a second biological replication. This resulted

in data available for 100 infection types pairs (poor germina-

tion limited the number of infection type pairs). Out of these

100 pairs, seven were inconsistently recorded as resistant (0,;,

1, or 2) in one replication and susceptible (3 or 4) in the other.

The reason for inconsistencies was likely due to heterogeneity

in accessions or error in visually scoring infection types. A total

of 93 of the infection type pairs were consistent representing a

repeatability of classifying resistance and susceptibility of 93%.

Similarly, we previously found the repeatability of classifying

resistance and susceptibility for the diploid wheat relative Triti-

cum monococcum L. to be greater than 95% (Rouse and Jin, 2011).

RESULTS

The seedling ITs of the A. tauschii accessions are available

as Supplemental Table S1. The frequencies of accessions

resistant, susceptible, and heterogeneous to the six races

are displayed in Table 3. Ninety-eight accessions (22.2%)

were resistant to race TTKSK, but only 12 of these acces-

sions (2.7%) were resistant to the  ve other races as well.

Race TRTTF was the most virulent race within this

germplasm (88.2% of the accessions were susceptible)

whereas QTHJC was the most avirulent (68.0% of the

accessions were susceptible). Relatively few of the acces-

sions were heterogeneous to any of the races (0.5 to 2.1%).

The diploid genetic stocks of Sr33, Sr45, and Sr46

(RL5288, RL5289, and AUS 18913, respectively)

2076 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, SEPTEMBER–OCTOBER 2011

and Fehrmann, 2004; Friesen et al., 2008; Ogbonnaya et

al., 2008). We evaluated a relatively large collection of A.

tauschii accessions in an attempt to identify resistance to

race TTKSK and other races with broad virulence.

Accessions resistant to the six Pgt races were con ned

to  ve geographic origin classi cations. Cox et al. (1992)

found that resistance in a subset of these accessions to Pgt

race TNM was con ned to Caspian Iran or Azerbaijan.

We con rmed that these countries possess a higher fre-

quency of resistance to multiple races of Pgt. The higher

number of accessions and wider geographic range of

germplasm tested in our study identi ed Turkmenistan as

an additional hotspot for Pgt resistance.

displayed unique infection type patterns to the races used

(Table 4). The diploid source of Sr46 was also included

in the germplasm screening (TA 1703, synonymous with

AUS 18913). Variation in the Sr46 lines in reaction to races

QTHJC and RKQQC may be attributed to (i) an unstable

intermediate reaction to these races and/or (ii) the screen-

ing of TA 1703 and AUS 18913 by di erent individuals in

di erent locations (i.e., E.L. Olson, Manhattan, KS; M.N.

Rouse, St. Paul, MN).

Signi cant positive associations were found for all race

pairwise comparisons except for races TTTTF and RKQQC

(Table 5). However, diverse IT patterns were observed indi-

cating the presence of multiple race-speci c resistance genes.

Resistance was not equally distributed among coun-

tries of origin (Table 1). The 12 accessions resistant to the

six Pgt races were distributed only among Azerbaijan,

Iran, Turkmenistan, and Uzbekistan and of unknown ori-

gin. These countries of origin also had higher percentages

of accessions resistant to race TTKSK compared to the

other countries, with the exception of Kazakhstan where

 ve of eight accessions were resistant to race TTKSK.

DISCUSSION

Previous studies have examined collections of A. tauschii or

synthetic hexaploid wheats created with A. tauschii acces-

sions for resistance to stem rust (Cox et al., 1992; Assefa

Table 1. Geographic origin of Aegilops tauschii Coss. accessions and percentage of accessions resistant or heterogeneous to

six Puccinia graminis f. sp. tritici races.

Percent resistant or heterogeneous

Country Accessions

TRTTF TTKSK TTTTF

QTHJC RKQQC TPMKC Combined

Afghanistan 83 16041780

Armenia 21 5 24 24 40 30 14 0

Azerbaijan 42 33 48 57 78 41 55 9

China 18 00061860

Georgia 14 0 14 7 43 29 0 0

Iran 64 35 43 20 52 39 36 9

Kazakhstan 8 0 63 38100 100100 0

Kyrgyzstan 4 0 25 0 0 75 25 0

Pakistan 10 0 22 0 0 10 0 0

Syria 5 0 20 0 20 20 20 0

Tajikistan 41 0 12 3 15 13 5 0

Turkey 30 41448 400

Turkmenistan 45 16 18 22 31 48 32 15

Unknown 36 17 34 22 48 23 33 7

Uzbekistan 30 3 27 17 34 37 27 3

Table 2. Races of Puccinia graminis f. sp. tritici used to screen Aegilops tauschii Coss. germplasm.

Isolate Race Origin Avirulence Virulence

04KEN156/04 TTKSK

†

Kenya 24 36 Tmp 5 6 7b 8a 9a 9b 9d 9e 9g 10 11 17 21 30 31 38 McN

06YEM34-1 TRTTF Yemen 8a 24 31 5 6 7b 9a 9b 9d 9e 9g 10 11 17 21 30 36 38 McN Tmp

01MN84A-1-2 TTTTF United States 24 31 5 6 7b 8a 9a 9b 9d 9e 9g 10 11 17 21 30 36 38 McN Tmp

75ND717C QTHJC United States 7b 9a 9e 24 30 31 36 38 Tmp 5 6 8a 9b 9d 9g 10 11 17 21 McN

99KS76A-1 RKQQC United States 9e 10 11 17 24 30 31 38 Tmp 5 6 7b 8a 9a 9b 9d 9g 21 36 McN

74MN1409 TPMKC United States 6 9a 9b 24 30 31 38 5 7b 8a 9d 9e 9g 10 11 17 21 36 Tmp McN

†

Race TTKSK (Ug99) virulence to Sr21 is uncertain (Jin et al., 2007).

Table 3. Number (and frequency) of Aegilops tauschii Coss.

accessions resistant, susceptible, and heterogeneous to

six races of Puccinia graminis f. sp. tritici and the combined

reaction to all races.

Race Total

Resistant

(%)

Susceptible

(%)

Heterogeneous

(%)

TRTTF 439 48 (10.9%) 387 (88.2%) 4 (0.91%)

TTKSK 442 98 (22.2%) 338 (76.5%) 6 (1.36%)

TTTTF 436 61 (14.0%) 366 (83.9%) 9 (2.06%)

QTHJC 413 130 (31.5%) 281 (68.0%) 2 (0.48%)

RKQQC 422 121 (28.7%) 299 (70.9%) 2 (0.47%)

TPMKC 423 95 (22.5%) 326 (77.1%) 2 (0.47%)

All races 448 12 (2.68%) 432 (96.4%) 4 (0.89%)

CROP SCIENCE, VOL. 51, SEPTEMBER–OCTOBER 2011 WWW.CROPS.ORG 2077

In a survey for worldwide virulence in Pgt (Huerta-

Espino, 1992), isolates with virulence to Sr33 were not

found. Seedling and adult plant resistance of hexaploid

monogenic lines carrying Sr33 to race TTKSK is on ly mod-

erate (Jin et al., 2007). The dilution of A. tauschii resistance

when expressed in hexaploids (Kerber and Dyck, 1979) may

be one reason why Sr33 resistance to race TTKSK is mod-

erate. The adult plant resistance to race TTKSK conferred

by Sr45 and Sr46 is unknown. Sr45 is ine ective to the

predominant races in North America (Table 4; Kerber and

Dyck, 1979; Marais et al., 1998). Our data indicate that Sr46

resistance is race speci c (Table 4). If these genes are used

to provide resistance to race TTKSK, additional resistance

genes must be used to create gene combinations that will

provide resistance to other Pgt races.

We interpret the signi cant positive associations of resis-

tance to various races observed as evidence for genes confer-

ring resistance to multiple races. However, only 12 accessions

were found to be resistant to the six races. Diverse IT patterns

were observed among the A. tauschii accessions. The diversity

of IT patterns prevented us from being able to con dently

postulate the presence of known genes in the germplasm

screened and likely indicate diversity for resistance genes,

modi er genes, or genetic background e ects. The IT pat-

terns of a subset of accessions with unknown genes are dis-

played in Table 4. Many IT patterns could not be accounted

for by the previously described genes alone or in combina-

tion. This suggests that additional stem rust resistance genes

are likely present in A. tauschii germplasm. As Sr33 provides

resistance to all six races, further studies are needed to test

the allelic relationship between resistance in the 12 combined

resistant accessions and Sr33. Preliminary evidence based on

ITs suggest that accessions with resistance to all races screened

possess a gene (or genes) independent of Sr33. For example,

accession TA 10171 exhibited resistance to the six races with

ITs much lower than observed on RL5288 (Table 4). Fur-

ther studies testing the allelic relationship between previously

described genes and potentially novel resistance are needed

to con rm the presence of novel resistance to race TTKSK

speci cally. We have initiated crosses to con rm the pres-

ence of novel resistance to race TTKSK, to map potentially

novel sources of resistance, and to introgress such resistance

into adapted wheat backgrounds.

Supplemental Information Available

Supplemental material is available free of charge at http://

www.crops.org/publications/cs.

The seedling infection types (ITs) of the Aegilops taus-

chii accessions are available as Supplemental Table S1.

Table 4. Infection types of Aegilops tauschii Coss. accessions with known stem rust resistance genes and selected lines with

unknown genes.

Accession Background Gene TRTTF TTKSK TTTTF QTHJC RKQQC TPMKC

Chinese Spring T. aesti vum –4

†

44344

RL5288 A. tauschii Sr33 – –2/2,2+2;,2-2

CSID 5405 T. aesti vum Sr33 – 2++ – 2,2- 2+ 2,2+

RL5289 A. tauschii Sr45 ––4444

CSID 5406 T. ae stivu m Sr45 40;4 3 43+

TA 1703 A. tauschii Sr46 2;,2-4 2-2++1,;

AUS 18913 A. tauschii Sr46 2;,1,2-3+33+2-

TA 10087 A. tauschii – 1 ;,2- ;,1C ;,1 3- 1

TA 10124 A. tauschii – 1,2 1,1+ 1,2-,3- ;,1 3,2++ 2,2-

TA 10147 A. tauschii – 4 ;,1N ;,1N 1-,2 ;0 ;0

TA 10171 A. tauschii – ; ;0;00;;

TA 1020 6 A. tauschii – 3+ ;,1 1,3-Z ;,1 ;,1 = ;,1 =

CIae 15 A. tauschii –2+,31,2-,;43+,42- 3

†

Infection types rated on a 0 (immune) to 4 (susceptible) scale where ‘;’ denotes hypersensitive ﬂ ecking, ‘N’ denotes necrosis, ‘C’ denotes chlorosis, and ‘+’ and ‘-’ signs indi-

cate more or less sporulation, respectively, compared to the standard infection type (Stakman et al., 1962). For accessions heterogeneous for infection types among plants,

a ‘/’ was used to separate different infection types corresponding to different plants. Symbol ‘,’ was used to separate different infection types present on the same leaf.

Table 5. Pairwise comparisons of the association between

reactions to the six races.

Association between

Race Race χ

Association type

†

p value

‡

TRTTF TTKSK 150.65 + 1.91 × 10

–32

TRTTF TTTTF 59.68 + 6.87 × 10

–13

TRTTF QTHJC 86.72 + 1.11 × 10

–18

TRTTF RKQQC 37.024 + 4.55 × 10

–08

TRTTF TPMKC 114.27 + 1.32 × 10

–24

TTKSK TTTTF 36.77 + 5.16 × 10

–08

TTKSK QTHJC 92.34 + 6.89 × 10

–20

TTKSK RKQQC 63.65 + 9.76 × 10

–14

TTKSK TPMKC 138.93 + 6.42 × 10

–30

TTTTF QTHJC 129.32 + 7.59 × 10

–28

TTTTF RKQQC 6.04 NS 0.11

TTTTF TPMKC 37.44 + 3.72 × 10

–08

QTHJC RKQQC 51.98 + 3.02 × 10

–11

QTHJC TPMKC 130.32 + 4.61 × 10

–28

RKQQC TPMKC 101.31 + 8.13 × 10

–22

†

For signiﬁ cant associations, ‘+’ indicates a positive association among resistant

accessions and ‘-’ indicates a negative association among resistant accessions.

NS, nonsigniﬁ cant association.

‡

Analyses performed with Microsoft Excel (Microsoft Corporation, 2007), critical p

value = 0.05.

2078 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, SEPTEMBER–OCTOBER 2011

Acknowledgments

We would like to acknowledge Harold Bockelman, USDA-

ARS, National Small Grains Collection, Aberdeen, Idaho, for

distributing Aegilops tauschii seed; Colin Heibert, Agriculture

and Agri-Food, Canada for providing RL5288 and RL5289;

Robert Bowden, USDA-ARS, Manhattan, Kansas for main-

taining Pgt cultures; Jon Raupp, Lucy Wanschura and Sam Gale

for technical assistance.

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