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Euphytica

, 215:55 | Cite as

Characterization of stem, stripe and leaf rust resistance in Tajik bread wheat accessions

  • Mahbubjon RahmatovEmail author
  • Munira Otambekova
  • Hafiz Muminjanov
  • Matthew N. Rouse
  • Mogens S. Hovmøller
  • Kumarse Nazari
  • Brian J. Steffenson
  • Eva Johansson
Open Access
Article

Abstract

Stem rust [causal organism: Puccinia graminis f. sp. tritici (Pgt)], stripe rust [Puccinia striiformis f. sp. tritici (Pst)], and leaf rust [Puccinia triticina (Pt)] are important fungal diseases of wheat in Central Asia and worldwide. Therefore, identification of seedling and adult plant resistance (APR) genes is of major importance for the national wheat breeding program in many countries. The objectives of this study were to identify genes that confer seedling and APR resistances in widely grown wheat cultivars, landraces and advanced lines from Tajikistan. A total of 41 wheat accessions were inoculated with eleven races of Pgt, twelve races of Pst and nine races of Pt for postulation of Sr (stem rust), Yr (yellow or stripe rust), and Lr Lr (leaf rust) resistance genes at the seedling stage. In addition, all of the accessions were tested in field trials for the response to stem rust and stripe rust. Genes for seedling stem rust resistance (i.e. Sr5, Sr6, Sr11, Sr31, and Sr38), stripe rust resistance (Yr9, Yr17, and Y27), and leaf rust resistance (Lr16 and Lr26) were postulated in the Tajik wheat. The presence of the pleiotropic APR genes Sr2/Yr30/Lr27 (associated with pseudo-black chaff phenotype) and Lr34/Yr18/Sr57 (associated with leaf tip necrosis phenotype), and also Lr37 were assessed in the field and confirmed with linked molecular markers. In most of the wheat accessions, resistance genes could not be postulated because their infection types did not match the avirulence or virulence profile of the Pgt, Pst and Pt races tested. Six, seven, and nine accessions were identified that likely possess new genes for resistance to stem rust, stripe rust, and leaf rust, respectively, which have not been described previously. The research demonstrates the presence of effective seedling resistance and APR genes in widely grown wheat accessions that could facilitate further rust resistance breeding in the national wheat breeding program in Tajikistan.

Keywords

Gene postulation Molecular marker Resistance gene Triticum aestivum 

Introduction

Bread wheat (Triticum aestivum L., 2n = 6x = 42, ~ 17 Gb, BBAADD genome) is one of the most important and widely cultivated food crops, contributing substantially to the daily nutrition and food security of a large proportion of the world’s population (Shiferaw et al. 2013). Unfortunately, many abiotic and biotic stresses limit wheat production across the globe. Among the most important biotic stresses of wheat are the three rust diseases, namely stem rust [caused by Puccinia graminis f. sp. tritici Erikss. & E. Henning (Pgt)], stripe rust [Puccinia striiformis Westend. f. sp. tritici Eriks. (Pst)], and leaf rust [Puccinia triticina Eriks. (Pt)]. Since ancient times, these rust diseases have caused many epidemics, resulting in significant and widespread crop losses (Kolmer 2005; Hovmøller et al. 2011; Szabo et al. 2014). Stem rust and stripe rust can cause complete crop loss, and losses due to leaf rust can be as high as 70% (Chen 2005; Huerta-Espino et al. 2011; Singh et al. 2015). In recent epidemics, yield losses ranging from 20 to 100% were reported for these three rust diseases in wheat growing regions worldwide (Huerta-Espino et al. 2011; Wellings 2011; Singh et al. 2015).

In Tajikistan, bread wheat is the most important food crop with respect to national food security (FAO 2015) but is constantly threatened by these three rust diseases. Epidemics of stripe rust occurred in 1952, 1958, 1966, 1997, 1998, 2003, 2010, and 2016, resulting in significant yield losses across the country (Eshonova et al. 2005; Rahmatov et al. 2011, 2012). Stem rust occurs mainly in the mountainous areas (Pett et al. 2005); however, when favorable environmental conditions prevail, the disease is capable of destroying the grain yield of wheat crops across all agroecological zones of Tajikistan. Leaf rust is more variable with respect to its impact on wheat in the country (Eshonova et al. 2005; Rahmatov et al. 2012).

Deployment of host genetic resistance is considered the most effective and low-cost management strategy for rust diseases, particularly in developing countries (Ellis et al. 2014). To control these rust diseases in Tajikistan, the national wheat breeding program has developed several rust resistant wheat cultivars by utilizing advanced breeding lines from the International Winter Wheat Improvement Program and Centro Internacional de Mejoramiento de Maíz y Trigo (CIMMYT). Genetic resistance to rust diseases has been broadly categorized into “seedling resistance,” which is often conferred by single genes with major phenotypic effects across all growth stages of the plant (Flor 1971), and “adult plant resistance” (APR), which is often conferred by multiple genes with more subtle phenotypic effects during the later ontogenetic stages of plant development (Knott 1989). In selecting and breeding for rust resistance, seedling and adult plant phenotyping assays are routinely performed along with molecular marker assays if available for specific resistance genes (Juliana et al. 2017). One of the greatest challenges in breeding for rust resistance in wheat is the genetic variability of the rust pathogens. The virulence diversity of the three rust pathogens in Central Asia is high, particularly in Tajikistan (Kolmer and Ordoñez 2007; Berlin et al. 2015; Ali et al. 2017). For example, the first time Pst virulence was found for the yellow rust (Yr) resistance genes of Yr1, Yr4 + , Yr3 N, Yr9, Yr10, Yr17 and Yr27 in Central Asia was in Tajikistan (Yahyaoui et al. 2012a, b). Eight barberry species have been reported in Tajikistan (Davlatov and Baikova 2011), which may play a role in disease epidemics and pathogen variation in the country since these species could potentially serve as alternate hosts for both Pgt and Pst.

Currently, more than 70 stem rust (Sr) resistance genes, 65 yellow rust (Yr) resistance genes and 79 leaf rust (Lr) resistance genes, including those with minor effects have been cataloged (McIntosh et al. 2017). Widely deployed cultivars with effective resistance genes can suffer yield losses when new, virulent races of the stem, stripe, and leaf rust pathogens emerge, leading to the “boom and bust” cycle of plant breeding (Pretorius et al. 2000; Huerta-Espino et al. 2011; Wellings 2011; Solh et al. 2012). Some of the most widely used and important resistance genes in wheat include Sr13, Sr24, Sr31, Sr36, Sr38, SrTmp and Sr1RSAmigo for stem rust, the Yr2, Yr6, Yr7, Yr8, Yr9, Yr17 and Yr27 for stripe rust, and Lr9, Lr14a, Lr16, Lr17a, Lr24, Lr26 and Lr39 for leaf rust all of which have now been overcome by newly detected pathogen races (Huerta-Espino et al. 2011; Singh et al. 2015; Ali et al. 2017). The lack of knowledge regarding the presence of major effect seedling and minor effect APR resistance genes in Tajik wheat germplasm makes it difficult to make informed decisions with respect to breeding for stable resistance in the national wheat breeding program. Therefore, the aims of this study were to (1) evaluate Tajik wheat accessions for seedling resistance and postulate the presence of underlying Sr, Yr and Lr genes; (2) identify the presence of gene(s) conferring APR to the three rust diseases; and (3) verify the presence of resistance genes postulated by available molecular markers.

Materials and methods

Plant and pathogen materials

A total of twenty-nine wheat cultivars, seven advanced breeding lines, and five landraces were used in the present study and tested for response to the three rusts. These wheat accessions were provided by the national wheat breeding program in Tajikistan. The pedigree and origin of the materials are given in Table 1. In addition, differential wheat accessions with characterized resistance genes for stem rust (Jin et al. 2007), stripe rust (Hovmøller et al. 2017), and leaf rust (Kolmer and Hughes 2013) were also included to facilitate the gene postulations. Eleven Pgt, twelve Pst and nine Pt races with different virulence/avirulence combinations and geographic origins were used (Tables 2, 3 and 4).
Table 1

List of wheat accessions evaluated in this study

#

Accession

Pedigree

Origin

Type

Accession status

1

Navruz

(S)MIRONOVSKAYA-YUBILEINAYA

Tajikistan

Facultative

Cultivar

2

Sarvar

CHEN/AEGILOPS SQUARROSA (TAUS)//BCN/3/BAV92

ESWYT25

Spring

Cultivar

3

Vahdat

VORONA/CNO79//KAUZ/3/MILAN

ESWYT25

Spring

Cultivar

4

Yusufi

SOROCA

ESWYT25

Spring

Cultivar

5

Isfara

SW89.5181/KAUZ

ESWYT25

Spring

Cultivar

6

Alex

PAYNE(PYN)/(BAU)BAGULA

1WWEERYT

Facultative

Cultivar

7

Oriyon

NORD-DESPREZ/VG-9144//KALYANSONA/BLUEBIRD/3/YACO/4/VEERY-5

N.A.

Facultative

Cultivar

8

Sadokat

JUPATECO-73/BLUEJAY//URES-81

Mexico

Spring

Cultivar

9

Ziroat-70

N.A.

N.A.

Facultative

Cultivar

10

Norman

OR-F-1-158/(FDL)FUNDULEA//(BLO)BOLILLO/3/SHI-4414/CROW

5FAWWON

Facultative

Cultivar

11

Somoni

N.A.

N.A.

Facultative

Cultivar

12

Tacicar

TR.AE/SPARROW//ZARAPITIN

5FAWWON

Facultative

Cultivar

13

Ormon

NWT/3/TAST/SPRW//TAW12399.75

8FAWWON

Facultative

Cultivar

14

Iqbol

RUSALKA,BGR/CA-8055//CHAM-6

N.A.

Facultative

Cultivar

15

Starshina

COLT/SPARTANKA

Russia

Winter

Cultivar

16

Shokiri

SHARK/F-4105-W-2-1

5WWEERYT

Facultative

Cultivar

17

Fayzbaksh

TAM200/KAUZ

6WWEERYT

Facultative

Cultivar

18

Nurbakhsh

PRINA/STAR

N.A.

Facultative

Cultivar

19

BASRIBEY-95

JUPATECO-73/(SIB)BLUEJAY//URES-81

Turkey

Facultative

Cultivar

20

Jagger

KS-82-W-418/STEPHENS

USA

Winter

Cultivar

21

Kaboi Panjakent

N.A.

Tajikistan

Facultative

Landrace

22

Surkhaki 5

N.A.

Tajikistan

Spring

Landrace

23

Zafar

N.A.

Tajikistan

Facultative

Cultivar

24

Steklovidnaya-24

BOGARNAYA-56/TEPLOKLYUCHENSKAYA-2//ROSTOVCHANKA

Kazakhstan

Winter

Cultivar

25

SIETE-CERROS-66

PENJAMO-62(SIB)/GABO-55

Mexico

Spring

Cultivar

26

Krasnodarskaya-99

LUTESCENS-2665-G-10233/ERYTHROSPERMUM-4695-h-449//LUTESCENS-2621-h-24-82

Russia

Winter

Cultivar

27

Jayhun

N.A.

Turkey

Facultative

Cultivar

28

IZ-80

KAUZ * 2/CHEN//BCN/3/MILAN

 

Facultative

Cultivar

29

AIKT-20

CBRD/KAUZ

 

Facultative

Cultivar

30

N.A.

OTUS TOBA 97

 

Facultative

Advanced line

31

N.A.

PASTOR/3/VORONA

 

Facultative

Advanced line

32

N.A.

CMN82A.1294/2*

 

Facultative

Advanced line

33

N.A.

HUAVUN INIA

 

Facultative

Advanced line

34

Trakua Hatti

N.A.

Turkey

Facultative

Advanced line

35

Murodi-2013

CHEN/AE.SQ//WEAVER/3/SSERI1

27ESWYT

Spring

Cultivar

36

N.A.

CHEN/AE.SQ//WEAVER/3/PASTOR

27ESWYT

Spring

Advanced line

37

Ganj

NAC/TH.AC//3 * PVN/3/MIRLO/BUC/4/2 *vPASTOR

27ESWYT

Spring

Cultivar

38

N.A.

NAC/TH.AC//3 * PVN/3/MIRLO/BUC/4/2 * PASTOR

27ESWYT

Spring

Advanced line

39

Safedaki Pomir

N.A.

Tajikistan

Spring

Landrace

40

Safedaki Ishkoshim

N.A.

Tajikistan

Spring

Landrace

41

Babilo Pomir

N.A.

Tajikistan

Spring

Landrace

N.A. not available, ESWYT elite spring wheat yield trial, FAWWON facultative and winter wheat observation nursery, WWEERYT winter wheat eastern european regional yield trial

Table 2

The origin and virulence phenotype of Puccinia graminis f. sp. tritici races used in this study

Race

Isolate

Origin

Virulence profile

Sr5

Sr21

Sr9e

Sr7b

Sr11

Sr6

Sr8a

Sr9 g

Sr36

Sr9b

Sr30

Sr17

Sr9a

Sr9d

Sr10

SrTmp

Sr24

Sr31

Sr38

SrMcN

RKQQC

99KS76A-1

USA

5

21

7b

6

8a

9 g

36

9b

9a

9d

McN

QTHJC

75ND717C

USA

5

21

11

6

8a

9 g

9b

17

9d

10

McN

TPMKC

74MN1409

USA

5

21

9e

7b

11

8a

9 g

36

17

9d

10

Tmp

McN

TTTTF

02MN84A-1-2

USA

5

21

9e

7b

11

6

8a

9 g

36

9b

30

17

9a

9d

10

Tmp

38

McN

TTKSK

04KEN156/04

Kenya

5

21

9e

7b

11

6

8a

9 g

9b

30

17

9a

9d

10

31

38

McN

TTTSK

07KEN24-4

Kenya

5

21

9e

7b

11

6

8a

9 g

36

9b

30

17

9a

9d

10

31

38

McN

TTKST

06KEN19-V-3

Kenya

5

21

9e

7b

11

6

8a

9 g

9b

30

17

9a

9d

10

24

31

38

McN

TRTTF

06YEM34-1

Yemen

5

21

9e

7b

11

6

9 g

36

9b

30

17

9a

9d

10

Tmp

38

McN

TKTTF

 

Turkey

5

21

9e

7b

6

8a

9 g

36

9b

30

17

9a

9d

10

McN

BCCBC

09CA115-2

USA

9 g

17

McN

MCCFC

59KS19

USA

5

7b

9 g

17

10

Tmp

McN

– Indication of avirulence

Table 3

The origin and virulence phenotype of Puccinia striiformis f. sp. tritici races used in this study

Race

Origin

Virulence profile

Yr1

Yr2

Yr3

Yr4

Yr5

Yr6

Yr7

Yr8

Yr9

Yr9+

Yr10

Yr15

Yr17

Yr24

Yr25

Yr27

Yr32

YrSd

YrSu

YrSp

YrAvS

SE205/12

Sweden

1

2

3

6

7

8

9

9+

17

25

32

Sd

AvS

UK94/519

UK

1

2

3

9

9+

17

25

Sd

Su

AvS

DK66/02

Denmark

2

6

7

8

9

25

Sd

AvS

TJ01a/10

Tajikistan

1

2

3

4

6

9

9+

25

32

Sd

Su

AvS

ER02/03

Eritrea

2

6

7

8

9

10

24

25

AvS

DK11/09

Denmark

3

4

6

25

32

Sd

Su

Sp

AvS

DK71/93

Denmark

1

2

3

25

32

Sd

AvS

AF87/12

Afghanistan

2

6

8

17

27

32

AvS

DK09/11

Denmark

1

2

3

4

6

7

9

9+

17

25

32

Sd

Su

Sp

AvS

DK122/09

Denmark

1

2

3

4

6

9

9+

17

25

32

Sd

Su

AvS

SE100/09

Denmark

7

8

10

TK34/11

Turkey

− 2

6

7

8

9

25

27

(Sd)

(Su)

AvS

– Indication of avirulence

Table 4

The origin and virulence phenotype of Puccinia triticina races used in this study

Race

Origin

Virulence profile

Lr1

Lr2a

Lr2c

Lr3

Lr9

Lr16

Lr24

Lr26

Lr3ka

Lr11

Lr17

Lr30

TDBJG

USA

1

2a

2c

3

24

TFBJQ

USA

1

2a

2c

3

24

26

TNRJJ

USA

1

2a

2c

3

9

24

3 ka

11

30

MLDSD

USA

1

3

9

17

MBDSB

USA

1

3

17

TBBGG

USA

1

2a

2c

3

KFBJG

USA

2a

2c

3

24

26

MHDSB

USA

1

3

16

26

17

TCRKG

 USA

1

2a

2c

3

26

3 ka

11

30

Race

Origin

Virulence profile

LrB

Lr10

Lr14a

Lr18

Lr21

Lr28

Lr39

Lr42

Lr3bg

Lr14b

Lr20

Lr23

TDBJG

USA

10

14a

28

14b

TFBJQ

USA

10

14a

21

28

14b

20

23

TNRJJ

USA

10

14a

28

39

14b

20

MLDSD

USA

B

10

14a

39

3bg

14b

20

23

MBDSB

USA

B

10

14a

3bg

14b

20

TBBGG

USA

10

28

 

3bg

14b

20

23

KFBJG

USA

10

14a

28

14b

20

23

MHDSB

USA

B

10

14a

3bg

14b

20

TCRKG

 USA

10

14a

18

28

3bg

14b

20

– Indication of avirulence

Seedling rust resistance assays

Seedling resistance assays to stem rust and leaf rust were conducted at the United States Department of Agriculture-Agricultural Research Service-Cereal Disease Laboratory (USDA-ARS-CDL) and the University of Minnesota in St. Paul, USA. Five seeds of each wheat genotype were included for each rust assay. The seeds were planted in pots containing vermiculite (Sun Gro Horticulture), watered daily, and fertilized with 20–20–20 NPK soluble fertilizer (Spectrum Group, St. Louis). Stored urediniospores of the stem and leaf rust pathogens were removed from a − 80 °C freezer, 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 solution, and then suspended in a lightweight mineral oil (Soltrol 170® Chevron Phillips Chemical Company LP, Woodlands, TX 77380) within gelatin capsules (size 00). Then, urediniospores were inoculated onto 8–10 day-old seedlings of the different accessions at the first leaf stage. Seedling resistance assays for stem rust were done according to the methods of Rouse et al. (2011) and those for leaf rust were done according to Oelke and Kolmer (2004). Infection types were scored 14 days after inoculation using a 0–4 scale (Stakman et al. 1962; Long and Kolmer 1989). Seedling resistance to Pgt race TKTTF (bulk collection from Turkey) was carried out at the Regional Cereal Rust Research Center (RCRRC), located at the Aegean Agricultural Research Institute, International Center for Agricultural Research in the Dry Areas (ICARDA) in Izmir, Turkey (Rahmatov et al. 2016). The methods used for this test were similar to those used for the other races, the exception being that fresh urediniospores collected from plants in the field were used instead of frozen urediniospores. Ten-day-old seedlings with the first leaves fully expanded were inoculated with race TKTTF according to Rahmatov et al. (2016).

All accessions were evaluated for seedling stripe rust resistance at the Global Rust Reference Center (GRRC) at Aarhus University in Flakkebjerg, Denmark and at the RCRRC. For these evaluations, ten seeds were sown in pots containing a mixture of peat moss and soil. Inoculations with races of Pst were carried out on 14-day-old seedlings when the second leaves were fully expanded. For inoculations completed at the GRRC and RCRRC, Pst urediniospores were suspended in Novec Fluid (3 M Novec™ 7100 Engineered Fluid) and lightweight mineral oil, respectively (Rahmatov et al. 2017). After inoculation, plants were moved to a dark chamber at 100% RH at 10 °C for 24 h for the infection period. Thereafter, plants were incubated in a greenhouse at 18 °C for 18 h during the day and 12 °C for 6 h during the night, protocols routinely used at both the GRRC and RCRRC (Hovmøller et al. 2017; Rahmatov et al. 2017). After 16 days of incubation, stripe rust infection types were scored using a 0–9 scale as described by McNeal et al. (1971).

Assessment of field response to stem rust and stripe rust

Adult plant stem rust responses were evaluated under field conditions at the Kenyan Agricultural and Livestock Research Organization in Njoro (2010 and 2011), at the RCRRC in Izmir (2014) and at the University of Minnesota in St. Paul (2014). In Tajikistan, the wheat accessions were exposed to naturally occurring races of Pst during the growing season of 2010. The stripe rust-infected leaves were collected in Tajikistan and sent to the GRRC for race analysis (Hovmøller et al. 2017), and the race TJ01a/10 was detected and subsequently used at the seedling resistance test. To provide sufficient stripe rust infection in the nurseries at RCRRC, mixtures of susceptible wheat cultivars were used as spreader rows surrounding and between the plots (Rahmatov et al. 2017). In Njoro and Minnesota, urediniospores of Pgt (TTKSK + TTKST, and MCCFC) were needle-injected (i.e. injecting urediniospores directly into the stems of susceptible spreader plants) at the tillering, booting and heading stages. Additionally, direct foliar inoculations were made on the spreader rows using a urediniospore/oil suspension (Rahmatov et al. 2016). In Izmir, the spreader rows were inoculated five times at the tillering, booting and heading stages by dusting a mixture of fresh urediniospores of Pgt (TKTTF) and Pst (TK34/11) together with talcum powder. After inoculation, the nurseries in Njoro and Izmir were mist-irrigated three times per day (i.e. morning, afternoon and evening) to ensure a moist environment and thereby enhance stem and stripe rusts development. The adult plant response to stem and stripe rust were assessed between growth stages 50–90 (Zadoks et al. 1974). Disease severity was assessed using the modified Cobb scale (Peterson et al. 1948) and adult plant infection types were rated according to Roelfs et al. (1992). The presence of the pseudo-black chaff (PBC) and leaf tip necrosis (LTN) phenotypes were assessed using 0–4 scale in all field trials (Juliana et al. 2015).

Molecular marker analysis

Total genomic DNA was isolated from the leaves of 10 day-old seedlings according to Edwards et al. (1991) with some slight modifications. The molecular markers XcsSr2, Xgwm533 and wMAS000005 for Sr2/Yr30/Lr27 (Spielmeyer et al. 2003; Mago et al. 2011), Xcfd43 for Sr6 (Tsilo et al. 2009) Xwmc364 for Yr2 (Lin et al. 2005), Xscm9 and Xiag95 for Sr31/Yr9/Lr26 (Saal and Wricke 1999; Mago et al. 2005), csLV34 and wMAS000003 for Lr34/Yr18/Sr57 (Lagudah et al. 2006), and VENTRIUP/LN2 for Sr38/Yr17/Lr37 (Helguera et al. 2003) were assessed. The PCR assays were conducted according to Rahmatov et al. (2016).

Results

Stem rust seedling response assays

A majority of the wheat accessions showed seedling resistance towards the Pgt races of RKQQC, QTHJC, TPMKC, BCCBC, and MCCFC with infection types (ITs) ranging from 0 to 2 + (Table 5). A lower proportion of the wheat accessions showed seedling resistance towards the more widely virulent Pgt races of TTTTF, TTKSK, TTTSK, TTKST, TRTTF and TKTTF (Table 5). The resistance gene Sr5 was postulated in Navruz and Steklovidnaya-24 based on its resistance reaction to race BCCBC (Table 5). Sr6 and Sr11 were postulated in Siete-Cerros-66 based on its resistance reactions to races RKQQC, TPMKC, TKTTF, MCCFC and BCCBC (Table 5). Resistance gene Sr31 was postulated in Alex, Sadokat, Ziroat-70 and Otus Toba97 based on their susceptible reactions to races TTKSK, TTTSK and TTKST (Table 5); and Sr38 in Jagger and IZ-80 based on their susceptible reactions to races TTTTF, TTKSK, TTTSK, TTKST and TRTTF (Table 5). The landraces of Kaboi Panjakent, Surkhaki-5, Jayhun, Safedaki Pomir, and Safedaki Ishkoshim were resistant to races TTKSK, TTTSK and TTKST (Table 5). Only Sarvar was highly resistant to all the tested races (Table 5). If any previously described resistance genes were present in this group of accessions, they could not be postulated because the resulting ITs did not match those of any differential accessions. Thus, these accessions either carry combinations of previously described genes or new resistance gene/s.
Table 5

Seedling infection types and field responses to stem rust, and molecular marker analysis for Sr6, Sr31, and Sr38

Accession

Sr seedling resistance

RKQQC

QTHJC

TPMKC

TTTTF

TTKSK

TTTSK

Rep. 1

Rep. 2

Rep. 1

Rep. 2

Navruz

1

0;/1

3+

3+

4

4

4

4

Sarvar

0;

0;

;1−

0;

22+

22+

0;

0;

Vahdat

0;

11+

1 + 2

0;

4

4

4

3+

Yusufi

1 + 2

1 + 2

1+

3+

4

4

3+

3+

Isfara

0;

1+

1;

3+

4

4

3+

3+

Alex

1;

11+

0;1

1;

4

4

3+

3+

Oriyon

0;

11+

11+

3+

4

4

3+

3+

Sadokat

0;

11+

1+

1+

4

4

3+

3+

Ziroat-70

0;

1 + 2

1

0;

4

4

3+

3+

Norman

4

1 + 2

0;1

3+

4

4

3+

3+

Somoni

1;1+

3+

3+

3+

4

4

3+

3+

Tacicar

4

3+

3+

3+

4

4

3+

3+

Ormon

3+

4

3+

3+

4

4

3+

3+

Iqbol

3+

3+

3+

1;

4

4

3+

3+

Starshina

22+

22+

4

3+

3+

3+

3+

3+

Shokiri

3+

3+

1;1+

3+

4

4

3+

3+

Fayzbaksh

0;

1+

2−

3+

4

4

3+

3+

PRINA/STAR

4

3+

4

3+

4

4

4

3+

BASRIBEY-95

2+

22+

3+

3+

4

4

3+

3+

Jagger

0;

0;

0;

3+

4

4

33+

3+

Kaboi Panjakent

1+

4

3+

4

2

2

1;

2

Surkhaki-5

2

4

3+

4

22+

22+

1;

2

Zafar

3+

2 + 3−

3+

3+

4+

4+

4

3+

Steklovidnaya-24

3+

3+

3+

3+

4

4

4

3+

SIETE-CERROS-66

1;

3+

;0

33+

4

4

3+

3+

Krasnodarskaya-99

1;

3+

33+

3+

4

4

3+

3+

Jayhun

2+

4

3+

3+

22+

22+

2

2

IZ-80

1;

0;

1;1+

3+

4

4

4

4

AIKT-20

0;

11+

1

3+

4

4

4

3+

OTUS TOBA 97

;

11+

1

0;1−

4

4

3+

3+

PASTOR/3/VORONA/CN079

0;

11+

1 + 2

1 + 2

4

4

3+

3+

CMN82A.1294/2*

1;

11+

1;1+

0;

4

4

3+

3+

HUAVUN INIA

;1

11+

1;1+

3+

4

4

3+

3+

Trakua Hatti

0;

11+

11+

3+

4

4

3+

3+

Murodi-2013

22+

1+

1;2−

3+

4

4

3+

3+

CHEN/AE.SQ//WEAVER/3

1 + 2

1 + 2/2+

22+

3+

4

4

3+

3+

Ganj

33−

2+

3−

3+

4

4

3+

3+

NAC/TH.AC//3 * PVN/3/MIR

3

2 + 3

2 + 3

3+

4

4

3+

3+

Safedaki Pomir

4

4

2+

3+

4

4

0;− 1

2

Safedaki Ishkoshim

3+

4

3+

3+

4

4

1;

2−

Babilo Pomir

4

22+

3+

3+

4

4

4

4

Accession

Sr seedling resistance

Sr Adult Plant Resistance

Sr gene postulation based on seedling and molecular marker

TTKST

TRTTF

TKTTF

BCCBC

MCCFC

TTKSK + TTKST

TTKS + TTKST

TKTTF

MCCFC

 

Rep. 1

Rep. 2

2010

2011

Navruz

4

3+

4

4

0;

4

50S

60MSS

60MSS

5RMR

Sr5,+

Sarvar

0;

22+

11+

0;

0;

;0

20MR

20MR

5R

TR

 

Vahdat

4

4

11+

3+

0;

;0

60S

70S

5R

TR

 

Yusufi

3+

3+

1+

4

0;

;1−

50S

60S

80S

TR

 

Isfara

3+

3+

1+

4

0;

;1−

60S

70S

80S

TR

 

Alex

4

3+

2−

1

0;

;0

40S

50MSS

10RMR

TR

Sr31

Oriyon

3+

3+

3+

3+

0;

;1−

50S

60S

90S

5RMR

 

Sadokat

4

3+

1+

1

0;

;0

40S

30S

10RMR

10RMR

Sr31

Ziroat-70

3+

3+

11+

1

0;

;0

40S

60S

20RMR

TR

Sr31

Norman

3+

3+

11+

4

0;

;0

40S

40S

70MSS

TR

 

Somoni

3+

3+

1+

3+

0;

;0

60S

60S

5RMR

TR

 

Tacicar

3+

3+

1 + 2

3+

0;

11−

60S

40S

70MSS

TR

 

Ormon

4

3+

4

4

0;

11−

60S

80S

70MSS

TR

 

Iqbol

3+

3+

1;

3+

0;

;0

50S

80S

5RMR

TR

 

Starshina

1 + 2

22+

4

2

0;

4

60MSS

70S

10RMR

TR

 

Shokiri

3+

33+

3 + 4

0;

0;

;0

40MSS

60S

10RMR

5RMR

 

Fayzbaksh

4+

3+

11+

3+

0;

;0

70S

90S

5RMR

TR

 

PRINA/STAR

4

3 +/2

4

4

0;

;0

40MSS

70S

40MSS

10MRMS

 

BASRIBEY-95

3+

3+

4

4

0;

4

80S

70S

80S

20MS

 

Jagger

3+

3+

4

1

0;

;0

40MS

50MS

5R

TR

Sr38

Kaboi Panjakent

22+

2

4

4

0;

4

30RMR

20RMR

40MR

30MR

 

Surkhaki-5

22+

2

3+

4

0;

4

20MR

30RMR

40MR

TR

 

Zafar

4

3+

4

4

0;

;1−

60S

80S

80S

10RMR

 

Steklovidnaya-24

3+

3+

3+

4

0;

4

60S

60S

80S

30MS

Sr5

SIETE-CERROS-66

4

3+

3+

1

0;

;0

50MSS

40MSS

10RMR

TR

Sr6, Sr11

Krasnodarskaya-99

3+

3+

3+

3+

0;

;0

50S

80S

20MRMS

TR

 

Jayhun

22+

22+

4

4

0;

4

30MR

30MR

70MSS

40MR

 

IZ-80

4

4

11+

;1−

0;

;0

50S

60S

20RMR

TR

38,+

AIKT-20

3+

3+

1+

;

0;

;0

40MS

50MS

20MR

TR

 

OTUS TOBA 97

3+

3+

11+

0;

0;

;0

60S

60MSS

10RMR

TR

Sr31

PASTOR/3/VORONA/CN079

3+

3+

11+

0;

0;

;0

20MSS

10MSS

20RMR

10RMR

 

CMN82A.1294/2*

3+

3+

11+

1−

0;

;0

40MRMS

50MR

30MR

5RMR

 

HUAVUN INIA

3+

3+

11+

3+

0;

;0

30MR

40MR

30MSS

TR

 

Trakua Hatti

3+

3+

3+

3+

0;

;1

40S

100S

50MSS

5R

 

Murodi-2013

3+

3+

4

3+

0;

1+

60S

60MSS

30MS

5RMR

 

CHEN/AE.SQ//WEAVER/3

3+

3+

4

3+

0;

1+

50S

50S

40MS

5RMR

 

Ganj

3+

3+

4

3+

0;

1 +/2+

40S

50S

40MR

5RMR

 

NAC/TH.AC//3 * PVN/3/MIR

3+

3+

4

3+

0;

1+

40S

60MSS

50MR

10RMR

 

Safedaki Pomir

1 + 2

22+

3+

3+

0;

4

60MSS

10RMR

 

Safedaki Ishkoshim

2

;2−

3+

3+

0;

4

60MSS

20MR

 

Babilo Pomir

4

;13

3+

3+

0;

;0

40MRMS

5R

 

Molecular marker analysis for Sr6, Sr31 and Sr38 are presented in Table 8.

Accessions exhibiting infection types of; 0 to 2 + were classified as resistant and those exhibiting infection types of 3–4 were classified as susceptible at the seedling stage. Adult plant rust severity was scored on a 0 to 100% basis and the infection responses on the size and type of uredinia where R (resistant), RMR (resistant to moderately resistant), MR (moderately resistant), MR-MS moderately resistant to moderately susceptible, MS (moderately susceptible), MS-S (moderately susceptible to susceptible) and S (susceptible). APR was tested only against races TTKSK + TTKST, MCCFC, and TKTTF

Stripe rust seedling response assays

Postulations for Yr genes were conducted using 12 Pst races (Table 3). Yr9 and Yr17 were confirmed based on the stem rust gene postulations for Sr31 and Sr38 plus molecular markers because of their tight linkage with the respective genes within the 1BL.1RS wheat-rye and 2NS/2AS translocations. These assays confirmed the presence of Yr9 in Alex, Sadokat, Ziroat-70, and Otus Toba97 and Yr17 in Jagger and IZ-80 (Tables 6, 8). Because Alex, Sadokat, Ziroat-70, Otus Toba97, Jagger and IZ-80 were resistant to most of the Pst races used in this study, including those carrying virulence for Yr9 and Yr17, thus it was not possible to postulate genes based on their ITs to the 12 Pst races used in this study (Table 6). The Yr27 was confirmed in Isfara based on the Yr27-virulent isolates AF87/12 and TR34/11 conferring ITs of 7 on Yr27 differential lines (Table 6). Sarvar, Fayzbakhsh, Otus Toba97, Vahdat, Oriyon, Sadokat and AIKT-20 were highly resistant (ITs 0–4) to all or nearly all races; thus, the genes they carry could not be postulated with the Pst races used in this study nor the molecular markers. These accessions carry combinations of previously described genes or new resistance gene/s (Table 6).
Table 6

Seedling infection types and field responses to stripe rust, and molecular marker analysis for Yr9 and Yr17

Accession

Yr seedling resistance

Yr adult plant resistance

Yr gene postulation based on seedling and molecular marker

SE205/12

UK94/519

DK66/02

TJ01a/10

ER02/03

DK11/09

DK71/93

AF87/12

DK09/11

DK122/09

SE100/09

TK34/11

TK34/11

TJ01a/10

Navruz

7

7

7

7

7

7

7

7

7

7

6

7

70MSS

100S

 

Sarvar

1

1

0

1

4

2

2

2

2

1

0

2

20RMR

5R

 

Vahdat

1

0

0

1

1

0

0

0

1

1

0

7

10RMR

10R

 

Yusufi

4

7

7

0

5

1

7

7

6

7

0

3

20RMR

10R

 

Isfara

0

0

0

1

0

0

1

7

1

0

0

7

20RMR

10R

Yr27,+

Alex

7

7

7

0

5

1

1

0

6

4

0

3

40MR

40MS

Yr9,+

Oriyon

4

2

0

0

4

0

2

7

0

4

3

2

30MR

20MR

 

Sadokat

3

0

7

2

4

0

1

0

1

2

0

3

30MR

10R

Yr9,+

Ziroat-70

2

7

0

7

7

0

0

0

5

5

0

7

60MSS

60S

Yr9,+

Norman

5

7

0

7

7

0

3

0

7

0

0

7

50MS

100S

 

Somoni

2

7

0

6

1

0

1

6

6

5

0

2

60MR

40MS

 

Tacikar

5

0

0

7

6

0

1

0

6

6

0

7

50MRMS

40MS

 

Ormon

4

0

7

4

1

0

1

6

1

0

0

7

10RMR

10R

 

Iqbol

6

0

0

7

0

0

1

0

6

5

0

2

40MRMS

100S

 

Starshina

5

7

7

0

0

0

6

6

6

7

0

4

30MR

10R

 

Shokiri

3

7

7

7

1

0

0

7

0

7

3

3

40MRMS

80S

 

Fayzbaksh

4

0

1

1

3

0

1

1

0

4

0

4

40RMR

20MR

 

PRINA/STAR

7

7

7

7

4

6

5

0

6

7

0

1

40RMR

60S

 

BASRIBEY-95

7

7

7

7

1

0

7

7

6

7

0

7

70S

60S

 

Jagger

6

7

0

1

0

0

1

0

6

7

0

4

5R

10R

17,+

Kaboi Panjakent

2

7

2

0

0

2

3

1

0

4

0

7

100S

20MR

 

Surkhaki-5

2

7

3

0

0

0

2

0

0

4

0

7

100S

40MR

 

Safedaki Ishkoshimi

7

7

7

7

7

6

7

6

6

7

0

3

20MR

70S

 

Safedaki Pomir

7

7

7

7

4

2

7

6

6

5

2

3

20RMR

70S

 

Babilo Pomir

7

7

7

4

6

1

7

0

6

2

0

4

30MR

60MR

 

Krasnodarskaya-99

7

0

7

7

1

0

7

1

6

7

0

3

30MRMS

50S

 

Jeyhun

7

0

7

7

1

0

7

6

6

7

3

4

40MRMS

50S

 

IZ-80

7

0

0

0

0

1

0

6

0

1

0

2

20RMR

10R

17,+

AIKT-20

2

0

7

0

0

1

1

1

0

1

0

2

40MR

10R

 

OTUS TOBA 97

4

0

0

1

2

0

0

0

0

2

0

4

30MR

10R

Yr9, + 

PASTOR/3/VORONA/CN079

3

0

0

7

0

0

0

0

6

6

0

3

20MRMS

100S

 

CMN82A.1294/2*

2

0

7

2

0

0

0

0

1

2

0

7

40MRMS

20RMR

 

HUAVUN INIA

4

0

7

2

0

0

0

0

1

2

0

7

60MSS

10RMR

 

Molecular marker analysis for Yr9 and Yr17 are presented in Table 8

Accessions exhibiting infection types of 0–4 were classified as resistant, those exhibiting 5–6 as moderately susceptible, and those exhibiting 7–9 as susceptible at the seedling stage. Adult plant rust severity was scored on a 0 to 100% basis and the infection responses on the size and type of uredinia where R (resistant), RMR (resistant to moderately resistant), MR (moderately resistant), MR-MS moderately resistant to moderately susceptible, MS (moderately susceptible), MS-S (moderately susceptible to susceptible) and S (susceptible). APR was tested only against races TJ01a/10 and TR34/11

Leaf rust seedling response assays

For the leaf rust seedling evaluations, nine Pt races were used (Table 4). The number of resistant and susceptible accessions for each of the races is presented in Table 7. Lr16 was postulated in Iqbol, OTUS TOBA97, and HUAVUN INIA based on their susceptible reactions (ITs of 33 +) to race MHDSB (Table 7). Lr26 was postulated in Alex, Sadokat, and Ziroat-70 based on their susceptible reactions (ITs 33 +) to races KFBJG, MHDSB, and TCRKG and molecular markers (Tables 7, 8). OTUS TOBA97 was resistant to all Pt races, except MHDSB (Table 7); therefore, the presence of Lr26 was confirmed based on the stem rust, stripe rust and molecular marker analysis (Tables 7, 8). Nine accessions (Sarvar, Vahdat, PRINA/STAR, Zafar, AIKT-20, PASTOR/3/VORONA, CMN82A.1294/2*, Murodi-2013, and Ganj) likely carry combinations of previously described Lr genes or new Lr gene/s.
Table 7

Seedling infection types to leaf rust, and molecular marker analysis for Lr26

Accession

Lr seedling resistance

 

TDBGG

TFBJQ

TNRJJ

MLDSD

MBDSB

TBBGJ

KFBJG

MHDSB

TCRKG

Lr gene postulation based on seedling and molecular marker

Navruz

;1-

3

3+

3

33+

33+

3+

3+

33+

 

Sarvar

0;

0;

;

3

;

;

;

;

;

 

Vahdat

;

;

;

;

;

;1−

32+

11+

;1−

 

Yusufi

;

;12

;1

33+

;

;1

3+

;

;1

 

Isfara

;1−

33+

3

3

;

;11+

33+

1 + 2

12

 

Alex

0;

;1

;

11+

;

;1−

33+

33+

33+

Lr26

Oriyon

;1−

;1

3

11+

;1+

;12−

3

3+

33+

 

Sadokat

;

;1−

;

1+

1−

;1−

2 + 3

3

;1

Lr26

Ziroat-70

;

;12

;

22+

11+

;1−

2;3

3

;1

Lr26

Norman

;1−

3

3+

33+

3

;1

3+

33+

3+

 

Somoni

2+

33+

3

22+

11+

33+

22+

2+

33+

 

Tacicar

;1−

;12

3

33+

;1−

;11+

33+

22+

33+

 

Ormon

;

;1/22 + 

33+

3

12

3

3

33+

;11+

 

Iqbol

;12

2

;12

11+

;1

11+

11+

33+

11 + 2−

Lr16

Starshina

;1−

3

3

3

22+

3

3+

3+

33+

 

Shokiri

;

;1

;

22+

1+

3

22+

33+

;1

 

Fayzbaksh

33+

22 + ;

3+

;1

;

;

;

3+

;1

 

PRINA/STAR

;1−

2 + 3

1

;1

11+

1 + 2

;1−

3+

;11+

 

BASRIBEY-95

;1−

33+

33+

2+

1+

;11+

3+

;1−

11+

 

Jagger

3+

3 + ;

2+

2+

11+

;1

33+

33+

1 + 2

 

Kaboi Panjakent

3+

3+

3+

3 + 4

3+

3 + 4

3 + 4

3 + 4

3+

 

Surkhaki 5

3+

33+

3+

3+

3 + 4

3 + 4

3 + 4

3 + 4

3+

 

Zafar

;1−

;1+

;

11+

;1

;1−

;1

;1

11+

 

Steklovidnaya-24

;2

3 + 

3+

12−

1 + 2

33+

3

3

12

 

SIETE-CERROS-66

;12

3+

3+

3+

33+

3+

3+

3+

3+

 

Krasnodarskaya-99

2 + 3

3+

3+

33+

2 + 3

3+

3+

3+

3+

 

Jayhun

3+

33+

3+

3+

;

3+

3+

3+

3+

 

IZ-80

33+

3+

;1

33+

3

3

;

3+

11+

 

AIKT-20

0;

0;

3

2

;

;

;

;

;

 

OTUS TOBA 97

;

;12−

;

;1

;1−

;

;

33+

;1−

Lr16, Lr26

PASTOR/3/VORONA

;

;12

;

;1

;1−

;1−

3

;

11+

 

CMN82A.1294/2*

;

;12

;

;1+

;1−

;11+

3

33+

11+

 

HUAVUN INIA

;

;12

0;

;12

;

;

11+

2 + 3

;1−

Lr16

Trakua Hatti

;2−

2

3+

3

2 + 3

2 + 3

33+

3+

11 + 2−

 

Murodi-2013

;

;1+

;12

12

12+

12+

33+

;

1 + 2

 

CHEN/AE.SQ//WEAVER/3/PASTOR

;1

22+

3

3

33+

33+

33+

33+

12

 

Ganj

;

22+

;1

11+

;1

;1

;

;

;1−

 

NAC/TH.AC//3*PVN/3/MIRL

;

22+

;

11+

;1

;1

;

;

;1−

 

Safedaki Pomir

3

2+

 

;1

  

3+

 

3+

 

Safedaki Ishkoshim

   

1+

  

3+

3+

  

Babilo Pomir

         

Not tested

Molecular marker analysis for Lr26 is presented in Table 8

Accessions exhibiting infection types of; 0 to 2 + were classified as resistant and those exhibiting 3–4 were classified as susceptible at the seedling stage

Table 8

Molecular marker analysis to determine the presence and absence of postulated Sr, Yr and Lr seedling and APR genes

Accession

PBC

LTN

Sr2/Yr30/Lr27

Yr2

Sr6

Sr31/Yr9/Lr26

Sr38/Yr17/Lr37

Lr34/Yr18/Sr57

Sr, Yr and Lr gene

Xgwm533

XcsSr2

wMAS000005

Xwmc364

Xcfd43

Xscm9

Xiag95

XREMS1303

VENTRIUP/LN2

csLV34

wMAS000003

Navruz

0

0

 

Sarvar

3

0

+

Sr2/Yr30/Lr27

Vahdat

2

3

+

*

+

+

Sr2/Yr30/Lr27, Lr34/Yr18/Sr57

Yusufi

3

1

+

*

Sr2/Yr30/Lr27

Isfara

1

3

+

*

+

+

Lr34/Yr18/Sr57

Alex

2

3

+

+

+

+

+

Sr2/Yr30/Lr27, Sr31/Yr9/Lr26, Lr34/Yr18/Sr57

Sadokat

1

3

+

+

+

+

+

+

Sr2/Yr30/Lr27, Sr31/Yr9/Lr26, Lr34/Yr18/Sr57

Ziroat-70

2

3

+

+

+

+

+

+

Sr2/Yr30/Lr27, Sr31/Yr9/Lr26, Lr34/Yr18/Sr57

Iqbol

1

3

+

*

+

+

Lr34/Yr18/Sr57

Shokiri

1

3

+

*

+

+

Lr34/Yr18/Sr57

PRINA/STAR

1

3

+

*

+

+

Lr34/Yr18/Sr57

Jagger

0

0

*

*

+

Sr38/Yr17/Lr37

SIETE-CERROS-66

1

1

+

+

*

Sr6

IZ-80

1

1

+

*

+

Sr38/Yr17/Lr37

OTUS TOBA 97

2

3

+

+

+

+

+

+

Sr2/Yr30/Lr27, Sr31/Yr9/Lr26, Lr34/Yr18/Sr57

PASTOR/3/VORONA/CN079

2

1

+

*

Sr2/Yr30/Lr27

HUAVUN INIA

1

3

+

*

+

+

Lr34/Yr18/Sr57

Murodi-2013

2

2

+

*

+

+

Sr2/Yr30/Lr27, Lr34/Yr18/Sr57

CHEN/AE.SQ//WEAVER/3

2

2

+

*

+

+

Sr2/Yr30/Lr27, Lr34/Yr18/Sr57

Ganj

2

1

+

*

Sr2/Yr30/Lr27

NAC/TH.AC//3 * PVN/3/MIRLO

2

1

+

*

Sr2/Yr30/Lr27

Safedaki Ishkoshim

0

2

*

*

*

+

+

Lr34/Yr18/Sr57

+  Presence − or absence of the genes according to corresponding marker alleles, and * indicates molecular markers not applied

wMAS000005 and wMAS000003 KASP markers were obtained from the MAS protocols: https://maswheat.ucdavis.edu/protocols/index.htm

The presence of PBC (Pseudo-Black Chaff) and LTN (Leaf Tip Necrosis) phenotypes were assessed using 0–4 scale in the field, and in addition were confirmed with linked molecular markers

Field stem rust responses

For all of the stem rust field evaluations in Kenya, Turkey, and USA, a high level of disease pressure was attained as severities were 100% in susceptible controls. Some accessions showing no discernible seedling resistance exhibited high levels of APR in the field evaluations (Table 5). Thus, despite susceptibility at the seedling stage for TTKSK and TTKST, accessions PASTOR/3/VORONA/CN079 (10MSS), CMN82A.1294/2* (50MR) and HUAVUN INIA (40MR) against the Pgt race TTKSK + TTKST were exhibited APR during 2010 and 2011 in Njoro (Table 5). Furthermore, the accessions Vahdat, Somoni, Iqbol, Fayzbaksh, Kaboi Panjakent, and Surkhaki-5 exhibited disease severities of 5 to 40% with R to MR infection types, whereas Murodi-2013, Ganj, Krasnodarskaya-99, and Babilo Pomir had severities of 20 to 40% with MR-MS or MS infection types against race TKTTF in Izmir (Table 5). To race MCCFC in the USA, Navruz, Starshina, Basirbey, Kaboi Panjakent, Surkhaki-5, Steklovidnaya-24, Jayhun, Safedaki Pomir, and Safedaki Ishkoshim exhibited severities of 5 to 40% with RMR to MRMS and MS infection types (Table 5). Four accessions exhibited all stage resistance against race TTKSK + TTKST, thirteen against race TKTTF, and 32 against race MCCFC (Table 5). Thereby, these lines carry seedling resistance genes that are effective into the adult plant stage and to diverse races at three different field sites (Table 5).

Field stripe rust responses

Stripe rust APR was detected in the seedling-susceptible accessions of Vahdat, Isfara, and Ormon (severities of 10 to 20% with infection types of R to MR) and also in Tacikar and CMN82A.1294/2* (severities of 40 to 50% with MR-MS infection types) against Pst race TK34/11 (Table 6). Somoni and Tacikar also possess some APR as they exhibited a stripe rust severity of 40% with MS infection types against race TJ01a/10 in Tajikistan. A total of twenty-one and eighteen accessions had all-stage resistance as they were highly resistant at both the seedling and adult plant stages to Pst races TK34/11 and TJ01a/10 in Turkey and Tajikistan, respectively (Table 6). The rest of the wheat accessions were susceptible at the seedling and adult plant stages (Table 6).

Phenotypic assessments of PBC and LTN in the field

The presence of the PBC and LTN phenotypes were associated with the pleiotropic Sr2/Yr30/Lr27 and Lr34/Yr18/Sr57 APR genes. The PBC phenotype (score of 2–3) was observed in 11 accessions, and the LTN phenotype (score of 2–3) was observed in 13 accessions in the field (Table 8).

Molecular marker analysis

The molecular markers Xscm9 (220 bp), Xiag95 (1100 bp) and Xrems1303 (309 bp) indicated the presence of the Sr31/Yr9/Lr26 resistance genes in Alex, Sadokat, Ziroat-70, and OTUS TOBA 97. Marker Xcfd43 (215 bp) indicated the presence of Sr6 in SIETE-CERROS-66, and marker VENTRIUP/LN2 (262 bp) indicated the presence of the Sr38/Yr17/Lr37 genes in Jagger and IZ-80. Marker Xgwm533 (120 bp), which is linked to the Sr2/Yr30/Lr27 pleiotropic resistance gene, was amplified in 25 accessions with the PBC phenotype (score 1–3) (Table 8). Markers XcsSr2 (172 bp) and wMAS000005 did not detect the presence of Sr2/Yr30/Lr27 in any accessions, while marker Xgwm533 detected its presence in all accessions with the PBC phenotype (score 1–3) (Table 8). Initially, all accessions with and without the LTN phenotype (score 0–3) were screened with the csLV34 (150 bp) marker. In thirteen cases, this marker indicated the presence of the Lr34/Yr18/Sr57 APR resistance genes, which were subsequently validated by the wMAS000003 Kompetitive Allele Specific PCR (KASP) marker (Table 8). Use of KASP marker wMAS000005 positively detected the presence of Sr2/Yr30/Lr27 in Hope and CS-Hope DS 3B, but failed to do so in the Tajik accessions; thus, this KASP marker is located in the “Hope and CS Hope DS 3B” allele. The Xwmc364 (207 bp) marker was used on all accessions to detect the presence of Yr2, but all of them amplified a 201 bp marker allele, indicating the absence of Yr2.

Discussion

In this study, we identified the presence of major-effect (seedling) and pleiotropic APR genes conferring resistance against three important rust diseases, i.e. stem rust, stripe rust and leaf rust pathogens in wheat cultivars, landraces and advanced breeding lines that are widely cultivated and used in the national wheat breeding program in Tajikistan. The major-effect resistance genes identified by seedling and adult plant responses, and molecular marker analysis were Sr5, Sr6, Sr11, Sr31/Yr9/Lr26, Sr38/Yr17/Lr37, Yr27, and Lr16. Additionally, the pleiotropic APR genes of Sr2/Yr30/Lr27 and Lr34/Yr18/Sr57 were also identified based on the PBC and LTN phenotypes in the field and confirmed with linked molecular markers. The APR gene Lr37 was detected by a molecular marker (VENTRIUP/LN2), which is completely linked with the Sr38/Yr17 genes. In addition, pedigree information (http://wheatpedigree.net/) also was used to augment gene postulation data. A number of the wheat accessions showed resistance to all races of the three rusts used in this study, and their infection type pattern did not correspond to the avirulence/virulence profiles of the races as identified on the differential accessions. Therefore, the resistance genes present in these accessions could not be postulated. We conclude that these accessions carry previously described gene(s) in combinations or new genes. To elucidate the genetic basis of resistance in these widely resistant accessions, biparental crosses, allelism tests and/or additional phenotyping tests with a wider array of rust races should be implemented (Li et al. 2015; Randhawa et al. 2015). The resistance gene Sr5 in Navruz and Sr6 and Sr11 in Siete-Cerros-66 were identified in this investigation. Navruz is commonly used as a control in all wheat breeding nurseries and official trials (Husenov et al., 2015), and Siete-Cerros-66 has been cultivated by Tajik farmers since 1970 (Muminjanov et al. 2008). Sr5, Sr6, and Sr11 have been effective and valuable stem rust resistance genes; however, Pgt races with virulence for these genes are spreading in many wheat growing regions worldwide (Singh et al. 2015). Combinations of seedling and APR genes (i.e. Sr2/Yr30/Lr27, Sr31/Yr9/Lr26, Lr34/Yr18/Sr57, Lr16 etc.) were also present in some of the accessions (Table 8), thus being promising sources for improved resistance to rusts in Tajik breeding programs. Gene pyramiding using the pleiotropic APR genes of Sr2/Yr30/Lr27 and Lr34/Yr18/Sr57 in a combination with seedling resistance genes in several wheat breeding programs has provided durable rust resistance (Ellis et al. 2014).

Four wheat accessions (Alex, Sadokat, Ziroat-70 and Otus Toba 97) were identified as carrying the Sr31/Yr9/Lr26 resistance genes. Accessions possessing this gene complex are known to have the 1BL.1RS wheat-rye translocation, originating from Petkus rye (Friebe et al. 1996). The Sr31/Yr9/Lr26 complex is very common in wheat accession due to the wide utilization of the wheat cultivars Kavkaz and Aurora in CIMMYT breeding programs worldwide (Rajaram et al. 1983). The individual genes in this complex have been overcome by virulent races of Pgt, Pst and Pt, respectively, in various wheat growing regions (Pretorius et al. 2000; Chen et al. 2010; Huerta-Espino et al. 2011; Wellings 2011). Sr31 has provided durable resistance to stem rust for more than 30 years, and still remains an effective source of resistance to many Pgt races with the exception of those in the Ug99 race group. Races of Pst with virulence for Yr9 have been reported from all major wheat production areas in Tajikistan based on trap nurseries and race surveys (http://wheatrust.org/). Additionally, virulence against the leaf rust resistance gene Lr26 is common in Tajikistan (Kolmer and Ordoñez 2007) and many other parts of the world. Thus, although the resistance genes on the 1BL.1RS translocation do not confer a high degree of resistance towards new races of the rust pathogens, wheat accessions carrying this translocation are cultivated throughout the country. Two wheat cultivars widely cultivated in Tajikistan (Jagger and IZ-80) were identified as possessing the Sr38/Yr17/Lr37 gene complex. Previous studies have characterized the Sr38/Yr17/Lr37 locus as a translocation of chromosome 2NS from Triticum ventricosum replacing the homoeologous region of 2AS in Triticum aestivum; thus, this translocation confers resistance against a range of races of Pgt, Pst and Pt (Helguera et al. 2003). The presence of Yr27 in Isfara and Lr16 in Iqbol, OTUS TOBA 97 and Murodi-2013 were postulated. Lr16 is known as an effective source of leaf rust resistance in wheat (Kolmer and Hughes 2013) and should provide stable resistance when pyramided with Lr27, Lr34, and Lr37 in the Tajik breeding program for the developing resistant wheat cultivar.

Both phenotyping (using 0–4 scale for the PBC phenotype) and genotyping (using the Xgwm533, XcsSr2, and wMAS000005 markers) were applied for detection of the Sr2/Yr30/Lr27 APR genes; thus, only 25 accessions with the Xgwm533 marker (score 1–3 for the PBC phenotype) were identified. However, only eleven accessions were considered to truly possess the Sr2/Yr30/Lr27 APR genes based on the Xgwm533 marker and PBC phenotype, i.e. score of 2 for medium pigmentation and 3 for high pigmentation (Table 8). The PBC phenotype is known to be associated with the Sr2/Yr30/Lr27 gene complex, although its expression is sometimes variable due to both the genotype and environment (McFadden 1930). In addition, the PBC phenotype is genetically associated with several quantitative trait loci (QTL) on the chromosome arms 2DS, 3BS, 4AL, and 7DS (Juliana et al. 2015). With respect to the molecular markers in the present study, XcsSr2 and wMAS000005 were only able to identify the Sr2/Yr30/Lr27 APR genes in the Hope and CS-Hope DS 3B lines, while the Xgwm533 marker positively detected the gene complex in 25 accessions. These results corroborate previous investigations that showed no perfect match between amplification of the XcsSr2/wMAS000005 and Xgwm533 markers in various accessions (Mago et al. 2011; Pretorius et al. 2012). Thus, in the present study, the PBC phenotype, with scores of 1–3 in 25 accessions, showed a high degree of correlation with amplification of the Xgwm533 marker. However, the Xgwm533 marker may also positively amplify even when Sr2/Yr30/Lr27 is not present in certain wheat accessions (Spielmeyer et al. 2003; Mago et al. 2011). Hope and CS-Hope DS 3B (172 bp) have been shown to carry Sr2/Yr30/Lr27 based on studies using the XcsSr2 marker (Mago et al. 2011). Initially, Sr2 was reported to be linked with the PBC phenotype in the cultivar Hope; thus, this phenotypic trait has become a valuable selection trait for wheat breeders in the field (McFadden 1930). The KASP marker wMAS000005 identified the allele in Hope and CS-Hope DS 3B, thereby identifying the presence of Sr2/Yr30/Lr27. However, this marker failed to amplify any signal in the Tajik wheat, thus indicating the absence of Sr2/Yr30/Lr27. Molecular markers csLV34 and wMAS000003 successfully identified the presence of the Lr34/Yr18/Sr57 APR genes in 13 accessions; therefore, these markers can be reliably used with LTN phenotype for assessing APR genes. In addition to gene postulation, the Xwmc364 marker can be used to confirm the presence or absence of Yr2 gene. This Xwmc364 (207 bp) marker positively confirmed Yr2 in the Kalyansona and Heines VII differential accessions, but amplified the 201 bp or null allele in all of the Tajik accessions, suggesting the absence of Yr2.

In this study, we demonstrated that some of the evaluated accessions carry seedling and pleiotropic APR resistance genes against all the used rust races. Thereby, our results show that some of the wheat accessions may be used as a diverse source of rust resistance. The gene postulation, together with the use of molecular markers, successfully applied to detect the presence of known seedling and APR genes in some of the evaluated accessions. Moreover, the genetic basis of resistance in some accessions should be characterized through other genetic analyses because gene postulation and molecular markers failed to do so in this study. In the meantime, these accessions can be used by the national wheat breeding program in Tajikistan as crossing parents to develop new varieties with durable rust resistance.

Notes

Acknowledgment

Funding from the Monsanto’s Beachell-Borlaug International Scholars is gratefully acknowledged. We thank Kenyan Agricultural and Livestock Research Organization Food Crops Research Center and CIMMYT-Kenya for conducting stem rust field screenings in Kenya, Njoro. The authors appreciate Dr. James Kolmer for his supervision in the leaf rust seedling resistance test at USDA-ARS-CDL.

Author’s contribution

MR designed the study and was responsible for conducting all experiments. MO and HM developed some of the wheat accessions and provided seeds. MNR and BJS supervised the stem rust seedling and adult plant tests in the University of Minnesota and USDA-ARS-CDL in USA. MSH supervised the stripe rust seedling test in the GRRC in Denmark. KN supervised the stem rust and stripe rust seedling and adult plant tests in the RCRRC in Turkey. MNR, BJS, and EJ supervised the overall study. MR wrote the manuscript and all authors contributed to writing and editing the manuscript.

Compliance with ethical standards

Conflict of interest

All authors have no conflict of interest.

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© The Author(s) 2019

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of Plant BreedingSwedish University of Agricultural SciencesAlnarpSweden
  2. 2.Tajik Agrarian UniversityDushanbeTajikistan
  3. 3.Cereal Disease LaboratoryUnited States Department of Agriculture-Agricultural Research ServiceSt. PaulUSA
  4. 4.Department of AgroecologyAarhus UniversitySlagelseDenmark
  5. 5.Regional Cereal Rust Research CenterAegean Agricultural Research InstituteIzmirTurkey
  6. 6.Department of Plant PathologyUniversity of MinnesotaSt. PaulUSA

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