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. 2019 Jul;121:7–10. doi: 10.1016/j.cropro.2019.03.003

Primary hexaploid synthetics: Novel sources of wheat disease resistance

Vladimir Shamanin a, Sergey Shepelev a, Violetta Pozherukova a, Elena Gultyaeva b, Tamara Kolomiets c, Elena Pakholkova c, Alexey Morgounov d,
PMCID: PMC6559260  PMID: 31274944

Abstract

Climate change is leading to increased occurrence of and yield losses to wheat diseases. Managing these diseases by introducing new, effective and diverse resistance genes into cultivars represents an important component of sustainable wheat production. In 2016 and 2017 a set of primary hexaploid synthetic wheat was studied under high disease pressure: powdery mildew, leaf and stem rust in Omsk; Septoria tritici and S. nodorum in Moscow. A total of 28 synthetics (19 CIMMYT synthetics and 9 Japanese synthetics) were selected as having combined resistance to at least two diseases in both years of testing. Two synthetics (entries 13 and 18) originating from crosses between winter durum wheat Ukrainka odesskaya-1530.94 and various Aegilopes taushii accessions, and four synthetics (entries 20, 21, 23 and 24) from cross between Canadian durum wheat Langdon and Ae. taushii were resistant to all four pathogens. Pathological and molecular markers evaluation of resistance suggests presence of new genes and diverse types of resistance. The novel genetic sources of disease resistance identified in this study can be successfully utilized in wheat breeding.

Keywords: Wheat, Rusts, Powdery mildew, Septoria, Genetic resistance

Highlights

  • Primary synthetics demonstrated resistance to several important diseases.

  • Six entries were resistant to powdery mildew, leaf/stem rust, Septoria in 2016/17.

  • Resistance type varied from immunity to slow disease development.

  • The resistance is controlled by both known and possibly new genes.

  • The novel genetic sources of resistance are valuable for wheat breeding.


Wheat is a staple food crop and provides about 20 percent of protein and calories consumed per capita (CRP WHEAT, 2016). It is grown on approximately 225 million hectares worldwide with a significant portion produced as a short season crop planted in April–May and harvested in August–September in high-latitude regions above 45 °N. The western Siberia region of Russia and northern Kazakhstan cultivates 17–18 million ha of spring wheat. This region plays an important role in regional and global food security as most of the grain produced is traded. The wheat production environment, biotic and abiotic stresses, breeding system, and varieties cultivated in the region have been described by Morgounov et al. (2000).

Leaf rust is historically the major wheat disease in this area and occurs nearly every year. However, in the last five to seven years, stem rust prevalence has been increasing and caused epidemics over 1–2 million ha in 2015–2017 with estimated crop losses of 20–30 percent. Septoria spp. is also causing increasing damage to wheat as zero tillage technologies become more popular. Unfortunately, the majority of cultivars are susceptible to the dominant diseases and there is limited genetic diversity of resistance genes available for use in breeding programs (Shamanin et al., 2016). This study therefore aimed to identify and characterize novel sources of spring wheat resistance to major pathogens.

Wild wheat relatives have been successfully used to identify and incorporate new disease resistance genes in wheat. Moreover, synthetic hexploid wheat has recently been used as a bridge to incorporate more genomes of wild species. The most popular synthetics are based on crosses between durum wheat (Triticum turgidum sp. durum, genome AB) and Ae. taushii (bread wheat D genome progenitor). Synthetic wheat plants resemble the semi-wild type with tight, hardly threshable spikes and poor agronomic performance, yet they contain new diversity for resistance to numerous abiotic stresses, diseases, and pests (Ogbonnaya et al., 2013). This study utilized two groups of germplasm (Supplement 1): 1) Synthetics developed by CIMMYT from crosses between winter durum wheat varieties from Ukraine and Romania and Ae. taushii from the Caspian Sea basin, as described by Morgounov et al. (2018), and 2) Synthetics developed in Japan from crosses between the US durum cultivar Langdon and Ae. taushii selected from the global diversity collection (Matsuoka et al., 2007).

Field experiments were conducted in 2016 and 2017 at Omsk, Russia, in replicated trials with a plot size of 1 m2. Experiments were planted in mid-May (after fallow) in both years and were harvested in early September. Plants' reactions to powdery mildew (Erisyphe graminis), leaf rust (Puccinia recondita), and stem rust (Puccinia graminis) were evaluated under natural disease pressure. In both years, 4–5 severity readings were taken for each disease and the Area Under Disease Progress Curve (AUDPC) was calculated. Common agronomic traits were recorded including days to heading, plant height, and yield components. Seedlings’ reactions to leaf rust was conducted using local Chelyabinsk population of the pathogen. The presence of molecular markers to resistance genes Lr9, Lr10, Lr19, Lr20, Lr21, Lr24, Lr26, Lr34, Lr37, Lr41, Lr67, Sr2, and Sr42 were evaluated using established protocols (http://maswheat.ucdavis.edu). Resistance to Septoria sp. was evaluated in the field under separate artificial inoculations of S. nodorum and S. tritici in the Moscow region during 2017. For all diseases, entries were classified into four main categories based on severity and AUDPC: R-resistant; MR-moderately resistant; MS-moderately susceptible; and S-susceptible (Supplement 2).

A total of 28 synthetics (19 CIMMYT synthetics and 9 Japanese synthetics) demonstrated combined resistance to at least two diseases in both years of testing (Supplement 1). Six synthetics (entries 13, 18, 20, 21, 23 and 24) were resistant to all four pathogens. Leaf rust severity and AUDPC for 2016 and 2017 is presented in Table 1. Local check variety Serebristaya showed high severity, indicating substantial disease pressure. Eleven entries demonstrated MR or R reactions across both years including six synthetics (entries 13, 14, 15, 19, 21, and 22), which possessed the Lr41 gene, either singly or in combination with other genes. This gene derives from Ae. taushii (Singh et al., 2004) and is effective against Siberian rust populations. Resistant entry 7 possessed Lr21, which is not effective against local rusts, suggesting that there are additional genes involved. Remaining four resistant synthetics did not possess known Lr genes. Entry 25 (LDN/Ae.tau.(KU-2092)) combined resistance to leaf rust at both the seedling and adult plant stages, suggesting presence of a major gene. Synthetics 20 (LDN/Ae.tau.(IG-126387)), 24 (LDN/Ae.tau.(KU-20-9)) and 28 (LDN/Ae.tau.(KU-2105)) were susceptible at the seedling stage but resistant in the field, indicating the presence of possibly new adult plant resistance genes.

Table 1.

Reaction of primary hexaploid synthetics to leaf rust, Omsk, Russia, 2016–2017.

Entry no. Pedigree Reaction,a 2016-17 Severity,b %
AUDPC,ccm2
Seedlings reactiond Genese
2016 2017 2016 2017
Serebristaya (Check) S-S 80 53 1597 1248 3–4
1 Aisberg/Ae.tau.(369) S-S 55 65 985 1392 3–4 Lr10,Lr34
2 MS-S 60 50 1097 999 3 Lr10
3 S-MS 40 55 797 954 3–4
4 MS-MS 30 60 862 1302 0
5 Aisberg/Ae.tau.(511) MS-S 30 8 787 128 3
6 MS-R 20 20 607 507 3 Lr10
7 Pandur/Ae.tau.(223) MR-MR 50 25 1107 464 4 Lr21
8 S-MR 50 30 932 717 2 Lr41
9 U.od.1530.94/Ae.tau.(1027) MS-MS 60 35 1107 703 3
10 S-MS 60 23 1097 420 4
11 S-MR 40 35 937 852 3–4 Lr21
12 MS-MS 5 15 137 324 3
13 R-R 0 13 0 195 0 Lr10,Lr41
14 U.od.1530.94/Ae.tau.(310) R-R 10 13 245 248 0–1 Lr41
15 R-R 40 15 745 290 0 Lr34,Lr41
16 U.od.1530.94/Ae.tau.(392) MS-R 80 50 1535 964 3–4
17 U.od.1530.94/Ae.tau.(458) S-MS 40 55 762 1128 3–4 Lr24
18 U.od.1530.94/Ae.tau.(629) MS-S 0 8 0 160 0
19 U.od.952.92/Ae.tau.(1031) R-R 50 15 547 261 3 Lr41
20 LDN/Ae.tau.(IG-126387) MR-R 25 13 602 248 3
21 LDN/Ae.tau.(IG-131606) MR-R 20 8 482 128 3–4 Lr41
22 LDN/Ae.tau.(IG-48042) MR-R 40 8 927 128 3–4 Lr41
23 LDN/Ae.tau.(KU-2075) MS-R 20 8 265 93 1–2 Lr41
24 LDN/Ae.tau.(KU-20-9) R-R 30 15 535 239 3
25 LDN/Ae.tau.(KU-2092) MR-R 40 30 807 417 0
26 LDN/Ae.tau.(KU-2093) MS-MR 50 30 982 487 4
27 LDN/Ae.tau.(KU-2096) MS-MR 10 8 182 130 3
28 LDN/Ae.tau.(KU-2105) R-R 50 25 1317 364 4
a

R-Resistant. MR- Moderately resistant, MS – Moderately susceptible, S- susceptible. First reading for 2016, 2nd reading for 2017.

b

Highest severity recorded during the season.

c

Area under disease progress curve calculated using 5 reading in 2016 and 4 readings in 2017.

d

Seedlings reaction (0; 1; 2 – resistant, 3; 4 – susceptible) to Chelyabinsk leaf rust population (Virulence/avirulence: 1,2a,2b,2c,3a,3bg,3ka,9,10,11,14a,14b,15,16, 17,18,20,21, 30/19,23,24,26,29) conducted by All-Russian Crop Protection Institute (St. Petersburg).

e

Molecular markers were used for identification of the following genes: Lr9, Lr10, Lr19, Lr20, Lr21, Lr24, Lr26, Lr34, Lr37, Lr41, Lr67.

Most of the synthetics (21 of 28) were resistant to stem rust under high disease pressure, while severity on the local check exceeded 80% in 2016 and 40% in 2017 (Table 2). Near immunity was recorded for entries 5 (Aisberg/Ae.tau.(511)), 9 (U.od.1530.94/Ae.tau.(1027)), 18 (U.od.1530.94/Ae.tau.(629)), and 26 (LDN/Ae.tau.(KU-2093)). The study only evaluated the presence of two genes: Sr2 and Sr42. None of the genotypes possessed gene Sr2. Eight synthetics carried gene Sr42 including six resistant to stem rust in both years. This gene is located on chromosome 6DS provides resistance to the Ug99 stem rust race TTKSK (Gao et al., 2015). Obviously, it migrated to the synthetics from Ae. taushii. Evaluation of the stem rust trap nursery demonstrated that the Sr42 gene is not as effective in Siberia, with severity reaching 40MS. However, it may contribute to reduced severity of stem rust. Variety Langdon, which was used as a durum parent in Japanese synthetics, is known to possess Sr9e (Luig, 1993). This gene provides intermediate protection under Siberian conditions with severity 10MS-20S. So high frequency of stem rust resistant synthetics is explained by contribution of genes from both parents. A recent study of stem rust resistant material in Siberia (Shamanin et al., 2016) demonstrated a very narrow genetic basis of resistance. Given that the majority of spring wheat cultivars from Siberia and Kazakhstan are highly susceptible to stem rust, these new, resistant synthetics offer valuable parental material.

Table 2.

Reaction of primary hexaploid synthetics to stem rust and powdery mildew, Omsk, Russia, 2016–2017.

Entry no. Pedigree Stem rust
Powdery mildew
Reaction, 2016-17 Severity,a %
AUDPCb,cm2
Genes Reaction, 2016-17 Severitya, %
AUDPCb,cm2
2016 2017 2016 2017 2016 2017 2016 2017
Serebristaya (Check) S-S 80 40 1011 725 S-S 80 70 1789 1870
1 Aisberg/Ae.tau.(369) MR-MR 50 15 478 207 R-R 0 20 0 367
2 MR-MS 40 18 448 320 R-MR 10 30 267 737
3 MR-R 40 5 375 67 R-MR 0 30 0 705
4 MR-R 30 5 330 84 R-R 10 10 267 277
5 Aisberg/Ae.tau.(511) R-R 0 10 0 102 MR-S 30 85 807 2112
6 MR-MS 20 20 418 347 Sr42 MR-MS 30 70 807 1382
7 Pandur/Ae.tau.(223) MR-R 30 5 314 49 Sr42 R-MR 10 35 267 677
8 MS-R 50 5 613 67 R-R 50 10 447 277
9 U.od.1530.94/Ae.tau.(1027) R-R 15 8 213 128 MS-MR 70 50 1087 987
10 MR-MR 30 20 275 277 R-MS 10 65 217 1237
11 MR-MS 40 25 400 347 MR-S 30 70 557 1587
12 S-MS 70 35 1048 574 R-R 0 10 0 277
13 MR-R 50 13 448 180 R-R 0 10 0 277
14 U.od.1530.94/Ae.tau.(310) MS-MR 60 13 608 226 R-MR 0 35 0 790
15 MR-R 20 8 255 128 MR-MR 30 25 557 552
16 U.od.1530.94/Ae.tau.(392) R-R 20 5 230 49 Sr42 R-R 10 20 142 482
17 U.od.1530.94/Ae.tau.(458) R-R 20 13 245 163 S-MR 80 30 1782 687
18 U.od.1530.94/Ae.tau.(629) R-R 5 13 60 180 R-R 10 10 267 277
19 U.od.952.92/Ae.tau.(1031) MR-MR 30 15 389 207 Sr42 R-MR 10 40 217 935
20 LDN/Ae.tau.(IG-126387) MR-R 50 5 502 49 R-MR 10 30 267 762
21 LDN/Ae.tau.(IG-131606) MR-R 40 8 425 110 MR-MR 30 50 557 927
22 LDN/Ae.tau.(IG-48042) R-R 20 3 200 23 Sr42 R-MR 0 30 0 687
23 LDN/Ae.tau.(KU-2075) R-R 20 5 173 49 Sr42 R-MR 10 20 142 545
24 LDN/Ae.tau.(KU-20-9) MR-R 50 3 373 23 MR-MR 50 30 627 687
25 LDN/Ae.tau.(KU-2092) MS-R 60 0 605 0 Sr42 R-R 10 10 217 277
26 LDN/Ae.tau.(KU-2093) R-R 10 5 98 49 R-R 0 10 0 277
27 LDN/Ae.tau.(KU-2096) MR-R 30 5 275 49 S-MR 90 40 2027 780
28 LDN/Ae.tau.(KU-2105) MR-R 50 10 450 102 Sr42 R-R 10 10 267 277
a

Highest severity recorded during the season.

b

Area under disease progress curve calculated using 5 reading in 2016 and 3 readings in 2017 for stem rust and, respectively, 4 and 4 in for powdery mildew.

A high level of resistance to powdery mildew is not common in bread wheat. A total of 21 synthetics demonstrated R or MR reactions to powdery mildew in both years, including nine that were practically immune: entries 1 and 4 (Aisberg/Ae.tau.(369)); 8 (Pandur/Ae.tau.(223)); 12 and 13 (U.od.1530.94/Ae.tau.(1027)); 16 (U.od.1530.94/Ae.tau.(392)); 18 (U.od.1530.94/Ae.tau.(629)); and 25, 26, and 28 (based on durum wheat Langdon). For most of these, powdery mildew severity did not exceed 10–20% and AUDPC was below 400, while the corresponding figures for the susceptible check exceeded 70% and 1,700. Ae. tauschii has proved to be a valuable source of powdery mildew resistance, providing genes Pm2, Pm10, Pm15, Pm19, Pm34, Pm35 (Alam et al., 2011) and Pm58 (Wiersma et al., 2017). Durum wheat is a less valuable source of powdery mildew resistance, though it contributed gene Pm3h. The presence of Pm genes has not been evaluated in this germplasm but deserves attention in the future.

Resistance to Septoria tritici was evaluated under artificial field inoculation near Moscow in 2017. The susceptible check was completely defeated by S. tritici, with a severity of 100%. Most CIMMYT synthetics demonstrated MR reactions with 5–10% flag leaf severity and severity of the 2nd and 3rd leaves up to 40% (Table 3). All Japanese synthetics demonstrated R reactions with 5% flag leaf severity and 20–30% 2nd and 3rd leaf severity. Reactions to S. tritici were also evaluated at the seedling stage under artificial inoculation by recording severity and number of spores per leaf. There was no significant correlation between disease severity on seedlings and adult plant leaves. However, the correlation between field severity and number of spores per leaf was significant and varied from 0.49 (seedlings – 2nd and 3rd leaves) to 0.56 (seedlings – flag leaf). Across the traits used to evaluate reactions to S. tritici, (field and seedling severity, number of spores per leaf) the following synthetics demonstrated superior resistance: 1 and 2 (Aisberg/Ae.tau.(369)), 8 (Pandur/Ae.tau.(223)), 13 (U.od.1530.94/Ae.tau.(1027)), 15 (U.od.1530.94/Ae.tau.(310)), 18 (U.od.1530.94/Ae.tau.(629)), 24 (LDN/Ae.tau.(KU-20-9)), 25 (LDN/Ae.tau.(KU-2092)), and 28 (LDN/Ae.tau.(KU-2105)). More than 20 S. tritici resistance genes have been identified in wheat, including Stb5, Stb8, Stb16q, and Stb17 (which originated from synthetic wheat) (Brown et al., 2015). Gene Stb16q – located on chromosome 3DL and originating from Ae. taushii accession C122 – provided a high level of resistance to global isolates at both the seedling and adult plant stages (Ghaffary et al., 2012). The type of resistance to S. tritici identified in the above listed synthetics was similar to Stb16q though specific study is needed to prove it.

Table 3.

Reaction of primary hexaploid synthetics to Septoria sp., Moscow region, Russia, 2017.

Entry no. Pedigree Reaction, 2017 Field artificial inoculation severity,a %
Seedlings artificial inoculation
2nd-3rd leaves Flag leaf Spike Severity (%): S. nodorum Severity (%): S. tritici Sporesb/leaf: S.tritici
OMGAU-90 (Check) S 100 100 60 56.5 33.7 223.4
1 Aisberg/Ae.tau.(369) MR 40 5 10 66.5 8.8 5.2
2 MR 40 5 20 44.3 8.0 5.2
3 MR 40 10 10 34.0 26.0 7.8
4 MR 40 5 25 35.7 26.7 6.7
5 Aisberg/Ae.tau.(511) MS 40 50 50 70.0 19.7 5.2
6 MS 20 80 40 47.0 22.2 19.1
7 Pandur/Ae.tau.(223) MS 60 5 25 9.5 6.0 1.5
8 MR 40 10 40 35.8 0.0 0.0
9 U.od.1530.94/Ae.tau.(1027) MR 40 10 40 29.0 9.0 21.8
10 MR 40 5 20 13.0 41.2 68.7
11 MR 40 5 20 41.5 7.7 15.6
12 MR 40 5 10 25.0 21.2 23.4
13 R 20 5 25 75.4 9.5 10.9
14 U.od.1530.94/Ae.tau.(310) MS 60 20 40 25.5 10.8 45.1
15 MR 40 5 15 3.1 0.4 0.0
16 U.od.1530.94/Ae.tau.(392) MS 60 5 20 69.0 11.8 29.3
17 U.od.1530.94/Ae.tau.(458) MR 40 10 20 59.5 23.3 46.8
18 U.od.1530.94/Ae.tau.(629) MR 40 5 10 13.7 9.0 7.8
19 U.od.952.92/Ae.tau.(1031) MS 60 10 50 43.2 3.0 0.0
20 LDN/Ae.tau.(IG-126387) R 20 5 10 35.2 13.2 2.2
21 LDN/Ae.tau.(IG-131606) R 20 5 30 17.1 9.7 17.2
22 LDN/Ae.tau.(IG-48042) R 20 5 25 87.2 52.5 6.2
23 LDN/Ae.tau.(KU-2075) R 20 5 40 100.0 58.3 64.2
24 LDN/Ae.tau.(KU-20-9) R 20 5 30 32.0 6.3 1.4
25 LDN/Ae.tau.(KU-2092) R 30 5 20 32.2 10.9 0.0
26 LDN/Ae.tau.(KU-2093) R 20 5 15 37.2 26.1 13.8
27 LDN/Ae.tau.(KU-2096) R 20 0 20 69.9 20.5 120.3
28 LDN/Ae.tau.(KU-2105) R 20 5 20 39.2 2.5 0.0
a

Inoculated by S. nodorum and S. trtici.

b

The values in 1000 spores.

For the susceptible check, spike disease severity due to S. nodorum reached 60%, while it ranged from 10 to 40% for the resistant genotypes, with MR or R leaf reactions. The correlation between flag leaf and spike severity was significant and reached 0.65, while the correlation between spike severity and seedlings inoculated by S. nodorum was insignificant (0.25). Only two genotypes combined S. nodorum resistance on spikes and seedlings: 18 (U.od.1530.94/Ae.tau.(629)) and 15 (U.od.1530.94/Ae.tau.(310)). Individual genes have less of an effect on the resistance reactions to S. nodorum, compared S. tritici, and toxins play an important role (Oliver et al., 2008). Identifying and utilizing novel sources of resistance is a vital part of controlling Septoria sp.

Synthetics’ agronomic traits were evaluated in a replicated yield trial during 2017 (Supplement 3). While several entries headed earlier than the check variety Serebristaya, the majority of synthetics headed 5–12 days later than the check. Synthetic germplasm generally displayed shorter plant height and a longer spike. Spike fertility in CIMMYT synthetics, expressed by the number of grains/spike, was comparable to the check, while the Japanese synthetics had substantially lower spike fertility. Several entries displayed very large grains, with 1000 kernel weight reaching 52–57 g, or 15–20% higher than the check. All the synthetics tested, especially the Japanese material, had lower grain yield per unit area than the check.

Climate change is leading to increased occurrence of and yield losses to wheat diseases, especially in high rainfall environments. The current practices of relying on chemical protection with little contribution of genetic resistance is not sustainable. Managing these diseases by introducing new, effective and diverse resistance genes into cultivars represents an important component of sustainable wheat production. The novel genetic sources of disease resistance identified in this study can be successfully utilized in breeding to reach this goal. However, considering their poor agronomic adaption and grain yield, using these synthetics in back- or top-crosses is more likely to result in competitive products. Seeds of all germplasm presented here are available upon request.

Acknowledgements

The study was supported by the Russian Science Foundation grant to Omsk State Agrarian University (project No. 16-16-10005). CIMMYT-Turkey is supported by Turkey’s Ministry of Food, Agriculture and Livestock and CRP WHEAT. CIMMYT thanks the Bill and Melinda Gates Foundation and UK Department for International Development (DFID) for providing financial support through grant OPP1133199. Technical editing by Emma Quilligan is appreciated.

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.cropro.2019.03.003.

Appendix A. Supplementary data

The following is the Supplementary data to this article:

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