Next Article in Journal
Predicting Crop Evapotranspiration under Non-Standard Conditions Using Machine Learning Algorithms, a Case Study for Vitis vinifera L. cv Tempranillo
Next Article in Special Issue
Evaluating Scald Reactions of Some Turkish Barley (Hordeum vulgare L.) Varieties Using GGE Biplot Analysis
Previous Article in Journal
‘Soil and Plant Nutrition’—A Section of Agronomy: Advances and Perspectives
Previous Article in Special Issue
Determination of Physiochemical Characteristics Associated with Various Degrees of Cadmium Tolerance in Barley Accessions
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 13
Issue 10
10.3390/agronomy13102462
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Sources of Resistance to Powdery Mildew in Wild Barley (Hordeum vulgare subsp. spontaneum) Collected in Jordan, Lebanon, and Libya

by
Jerzy H. Czembor
* and
Elzbieta Czembor
Plant Breeding and Acclimatization Institute—National Research Institute, Radzikow, 05-870 Blonie, Poland
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(10), 2462; https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy13102462
Submission received: 20 July 2023 / Revised: 5 September 2023 / Accepted: 21 September 2023 / Published: 23 September 2023
(This article belongs to the Special Issue Barley Genetic Resources: Advancing Conservation and Applications for Breeding – Series II)
Browse Figures
Versions Notes

Abstract

:
Barley powdery mildew (BPM) is caused by the pathogen Blumeria hordei (Bh) and can lead to severe yield loss. Plant pathologists are looking for new sources of resistance to BPM. Barley accessions, including the wild subspecies Hordeum vulgare subsp. spontaneum (Hvs), are stored in many gene banks and are often a valuable source of economically important characteristics. The wild barley Hvs could be a valuable resistance source for BPM. The aim of the presented investigation was to detect new sources of BPM resistance in 81 accessions of Hvs collected in Jordan (46), Lebanon (24), and Libya (11). European differential isolates of BPM were used, and resistant single plant lines were selected for use from fifteen accessions from Jordan and Libya. These resistant single plant lines were tested for the presence of specific resistance genes using a differential set of Bh isolates. Hypotheses about the presence of specific resistance genes were made by comparing the reaction spectra of the tested lines with those of differential lines. After an analysis of the obtained results, it was concluded that all 31 tested single plant lines of Hvs had genes for resistance that are not represented in the barley differential set for resistance genes to Bh. Twenty-six lines of Hvs selected from accessions originated in Jordan and Libya showed resistance reactions to all isolates used. These lines will be further tested as new sources of effective resistance and used in barley prebreeding programs.

1. Introduction

Among cereals, barley (Hordeum vulgare L.) is the fourth-most important in the world. It is used for feed, malt, and food. Recently, the use of barley as a food has become more and more popular due to its health properties [1,2,3,4,5].
Barley’s primary gene pool includes two subspecies: domesticated barley (Hordeum vulgare subsp. vulgare) and wild barley (Hordeum vulgare subsp. spontaneum) (Hvs). Wild barley differs from cultivated barley in several traits, including a brittle rachis, and it is considered a progenitor of cultivated barley [3,6]. Hvs occurs in Southwest Asia and, most probably due to human activities, populations of Hvs are present in Morocco, Ethiopia, and Tibet [1,2].
Blumeria graminis (DC.) Golovin ex Speer f.sp. hordei Em. Marchal (Bh) is a fungus that causes barley powdery mildew (BPM). It is considered to be one of the most economically important pathogens acting on barley, and can cause significant yield losses. Many studies have shown that Bh is rapidly developing many new races and that its spores are dispersed by wind over long distances [7,8,9,10,11,12,13,14,15,16,17]. It occurs in many barley-growing regions of the world, but it is especially important in Europe. This is due to the maritime climate in most areas of Europe being suitable for the development of BPM. In addition, barley is grown in Europe in large areas and more than 60% of the world’s production of barley originates from this continent [13,14]. The average annual losses caused by this disease in barley production in Central Europe are estimated at about 10%. However, in many experiments, barley yield losses due to the occurrence of heavy infestation by BPM exceeded 25%. The grain yield obtained from barley fields where BPM was present was very often characterized by lower-quality characteristics important in malt production, such as higher grain protein content and lack of proper grain size uniformity [18,19,20].
Chemical control and agronomic practices are used to reduce BPM incidence. However, these methods are often not effective, and, in addition, there is a growing emergence of BPM resistance to fungicides [21,22]. A commonly used method to control BPM is the incorporation of new effective genes for powdery mildew resistance into barley cultivars [13,23]. This is the most effective and environmentally safe method to control this disease. Effective resistance not only protects the cultivated varieties but also reduces the production of inoculum and the spread of the pathogen to larger areas, leading to epiphytosis [12,13,14,24,25,26]. In most cases of growing cereals, including barley, in agricultural practice, control against fungal pathogens is based on integrated pest management (IPM) principles [23,27,28]. This approach to managing pests is based on combining biological, cultural, physical, and chemical methods to minimize economic, health, and environmental risks. Recently, the use of genetic resistance as a component of IPM has become more important due to the implementation of more environmentally friendly agricultural policies in many countries of the world [28,29].
In the last century, many gene banks were established because of increasing crop erosion. The main goal of gene banks is to preserve key plant genetic resources in order to meet current and future needs concerning food production [30,31,32,33]. This is achieved by introducing them into breeding programs to achieve biological progress and for use in direct production. To achieve this effectively, there is a need for phenotyping and genotyping data for major gene bank collections [6,30,31,32,33,34,35]. There are large collections of the genus Hordeum stored in many gene banks worldwide. It is estimated that about 485,000 accessions of this genus are stored at more than 200 institutions worldwide. These collections include H. vulgare ssp. vulgare (299,165 accessions), wild barley Hvs (32,385 accessions), and wild species of Hordeum (4681 accessions) [31,36]. However, these collections are very often duplicated and not properly characterized, especially concerning data about effective resistance to major pathogens.
Countries in West Asia and North Africa (WANA), including Jordan, Lebanon, and Libya, have diverse agroecological zones and different types of agriculture, varying in intensity. Wild barley is a widespread species in this region, and genetically diverse populations of Hvs are reported to be collected [37,38,39,40]. Currently, there is also increasing interest in the study of both landraces and Hvs as potential sources of economically important characteristics to breed cultivars resistant to abiotic and biotic stresses, well adapted to changing climate conditions [41,42,43,44,45,46,47,48].
Hvs has been used since the very beginning of genetic studies on the resistance of barley to BPM. The very first study was conducted by Biffen, in 1907, who analyzed the mode of inheritance of BPM resistance in progenies created by crossing H. vulgare with Hvs [49]. Since that time, race-specific resistance genes have mainly been identified in cultivated barley landraces [50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65] and wild barley [66,67,68,69,70,71,72,73,74,75,76,77] mostly originating from the WANA region [7,9,13]. Based on genetic studies, many specific resistant genes were described in wild barley, including Mla16-Mla21, Mla25-Mla29, Mla32, MlaLv, Mlf, Mlj, mlt, Ml(Ro), and Ml(Ve) [32,68,75]. Barley breeders used many BPM resistance genes, especially in the Mla locus and Mlra, Mlk, MlLa, Mlg, and Mlh [7,9,13]. However, many of these genes have lost their effectiveness as a result of pathogen adaptation and the emergence of virulent races to these genes [7,8,9,10,11,12,13,14]. In the last 40 years, only barley cultivars with Mlo resistance have been characterized as those with durable resistance to BPM, because no known virulence for mlo genes has been identified. This type of resistance to BPM was identified in barley mutants and in landraces, but not in Hvs [13,78,79,80].
Many studies have proved that work on the genetics of resistance to BPM using a differential set of BPM isolates can be successfully used for investigations to determine the presence of specific resistance genes in barley genetic resources [7,13,14]. New, efficient sources of resistance to BPM for proper crosses in breeding programs are crucial to conducting resistance breeding [9,13,24,25,26]. The use of seedlings in studies conducted to postulate specific BPM resistance genes using a differential set of Bh isolates was proven to be an effective and sufficient method. This method is commonly used for the characterization of barley germplasm, concerning its BPM resistance [33,50,53,60,61,62,64,65].
The presented investigation goal was to detect new sources of BPM resistance in accessions of Hvs collected in Jordan, Lebanon, and Libya.

2. Materials and Method

2.1. Plant Material

Eighty-one accessions of wild barley (H. vulgare subsp. spontaneum) (Hvs) collected in Jordan, Lebanon, and Libya were obtained from the ICARDA gene bank. These accessions were collected in 10 expeditions (LBY81, LBY82, LBY90, LBN92-2, LBN93, LBN94-1, JOR81-2, JOR85, JOR88-1, and JOR95) during the period 1981–1995 (Supplementary Materials Table S1).

2.2. Pathogen

Twenty B. graminis f. sp. hordei Em Marschal (Bh) isolates were used to determine the resistance genes present in the tested accessions. They were selected from our collection of isolates to have possessed virulence genes corresponding to the most known resistance genes used in barley resistance programs in Europe (Table 1). Isolates originated from the collections in Risø National Laboratory, Roskilde, Denmark; Danish Institute for Plant and Soil Science, Lyngby, Denmark; Edigenossische Technische Hochschule—ETH, Zurich, Switzerland; and Plant Breeding and Acclimatization Institute—National Research Institute (PBAI-NRI) IHAR-PIB Radzików, Poland. The isolates were chosen according to differences in virulence spectra that were observed on the Pallas isolines differential set and on additional cultivars with resistance genes not present in Pallas isolines [75,81]. Each of them represented a different pathotype, determined using the selected set of 20 differential Pallas isolines. Isolate Bgh33 was the most avirulent isolate in the collection.
They were purified using single pustule isolation and were maintained and propagated on young seedlings of the powdery mildew susceptible cultivar Manchuria (CI 2330). Frequent virulence checks were made to ensure the purity of isolates throughout the experiment.

2.3. Populations and Single Plant Lines Resistance Tests

In the preliminary study, thirty plants per accession were evaluated with the Bgh33 isolate. Next, the selected single plant lines represented by five plants were tested with 20 differential isolates of Bh.
All these tests were conducted under controlled conditions with a 16/8 h day/night photoperiod and a 22/16 °C temperature regime. In all tests, the cultivar Manchuria CI 2330 was used as a susceptible control.
Seedlings with a fully expanded first leaf were inoculated with Bh by shaking conidia from the susceptible cv. Manchuria CI 2330. After 8–10 days, the reaction type (RT) of plants to infection by Bh was scored. A five-point RT scale was used: 0, no visible symptoms; 0(4), sparse, small colonies originating from the stomatal subsidiary cells (Mlo resistance); 1, minute necrotic flecks, no mycelial growth, and no sporulation; 2, frequent chlorosis, reduced mycelial growth, and no or very scarce sporulation; 3, moderate mycelial growth, moderate sporulation, and occasional chlorosis; 4, profuse sporulation of well-developed colonies (Figure 1) [52,82]. Plants with RT of 0, 0(4), and 1 were classified as highly resistant (R), plants that scored 2 as moderately resistant (M), and plants with ratings of 3 and 4 as susceptible and very susceptible.

2.4. Postulation of Resistance Alleles

The postulation of the presence of resistant genes was based on a comparison of reaction spectra observed on tested accessions and the barley differential set (Table 1). This was undertaken based on the gene-for-gene hypothesis [83]. The RT observed on each accession was compared with the Bh virulence spectrum on the barley differential set.

3. Results

In the preliminary study, among 81 tested accessions of H. vulgare subsp. spontaneum collected in Jordan (46), Lebanon (24), and Libya (11), 15 accessions expressed resistance to isolate Bgh33 of Bh (Table 2, Figure 2). Eleven of them originated from Jordan (23.9% evaluated) and four from Libya (36.4% evaluated).
None of the plants with accessions from Lebanon showed powdery mildew resistance in preliminary testing with isolate Bgh33. Twelve of the tested accessions in which plants were resistant to isolate Bgh33 showed heterogenous RT to powdery mildew: three of them showed only one type of reaction, eleven showed two different types, and one showed three types (0, 2, and 4).
Among the scored resistance RTs in tested lines with 20 differential isolates, the most common reaction was 0 (immunity) (Table 3, Figure 2). This RT was observed in all tested lines, with a frequency of 65.5%. The remaining RTs occurred with frequencies of 1—0.96%, 2—31.1%, and 4—2.4%. Reaction types 3 and 0(4) were not observed. In total, 97.6 observed reactions represented resistance RTs (0, 1, and 2). The analysis was conducted, comparing the spectrum of RTs of 31 tested lines to infection with 20 differential isolates, with results observed on a differential set of barley. Based on this analysis, it was concluded that all of the tested lines had an unknown gene or genes for resistance which were not represented in the differential set. Twenty-six of these lines (83.9%) showed resistance RTs to all isolates used. After the analysis of the obtained results, it was concluded that all selected 31 single plant lines of wild barley had unknown genes for resistance, which were not represented in the Pallas isolines differential set.

4. Discussion

In the presented study, new, well-characterized sources of highly effective BPM resistance for European conditions were identified. Such well-characterized single plant lines are crucial as genetic resources for barley resistance breeding and for applying genetic control of this fungus in agricultural practice. Two major strategies for BPM control are available. The first is to use genetic control by growing resistant cultivars, and the second is the application of fungicides [2,7,13,23,27,28,29]. However, in many countries, Bh races resistant to commonly used fungicides have been described [23,27,28,29]. In addition, the cost of fungicides and concerns about the environment have led many countries to restrict their use in disease control [27,28]. Taking this into account, BPM control using effective resistance genes is increasingly important in IPM strategies in Europe and other parts of the world. In addition, breeding for resistance as a strategy to control plant pests and diseases is increasingly understood and accepted by societies as ecologically safe.
In the present study, it was confirmed that Hvs accessions from Jordan, Lebanon, and Libya are diverse and possess valuable characteristics for breeding purposes. This diversity is due to the presence of many mountainous regions and different climate zones in these countries. Such conditions are favorable for the evolution of very diverse genotypes of plants, including wild barley [37,38,39]. Powdery mildew occurs commonly in this area on barley and wild barley. Because the area of the Fertile Crescent is considered the center of origin and diversification of barley, it is also the center of the presence of very diverse resistance genes to BPM [1,2,9,10,13]. This was confirmed in the present study, in which new sources of resistance to BPM in selections from accessions of Hvs from Jordan and Libya were identified.
Eleven of these selections originated from Jordan, four from Libya, and none from Lebanon. Twelve tested accessions showed heterogenous resistance reactions to powdery mildew: three of them showed only one type of reaction, eleven showed two types, and one showed three types (0, 2, and 4). Heterogenous reactions of Hvs accessions to powdery mildew were also reported in other studies [76,77]. In populations of Hvs, BPM did not develop to levels that significantly damage plants. This is the result of both the stabilizing effect of the genetic heterogeneity within the populations of Hvs and the presence of resistance sufficient to control limited disease development [75,76,77].
In tested lines with 20 differential BPM isolates, the most common RT was 0 (immunity). This kind of RT was observed in all tested lines and with 65.5% of all observed RTs. The remaining RTs occurred with frequencies of 1—0.96%, 2—31.1%, and 4—2.4%. Reaction types 3 and 0(4) were not observed. In total, 97.6 observed reactions represented resistance RTs (0, 1, and 2). Such a high percentage of resistance RTs showed that Hvs collected in Jordan and Libya are valuable sources of resistance for European barley breeding, which is in agreement with other studies [66,67,73,74,75,76].
In the presented study, new sources of BPM resistance were identified, which are very important for applying genetic control of this fungus, because Bh is characterized by a high level of genetic variability. It can develop new races in a short time that can spread across long distances [7,8,9,10,11,12,13,14,15,16,17]. This results in a rapidly reduced number of resistance genes effectively controlling the occurrence and spread of Bh being available for barley breeders [13,14]. At the same time, modern barley cultivars, which are grown in large areas across Europe, often have no partial type of host resistance due to breeding for a variant-specific type of BPM resistance in most modern breeding programs [13,24,25]. The presence of such resistance should be investigated in tested Hvs accessions in additional specific tests, and not only in the seedling stage conducted in the presented study. It will be especially interesting to test Hvs accessions in the adult stage of plant development to identify adult plant BPM resistance. The loss of these types of resistance during the breeding process was recognized a long time ago by plant pathologists and plant breeders, and several ways to increase the durability of race-specific resistance genes were proposed. Major strategies were proposed and implemented: the use of multiline cultivars, the combining (“pyramiding”) of different resistance genes into one variety, and the deployment of many cultivars with different resistance genes in space (e.g., cultivar mixtures) or time (winter versus spring barley) [7,13,24,25]. However, for such BPM strategies for genetic control, it is very useful to introduce new and effective sources of resistance into breeding materials. Such newly identified sources of BPM resistance are still being found in barley landraces and wild relatives [13,60,61,62,63,64,65,75,76,77]. There are many examples of the new sources of resistance to BPM originating from Hvs populations being successfully used by barley breeders to develop new resistant cultivars. In most cases, these new resistance genes were deployed in new cultivars under different strategies to prolong the duration of their effectiveness against BPM 7,13,23,24]. The use of newly identified sources of resistance to BPM is important in breeding new varieties with effective resistance deployed in agriculture in various strategies. The additional advantage to barley breeders of using germplasm from Hvs is the possibility of introducing other desirable agronomic traits, e.g., tolerance to drought conditions and other biotic and abiotic stresses [41,42,43,44,45,46,47]. However, for many barley breeders, the heterogeneity of Hvs accessions is a problem because it complicates and prolongs the breeding process. Often, prebreeding activities resulting in well-characterized single plant lines of Hvs with many important economically traits, including resistance to BPM, are needed. The prebreeding activities presented here provide breeders with new BPM sources of resistance to be used in different breeding strategies [7,24,25]. The big advantage of the use of Hvs genetic resources in barley breeding is a lack of problems with sterility. Such problems are often present if H. bulbosum or mutants are used [7,13].
In the presented study, a test with a set of differential BPM isolates was used and the selection of single plant lines was conducted to identify new sources of resistance in wild barley accessions. This method was described in many studies to identify specific resistance genes in barley accessions and breeding lines [7,13,14]. In addition, it was successfully used in many studies to screen both landraces and wild barleys for new effective resistance genes [14,50,51,52,53,56,57,58,59,64,65,75,76,77]. However, for the description of the partial type of resistance to BPM, this kind of test is not sufficient. For the detection of this kind of resistance, there is a need to obtain, in addition to the RT, the measurements of resistance parameters in different stages of plant development (e.g., at the adult plant stage) [84,85]. The adult plant resistance of tested accessions should be investigated in additional specific tests because almost all wild barleys contain major specific resistance genes which very often mask minor resistance genes determining the partial resistance or the presence of adult resistance [7,13,84,85,86,87,88,89,90,91].
A very interesting genetic resource for the breeding of resistant barley is the 31 single plant lines of wild barley which have genes for resistance not represented in the BPM differential set. These newly identified sources of highly effective resistance to BPM in single plant lines of Hvs from Jordan and Libya will be used in the barley prebreeding program.
Further studies are needed to determine the mode of action of resistance genes in identified new sources of BPM resistance described in the presented study based on the results of testing hybrids resulting from crosses among appropriate genotypes [50,55,62]. In the future, some other available methods for the characterization of resistant lines will have to be used, especially those for the study of partial and adult resistance [84,85,86,87,88,89,90,91].
In addition, modern molecular methods have to be used for the further characterization of resistance genes identified to be efficiently used in barley breeding [3,86,92,93,94].

5. Conclusions

The Hvs populations from Jordan and Libya are valuable sources of BPM resistance. Selected single plant lines of Hvs may be used in prebreeding programs to provide barley breeders with new, well-characterized sources of BPM resistance. Future studies will concentrate on determining the genetic basis of resistance occurring in 31 Hvs selections. They will include the crosses of investigated selections with well-chosen parents and the development of molecular markers. To successfully introduce the described new sources of BPM resistance into barley elite cultivars, prebreeding work is needed in the creation of initial, well-characterized plant materials. A necessary step is to use barley germplasm from gene banks, first in breeding programs and second in agricultural practice, as an elite cultivar.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/agronomy13102462/s1, Table S1. Collection data of 81 accessions of wild barley (H. vulgare subsp. spontaneum) collected in Jordan, Lebanon, and Lybia.

Author Contributions

Conceptualization, J.H.C.; methodology, J.H.C.; formal analysis, J.H.C. and E.C.; investigation, J.H.C.; resources, J.H.C.; writing—original draft preparation, J.H.C. and E.C.; visualization, E.C.; project administration, J.H.C.; funding acquisition, J.H.C. All authors have read and agreed to the published version of the manuscript.

Funding

Ministry of Education and Science, Poland.

Data Availability Statement

Data are available in tables. The corresponding author is Jerzy H. Czembor, Plant Breeding and Acclimatization Institute—National Research Institute, Radzikow, 05-870 Blonie, Poland.

Acknowledgments

H. J. Schaerer (ETH, Zurich, Switzerland) is thanked for the powdery mildew isolates, and L. Munk (Royal Agricultural and Veterinary University, Copenhagen, Denmark) is thanked for the near-isogenic lines of “Pallas”.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Dai, F.; Zhang, G. Domestication and improvement of cultivated barley. In Exploration, Identification and Utilization of Barley Germplasm; Zhang, L.C., Ed.; Elsevier: Amsterdam, The Netherlands, 2016; pp. 1–26. [Google Scholar] [CrossRef]
  2. El-Hashash, E.F.; El-Absy, K.M. Barley (Hordeum vulgare L.) Breeding. In Advances in Plant Breeding Strategies: Cereals; Al-Khayri, J., Jain, S., Johnson, D., Eds.; Springer: Cham, Switzerland, 2019; pp. 1–45. [Google Scholar] [CrossRef]
  3. Dracatos, P.M.; Lu, J.; Sánchez-Martín, J.; Wulff, B.B. Resistance that stacks up: Engineering rust and mildew disease control in the cereal crops wheat and barley. Plant Biotechnol. J. 2023, 21, 1938–1951. [Google Scholar] [CrossRef] [PubMed]
  4. Geng, L.; Li, M.; Zhang, G.; Ye, L. Barley: A Potential Cereal for Producing Healthy and Functional Foods. Food Qual. Saf. 2022, 6, fyac012. [Google Scholar] [CrossRef]
  5. Lukinac, J.; Jukić, M. Barley in the Production of Cereal-Based Products. Plants 2022, 11, 3519. [Google Scholar] [CrossRef]
  6. Newton, A.C.; Akar, T.; Baresel, J.P.; Bebeli, P.J.; Bettencourt, E.; Bladenopoulos, K.V.; Czembor, J.H.; Fasoula, D.A.; Katsiotis, A.; Koutis, K.; et al. Cereal landraces for sustainable agriculture. A review. Agron. Sustain. Dev. 2010, 30, 237–269. [Google Scholar] [CrossRef]
  7. Weise, S.; Lohwasser, U.; Oppermann, M. Document or Lose It—On the Importance of Information Management for Genetic Resources Conservation in Genebanks. Plants 2020, 9, 1050. [Google Scholar] [CrossRef]
  8. Kaur, V.; Aravind, J.; Jacob, S.R.; Kumari, J.; Panwar, B.S.; Pal, N.; Rana, J.C.; Pandey, A.; Kumar, A. Phenotypic Characterization, Genetic Diversity Assessment in 6778 Accessions of Barley (Hordeum vulgare L. ssp. vulgare) Germplasm Conserved in National Genebank of India and Development of a Core Set. Front. Plant Sci. 2022, 13, 771920. [Google Scholar] [CrossRef]
  9. Khoury, C.K.; Brush, S.; Costich, D.E.; Curry, H.A.; Haan, S.D.; Engels, J.M.M.; Guarino, L.; Hoban, S.; Mercer, K.L.; Miller, A.J.; et al. Crop genetic erosion: Understanding and responding to loss of crop diversity. New Phytol. 2022, 233, 84–118. [Google Scholar] [CrossRef] [PubMed]
  10. Ramirez-Villegas, J.; Khoury, C.K.; Achicanoy, H.A.; Diaz, M.V.; Mendez, A.C.; Sosa, C.C.; Kehel, Z.; Guarino, L.; Abberton, M.; Aunario, J.K.; et al. State of ex situ conservation of landrace groups of 25 major crops. Nat. Plants 2022, 8, 491–499. [Google Scholar] [CrossRef]
  11. Brown, J.K.; Wulff, B.B. Diversifying the menu for crop powdery mildew resistance. Cell 2022, 185, 761–763. [Google Scholar] [CrossRef]
  12. Czembor, J.H.; Czembor, E.; Krystek, M.; Pukacki, J. AgroGenome: Interactive Genomic-Based Web Server Developed Based on Data Collected for Accessions Stored in Polish Genebank. Agriculture 2023, 13, 193. [Google Scholar] [CrossRef]
  13. Knupfer, R. Triticeae genetic resources in ex situ genebank collections. In Genetic and Genomics of the Triticeae. Plant Genetics and Genomics: Crops and Models; Muelbauer, G.J., Feuillet, C., Eds.; Springer Science: New York, NY, USA, 2009; Volume 7, pp. 31–80. [Google Scholar] [CrossRef]
  14. Shakhatreh, Y.; Haddad, N.; Alrababah, M.; Grando, S.; Ceccarelli, S. Phenotypic diversity in wild barley (Hordeum vulgare L. ssp. spontaneum (C. Koch) Thell.) accessions collected in Jordan. Genet. Res. Crop Evol. 2010, 57, 131–146. [Google Scholar] [CrossRef]
  15. Thormann, I.; Reeves, P.; Reilley, A.; Engels, J.M.M.; Lohwasser, U.; Börner, A.; Pillen, K.; Richards, C.M. Geography of genetic structure in barley wild relative Hordeum vulgare subsp. spontaneum in Jordan. PLoS ONE 2016, 11, e0160745. [Google Scholar] [CrossRef] [PubMed]
  16. Al-Hajaj, N.; Grando, S.; Ababnah, M.; Alomari, N.; Albatianh, A.; Nesir, J.; Migdali, H.; Shakhatreh, Y.; Ceccarelli, S. Phenotypic evolution of the wild progenitor of cultivated barley (Hordeum vulgare L. subsp. spontaneum (K. Koch) Thell.) across bioclimatic regions in Jordan. Genet. Resour. Crop. Evol. 2022, 69, 1485–1507. [Google Scholar] [CrossRef]
  17. Chang, C.W.; Fridman, E.; Mascher, M.; Himmelbach, A.; Schmid, K. Physical geography, isolation by distance and environmental variables shape genomic variation of wild barley (Hordeum vulgare L. ssp. spontaneum) in the Southern Levant. Heredity 2022, 128, 107–119. [Google Scholar] [CrossRef]
  18. Rehman, S.; Amouzoune, M.; Hiddar, H.; Aberkane, H.; Benkirane, R.; Filali-Maltouf, A.; Al-Jaboobi, M.; Acqbouch, L.; Tsivelikas, A.; Verma, R.P.S.; et al. Traits discovery in Hordeum vulgare sbsp. spontaneum accessions and in lines derived from interspecific crosses with wild Hordeum species for enhancing barley breeding efforts. Crop Sci. 2020, 61, 219–233. [Google Scholar] [CrossRef]
  19. Milner, S.G.; Jost, M.; Taketa, S.; Mazón, E.R.; Himmelbach, A.; Oppermann, M.; Weise, S.; Knüpffer, H.; Basterrechea, M.; König, P.; et al. Genebank genomics highlights the diversity of a global barley collection. Nat. Genet. 2019, 51, 319–326. [Google Scholar] [CrossRef]
  20. Capasso, G.; Santini, G.; Petraretti, M.; Esposito, S.; Landi, S. Wild and Traditional Barley Genomic Resources as a Tool for Abiotic Stress Tolerance and Biotic Relations. Agriculture 2021, 11, 1102. [Google Scholar] [CrossRef]
  21. Clare, S.J.; Oğuz, A.Ç.; Effertz, K.; Poudel, R.S.; See, D.R.; Karakaya, A.; Brueggeman, R.S. Genome-wide association mapping of Pyrenophora teres f. maculata and Pyrenophora teres f. teres resistance loci utilizing natural Turkish wild and landrace barley populations. G3: Genes|Genomes|Genetics, 11. G3 (Bethesda) 2021, 11, jkab269. [Google Scholar] [CrossRef]
  22. Henningsen, E.C.; Sallam, A.H.; Matny, O.N.; Szinyei, T.; Figueroa, M.; Steffenson, B.J. Rpg7: A New Gene for Stem Rust Resistance from Hordeum vulgare ssp. spontaneum. Phytopathology 2021, 111, 548–558. [Google Scholar] [CrossRef]
  23. Hovmoller, M.S.; Caffier, V.; Jalli, M.; Andersen, O.; Besenhofer, G.; Czembor, J.H.; Dreiseitl, A.; Flath, K.; Fleck, A.; Heinrics, F.; et al. The Eurpean barley powdery mildew virulence survey and disease nursery 1993–1999. Agonomie 2000, 20, 729–744. [Google Scholar] [CrossRef]
  24. Mehnaz, M.; Dracatos, P.M.; Park, R.F.; Singh, D. Mining Middle Eastern and Central Asian Barley Germplasm to Understand Diversity for Resistance to Puccinia hordei, Causal Agent of Leaf Rust. Agronomy 2021, 11, 2146. [Google Scholar] [CrossRef]
  25. Mehnaz, M.; Dracatos, P.M.; Pham, A.; March, T.J.; Maurer, A.; Pillen, K.; Forrest, K.L.; Kulkarni, T.V.; Pourkheirandish, M.; Park, R.F.; et al. Discovery and fine mapping of Rph28: A new gene conferring resistance to Puccinia hordei from wild barley. Theor. Appl. Genet. 2021, 134, 2167–2179. [Google Scholar] [CrossRef] [PubMed]
  26. Sayed, M.A.; Tarawneh, R.A.; Youssef, H.M.; Pillen, K.; Börner, A. Detection and Verification of QTL for Salinity Tolerance at Germination and Seedling Stages Using Wild Barley Introgression Lines. Plants 2021, 10, 2246. [Google Scholar] [CrossRef]
  27. Jørgensen, J.H.; Wolfe, M. Genetics of Powdery Mildew Resistance in Barley. Crit. Rev. Plant Sci. 1994, 13, 97–119. [Google Scholar] [CrossRef]
  28. Weibull, J.; Walther, U.; Sato, K.; Habekuß, A.; Kopahnke, D.; Proeseler, G. Diversity in resistance to biotic stresses. In Diversity in Barley (Hordeum Vulgare); Von Bothmer, R., van Hintum, T., Knüpfer, H., Sato, K., Eds.; Elsevier Science, B.V.: Amsterdam, The Netherlands, 2003; Chapter 8; pp. 143–178. [Google Scholar]
  29. Dreiseitl, A. The Hordeum vulgare subsp. spontaneum-Blumeria graminis f. sp. hordei pathosystem: Its position in resistance research and breeding applications. Eur. J. Plant Pathol. 2014, 138, 561–568. [Google Scholar] [CrossRef]
  30. Dreiseitl, A. Great pathotype diversity and reduced virulence complexity in a Central European population of Blumeria graminis f. sp. hordei in 2015–2017. Eur. J. Plant Pathol. 2019, 153, 801–811. [Google Scholar] [CrossRef]
  31. Kusch, S.; Qian, J.; Loos, A.; Kümmel, F.; Spanu, P.D.; Panstruga, R. Long-term and rapid evolution in powdery mildew fungi. Mol. Ecol. 2023. [Google Scholar] [CrossRef]
  32. Dreiseitl, A. Specific resistance of barley to powdery mildew, its use and beyond: A concise critical review. Genes 2020, 11, 971. [Google Scholar] [CrossRef]
  33. Dreiseitl, A. Powdery mildew resistance genes in European barley cultivars registered in the Czech Republic from 2016 to 2020. Genes 2022, 13, 1274. [Google Scholar] [CrossRef]
  34. Zhu, J.; Zhou, Y.; Shang, Y.; Hua, W.; Wang, J.; Jia, Q.; Liu, M.; Yang, J. Genetic evidence of local adaption and long distance migration in Blumeria graminis f. sp. hordei populations from China. J. Gen. Plant Pathol. 2016, 82, 69–81. [Google Scholar] [CrossRef]
  35. Wang, Y.; Zhang, G.; Wang, F.; Lang, X.; Zhao, X.; Zhu, J.; Hu, C.; Hu, J.; Zhang, Y.; Yao, X.; et al. Virulence Variability and Genetic Diversity in Blumeria graminis f. sp. hordei in Southeastern and Southwestern China. Plant Dis. 2023, 107, 809–819. [Google Scholar] [CrossRef] [PubMed]
  36. Wang, Y.; Zhuoma, Q.; Xu, Z.; Peng, Y.; Wang, M. Virulence and Genetic Types of Blumeria graminis f. sp. hordei in Tibet and Surrounding Areas. J. Fungi 2023, 9, 363. [Google Scholar] [CrossRef]
  37. Murray, G.M.; Brennan, J.P. Estimating Disease Losses to the Australian Barley Industry. Australas. Plant Pathol. 2010, 39, 85–96. [Google Scholar] [CrossRef]
  38. Kauppi, K.; Rajala, A.; Huusela, E.; Kaseva, J.; Ruuttunen, P.; Jalli, H.; Alakukku, L.; Jalli, M. Impact of Pests on Cereal Grain and Nutrient Yield in Boreal Growing Conditions. Agronomy 2021, 11, 592. [Google Scholar] [CrossRef]
  39. Hysing, S.C.; Rosenqvist, H.; Wiik, L. Agronomic and economic effect of host resistance vs. fungicide control of barley powdery mildew in southern Sweden. Crop. Prot. 2012, 41, 122–127. [Google Scholar] [CrossRef]
  40. Hollomon, D.W. Fungicide resistance: Facing the challenge. Plant Prot. Sci. 2015, 51, 170–176. [Google Scholar] [CrossRef]
  41. Vielba-Fernández, A.; Polonio, Á.; Ruiz-Jiménez, L.; de Vicente, A.; Pérez-García, A.; Fernández-Ortuño, D. Fungicide Resistance in Powdery Mildew Fungi. Microorganisms 2020, 8, 1431. [Google Scholar] [CrossRef]
  42. McDonald, B.A.; Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 2002, 40, 349–379. [Google Scholar] [CrossRef]
  43. Burdon, J.J.; Barrett, L.G.; Rebetzke, G.; Thrall, P.H. Guiding deployment of resistance in cereals using evolutionary principles. Evol. Appl. 2014, 7, 609–624. [Google Scholar] [CrossRef]
  44. Mundt, C.H. Pyramiding for resistance durability: Theory and practise. Phytopathology 2018, 108, 792–802. [Google Scholar] [CrossRef]
  45. Walters, D.R.; Avrova, A.; Bingham, I.J.; Burnett, F.J.; Fountaine, J.; Havis, N.D.; Hoad, S.P.; Hughes, G.; Looseley, M.; Oxley, S.J.P.; et al. Control of foliar diseases in barley: Towards an integrated approach. Eur. J. Plant Pathol. 2012, 133, 33–73. [Google Scholar] [CrossRef]
  46. Jørgensen, L.N.; Hovmoller, M.; Hansen, J.G.; Lassen, P.; Clark, B.; Bayles, R.; Rodemann, B.; Flath, K.; Jahn, M.; Goral, T.; et al. IPM Strategies and Their Dilemmas Including an Introduction to www.eurowheat.org. J. Integr. Agric. 2014, 13, 265–281. [Google Scholar] [CrossRef]
  47. Lamichhane, J.R.; Arseniuk, E.; Boonekamp, P.; Czembor, J.H.; Decroocq, V.; Enjalbert, J.; Finckh, M.R.; Korbin, M.; Koppel, M.M.; Kudsk, P.; et al. Advocating a need for suitable breeding approaches to boost Integrated Pest Management: A European perspective. Pest Manag. Sci. 2018, 74, 1219–1227. [Google Scholar] [CrossRef] [PubMed]
  48. Stetkiewicz, S.; Bruce, A.; Burnett, F.J.; Ennos, R.A.; Topp, C.F.E. An interdisciplinary method for assessing IPM potential: Case study in Scottish spring barley. CABI Agric. Biosci. 2022, 3, 23. [Google Scholar] [CrossRef]
  49. Biffen, R.H. Studies in the inheritance of disease resistance. J. Agric. Sci. 1907, 2, 109–128. [Google Scholar] [CrossRef]
  50. Czembor, J.H.; Johnston, M.R. Resistance to powdery mildew in selections from Tunisian barley landraces. Plant Breed. 1999, 118, 503–509. [Google Scholar] [CrossRef]
  51. Czembor, J.H.; Czembor, H.J. Resistance to powdery mildew in barley landraces collected from Jordan. Plant Breed. Seed Sci. 1999, 43, 65–80. [Google Scholar]
  52. Czembor, J.H. Resistance to powdery mildew in barley (Hordeum vulgare L.) landraces from Egypt. Plant Genet. Resour. Newsl. 2000, 123, 52–60. [Google Scholar]
  53. Czembor, J.H. Resistance to powdery mildew in populations of barley landraces from Morocco. Australas. Plant Pathol. 2000, 29, 137–148. [Google Scholar] [CrossRef]
  54. Czembor, J.H. Powdery mildew resistance in selections from barley landraces collected in Jordan, Egypt, Libya and Tunisia. Sci. Agric. Bohem. 2001, 32, 43–65. [Google Scholar]
  55. Czembor, J.H.; Czembor, H.J. Inheritance of resistance to powdery mildew (Blumeria graminis f.sp. hordei) in selections from Moroccan landraces of barley. Cereal Res. Comm. 2001, 29, 281–288. [Google Scholar] [CrossRef]
  56. Czembor, J.H. Sources of resistance to powdery mildew (Blumeria graminis f. sp. hordei) in Moroccan barley landraces. Can. J Plant Path Rev. Can. De Phytopathol. 2001, 23, 260–269. [Google Scholar] [CrossRef]
  57. Czembor, J.H.; Czembor, H.J. Selections from barley landrace collected in Libya as new sources of effective resistance to powdery mildew (Blumeria graminis f.sp. hordei). Rostl. Vyrob. 2002, 48, 217–223. [Google Scholar] [CrossRef]
  58. Czembor, J.H. Resistance to powdery mildew in selections from Moroccan barley landraces. Euphytica 2002, 125, 397–409. [Google Scholar] [CrossRef]
  59. Czembor, J.H.; Frese, L. Powdery mildew resistance in selections from barley landraces collected from Turkey. Die Bodenkult. 2003, 54, 35–40. [Google Scholar]
  60. Silvar, C.; Flath, K.; Kopahnke, D.; Gracia, M.P.; Lasa, J.M.; Casas, A.M.; Igartua, E.; Ordon, F. Analysis of powdery mildew resistance in the Spanish barley core collection. Plant Breed. 2011, 130, 195–202. [Google Scholar] [CrossRef]
  61. Surlan-Momirovic, G.; Flath, K.; Silvar, C.; Brankovic, G.; Kopahnke, D.; Knezevic, D.; Schliephake, E.; Ordon, F.; Perovic, D. Exploring the Serbian GenBank barley (Hordeum vulgare L. subsp. vulgare) collection for powdery mildew resistance. Genet. Resour. Crop Evol. 2016, 63, 275–287. [Google Scholar] [CrossRef]
  62. Piechota, U.; Czembor, P.C.; Słowacki, P.; Czembor, J.H. Identifying a novel powdery mildew resistance gene in a barley landrace from Morocco. J. Appl. Genet. 2019, 60, 243–254. [Google Scholar] [CrossRef]
  63. Piechota, U.; Czembor, P.C.; Czembor, J.H. Evaluating barley landraces collected in North Africa and the Middle East for powdery mildew infection at seedling and adult plant stages. Cereal Res. Commun. 2020, 48, 179–185. [Google Scholar] [CrossRef]
  64. Czembor, J.H.; Czembor, E. Mlo resistance to powdery mildew (Blumeria graminis f. sp. hordei) in barley landraces collected in Yemen. Agronomy 2021, 11, 1582. [Google Scholar] [CrossRef]
  65. Czembor, J.H.; Czembor, E. Sources of Resistance to Powdery Mildew in Barley Landraces from Turkey. Agriculture 2021, 11, 1017. [Google Scholar] [CrossRef]
  66. Fischbeck, G.; Schwarzbach, E.; Sobel, Z.; Wahl, I. Mildew resistance in Israeli populations of 2-rowed wild barley (Hordeum spontaneum). Z. Pflanz. 1976, 76, 163–166. [Google Scholar]
  67. Moseman, J.G.; Nevo, E.; Zohary, D. Resistance of Hordeum spontaneum collected in Israel to infection with Erysiphe graminis hordei. Crop Sci. 1983, 23, 1115–1119. [Google Scholar] [CrossRef]
  68. Jahoor, A.; Fischbeck, G. Identification of new genes for mildew resistance of barley at the Mla locus in lines derived from Hordeum spontaneum. Plant Breed. 1993, 110, 116–122. [Google Scholar] [CrossRef]
  69. Kintzios, S.; Jahoor, A.; Fischbeck, G. Powdery-mildew-resistance genes Mla29 and Mla32 in H. spontaneum derived winter-barley lines. Plant Breed. 1995, 114, 265–266. [Google Scholar] [CrossRef]
  70. Kintzios, S.; Fischbeck, G. Identification of new sources for resistance to powdery mildew in H. spontaneum derived winter barley lines. Genet. Resour. Crop Evol. 1996, 43, 25–31. [Google Scholar] [CrossRef]
  71. Mastebroek, H.D.; Balkema-Bomstra, A.G.; Gaj, M. Genetic analysis of powdery mildew (Erysiphe graminis f. sp. hordei) resistance derived from wild barley (Hordeum vulgare ssp. spontaneum). Plant Breed. 1995, 114, 121–125. [Google Scholar] [CrossRef]
  72. Fetch, T.G.; Steffenson, B.J.; Nevok, E. Diversity and sources of multiple disease resistance in Hordeum spontaneum. Plant Dis. 2003, 87, 1439–1448. [Google Scholar] [CrossRef]
  73. Dreiseitl, A.; Bockelman, H.E. Sources of powdery mildew resistance in a wild barley collection. Genet. Resour. Crop Evol. 2003, 50, 345–350. [Google Scholar] [CrossRef]
  74. Dreiseitl, A.; Dinoor, A. Phenotypic diversity of barley powdery mildew resistance sources. Genet. Resour. Crop Evol. 2004, 51, 251–258. [Google Scholar] [CrossRef]
  75. Ames, N.; Dreiseitl, A.; Steffenson, B.J.; Muehlbauer, G.J. Mining wild barley for powdery mildew resistance. Plant Pathol. 2015, 64, 1396–1406. [Google Scholar] [CrossRef]
  76. Dreiseitl, A. High diversity of powdery mildew resistance in the ICARDA wild barley collection. Crop Pasture Sci. 2017, 68, 134–139. [Google Scholar] [CrossRef]
  77. Dreiseitl, A. Heterogeneity of powdery mildew resistance revealed in accessions of the ICARDA wild barley collection. Front. Plant Sci. 2017, 8, 202. [Google Scholar] [CrossRef] [PubMed]
  78. Czembor, J.H.; Czembor, E. Mlo resistance of barley to powdery mildew (Blumeria graminis f.sp. hordei) Part II. Sources of resistance and their use in barley breeding. Biul. IHAR 2003, 230, 355–374. [Google Scholar]
  79. Czembor, J.H.; Czembor, E. Mlo resistance of barley to powdery mildew (Blumeria graminis f.sp. hordei) Part III. Durability of resistance. Biul. IHAR 2003, 230, 375–386. [Google Scholar]
  80. Reinstädler, A.; Müller, J.; Czembor, J.H.; Piffanelli, P.; Panstruga, R. Novel induced mlo mutant alleles in 1 combination with site-directed mutagenesis reveal functionally important domains in the heptahelical barley Mlo protein. BMC Plant Biol. 2010, 10, 31. [Google Scholar] [CrossRef]
  81. Kølster, P.; Munk, L.; Stølen, O.; Løhde, J. Near-Isogenic Barley Lines with Genes for Resistance to Powdery Mildew. Crop. Sci. 1986, 26, 903–907. [Google Scholar] [CrossRef]
  82. Mains, E.B.; Dietz, S.M. Physiologic forms of barley mildew, Erysiphe graminis hordei Marchal. Phytopathology 1930, 20, 229–239. [Google Scholar]
  83. Flor, H.H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 1971, 9, 275–296. [Google Scholar] [CrossRef]
  84. Spies, A.; Korzun, V.; Bayles, R.; Rajaraman, J.; Himmelbach, A.; Hedley, P.E.; Schweizer, P. Allele mining in barley genetic resources reveals genes of race-non-specific powdery mildew resistance. Front. Plant Sci. 2012, 2, 113. [Google Scholar] [CrossRef]
  85. Hickey, L.T.; Lawson, W.; Platz, G.J.; Fowler, R.A.; Arief, V.; Dieters, M.; German, S.; Fletcher, S.; Park, R.F.; Singh, D.; et al. Mapping quantitative trait loci for partial resistance to powdery mildew in an Australian barley population. Crop Sci. 2012, 52, 1021–1032. [Google Scholar] [CrossRef]
  86. Bengtsson, T.; Åhman, I.; Manninen, O.; Reitan, L.; Christerson, T.; Due Jensen, J.; Krusell, L.; Jahoor, A.; Orabi, J.A. Novel QTL for Powdery Mildew Resistance in Nordic Spring Barley (Hordeum vulgare L. ssp. vulgare) Revealed by Genome-Wide Association Study. Front Plant Sci. 2017, 8, 1954. [Google Scholar] [CrossRef] [PubMed]
  87. Cowger, C.; Brown, J.K. Durability of quantitative resistance in crops: Greater than we know? Annu. Rev. Phytopathol. 2019, 57, 253–277. [Google Scholar] [CrossRef] [PubMed]
  88. Gupta, S.; D’Antuono, M.; Bradley, J.; Li, C.; Loughman, R. Identification and expression of adult plant resistance in barley to powdery mildew (Blumeria graminis f. sp. hordei) in Australia. Euphytica 2015, 203, 595–605. [Google Scholar] [CrossRef]
  89. Arabi, M.I.; Jawhar, M.; Al-shehadah, E. Identification of Barley Lines with Resistance to Powdery Mildew Based on Seedling and Adult Plant Responses. Acta Phytopathol. Entomol. Hung. 2020, 55, 3–10. [Google Scholar] [CrossRef]
  90. Ge, C.; Wentzel, E.; Ellwood, S.R.; Souza, N.D.; Chen, K.; Oliver, R.P. Adult resistance genes to barley powdery mildew confer basal penetration resistance associated with broad-spectrum resistance. Plant Genome 2021, 14, e20129. [Google Scholar] [CrossRef] [PubMed]
  91. Genievskaya, Y.; Zatybekov, A.; Abugalieva, S.; Turuspekov, Y. Identification of Quantitative Trait Loci Associated with Powdery Mildew Resistance in Spring Barley under Conditions of Southeastern Kazakhstan. Plants 2023, 12, 2375. [Google Scholar] [CrossRef]
  92. Czembor, J.H.; Czembor, E.; Suchecki, R.; Watson-Haigh, N.S. Genome-Wide Association Study for Powdery Mildew and Rusts Adult Plant Resistance in European Spring Barley from Polish Gene Bank. Agronomy 2022, 12, 7. [Google Scholar] [CrossRef]
  93. Singh, B.; Mehta, S.; Aggarwal, S.K.; Tiwari, M.; Bhuyan, S.I.; Bhatia, S.; Islam, A. Barley, Disease Resistance, and Molecular Breeding Approaches. In Disease Resistance in Crop Plants; Wani, S.H., Ed.; Springer Nature Switzerland AG: Basel, Switzerland, 2019; Chapter 11; pp. 261–299. [Google Scholar] [CrossRef]
  94. Riaz, A.; Kanwal, F.; Börner, A.; Pillen, K.; Dai, F.; Alqudah, A.M. Advances in Genomics-Based Breeding of Barley: Molecular Tools and Genomic Databases. Agronomy 2021, 11, 894. [Google Scholar] [CrossRef]
Agronomy 13 02462 g001
Figure 1. Range of barley seedling infection types for the Blumeria hordei interactions (image by Jerzy H. Czembor). Each infection type is based on a 0–4 scale, where 0 (the immune reaction) is no visible symptoms; 0(4), sparse small colonies originating from the stomatal subsidiary cells (Mlo resistance); 1 (resistant), minute necrotic flecks, no mycelial growth, and no sporulation; 2 (moderately resistant), frequent chlorosis, reduced mycelial growth, and no or very scarce sporulation; 3 (susceptible), moderate mycelial growth, moderate sporulation, and occasional chlorosis; and 4 (very susceptible), profuse sporulation of well-developed colonies. Infection types 3 and 4 are considered to be compatible (i.e., virulent pathogen/susceptible host).
Figure 1. Range of barley seedling infection types for the Blumeria hordei interactions (image by Jerzy H. Czembor). Each infection type is based on a 0–4 scale, where 0 (the immune reaction) is no visible symptoms; 0(4), sparse small colonies originating from the stomatal subsidiary cells (Mlo resistance); 1 (resistant), minute necrotic flecks, no mycelial growth, and no sporulation; 2 (moderately resistant), frequent chlorosis, reduced mycelial growth, and no or very scarce sporulation; 3 (susceptible), moderate mycelial growth, moderate sporulation, and occasional chlorosis; and 4 (very susceptible), profuse sporulation of well-developed colonies. Infection types 3 and 4 are considered to be compatible (i.e., virulent pathogen/susceptible host).
Agronomy 13 02462 g001
Agronomy 13 02462 g002
Figure 2. The frequency distribution histogram presents the percentage of populations with only susceptible plants and with resistant plants of Hvs originating from Lebanon (LBN), Jordan (JOR), and Libya (LBY) tested with isolate Bgh33 and the percentage of selected resistant single plant lines from Hvs populations from these countries.
Figure 2. The frequency distribution histogram presents the percentage of populations with only susceptible plants and with resistant plants of Hvs originating from Lebanon (LBN), Jordan (JOR), and Libya (LBY) tested with isolate Bgh33 and the percentage of selected resistant single plant lines from Hvs populations from these countries.
Agronomy 13 02462 g002
Table 1. Blumeria hordei isolates used for artificial inoculation and their virulence spectra against resistance genes on the differential set of Pallas near-isogenic lines.
Table 1. Blumeria hordei isolates used for artificial inoculation and their virulence spectra against resistance genes on the differential set of Pallas near-isogenic lines.
No.Near-Isogenic Lines/CultivarsResistance GenesIsolates
1234567891011121314151617181920
Bgh 1Bgh 2Bgh 3Bgh 4Bgh 8Bgh 9Bgh 11Bgh 13Bgh 14Bgh 24Bgh 28Bgh 29Bgh 31Bgh 33Bgh 36Bgh 40Bgh 48Bgh 51Bgh 57Bgh 63
1PallasMla844444444444444444444
2P1Mla100444000000400400400
3P2Mla310000000000400440000
4P3Mla6, Mla1400000040404000444444
5P4AMla7, Mlk, +?22222222224240222442
6P4BMla7, +?44410224402441441444
7P6Mla7, MlLG244- *00212402240420444
8P7Mla9, Mlk40400004000400000040
9P8AMla9, Mlk40400004000400000040
10P8BMla940400004040400000040
11P9Mla10, MlDu244401404020444400444
12P10Mla1200400400400440440404
13P11Mla13, MlRu340400000440040000404
14P12Mla2244044040444440044400
15P13Mla2311212121111211111111
16P14Mlra44404444044444444444
17P15Ml(Ru2)44443424420442444444
18P17Mlk44422224220442422444
19P18Mlnn44444244422444444422
20P19Mlp22222222222222222222
21P20Mlat22242224222222242422
22P21Mlg, Ml(CP)44400040404444440404
23P22mlo50(4)0(4)0(4)0(4)0(4)0(4)30(4)0(4)0(4)0(4)0(4)0(4)0(4)0(4)0(4)0(4)0(4)0(4)0(4)
24P23Ml(La)44444244444444444444
25P24Mlh44404444444444044444
26BenedicteMla9, Ml(IM9)00400000400440440404
27LenkaMla13, Ml(Ab)40400000400040000404
28GunnarMla3, Ml(Tu2)00000000000000000000
29SteffiMl(St1), Ml(St2)22200000400230420204
30KreditMl(Kr)42402002444240422444
31JarekMl(Kr), +?44444244444444424424
32TrumphMla7, Ml(Ab)44444444444444444444
33BorwinaMl(Bw)43304044422344434422
34Manchurian 44444444444444444444
* No data.
Table 2. Resistance of lines selected from accessions H. vulgare subsp. spontaneum from Jordan (JOR), Lebanon (LBN), and Libya (LBY) to B. hordei to isolate Bgh33 after inoculation at the seedling stage.
Table 2. Resistance of lines selected from accessions H. vulgare subsp. spontaneum from Jordan (JOR), Lebanon (LBN), and Libya (LBY) to B. hordei to isolate Bgh33 after inoculation at the seedling stage.
No.ICARDAOTHERNUMB ***
(IHAR No.)		Isolate Bh
Bgh 33		No.ICARDAOTHERNUMB
(IHAR No.)		Bgh 33
IG *Crop NoORI ID **IGCrop NrORI ID
138616180007JOR107544140177181568LBN11164
238617180008JOR107644240178181569LBN11174
338618180009JOR107744340179181570LBN11184
438619180010JOR107844440180181571LBN11194
538620180011JOR107944540181181572LBN11204
638621180012JOR108044640182181573LBN11214
738622180013JOR108144740183181574LBN11224
838623180014JOR108244840184181575LBN11244
938624180015JOR10830, 44940185181576LBN11254
1038625180016JOR10840, 45040186181577LBN11264
1138626180017JOR108545140187181578LBN11274
1238627180018JOR108605240188181579LBN11284
1338628180019JOR108745340189181580LBN11294
1438629180020JOR108845440190181581LBN11304
1538630180021JOR10890, 45540191181582LBN11314
1638631180022JOR109045640193181584LBN11324
1738632180023JOR109145740194181585LBN11334
1838633180024JOR1092458112846181657LBY11340, 2, 4
1939398180789JOR1093459112847181658LBY11354
2039821181212JOR10942, 460110816181628LBN11364
2139822181213JOR1095461110819181629LBN11374
2239823181214JOR1096462110823181630LBN11384
2339824181215JOR1097463110831181631LBN11394
2439825181216JOR1098464110833181632LBN11404
2539826181217JOR1099465116004181639LBY11414
2639827181218JOR1100466116005181640LBY11420, 4
2739828181219JOR11012, 467115780181660JOR11434
2839829181220JOR1102468115781181661JOR11440, 4
2939850181241JOR1103469115782181662JOR11454
3039851181242JOR1104470115784181664JOR11460
3139877181268JOR1105471115785181665JOR11474
3239933181324LBY1107472115786181666JOR11482, 4
3339934181325LBY1108373115787181667JOR11494
3439935181326LBY11090, 274115788181668JOR11504
3539936181327LBY1110475115789181669JOR11514
3639937181328LBY11110, 476115790181670JOR11520
3739938181329LBY1112477115791181671JOR11534
3839939181330LBY1113478115792181672JOR11544
3940156181547LBN1114479115793181673JOR11550, 2
4040168181559LBN1115480115795181674JOR11564
81115796181675JOR11574
* ICARDA number of accession; ** Country of origin: Lebanon (LBN), Jordan (JOR), and Libya (LBY); *** Other number—IHAR number.
Table 3. Resistance of lines selected from accessions H. vulgare subsp. spontaneum to B. hordei isolates after inoculation at the seedling stage.
Table 3. Resistance of lines selected from accessions H. vulgare subsp. spontaneum to B. hordei isolates after inoculation at the seedling stage.
No.ICARDAOthernumb (IHAR Project No.-Line)IsolatesPostulated Resistance Alleles
ICARDA-IGIG Line No.Crop NoORI ID1234567891011121314151617181920
Bgh 1Bgh 2Bgh 3Bgh 4Bgh 8Bgh 9Bgh 11Bgh 13Bgh 14Bgh 24Bgh 28Bgh 29Bgh 31Bgh 33Bgh 36Bgh 40Bgh 48Bgh 51Bgh 57Bgh 63
1386241180015JOR1083-100002020000000000000un *
2386251180016JOR1084-100002020000000000200un
3386252180016JOR1084-300000020020000000200un
4386253180016JOR1084-400000020020000000000un
5386271180018JOR1086-200000020000000000000un
6386301180021JOR1089-120200020000000002000un
7398211181212JOR1094-140400020022402000220un
8398212181212JOR1094-220400220020402010002un
9398281181219JOR1101-1202- **0-2000-20-000---un
10398282181219JOR1101-2000-022002020-000--0un
11398283181219JOR1101-320200222220222000000un
12399351181326LBY1109-100000020020000000200un
13399352181326LBY1109-2000-002002000-000--0un
14399353181326LBY1109-300022222022202200020un
15399354181326LBY1109-400202022020202200000un
16399371181328LBY1111-100002022040200200220un
17399372181328LBY1111-200000022020000000220un
181128461181657LBY 1134-100210020020000000000un
191128462181657LBY 1134-200000020000202000200un
201160051181640LBY 1142-100200022020000200220un
211157811181661JOR1144-1424-002202020-240--2un
221157812181661JOR1144-200000020020000200000un
231157813181661JOR1144-300000020020000200200un
241157841181664JOR1146-100000-0000-00000000-un
251157861181666JOR1148-200020-2202-22220000-un
261157901181670JOR1152-100000010200000000000un
271157902181670JOR1152-200000020000000000000un
281157931181673JOR1155-100000020000000000000un
291157932181673JOR1155-300000020200000100200un
301157933181673JOR1155-300020020000002200000un
311157932181673JOR1155-200000020042200200000un
* Unknown resistance gene. ** No data.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Czembor, J.H.; Czembor, E. Sources of Resistance to Powdery Mildew in Wild Barley (Hordeum vulgare subsp. spontaneum) Collected in Jordan, Lebanon, and Libya. Agronomy 2023, 13, 2462. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy13102462

AMA Style

Czembor JH, Czembor E. Sources of Resistance to Powdery Mildew in Wild Barley (Hordeum vulgare subsp. spontaneum) Collected in Jordan, Lebanon, and Libya. Agronomy. 2023; 13(10):2462. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy13102462

Chicago/Turabian Style

Czembor, Jerzy H., and Elzbieta Czembor. 2023. "Sources of Resistance to Powdery Mildew in Wild Barley (Hordeum vulgare subsp. spontaneum) Collected in Jordan, Lebanon, and Libya" Agronomy 13, no. 10: 2462. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy13102462

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop