Next Article in Journal
Monitoring of Nitrogen Concentration in Soybean Leaves at Multiple Spatial Vertical Scales Based on Spectral Parameters
Next Article in Special Issue
The Emerging Role of 2OGDs as Candidate Targets for Engineering Crops with Broad-Spectrum Disease Resistance
Previous Article in Journal
Phytochemical Profile, GC-MS Profiling and In Vitro Evaluation of Some Biological Applications of the Extracts of Origanum syriacum L. and Cousinia libanotica D.C.
Previous Article in Special Issue
NLR- and mlo-Based Resistance Mechanisms against Powdery Mildew in Cannabis sativa
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Opinion

Mlo-Mediated Broad-Spectrum and Durable Resistance against Powdery Mildews and Its Current and Future Applications

by
Antonín Dreiseitl
Department of Integrated Plant Protection, Agrotest Fyto, Ltd., 767 01 Kroměříž, Czech Republic
Plants 2024, 13(1), 138; https://doi.org/10.3390/plants13010138
Submission received: 27 November 2023 / Revised: 2 January 2024 / Accepted: 2 January 2024 / Published: 4 January 2024
(This article belongs to the Special Issue Broad-Spectrum Disease Resistance in Plants)

Abstract

:
Mlo is a well-known broad-spectrum recessively inherited monogenic durable resistance to powdery mildew caused by Blumeria hordei found first in barley, originally in an induced mutant in 1942 and later in other mutants and also in Ethiopian landraces. The first commercial varieties possessing Mlo resistance were released during 1979–1986, but these often showed symptoms of necrotic leaf spotting associated with reduced grain yield. However, this yield penalty was successfully reduced by breeding Mlo-resistant varieties of spring barley predominate in Europe; for example, in the Czech Republic, their ratio surpassed 90% of the total number of newly released varieties. However, outside Europe, Mlo-varieties are not yet popular and can be exploited more widely. Winter barley varieties are generally non-resistant, but the use of Mlo for their breeding is controversial despite the limited adaptability of the pathogen to this resistance. The renewal of mechanically disturbed epidermal plant cell walls, including the penetration of mildews, is common in plants, and the Mlo-type resistance is exploited in many other crop species, including wheat.

1. Introduction

Broad-spectrum resistance is a general term that involves different kinds of resistance to plant pathogens, including specific resistances via the accumulation of QTLs in adult plants, and non-specific or non-host resistance that confers resistance to several diseases [1,2,3,4,5]. In the case of barley powdery mildew, due to its remarkable ability to quickly overcome plant immunity [6], the durability of resistance based on non-specificity is a key requirement.
Non-specific resistance simply means that no virulent pathotype exists, and to confirm that this requires testing the resistant host against a wide range of pathogen isolates or populations. There is a high probability that virulent pathotypes to a new and effective resistance exist in the geographical region where the source accession(s) is found and where the pathogen has already had a chance to adapt to the resistance. In addition to this, two centers of virulence diversity and complexity of Blumeria hordei, M. Liu and Hambl. (Bh), that cause powdery mildew (PM) are found in barley (Hordeum vulgare L.). The first is located in the center of wild barley diversity (H. v. subsp. spontaneum), where the host and the pathogen have coexisted for a long time. It is characterized by a broad spectrum of virulences against resistance genes that are present in this barley subspecies [7]. The second center has developed recently in Europe [8], especially in the central and northwest areas, where there has been a massive exploitation of specific resistances in breeding crop varieties [9,10].
Specific resistances are often initially effective against known pathotypes (virulence frequency—VF = 0%). For example, no virulent isolates of the three corresponding Ml resistance genes (aLv, p, and Ve) were recorded before 2009–2012 (Table 1). This may also be the case of Roxana (Ro) resistance [11], but the inclusion of ‘Ro-varieties’ in a differential set only took place in 2008. This was some time after the varieties with this resistance had already been grown in Germany, and hence a small proportion of virulent isolates found in 2008 [12] were probably pathotypes originating in that country.
Increasing VF in the pathogen population is followed by decreased varietal resistance in the field (Table 2). There are many examples of this phenomenon, and one of the best known is the case of varieties with Mla13 that maintained their resistance in the Czech Republic for ten years (1976–1985). The resistance was subsequently overcome there and throughout Europe shortly afterward [21]. Since 1989, varieties possessing Mla13 have been among the most susceptible [22].
After performing tests against many isolates and multiple locations, only resistances based on mlo and Mlp genes remained effective, and both were considered potentially non-specific [24]. However, in the samples of the Bh population collected from wild barley in Israel, VF to Mlp (VFp) was 96% in 1997 and 100% in 1999 [7]. In the Czech population (central Europe), virulence against Mlp was not found before 2012 [17], but after varieties carrying this gene started to grow, VFp reached almost 70% in 2023 [19].
When 1 383 accessions of the U.S.A. wild barley collection were tested with mostly European Bh isolates, it was found that 123 accessions were resistant to all of them [25]. These accessions were tested with 38 Israeli isolates, and apart from the check lines containing mlo and Mlhb2, only PI 466634 remained resistant [26]. Therefore, the derivatives from bulbous barley (Hordeum bulbosum L.) [27,28] and wild barley accession PI 466634 may be potential sources of non-specific resistance.

2. Mlo Resistance in Barley

A broad-spectrum recessively inherited monogenic resistance to powdery mildew was first recognized in an induced mutant M66 derived from Haisa [29]. The same resistance was subsequently found in other induced barley mutants and landraces collected in Ethiopia [30]. These genes were assigned to a new locus designated Mlo [31]. Ten alleles in the mutants and the alleles present in the landraces were numbered mlo1mlo10 and mlo11, respectively [32], and were located at this locus, which has at least three sites [33] on the barley chromosome 4HL [34]. Many other mutants with different mlo alleles have since been reported. Mutations with a similar phenotype, characterized by the occurrence of occasional small mildew colonies and an identical resistance function, can occur at these locus sites. The number of colonies may vary according to environmental conditions and the presence of an mlo allele and the genotype of the recipient variety, which may contain specific resistance genes [35].
Over a period of four years, the first three commercial spring barley varieties carrying mlo11, derived from potentially different Ethiopian landraces, were registered (Atem in 1979, Salome in 1981, and Apex in 1982). These were followed by the registration of the first variety (Alexis 1986) with an induced Mlo resistance (mlo9) [35] derived from a Czech EMS mutant SZ 5139 [36]. This mutant was obtained from a well-known domestic semi-dwarf and highly tillering variety Diamant—an Rtg mutant from Valticky, a world donor of high malting quality grain.
In the Czech Republic, spring barley is an important crop used mostly for malt and beer production, and both these commodities are exported. However, the cultivated area of the crop fell from a yearly average of 624,000 hectares during 1975–1982 to 220,000 ha during 2016–2021. Despite this reduction, the country is still a good seed market for Central and Western European companies. This explains why 164 commercial varieties bred in numerous companies and breeding stations in nine countries were registered here over the last 31 years (Table 3). This set of varieties truly reflects the focus of the breeding programs in these European regions.
In the inland Czech Republic, PM is the most frequent disease of non-resistant barley varieties [39], and therefore, the immigration of airborne spores with the potential to be transmitted for hundreds of kilometers [40] is not limited. Gene flow is an important evolutionary force [41] and, together with a suite of other factors [42], PM has higher importance than elsewhere, and the demand for resistant varieties has always been important.
Varieties with Mlo resistance have been tested in the country since 1986, initially only in registration trials. The first commercial variety with a broad-spectrum durable Mlo resistance was the Czech-bred Forum, which was registered in 1993 [43]. At the end of 2023, 114 of these varieties were registered in the Czech Republic, and 92 of these varieties registered up to 2020 were published (Table 4).
Varieties carrying Mlo attained almost 96% of newly registered strains in the last monitored period (Table 5), and for 38 years, they were the most resistant to PM [22].
Genotypes carrying induced as well as naturally occurring mlo alleles were originally associated with negative characteristics, such as necrotic leaf spotting and reduced grain yield. But even in the early 1990s when many fewer Mlo commercial varieties existed, it was reported that these negative attributes “have been overcome by recent breeding work” and “absence of necrotic leaf spotting may be an easy selection criterion for removing undesirable pleiotropic effects of the mlo resistance genes” [35]. Hundreds of commercial Mlo varieties that were released in Europe have performed well in trials of breeding companies and registration trials, and they are widely accepted on the seed market and among growers. In some specific conditions and on some varieties, more colonies of the pathogen and more necrotic leaf spotting can occur, but there are no obstacles to the further use of this admirable non-specific durable resistance because the benefits of strong Mlo-based resistance outweigh any small penalties [47,48].
There are two barley crops grown concurrently in much of Europe: spring, whose PM resistance is generally high and mostly based on Mlo, and winter, where varieties are often susceptible despite the frequent presence of more than one gene of specific resistance. Therefore, there is a question regarding the use of Mlo resistance in winter barley. The answer requires the knowledge of whether there is a potential for the pathogen to adapt to such “special” resistance response. To investigate this, a barley mlo mutant was inoculated in 37 vegetative reproduction cycles with a pure field Bh isolate and its progeny. The results showed that the number of colonies and the number of spores per colony increased, leading to a significantly higher number of spores per leaf area compared with a variant when the mutant was inoculated with the original field isolate [49]. When varieties with Mlo were already widely grown, subsequent tests with field isolates at several locations showed that the pathogen could adapt to Mlo to a limited extent [50].
Based on the available data, it was predicted that Mlo will be a very durable resistance. Nevertheless, if Mlo-resistant spring and winter barley varieties are grown extensively and their areas overlap, it is possible that the powdery mildew fungus will slowly evolve with increased aggressiveness (partial virulence) and gradually cause disease that may approach the threshold level for crop losses [35]. This conclusion is generally accepted, and Mlo resistance has not been used in the breeding of commercial winter barley varieties.
Despite this reservation, there were two attempts to use Mlo in winter barley breeding programs. The Czech winter barley KM 2099 was tested in domestic registration trials in 1990–1993 and exhibited some favorable agronomic traits, including effective PM resistance based on an mlo allele [51]. Because it was not morphologically uniform, reselection of this variety was considered. However, the presence of Mlo resistance did not support further testing of KM 2099 or its selected lines, and similar breeding efforts were curtailed. The second example relates to a Polish research project that started in 2005 and aimed at the transfer of Mlo into winter barley genotypes. A set of lines with the possible presence of Mlo resistance and acceptable agronomical traits were bred, and one line (BKH 5735) was selected [52]. The fate of this variety is not known.
The protection of European spring barley against PM is based mainly on Mlo resistance, but the reported results do not support the use of Mlo resistance for winter barley breeding under present European conditions where vegetative reproduction of the pathogen could occur throughout the year in winter and spring barleys carrying Mlo. Mlo does not only provide resistance against PM but its action is manifested by a general renewal of mechanical damage of epidermal plant cell walls (including penetration of PM), although possible adaptation to partial virulence is known. Therefore, without more research on this topic, there must be caution regarding the breeding of winter barley carrying Mlo until the following unanswered question can be addressed—“Spring and winter barley cultivars with the mlo resistance gene to powdery mildew—is there a threat of pathogen adaptation?” [51].

3. Mlo Resistance in Other Crops and Plant Species

In plants with Mlo resistance, the renewal of mechanically disturbed epidermal plant cell walls is wound-sealed by the formation of a callose-rich cell wall apposition below the encounter site. This fundamental mechanism is generally found in higher plants, and it was predicted that such kind of mildew resistance should also occur in other plant species [35]. This prediction inspired the search for Mlo resistance in a wide range of plants, and until 2017, such functionally validated resistance was detected in 12 other species in addition to barley [53]. Based on continuing research, the number and range of plant species with Mlo resistance are increasing [54,55,56,57], and wheat, for example, could result in the use of Mlo resistance without pleiotropic effects causing growth penalties [58,59]. New technologies, including CRISPR-Cas9, can further accelerate the exploitation of Mlo resistance for the protection of many crops [60].

4. Conclusions

  • Mlo resistance in barley is a very effective broad-spectrum durable resistance against powdery mildew based on the recessive mlo gene.
  • The yield penalty for Mlo resistance, known from research conducted several decades ago, was successfully reduced by breeding.
  • Outside Europe, using Mlo in barley breeding is not a high priority and has great potential for the increased utilization of this resistance.
  • Even though the pathogen has a limited ability to adapt, the joint use of Mlo in both spring and winter barleys could be risky in areas where these crops are grown extensively.
  • The renewal of mechanically disturbed epidermal plant cell walls, including the penetration of mildews, is common in plants, and Mlo-type resistance is found in many crops.
  • The detection of this resistance type and related research probably continue in other plant species.

Funding

This study was funded by the Ministry of Agriculture of the Czech Republic, institutional support No. MZE-RO1123.

Data Availability Statement

All relevant data are presented in the article.

Conflicts of Interest

The author declares no conflicts of interest.

Correction Statement

This article has been republished with a minor correction to the readability of Table 4. This change does not affect the scientific content of the article.

References

  1. Kou, Y.; Wang, S.P. Broad-spectrum and durability: Understanding of quantitative disease resistance. Curr. Opin. Plant Biol. 2010, 13, 181–185. [Google Scholar] [CrossRef] [PubMed]
  2. Carrillo, M.G.C.; Martin, F.; Variar, M.; Bhatt, J.C.; Perez-Quintero, A.L.; Leung, H.; Leach, J.E.; Cruz, C.M.V. Accumulating candidate genes for broad-spectrum resistance to rice blast in a drought-tolerant rice cultivar. Scient. Rep. 2021, 11, 21502. [Google Scholar] [CrossRef] [PubMed]
  3. Ge, C.; Wentzel, E.; D’Souza, N.; Chen, K.; Oliver, R.P.; Ellwood, S.R. 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]
  4. Moolhuijzen, P.; Ge, C.; Palmiero, E.; Ellwood, S.R.R. A unique resistance mechanism is associated with RBgh2 barley powdery mildew adult plant resistance. Theor. Appl. Genet. 2023, 136, 145. [Google Scholar] [CrossRef] [PubMed]
  5. Wu, Y.; Sexton, W.; Yang, B.; Xiao, S.Y. Genetic approaches to dissect plant nonhost resistance mechanisms. Molec. Plant Pathol. 2023, 24, 272–283. [Google Scholar] [CrossRef] [PubMed]
  6. Kusch, S.; Qian, J.Z.; Loos, A.; Kuemmel, F.; Spanu, P.D.; Panstruga, R. Long-term and rapid evolution in powdery mildew fungi. Mol. Ecol. 2023. Early Access. [Google Scholar] [CrossRef]
  7. Dreiseitl, A.; Dinoor, A.; Kosman, E. Virulence and diversity of Blumeria graminis f.sp. hordei in Israel and in the Czech Republic. Plant Dis. 2006, 90, 1031–1038. [Google Scholar] [CrossRef]
  8. Dreiseitl, A. Pathogenic divergence of Central European and Australian populations of Blumeria graminis f. sp. hordei. Ann. Appl. Biol. 2014, 165, 364–372. [Google Scholar] [CrossRef]
  9. Brown, J.K.M.; Jørgensen, J.H. A catalogue of mildew resistance genes in European barley varieties. In Integrated Control of Cereal Mildews: Virulence and Their Change, Proceedings of the Second European Workshop on Integrated Control of Cereal Mildews, Risø National Laboratory, Roskilde, Denmark, 23–25 January 1990; Jørgensen, J.H., Ed.; Risø National Laboratory: Roskilde, Denmark, 1991; pp. 263–286. [Google Scholar]
  10. Hovmøller, M.S.; Caffier, V.; Jalli, M.; Andersen, O.; Besenhofer, G.; Czembor, J.H.; Dreiseitl, A.; Felsenstein, F.; Fleck, A.; Heinrics, F.; et al. The European barley powdery mildew virulence survey and disease nursery 1993–1999. Agronomie 2000, 20, 729–743. [Google Scholar] [CrossRef]
  11. Dreiseitl, A. Resistance of ‘Roxana’ to powdery mildew and its presence in some European spring barley cultivars. Plant Breed. 2011, 130, 419–422. [Google Scholar] [CrossRef]
  12. Dreiseitl, A. Unpublished. (From experiments done within the population study 2008 only the results obtained on 17 winter barley differentials were published, whereas those on the spring barley varieties – Pallas near isogenic lines and Kangoo – were omitted).
  13. Dreiseitl, A. Postulation of genes for resistance to powdery mildew in spring barley cultivars registered in the Czech Republic from 1996 to 2010. Euphytica 2013, 191, 183–189. [Google Scholar] [CrossRef]
  14. Dreiseitl, A. Changes in virulence frequencies and higher fitness of simple pathotypes in the Czech population of Blumeria graminis f. sp. hordei. Plant Protect. Sci. 2015, 51, 67–73. [Google Scholar] [CrossRef]
  15. Dreiseitl, A. Resistance of ‘Laverda’ to powdery mildew and its presence in some winter barley cultivars. Cereal Res. Commun. 2011, 39, 569–576. [Google Scholar] [CrossRef]
  16. Dreiseitl, A. Virulence frequency to powdery mildew resistances in winter barley cultivars. Czech J. Genet. Plant Breed. 2008, 44, 160–166. [Google Scholar] [CrossRef]
  17. Dreiseitl, A. Rare virulences of barley powdery mildew found in aerial populations in the Czech Republic from 2009 to 2014. Czech J. Genet. Plant Breed. 2015, 51, 1–8. [Google Scholar] [CrossRef]
  18. Dreiseitl, A. Emerging Blumeria graminis f. sp. hordei pathotypes reveal ‘Psaknon’ resistance in European barley varieties. J. Agric. Sci. 2016, 154, 1082–1089. [Google Scholar] [CrossRef]
  19. Dreiseitl, A. Rare virulences and great pathotype diversity of a Central European Blumeria hordei population. J. Fungi 2023, 9, 1045. [Google Scholar] [CrossRef]
  20. 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]
  21. Wolfe, M.S.; Brändle, U.; Koller, B.; Limpert, E.; McDermott, J.M.; Müller, K.; Schaffner, D. Barley mildew in Europe: Population biology and host resistance. Euphytica 1992, 63, 125–139. [Google Scholar] [CrossRef]
  22. Dreiseitl, A. Adaptation of Blumeria graminis f.sp. hordei to barley resistance genes in the Czech Republic in 1971–2000. Plant Soil Environ. 2003, 49, 241–248. [Google Scholar] [CrossRef]
  23. Dreiseitl, A.; Jørgensen, J.H. Powdery mildew resistance in Czech and Slovak barley cultivars. Plant Breed. 2000, 119, 203–209. [Google Scholar] [CrossRef]
  24. Favret, E.A. The host-pathogen system and its genetic relationships. In Barley Genetics II, Proceedings of Second International Barley Genetics Symposium, Washington State University, Pullman, Washington, July 6–11, 1969; Nilan, R.A., Ed.; Washington State University Press: Washington, DC, USA, 1971; pp. 457–471. [Google Scholar]
  25. 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]
  26. Dreiseitl, A.; Dinoor, A. Phenotypic diversity of barley powdery mildew resistance sources. Genet. Resour. Crop Evol. 2004, 51, 251–258. [Google Scholar] [CrossRef]
  27. Xu, J.; Kasha, K.J. Transfer of a dominant gene for powdery mildew resistance and DNA from Hordeum bulbosum into cultivated barley (Hordeum vulgare). Theor. Appl. Genet. 1992, 84, 771–777. [Google Scholar] [CrossRef] [PubMed]
  28. Pickering, R.A.; Hill, A.M.; Michel, M.; Timmerman-Vaughan, G.M. The transfer of a powdery mildew resistance gene from Hordeum bulbosum L. to barley (H. vulgare L.) chromosome 2 (2I). Theor. Appl. Genet. 1995, 91, 1288–1292. [Google Scholar] [CrossRef] [PubMed]
  29. Freisleben, R.; Lein, A. Über die Auffindung einer mehltauresistenten Mutante nach Röentgenbestrahlung einer anfälligen reinen Linie von Sommergerste. Naturwiss 1942, 30, 608. [Google Scholar] [CrossRef]
  30. Hoffmann, W.; Nover, I. Ausgangsmaterial für die Züchtung mehltauresistenter Gersten. Z. Pflanzenzücht. 1959, 42, 68–78. [Google Scholar]
  31. Favret, E.A. Different categories of mutations for disease reaction in the host organism. In Mutation Breeding for Disease Resistance; IAEA-PL-412/12; Vienna, 1971; pp. 107–116. Available online: https://inis.iaea.org/search/search.aspx?orig_q=RN:2011907 (accessed on 20 November 2023).
  32. Jørgensen, J.H. Identification of powdery mildew resistant mutants and their allelic relationship. In Barley Genetics III; Verlag Karl Thiemig: München, Germany, 1976; pp. 446–455. [Google Scholar]
  33. Jørgensen, J.H.; Jensen, H.P. Inter-allelic recombination in the ml-o locus in barley. Barley Genet. Newsl. 1979, 9, 37–39. [Google Scholar]
  34. Jørgensen, J.H. Durability of the ml-o powdery mildew resistance genes in barley. Vortr. Pflanzenzücht. 1984, 6, 22–31. [Google Scholar]
  35. Jørgensen, J.H. Discovery, characterisation and exploitation of Mlo powdery mildew resistance in barley. Euphytica 1992, 63, 141–152. [Google Scholar] [CrossRef]
  36. Schwarzbach, E. Recessive total resistance of barley to mildew (Erysiphe graminis D.C. f. sp. hordei Marchal) as a mutation induced by Ethylmethansulfonate. Genet. Slecht. 1967, 3, 159–162. [Google Scholar]
  37. Available online: https://en.wikipedia.org/wiki/Central_Europe (accessed on 27 October 2023).
  38. Available online: https://en.wikipedia.org/wiki/Northwestern_Europe (accessed on 27 October 2023).
  39. Dreiseitl, A. Differences in powdery mildew epidemics in spring and winter barley based on 30-year variety trials. Ann. Appl. Biol. 2011, 159, 49–57. [Google Scholar] [CrossRef]
  40. Brown, J.K.M.; Hovmoller, M.S. Epidemiology—Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 2002, 297, 537–541. [Google Scholar] [CrossRef] [PubMed]
  41. McDonald, B.A.; Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 2002, 40, 349–379. [Google Scholar] [CrossRef]
  42. Dreiseitl, A. Specific resistance of barley to powdery mildew, its use and beyond: A concise critical review. Genes 2020, 11, 971. [Google Scholar] [CrossRef]
  43. Brückner, F. The breeding of the malting barley cultivar of new morphotype Forum. Genet. Šlecht. 1993, 29, 199–203. [Google Scholar]
  44. Dreiseitl, A. Powdery mildew resistance of foreign spring barley varieties in Czech official trials. Czech J. Genet. Plant Breed. 2006, 42, 1–8. [Google Scholar] [CrossRef]
  45. Dreiseitl, A. Genes for resistance to powdery mildew in European barley cultivars registered in the Czech Republic from 2011 to 2015. Plant Breed. 2017, 136, 351–356. [Google Scholar] [CrossRef]
  46. Dreiseitl, A.; Križanová, K. Powdery mildew resistance genes in spring barley cultivars registered in Slovakia from 2000 to 2010. Cereal Res. Commun. 2012, 40, 494–501. [Google Scholar] [CrossRef]
  47. Brown, J.K.M. Achievements in breeding cereals with durable disease resistance in Northwest Europe. In Achieving Durable Disease Resistance in Cereals; Oliver, R., Ed.; Burleigh Dodds Science Publishing Limited: Cambridge, UK, 2021; pp. 825–871. [Google Scholar] [CrossRef]
  48. Brown, J.K.M.; Wulff, B.B.H. Diversifying the menu for crop powdery mildew resistance. Cell 2022, 185, 761–763. [Google Scholar] [CrossRef]
  49. Schwarzbach, E. Response to selection for virulence against the ml-o based mildew resistance in barley, not fitting the gene-for-gene hypothesis. Barley Genet. Newsl. 1979, 9, 85–88. [Google Scholar]
  50. Schwarzbach, E. Shifts to increased pathogenicity on mlo varieties. In Integrated Control of Cereal Mildews: Monitoring the Pathogen, Proceedings of a Seminar in the Community Programme of Coordinated Research on Energy in Agriculture, Freising-Weihenstephan, Federal Republic of Germany, 4–6 November 1986; Wolfe, M.S., Limpert, E., Eds.; Martinus Nijhoff Publishers: Dordrecht, The Netherlands, 1987; pp. 5–7. [Google Scholar]
  51. Dreiseitl, A. Spring and winter barley cultivars with the mlo resistance to powdery mildew—Is there threat of the pathogen adaptation? In Adaptation in Plant Breeding. In Proceedings of the XIV EUCARPIA Congress; University of Jyvaskyla: Jyvaskyla, Finland, 1995; p. 46. [Google Scholar]
  52. Czembor, J.H.; Czembor, P.C.; Doraczyńska, O.; Pietrusińska, A.; Radecka-Janusik, M. Transfer of the mlo resistance gene into to the genome of winter barley. Progress Plant Potect. 2016, 56, 379–387. [Google Scholar] [CrossRef]
  53. Kusch, S.; Panstruga, R. mlo-based resistance: An apparently universal “weapon” to defeat powdery mildew disease. Mol. Plant-Microbe Interact. 2017, 30, 179–189. [Google Scholar] [CrossRef] [PubMed]
  54. Li, W.; Deng, Y.; Ning, Y.; He, Z.; Wang, G.L. Exploiting broad-spectrum disease resistance in crops: From molecular dissection to breeding. Ann. Rev. Plant Biol. 2020, 71, 575–603. [Google Scholar] [CrossRef] [PubMed]
  55. Traore, S.M.; Han, S.; Binagwa, P.; Xu, W.; Chen, X.G.; Liu, F.Z.; He, G.H. Genome-wide identification of mlo genes in the cultivated peanut (Arachis hypogaea L.). Euphytica 2021, 217, 61. [Google Scholar] [CrossRef]
  56. Giuseppe, A.; Raffaella, E.M. The first genome-wide mildew locus O genes characterization in the Lamiaceae plant family. Int. J. Mol. Sci. 2023, 24, 13627. [Google Scholar] [CrossRef] [PubMed]
  57. Xu, J.P.; Naing, A.H.; Kang, H.H.; Lee, S.Y.; Li, W.L.; Chung, M.Y.; Kim, C.K. CRISPR-Cas9-mediated editing of PhMLO1 confers powdery mildew resistance in petunia. Plant Biotechnol. Rep. 2023, 17, 767–775. [Google Scholar] [CrossRef]
  58. Li, S.; Lin, D.; Zhang, Y.W.; Deng, M.; Chen, Y.X.; Lv, B.; Li, B.; Lei, Y.; Wang, Y.P.; Zhao, L.; et al. Genome-edited powdery mildew resistance in wheat without growth penalties. Nature 2022, 602, 455–460. [Google Scholar] [CrossRef]
  59. Ingvardsen, C.R.; Massange-Sanchez, J.A.; Borum, F.; Fuchtbauer, W.S.; Bagge, M.; Knudsen, S.; Gregersen, P.L. Highly effective mlo-based powdery mildew resistance in hexaploid wheat without pleiotropic effects. Plant Sci. 2023, 335, 111785. [Google Scholar] [CrossRef]
  60. Wang, Y.P.; Cheng, X.; Shan, Q.W.; Zhang, Y.; Liu, J.X.; Gao, C.X.; Qiu, J.L. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 2014, 32, 947–951. [Google Scholar] [CrossRef]
Table 1. Virulence frequency (VF) in the Czech Blumeria hordei population that overcomes specific powdery mildew (Ml) resistance genes in barley varieties.
Table 1. Virulence frequency (VF) in the Czech Blumeria hordei population that overcomes specific powdery mildew (Ml) resistance genes in barley varieties.
VarietyRegistrationMl GeneYearVF (%)YearVF (%)YearVF (%)
Kangoo 12008Ro 20082.4 2201471.7 3
Laverda 42007aLv20080 520090.7 6201123.3 3
Saturn 72012p20110 620120.7 6201969.5 8
SU Celly 92020Ve20090 620110.7 6202326.2 8
1 [13], 2 [12], 3 [14], 4 [15], 5 [16], 6 [17], 7 [18], 8 [19], 9 [20].
Table 2. The breakdown of specific powdery mildew (Ml) resistance genes present in barley varieties recorded in Czech registration trials.
Table 2. The breakdown of specific powdery mildew (Ml) resistance genes present in barley varieties recorded in Czech registration trials.
Ml Gene(s)VarietyRegistrationAverage Resistance 1
a6Ametyst 2197219717.20 319774.33
a6, gRapid 2197619744.9319773.67 4
a7, gElgina 5197319718.9019747.14
a7Diabas 2197719755.2919784.33
a9Spartan 2197719768.6019833.38
a12Zefir 2198119787.0019813.24
a13, gKoral 2197819779.0019865.50
a13, gKrystal 2198119849.0019893.95
1 [22]; 2 [23]; 3 9 = resistant; 4 Bold—the most resistant/susceptible variety in that year; 5 [9].
Table 3. Spring barley varieties registered in the Czech Republic during 1993–2023: numbers of those with Mlo powdery mildew resistance and their country and region of origin.
Table 3. Spring barley varieties registered in the Czech Republic during 1993–2023: numbers of those with Mlo powdery mildew resistance and their country and region of origin.
Country of OriginRegion of EuropeTotalMlo%
GermanyCentral 1574070.2
Czech RepublicCentral352262.9
FranceNorthwest 2343191.2
NetherlandsNorthwest11327.3
DenmarkNorthwest9777.8
SlovakiaCentral6233.3
United KingdomNorthwest66100.0
AustriaCentral300.0
SwitzerlandCentral33100.0
Sum 164114
1 Region of Europe [37], 2 Subregion of Europe [38].
Table 4. List of 92 spring barley varieties registered in the Czech Republic during 1993–2020 and possessing Mlo resistance against powdery mildew.
Table 4. List of 92 spring barley varieties registered in the Czech Republic during 1993–2020 and possessing Mlo resistance against powdery mildew.
VarietyCountryRegistrationReference(s)VarietyCountryRegistrationReference(s)
of Origin 1 of Origin 1
AccordineG2018[20]LG MonusF2017[20]
AcrobatF2008[13,44]LG NabucoF2018[20]
AdamG2020[19,20]LG ToscaF2020[20]
AdventCZ2009[13]LibušeG2016[20]
AF CesarCZ2014[45]MadeiraG1999[13,44]
AksamitCZ2007[13]Madonna 3G1998[44]
AktivCZ2008[13]MantaG2016[20]
AligatorG2016[20]Marthe 2G2008[44]
AtributCZ1996[23]MonalisaF2011[45]
AvusG2020[20]MontoyaG2014[45]
BerliozF2010[13]NitranSK2004[46]
BernsteinF2008[13,44]NordusG1998[13,44]
BiatlonUK2003[44]OdysseyF2014[45]
Blanik 2NL2007[44]OlbramCZ1996[23]
BojosCZ2005[13]OlympicF2013[45]
BraemarUK2006[44]OvationF2017[20]
BritneyG2014[45]OvertureF2014[45]
CalgaryF2003[13,44]Paulis 3CZ2010[13]
Class (Topic)F2005[13,44]PetrusF2013[45]
ConcertoF2011[45]PhiladelphiaG2002[13,44]
CosmopolitanDK2019[20]PiloteCH2018[20]
DanielleG2013[45]PoetDK2007[13,44]
DelphiDK2011[45]PrestigeF2002[13,44]
DespinaG2011[45]PrunellaF2015[45]
EurojetG2004[13]PublicanUK2008[13,44]
FandagaG2020[20]RadegastCZ2005[13]
FormanG2017[20]Respekt 3CZ2003[13]
ForumCZ1993[23]RGT OtakarF2014[45]
Francin 3CZ2014[45]RunnerG2019[20]
GladysNL2010[13]SabelUK2001[13]
HenleyF2009[13]SaloonUK2002[44]
HerisCZ1998[23]SanetteCH2015[45]
IsmenaG2019[20]ShuffleG2013[45]
JerseyNL2000[44]SignoraF2009[46]
KontikiDK2009[13]SignumCZ2012[45]
KronaG1996[13]SladarSK2010[46]
KvorningG2015[45]SolistG2015[45]
KWSAmadoraG2015[45]SoulmateDK2017[20]
KWS AstaG2014[45]Spitfire 3CZ2018[20]
KWS FantexG2018[20]StreifG2009[13]
KWS IrinaG2014[45]SU ZazaG2014[45]
Laudis 550CZ2013[45]TangoF2016[20]
LaureateG2019[20]WestminsterUK2007[13,44]
LeenkeG2017[19,20]WiebkeG2012[45]
LG AurusF2019[20]Xanadu 2G2006[44]
LG EsterF2020[20]ZhanaF2013[45]
1 CZ—Czech Republic, DK—Denmark, F—France, G—Germany, NL—Netherlands, SK—Slovakia, CH—Switzerland, UK—United Kingdom. 2 In the cited article, Blanik, Marthe, and Xanadu are given the code numbers Ceb 0367, NORD 02/2338, and NORD 00/2310, respectively. 3 Heterogeneous variety, beside Mlo resistance, a line with specific resistance gene(s) is present.
Table 5. Number of spring barley varieties newly registered in the Czech Republic over a period of 31 years and the numbers and proportion of those carrying the Mlo resistance.
Table 5. Number of spring barley varieties newly registered in the Czech Republic over a period of 31 years and the numbers and proportion of those carrying the Mlo resistance.
YearsTotalMlo%
1993–19958112.5
1996–200017847.1
2001–2005211257.1
2006–2010312064.5
2011–2015352777.1
2016–2020292482.8
2021–2023232295.7
Sum164114
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

Dreiseitl, A. Mlo-Mediated Broad-Spectrum and Durable Resistance against Powdery Mildews and Its Current and Future Applications. Plants 2024, 13, 138. https://doi.org/10.3390/plants13010138

AMA Style

Dreiseitl A. Mlo-Mediated Broad-Spectrum and Durable Resistance against Powdery Mildews and Its Current and Future Applications. Plants. 2024; 13(1):138. https://doi.org/10.3390/plants13010138

Chicago/Turabian Style

Dreiseitl, Antonín. 2024. "Mlo-Mediated Broad-Spectrum and Durable Resistance against Powdery Mildews and Its Current and Future Applications" Plants 13, no. 1: 138. https://doi.org/10.3390/plants13010138

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