Mlo-Mediated Broad-Spectrum and Durable Resistance against Powdery Mildews and Its Current and Future Applications
Abstract
:1. Introduction
2. Mlo Resistance in Barley
3. Mlo Resistance in Other Crops and Plant Species
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
Data Availability Statement
Conflicts of Interest
Correction Statement
References
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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).
- 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]
- 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]
- 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]
- Dreiseitl, A. Virulence frequency to powdery mildew resistances in winter barley cultivars. Czech J. Genet. Plant Breed. 2008, 44, 160–166. [Google Scholar] [CrossRef]
- 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]
- 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]
- Dreiseitl, A. Rare virulences and great pathotype diversity of a Central European Blumeria hordei population. J. Fungi 2023, 9, 1045. [Google Scholar] [CrossRef]
- 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]
- 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]
- 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]
- Dreiseitl, A.; Jørgensen, J.H. Powdery mildew resistance in Czech and Slovak barley cultivars. Plant Breed. 2000, 119, 203–209. [Google Scholar] [CrossRef]
- 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]
- 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]
- Dreiseitl, A.; Dinoor, A. Phenotypic diversity of barley powdery mildew resistance sources. Genet. Resour. Crop Evol. 2004, 51, 251–258. [Google Scholar] [CrossRef]
- 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]
- 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]
- 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]
- Hoffmann, W.; Nover, I. Ausgangsmaterial für die Züchtung mehltauresistenter Gersten. Z. Pflanzenzücht. 1959, 42, 68–78. [Google Scholar]
- 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).
- 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]
- 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]
- Jørgensen, J.H. Durability of the ml-o powdery mildew resistance genes in barley. Vortr. Pflanzenzücht. 1984, 6, 22–31. [Google Scholar]
- Jørgensen, J.H. Discovery, characterisation and exploitation of Mlo powdery mildew resistance in barley. Euphytica 1992, 63, 141–152. [Google Scholar] [CrossRef]
- 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]
- Available online: https://en.wikipedia.org/wiki/Central_Europe (accessed on 27 October 2023).
- Available online: https://en.wikipedia.org/wiki/Northwestern_Europe (accessed on 27 October 2023).
- 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]
- 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]
- McDonald, B.A.; Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 2002, 40, 349–379. [Google Scholar] [CrossRef]
- Dreiseitl, A. Specific resistance of barley to powdery mildew, its use and beyond: A concise critical review. Genes 2020, 11, 971. [Google Scholar] [CrossRef]
- Brückner, F. The breeding of the malting barley cultivar of new morphotype Forum. Genet. Šlecht. 1993, 29, 199–203. [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Brown, J.K.M.; Wulff, B.B.H. Diversifying the menu for crop powdery mildew resistance. Cell 2022, 185, 761–763. [Google Scholar] [CrossRef]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
Variety | Registration | Ml Gene | Year | VF (%) | Year | VF (%) | Year | VF (%) |
---|---|---|---|---|---|---|---|---|
Kangoo 1 | 2008 | Ro | 2008 | 2.4 2 | 2014 | 71.7 3 | ||
Laverda 4 | 2007 | aLv | 2008 | 0 5 | 2009 | 0.7 6 | 2011 | 23.3 3 |
Saturn 7 | 2012 | p | 2011 | 0 6 | 2012 | 0.7 6 | 2019 | 69.5 8 |
SU Celly 9 | 2020 | Ve | 2009 | 0 6 | 2011 | 0.7 6 | 2023 | 26.2 8 |
Ml Gene(s) | Variety | Registration | Average Resistance 1 | |||
---|---|---|---|---|---|---|
a6 | Ametyst 2 | 1972 | 1971 | 7.20 3 | 1977 | 4.33 |
a6, g | Rapid 2 | 1976 | 1974 | 4.93 | 1977 | 3.67 4 |
a7, g | Elgina 5 | 1973 | 1971 | 8.90 | 1974 | 7.14 |
a7 | Diabas 2 | 1977 | 1975 | 5.29 | 1978 | 4.33 |
a9 | Spartan 2 | 1977 | 1976 | 8.60 | 1983 | 3.38 |
a12 | Zefir 2 | 1981 | 1978 | 7.00 | 1981 | 3.24 |
a13, g | Koral 2 | 1978 | 1977 | 9.00 | 1986 | 5.50 |
a13, g | Krystal 2 | 1981 | 1984 | 9.00 | 1989 | 3.95 |
Country of Origin | Region of Europe | Total | Mlo | % |
---|---|---|---|---|
Germany | Central 1 | 57 | 40 | 70.2 |
Czech Republic | Central | 35 | 22 | 62.9 |
France | Northwest 2 | 34 | 31 | 91.2 |
Netherlands | Northwest | 11 | 3 | 27.3 |
Denmark | Northwest | 9 | 7 | 77.8 |
Slovakia | Central | 6 | 2 | 33.3 |
United Kingdom | Northwest | 6 | 6 | 100.0 |
Austria | Central | 3 | 0 | 0.0 |
Switzerland | Central | 3 | 3 | 100.0 |
Sum | 164 | 114 |
Variety | Country | Registration | Reference(s) | Variety | Country | Registration | Reference(s) |
---|---|---|---|---|---|---|---|
of Origin 1 | of Origin 1 | ||||||
Accordine | G | 2018 | [20] | LG Monus | F | 2017 | [20] |
Acrobat | F | 2008 | [13,44] | LG Nabuco | F | 2018 | [20] |
Adam | G | 2020 | [19,20] | LG Tosca | F | 2020 | [20] |
Advent | CZ | 2009 | [13] | Libuše | G | 2016 | [20] |
AF Cesar | CZ | 2014 | [45] | Madeira | G | 1999 | [13,44] |
Aksamit | CZ | 2007 | [13] | Madonna 3 | G | 1998 | [44] |
Aktiv | CZ | 2008 | [13] | Manta | G | 2016 | [20] |
Aligator | G | 2016 | [20] | Marthe 2 | G | 2008 | [44] |
Atribut | CZ | 1996 | [23] | Monalisa | F | 2011 | [45] |
Avus | G | 2020 | [20] | Montoya | G | 2014 | [45] |
Berlioz | F | 2010 | [13] | Nitran | SK | 2004 | [46] |
Bernstein | F | 2008 | [13,44] | Nordus | G | 1998 | [13,44] |
Biatlon | UK | 2003 | [44] | Odyssey | F | 2014 | [45] |
Blanik 2 | NL | 2007 | [44] | Olbram | CZ | 1996 | [23] |
Bojos | CZ | 2005 | [13] | Olympic | F | 2013 | [45] |
Braemar | UK | 2006 | [44] | Ovation | F | 2017 | [20] |
Britney | G | 2014 | [45] | Overture | F | 2014 | [45] |
Calgary | F | 2003 | [13,44] | Paulis 3 | CZ | 2010 | [13] |
Class (Topic) | F | 2005 | [13,44] | Petrus | F | 2013 | [45] |
Concerto | F | 2011 | [45] | Philadelphia | G | 2002 | [13,44] |
Cosmopolitan | DK | 2019 | [20] | Pilote | CH | 2018 | [20] |
Danielle | G | 2013 | [45] | Poet | DK | 2007 | [13,44] |
Delphi | DK | 2011 | [45] | Prestige | F | 2002 | [13,44] |
Despina | G | 2011 | [45] | Prunella | F | 2015 | [45] |
Eurojet | G | 2004 | [13] | Publican | UK | 2008 | [13,44] |
Fandaga | G | 2020 | [20] | Radegast | CZ | 2005 | [13] |
Forman | G | 2017 | [20] | Respekt 3 | CZ | 2003 | [13] |
Forum | CZ | 1993 | [23] | RGT Otakar | F | 2014 | [45] |
Francin 3 | CZ | 2014 | [45] | Runner | G | 2019 | [20] |
Gladys | NL | 2010 | [13] | Sabel | UK | 2001 | [13] |
Henley | F | 2009 | [13] | Saloon | UK | 2002 | [44] |
Heris | CZ | 1998 | [23] | Sanette | CH | 2015 | [45] |
Ismena | G | 2019 | [20] | Shuffle | G | 2013 | [45] |
Jersey | NL | 2000 | [44] | Signora | F | 2009 | [46] |
Kontiki | DK | 2009 | [13] | Signum | CZ | 2012 | [45] |
Krona | G | 1996 | [13] | Sladar | SK | 2010 | [46] |
Kvorning | G | 2015 | [45] | Solist | G | 2015 | [45] |
KWSAmadora | G | 2015 | [45] | Soulmate | DK | 2017 | [20] |
KWS Asta | G | 2014 | [45] | Spitfire 3 | CZ | 2018 | [20] |
KWS Fantex | G | 2018 | [20] | Streif | G | 2009 | [13] |
KWS Irina | G | 2014 | [45] | SU Zaza | G | 2014 | [45] |
Laudis 550 | CZ | 2013 | [45] | Tango | F | 2016 | [20] |
Laureate | G | 2019 | [20] | Westminster | UK | 2007 | [13,44] |
Leenke | G | 2017 | [19,20] | Wiebke | G | 2012 | [45] |
LG Aurus | F | 2019 | [20] | Xanadu 2 | G | 2006 | [44] |
LG Ester | F | 2020 | [20] | Zhana | F | 2013 | [45] |
Years | Total | Mlo | % |
---|---|---|---|
1993–1995 | 8 | 1 | 12.5 |
1996–2000 | 17 | 8 | 47.1 |
2001–2005 | 21 | 12 | 57.1 |
2006–2010 | 31 | 20 | 64.5 |
2011–2015 | 35 | 27 | 77.1 |
2016–2020 | 29 | 24 | 82.8 |
2021–2023 | 23 | 22 | 95.7 |
Sum | 164 | 114 |
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. |
© 2024 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
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
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 StyleDreiseitl, 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