Identification of QTLs for powdery mildew (Podosphaera aphanis; syn. Sphaerotheca macularis f. sp. fragariae) susceptibility in cultivated strawberry (Fragaria ×ananassa)

Autoři: Daniel J. Sargent aff001;  Matteo Buti aff003;  Nada Šurbanovski aff001;  May Bente Brurberg aff004;  Muath Alsheikh aff005;  Matthew P. Kent aff007;  Jahn Davik aff004
Působiště autorů: PlantSci Consulting Ltd. Kent, United Kingdom aff001;  Fondazione Edmund Mach, San Michele all’Adige, Trentino, Italy aff002;  Department of Agriculture, Food, Environment and Forestry, University of Florence, Florence, Italy aff003;  Division of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research, Ås, Norway aff004;  Department of Plant Sciences, Norwegian University of Life Sciences, Ås, Norway aff005;  Graminor Breeding Ltd., Ridabu, Norway aff006;  Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway aff007
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222829


Strawberry powdery mildew (Podosphaera aphanis Wallr.) is a pathogen which infects the leaves, fruit, stolon and flowers of the cultivated strawberry (Fragaria ×ananassa), causing major yield losses, primarily through unmarketable fruit. The primary commercial control of the disease is the application of fungicidal sprays. However, as the use of key active ingredients of commercial fungicides is becoming increasingly restricted, interest in developing novel strawberry cultivars exhibiting resistance to the pathogen is growing rapidly. In this study, a mapping population derived from a cross between two commercial strawberry cultivars (‘Sonata’ and ‘Babette’) was genotyped with single nucleotide polymorphism (SNP) markers from the Axiom iStraw90k genotyping array and phenotyped for powdery mildew susceptibility in both glasshouse and field environments. Three distinct, significant QTLs for powdery mildew resistance were identified across the two experiments. Through comparison with previous studies and scrutiny of the F. vesca genome sequence, candidate genes underlying the genetic control of this trait were identified.

Klíčová slova:

Biology and life sciences – Genetics – Genetic loci – Quantitative trait loci – Genomics – Heredity – Genetic linkage – Plant science – Plant pathology – Plant pathogens – Plant fungal pathogens – Powdery mildew – Plant anatomy – Leaves – Molecular biology – Molecular biology techniques – Gene mapping – Linkage mapping – Research and analysis methods – Database and informatics methods – Bioinformatics – Sequence analysis


1. Nelson MD, Gubler WD, Shaw DV (1995) Inheritance of powdery mildew resistance in greenhouse-grown versus field-grown California strawberry cultivars. Phytopathology 85: 421–424.

2. Janisiewicz WJ, Takeda F, Nicols B, Glenn DM, Jurick WM II, Camp MJ (2016) Use of low-dose UV-C irradiation to control powdery mildew caused by Podosphera aphanis on strawberry plants. Can J Plant Pathol 38: 430–439.

3. Colla P, Gilardi G, Gullino ML (2012) A review and critical analysis of the European situation of soilborne disease managment in the vegetable sector. Phytoparasitica 40: 515–523.

4. Sombardier A, Savary S, Blancard D, Jolivet J, Willocquet L (2009) Effects of leaf surface and temperature on monocyclic processes in Podosphaera aphanis, causing powdery mildew of strawberry. Can J Plant Pathol 31: 439–448.

5. Xiao CL, Chandler CK, Price JF, Duval JR, Mertely JC, Legard DE (2001) Comparison of epidemics of Botrytis fruit rot and powdery mildew of strawberry in large plastic tunnel and field production systems. Plant Dis 85: 901–909. doi: 10.1094/PDIS.2001.85.8.901 30823060

6. Davik J, Honne BI (2005) Genetic variance and breeding values for resistance to a wind-borne disease [Sphaerotheca macularis (Wall. ex Fr.)] in strawberry (Fragaria x ananassa Duch.) estimated by exploring mixed and spatial models and pedigree information. Theor Appl Genet 111: 256–264. doi: 10.1007/s00122-005-2019-3 15937703

7. Kennedy C, Hasing TN, Peres NA, Whitaker VM (2013) Evaluation of strawberry species and cultivars for powdery mildew resistance in open-field and high tunnel production systems. HortScience 48: 1125–1129.

8. Pessina S, Pavan S, Catalano D, Gallotta A, Visser RGF, Bai Y et al (2014) Characterization of the MLO gene family in Rosaceae and gene expression in Malus domestica. BMC Genomics 15: 618. doi: 10.1186/1471-2164-15-618 25051884

9. Lyngkjaer MF, Newton AC, Atzema JL, Baker SJ (2000) The Barley mlo-gene: an important powdery mildew resistance source. Agronomie 20: 745–756.

10. Pessina S, Angeli D, Martens S, Visser RG, Bai Y, Salamini F et al (2016) The knock-down of the expression of MdMLO19 reduces susceptibility to powdery mildew (Podosphaera leucotricha) in apple (Malus domestica). Plant Biotech J 14: 2033–2044.

11. Jiwan D, Roalson EH, Main D, Dhingra A (2013) Antisense expression of peach mildew resistance locus O (PpMlo1) gene confers cross-species resistance to powdery mildew in Fragaria x ananassa. Transgenic Res 22: 1119–1131. doi: 10.1007/s11248-013-9715-6 23728780

12. Miao LX, Jiang M, Zhang YC, Yang XF, Zhang HQ, Zhang ZF et al (2016) Genomic identification, phylogeny, and expression analysis of MLO genes involved in susceptibility to powdery mildew in Fragaria vesca. Genet Mol Res 15: 1.

13. Jambagi S, Dunwell JM (2017) Identification and expression analysis of Fragaria vesca MLO genes involved in interaction with powdery mildew (Podosphaera aphanis). J Adv Plant Biol 40–54.

14. Edger PP, VanBuren R, Colle M, Poorten TJ, Man Wai C, Niederhuth CE et al (2018) Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. GigaScience 7: 1–2.

15. Koishihara H, Enoki H, Muramatsu M, Nishimura S, Yui S, Honjo M (2015) Marker associated with powdery mildew resistance in plant of genus fragaria and use thereof. US patent application # US20180112267A1.

16. Cockerton HM, Vickerstaff RJ, Karlstöm A, Wilson F, Sobczyk M, He JQ et al (2018) Identification of powdery mildew resistance QTL in strawberry (Fragaria × ananassa). Theor Appl Genet 131: 1995–2007. doi: 10.1007/s00122-018-3128-0 29971472

17. Bassil NV, Davis TM, Zhang H, Ficklin S, Mittmann M, Webster T et al (2015) Development and preliminary evaluation of a 90 K Axiom SNP Array for the allo-octoploid cultivated strawberry Fragaria x ananassa. BMC Genomics 16: 155. doi: 10.1186/s12864-015-1310-1 25886969

18. Verma S, Bassil NV, Van de Weg E, Harrison RJ, Monfort A, Hidalgo JM et al (2017) Development and evaluation of the Axiom IStraw35 384HT array for the allo-octoploid cultivated strawberry Fragaria ×ananassa. Acta Horticultura 1156.

19. Davik J, Sargent DJ, Brurberg MB, Lien S, Kent M, Alsheikh M (2015) A ddRAD based linkage map of the cultivated strawberry, Fragaria xananassa. PLoS ONE doi: 10.1371/journal.pone.0137746 26398886

20. Williams ER (1986) A neighbour model for field experiments. Biometrika 73: 279–287.

21. Aslaf B, Gadoury DM, Tronsmo AM, Seem RC, Dobson A, Peres NA et al (2014) Ontogenetic resistance of leaves and fruit, and how leaf folding influences the distribution of powdery mildew on strawberry plants colonized by Podosphaera aphanis. Phytopathology 104: 954–964. doi: 10.1094/PHYTO-12-13-0345-R 24624951

22. Simpson DW (1987) The inheritance of mildew resistance in everbearing and day-neutral strawberry seedlings. J Hort Sci 62: 329–334.

23. Gilmour AR, Cullis BR, Verbyla AP (1997) Accounting for natural and extraneous variation in the analysis of field experiments. J Agric Biol Env Stats 2: 269–293.

24. Self SG, Liang K-Y (1987) Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J Amer Stat Soc 82: 605–610.

25. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml User Guide Release 3.0.

26. Sargent DJ, Yang Y, Surbanovski N, Bianco L, Buti M, Velasco R et al (2016) HaploSNP affinities and linkage map positions illuminate subgenome composition in the octoploid, cultivated strawberry (Fragaria × ananassa). Plant Sci 242: 140–150. doi: 10.1016/j.plantsci.2015.07.004 26566832

27. Edger PP, Poorten TJ, VanBuren R, Hardigan MA, Colle M, McKain MR et al (2019) Origin and evolution of the octoploid strawberry genome. Nat Genet 51: 541–547. doi: 10.1038/s41588-019-0356-4 30804557

28. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43: 109–116. doi: 10.1038/ng.740 21186353

29. Jung S, Ficklin SP, Lee T, Cheng C-H, Blenda A, Zheng P et al (2013) The Genome Database for Rosaceae (GDR): year 10 update. Nucleic Acids Res 42: D1237–D1244. doi: 10.1093/nar/gkt1012 24225320

30. Tennessen JA, Govindarajulu R, Ashman T-L, Liston A (2014) Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted linkage maps. Genome Biol Evol 6: 3295–3313. doi: 10.1093/gbe/evu261 25477420

31. Leipe DD, Koonin EV, Aravind L (2004) STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: Multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 343: 1–28. doi: 10.1016/j.jmb.2004.08.023 15381417

32. Arya P, Kumar G, Acharya V, Singh AK (2014) Genome-wide identification and expression analysis of NBS-encoding genes in Malus x domestica and expansion of NBS genes family in Rosaceae. PLoS ONE 9: e107989. doi: 10.1371/journal.pone.0107989

33. Sekhwal MK, Li P, Lam I, Wang X, Cloutier S, You FM (2015) Disease resistance gene analogs (RGAs) in plants. Int J Mol Sci 16: 19248–19290. doi: 10.3390/ijms160819248 26287177

34. Zhou F, Kurth J, Wei F, Elliott C, Valè G, Yahiaoui N et al (2001) Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signalling pathway. The Plant Cell 13: 337–350. doi: 10.1105/tpc.13.2.337 11226189

35. Liu W, Frick M, Huel R, Nikiforuk CL, Wang X, Gaudet DA et al (2014) The stripe rust resistance gene γr10 encodes en evolutionary-conserved and unique CC-NBS-LRR sequence in wheat. Mol Plant 7: 1740–1755. doi: 10.1093/mp/ssu112 25336565

36. Noël L, Moores TL, van der Biezen EA, Parniske M, Daniels MJ, Parker JE et al (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. The Plant Cell 11: 2099–2111. 10559437

Článek vyšel v časopise


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Zvyšte si kvalifikaci online z pohodlí domova

Ulcerative colitis_muž_břicho_střeva
Ulcerózní kolitida
nový kurz

Blokátory angiotenzinových receptorů (sartany)
Autoři: MUDr. Jiří Krupička, Ph.D.

Antiseptika a prevence ve stomatologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Citikolin v neuroprotekci a neuroregeneraci: od výzkumu do klinické praxe nejen očních lékařů
Autoři: MUDr. Petr Výborný, CSc., FEBO

Zánětlivá bolest zad a axiální spondylartritida – Diagnostika a referenční strategie
Autoři: MUDr. Monika Gregová, Ph.D., MUDr. Kristýna Bubová

Všechny kurzy