Appropriate sampling to aid on-farm assessments of the haplotype composition of Zymoseptoria tritici populations.

CYP51 Zymoseptoria tritici azole fungicide resistance haplotype

Journal

Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744

Informations de publication

Date de publication:
11 Oct 2024
Historique:
revised: 27 08 2024
received: 27 10 2023
accepted: 16 09 2024
medline: 11 10 2024
pubmed: 11 10 2024
entrez: 11 10 2024
Statut: aheadofprint

Résumé

Zymoseptoria tritici causes Septoria tritici blotch (STB), which is the biggest threat to wheat in the UK. Azole fungicides have been used since the 1980s to control STB, but resistance to these chemicals is now widespread. The main resistance mechanism is based on the accumulation of CYP51 mutations, with 33 mutations reported. Hence, farmers need an accurate estimate of the haplotype composition of Z. tritici populations to develop effective fungicide treatments and resistance management. Isolates from Z. tritici lesions were collected from three fields across three commercial farms using two sampling approaches. Analysis of the isolate sequences revealed that the number of distinct haplotypes and the haplotype composition of the most dominant haplotypes varied only between and not within farms. Conventional W-shaped and point sampling both found the same percentage of distinct haplotypes and frequencies of the six most dominant haplotypes. The results from this survey suggest that farm-resistance-management strategies should be based on farm-specific rather than national data, and that sampling within a single field is sufficient. W-shaped sampling is often recommended in sampling approaches, but this survey finds no evidence of this approach being more appropriate for detecting a greater percentage of distinct haplotypes which may aid the discovery of potential new resistance threats. © 2024 Fera Science Ltd. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Sections du résumé

BACKGROUND BACKGROUND
Zymoseptoria tritici causes Septoria tritici blotch (STB), which is the biggest threat to wheat in the UK. Azole fungicides have been used since the 1980s to control STB, but resistance to these chemicals is now widespread. The main resistance mechanism is based on the accumulation of CYP51 mutations, with 33 mutations reported. Hence, farmers need an accurate estimate of the haplotype composition of Z. tritici populations to develop effective fungicide treatments and resistance management.
RESULTS RESULTS
Isolates from Z. tritici lesions were collected from three fields across three commercial farms using two sampling approaches. Analysis of the isolate sequences revealed that the number of distinct haplotypes and the haplotype composition of the most dominant haplotypes varied only between and not within farms. Conventional W-shaped and point sampling both found the same percentage of distinct haplotypes and frequencies of the six most dominant haplotypes.
CONCLUSION CONCLUSIONS
The results from this survey suggest that farm-resistance-management strategies should be based on farm-specific rather than national data, and that sampling within a single field is sufficient. W-shaped sampling is often recommended in sampling approaches, but this survey finds no evidence of this approach being more appropriate for detecting a greater percentage of distinct haplotypes which may aid the discovery of potential new resistance threats. © 2024 Fera Science Ltd. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Identifiants

pubmed: 39390891
doi: 10.1002/ps.8454
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Innovate UK
ID : 102088

Informations de copyright

© 2024 Fera Science Ltd. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Références

McDonald BA and Mundt CC, How knowledge of pathogen population biology informs management of Septoria Tritici Blotch. Phytopathology 106:948–955 (2016).
Fones H and Gurr S, The impact of Septoria tritici blotch disease on wheat: an EU perspective. Fungal Genet Biol 79:3–7 (2015).
Gosling P and Roberts AMI, Estimating costs of septoria leaf blotch (Zymoseptoria tritici) on wheat to the UK agricultural sector. Asp Appl Biol 134:29–35 (2017).
Vagndorf N, Justesen AF, Andersen JR, Jahoor A, Sindberg S and Jørgensen LN, Resistance stability to Septoria tritici blotch and comparison of screening methods for ranking STB disease. J Plant Dis Prot 126:191–201 (2019).
Chaloner TM, Fones HN, Varma V, Bebber DP and Gurr SJ, A new mechanistic model of weather‐dependent Septoria tritici blotch disease risk. Philos Trans R Soc B 374:20180266 (2019).
Castro AC, Fleitas MC, Schierenbeck M, Gerard GS and Simón MR, Evaluation of different fungicides and nitrogen rates on grain yield and bread‐making quality in wheat affected by Septoria tritici blotch and yellow spot. J Cereal Sci 83:49–57 (2018).
Lucas JA, Hawkins NJ and Fraaije BA, Chapter two ‐ the evolution of fungicide resistance, Adv Appl Microbiol 90:29–92 (2015).
Fraaije BA, Burnett FJ, Clark WS and Lucas JA, Development and field testing of fungicide anti‐resistance strategies, with particular reference to strobulurin QoI group of fungicides, p. 112 (2006).
Brunner PC, Stefanato FL and McDonald BA, Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Mol Plant Pathol 9:305–316 (2008).
Dorigan AF, Moreira SI, da Silva Costa Guimarães S, Cruz‐Magalhães V and Alves E, Target and non‐target site mechanisms of fungicide resistance and their implications for the management of crop pathogens. Pest Manag Sci 79:4731–4753 (2023).
Cools HJ and Fraaije BA, Update on mechanisms of azole resistance in Mycosphaerella graminicola and implications for future control. Pest Manag Sci 69:150–155 (2013).
Huf A, Rehfus A, Lorenz KH, Bryson R, Voegele RT and Stammler G, Proposal for a new nomenclature for CYP51 haplotypes in Zymoseptoria tritici and analysis of their distribution in Europe. Plant Pathol 67:1706–1712 (2018).
Hellin P, Duvivier M, Heick TM, Fraaije BA, Bataille C, Clinckemaillie A et al., Spatio‐temporal distribution of DMI and SDHI fungicide resistance of Zymoseptoria tritici throughout Europe based on frequencies of key target‐site alterations. Pest Manag Sci 77:5576–5588 (2021).
Ballu A, Ugazio C, Duplaix C, Noly A, Wullschleger J, Torriani SFF et al., Preventing multi‐resistance: new insights for managing fungal adaptation. Environ Microbiol 26:e16614 (2024).
Dooley H, Fungicide‐Resistance Management Tactics: Impacts on Zymoseptoria Tritici Populations. University of Reading, Reading (2015).
Fraaije BA, Burnett FJ, Cools HJ, Clark WS, Paveley N, Norman K et al., Understanding evolution and selection of azole resistance mechanisms in UK populations of Mycosphaerella graminicola; Project Report No. 475. HGCA, pp. 124 (2011).
Tamura K, Stecher G, Peterson D, Filipski A and Kumar S, MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 (2013).
Cools HJ, Bayon C, Atkins S, Lucas JA and Fraaije BA, Overexpression of the sterol 14α‐demethylase gene (MgCYP51) in Mycosphaerella graminicola isolates confers a novel azole fungicide sensitivity phenotype. Pest Manag Sci 68:1034–1040 (2012).
R Core Team, R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2021).
Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR et al., Vegan: Community Ecology Package. R Package Version 2.6‐4 (2022).
Singh NK, Karisto P and Croll D, Population‐level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici. Microb Genomics 7:14 (2021).
Zhan J, Pettway RE and McDonald BA, The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genet Biol 38:286–297 (2003).
Jørgensen LN, Matzen N, Heick TM, Havis N, Holdgate S, Clark B et al., Decreasing azole sensitivity of Z. tritici in Europe contributes to reduced and varying field efficacy. J Plant Dis Prot 128:287–301 (2021).
Vagndorf N, Heick TM, Justesen AF, Andersen JR, Jahoor A, Jørgensen LN et al., Population structure and frequency differences of CYP51 mutations in Zymoseptoria tritici populations in the Nordic and Baltic regions. Eur J Plant Pathol 152:327–341 (2018).
Bellah H, Gazeau G, Gélisse S, Amezrou R, Marcel TC and Croll D, A highly multiplexed assay to monitor pathogenicity, fungicide resistance and gene flow in the fungal wheat pathogen Zymoseptoria tritici. PLoS One 18:e0281181 (2023).

Auteurs

Catherine Harrison (C)

Plants Program, Fera Science Ltd., York Biotech Campus, York, UK.

Neil Boonham (N)

School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.

Roy Macarthur (R)

Plants Program, Fera Science Ltd., York Biotech Campus, York, UK.

Michael David Parr (MD)

Plants Program, Fera Science Ltd., York Biotech Campus, York, UK.

Femke van den Berg (F)

Plants Program, Fera Science Ltd., York Biotech Campus, York, UK.
School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK.

Classifications MeSH