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Fungicide Resistance in Plant Pathogens

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Plant Microbe Interactions".

Deadline for manuscript submissions: closed (30 September 2021) | Viewed by 73102

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Special Issue Editors

Prof. Dr. Dolores Fernández-Ortuño

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Guest Editor

Departamento de Microbiología, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain
Interests: agricultural fungicides; cross-resistance; fitness cost of resistance; fungicide targets; genetics and stability of fungicide resistance; modeling analysis of resistance management; molecular mechanisms of resistance; monitoring resistance; multidrug resistance; plant pathogenic fungi; practical fungicide resistance management

Prof. Dr. Guido Schnabel

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Guest Editor

Department of Plant and Environmental Sciences, Clemson University, Clemson, SC, USA
Interests: fungicide resistance in Colletotrichum, Monilinia, and Botrytis; monitors resistance in the field; determines the efficacy of fungicides both in vitro and in field trials

Dr. Anne-Sophie Walker

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Guest Editor

UMR BIOGER, INRA, AgroParisTech, Université Paris‐Saclay, Thiverval‐Grignon, France
Interests: adaptation of pathogen populations; fungicide resistance management

Special Issue Information

Dear Colleagues,

Plant diseases play a major role in the current food supply deficit. They are caused by a large number of plant pathogens, with fungi being the main cause of loss of crop yield and quality worldwide. Although several control strategies have been developed to reduce the negative effects of plant diseases, fungicide treatments are, and will remain, essential for maintaining healthy crops and high-quality yields. They are a key component of integrated disease management; however, fungicides often encounter the problem of resistance development in target pathogens.

This Special Issue will offer comprehensive coverage of the general principles and advances in fungicide resistance in plant pathogens. I kindly invite authors to submit a review article, an original research article, or a short communication on topics related to the development, mechanisms, and monitoring of resistance, including the latest advances in molecular diagnostics. Several cases outlining the practical aspects of resistance management and fungicide-use strategies on several key crops are also welcome.

As Guest Editor of this Special Issue, I look forward to reviewing your interesting submissions.

Prof. Dr. Dolores Fernández-Ortuño
Prof. Dr. Guido Schnabel
Dr. Anne-Sophie Walker
Guest Editor

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Published Papers (11 papers)

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Research

Jump to: Review

18 pages, 3128 KiB

Open AccessArticle

Are Efficient-Dose Mixtures a Solution to Reduce Fungicide Load and Delay Evolution of Resistance? An Experimental Evolutionary Approach

by Agathe Ballu, Anne Deredec, Anne-Sophie Walker and Florence Carpentier

Microorganisms 2021, 9(11), 2324; https://doi.org/10.3390/microorganisms9112324 - 10 Nov 2021

Cited by 7 | Viewed by 2544

Abstract

Pesticide resistance poses a critical threat to agriculture, human health and biodiversity. Mixtures of fungicides are recommended and widely used in resistance management strategies. However, the components of the efficiency of such mixtures remain unclear. We performed an experimental evolutionary study on the fungal pathogen Z. tritici to determine how mixtures managed resistance. We compared the effect of the continuous use of single active ingredients to that of mixtures, at the minimal dose providing full control of the disease, which we refer to as the “efficient” dose. We found that the performance of efficient-dose mixtures against an initially susceptible population depended strongly on the components of the mixture. Such mixtures were either as durable as the best mixture component used alone, or worse than all components used alone. Moreover, efficient dose mixture regimes probably select for generalist resistance profiles as a result of the combination of selection pressures exerted by the various components and their lower doses. Our results indicate that mixtures should not be considered a universal strategy. Experimental evaluations of specificities for the pathogens targeted, their interactions with fungicides and the interactions between fungicides are crucial for the design of sustainable resistance management strategies. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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15 pages, 945 KiB

Open AccessArticle

Resistance to Boscalid, Fluopyram and Fluxapyroxad in Blumeriella jaapii from Michigan (U.S.A.): Molecular Characterization and Assessment of Practical Resistance in Commercial Cherry Orchards

by Jacqueline Gleason, Jingyu Peng, Tyre J. Proffer, Suzanne M. Slack, Cory A. Outwater, Nikki L. Rothwell and George W. Sundin

Microorganisms 2021, 9(11), 2198; https://doi.org/10.3390/microorganisms9112198 - 21 Oct 2021

Cited by 7 | Viewed by 2198

Abstract

Management of cherry leaf spot disease, caused by the fungus Blumeriella jaapii, with succinate dehydrogenase inhibitor (SDHI) fungicides has been ongoing in Michigan tart cherry orchards for the past 17 years. After boscalid-resistant B. jaapii were first isolated from commercial orchards in 2010, premixes of SDHI fungicides fluopyram or fluxapyroxad with a quinone outside inhibitor were registered in 2012. Here, we report widespread resistance to fluopyram (Fluo^R), fluxapyroxad (Flux^R), and boscalid (Bosc^R) in commercial orchard populations of B. jaapii in Michigan from surveys conducted between 2016 and 2019. A total of 26% of 1610 isolates from the 2016–2017 surveys exhibited the fully-resistant Bosc^R Fluo^R Flux^R phenotype and only 7% were sensitive to all three SDHIs. Practical resistance to fluopyram and fluxapyroxad was detected in 29 of 35 and 14 of 35 commercial tart cherry orchards, respectively, in surveys conducted in 2018 and 2019. Sequencing of the SdhB, SdhC, and SdhD target genes from 22 isolates with varying resistance phenotypes showed that Bosc^S Fluo^R Flux^S isolates harbored either an I262V substitution in SdhB or an S84L substitution in SdhC. Bosc^R Fluo^R Flux^R isolates harbored an N86S substitution in SdhC, or contained the N86S substitution with the additional I262V substitution in SdhB. One Bosc^R Fluo^R Flux^R isolate contained both the I262V substitution in SdhB and the S84L substitution in SdhC. These mutational analyses suggest that Bosc^R Fluo^R Flux^R isolates evolved from fully sensitive Bosc^S, Fluo^S, Flux^S isolates in the population and not from boscalid-resistant isolates that were prevalent in the 2010–2012 time period. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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15 pages, 1705 KiB

Open AccessArticle

Fungicide Resistance Evolving in Ramularia collo-cygni Population in Estonia

by Riinu Kiiker, Marite Juurik and Andres Mäe

Microorganisms 2021, 9(7), 1514; https://doi.org/10.3390/microorganisms9071514 - 15 Jul 2021

Cited by 8 | Viewed by 3607

Abstract

Ramularia leaf spot caused by the fungus Ramularia collo-cygni, has recently become widespread in Estonian barley fields. Currently, disease control in barley fields relies on SDHI and DMI fungicides, which might be threatened by R. collo-cygni isolates that are well-adapted to fungicide pressure. In a two-year study, 353 R. collo-cygni isolates were collected from spring barley fields in Estonia. A total of 153 R. collo-cygni isolates were examined for sensitivity to azoles (DMIs; prothioconazole-desthio, epoxiconazole, mefentrifluconazole) and succinate dehydrogenase inhibitors (SDHIs; boscalid, fluxapyroxad). Epoxiconazole was the least effective and a new fungicide mefentrifluconazole was the most effective DMI. Among SDHIs, fluxapyroxad was more effective than boscalid. Also, single R. collo-cygni isolates with high resistance to tested fungicides occurred, which could affect fungicide control of the pathogen. The entire collection of R. collo-cygni was analysed for mutations in fungicide target proteins. Six mutations were identified in CYP51 gene, the most dominant being I381T, I384T, and S459C. Also, numerous point mutations in the SdhC gene were present. The mutation G143A in strobilurin target protein CytB dominates in over 80% of the R. collo-cygni population, confirming the low efficacy of strobilurin fungicides in barley disease control. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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18 pages, 2623 KiB

Open AccessArticle

DMI-Fungicide Resistance in Venturia nashicola, the Causal Agent of Asian Pear Scab—How Reliable Are Mycelial Growth Tests in Culture?

by Hideo Ishii, Hans Jorgen Cools, Kumiko Nishimura, Lorenzo Borghi, Kenji Kikuhara and Yuichi Yamaoka

Microorganisms 2021, 9(7), 1377; https://doi.org/10.3390/microorganisms9071377 - 24 Jun 2021

Cited by 9 | Viewed by 3443

Abstract

Scab, caused by Venturia nashicola, is among the most serious diseases of Asian pears and control of this disease largely relies on sterol demethylation inhibitor (DMI) fungicides. However, pear growers have complained about field performance of DMIs since the mid-2000s. In this study, to evaluate pathogen sensitivity, mycelial growth tests and inoculation tests were conducted using DMI-amended culture medium and fungicide-sprayed potted pear trees, respectively. Results confirmed distribution of isolates resistant to fenarimol, hexaconazole, and difenoconazole in the field populations. Importantly, results from tests in culture did not fully correlate with those from tests in planta. Due to phenotypic instability of resistance and poor sporulation of this pathogen in culture, resistance is generally assessed by laborious and time-consuming inoculation with conidia collected from a field. To improve the result interpretation from in vitro tests, the isolates were genotyped: the CYP51 gene which encodes the target sterol 14α-demethylase was sequenced and various mutations have been detected in the coding sequence of DMI-resistant isolates. In addition to the detected single nucleotide polymorphisms, alternative mechanisms, not based on changes in the structure of the target protein, may also increase DMI resistance. Development of molecular methods for the diagnosis of DMI resistance seems to be challenging in V. nashicola. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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15 pages, 1667 KiB

Open AccessArticle

Changes in DMI, SDHI, and QoI Fungicide Sensitivity in the Estonian Zymoseptoria tritici Population between 2019 and 2020

by Riinu Kiiker, Marite Juurik, Thies Marten Heick and Andres Mäe

Microorganisms 2021, 9(4), 814; https://doi.org/10.3390/microorganisms9040814 - 12 Apr 2021

Cited by 17 | Viewed by 3599

Abstract

Zymoseptoria tritici (Zt) populations adapt under the selection pressure of fungicides applied for disease control. The primary objective of this study was to assess fungicide sensitivity in the Estonian Zt population. A total of 282 Zt isolates from 2019 and 2020 were tested for sensitivity to azoles (DMIs; prothioconazole-desthio, epoxiconazole, mefentrifluconazole) and succinate dehydrogenase inhibitors (SDHIs; boscalid, fluxapyroxad). The efficacy of the tested fungicides varied considerably between the Estonian counties, but the Zt population is mainly sensitive to DMIs. Additionally, the frequencies of CYP51 gene alterations varied; D134G, V136C, A379G, and S524T had increased, but V136A and I381V showed a moderate decrease in 2020 in comparison to 2019. Sensitivity to SDHIs was stable, but boscalid was less effective than fluxapyroxad. SdhC gene mutations C-T33N, C-T34N, and C-N86S were common, but not linked with SDHI fungicide sensitivity assay results. Otherwise, mutation B-N225I in the SdhB subunit occurred in isolates with reduced sensitivity to SDHIs. Sensitivity to strobilurins was evaluated by the mutation G143A in the CytB gene, which was present in nearly half of the population. The data presented confirm the ongoing evolution of fungicide sensitivity in the Zt population in Estonia and highlight the importance of knowledge-based decisions for optimizing anti-resistance strategies in the field. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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13 pages, 868 KiB

Open AccessArticle

Characterization of the Field Fludioxonil Resistance and Its Molecular Basis in Botrytis cinerea from Shanghai Province in China

by Weizhen Wang, Yuan Fang, Muhammad Imran, Zhihong Hu, Sicong Zhang, Zhongqiao Huang and Xili Liu

Microorganisms 2021, 9(2), 266; https://doi.org/10.3390/microorganisms9020266 - 28 Jan 2021

Cited by 29 | Viewed by 2972

Abstract

Botrytis cinerea is a destructive necrotrophic pathogen that can infect many plant species. The control of gray mold mainly relies on the application of fungicides, and the fungicide fludioxonil is widely used in China. However, the field fungicide resistance of B. cinerea to this compound is largely unknown. In this study, B. cinerea isolates were collected from different districts of Shanghai province in 2015–2017, and their sensitivity to fludioxonil was determined. A total of 65 out of 187 field isolates (34.76%) were found to be resistant to fludioxonil, with 36 (19.25%) showing high resistance and 29 (15.51%) showing moderate resistance. Most of these resistant isolates also showed resistance to iprodione, and some developed resistance to fungicides of other modes of action. AtrB gene expression, an indicator of MDR1 and MDR1h phenotypes, was not dramatically increased in the tested resistant isolates. Biological characteristics and osmotic sensitivity investigations showed that the fitness of resistant isolates was lower than that of sensitive ones. To investigate the molecular resistance mechanisms of B. cinerea to fludioxonil, the Bos1 amino acid sequences were compared between resistant and sensitive isolates. Resistant isolates revealed either no amino acid variations or the mutations I365S, I365N, Q369P/N373S, and N373S. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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Review

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15 pages, 332 KiB

Open AccessReview

Grapevine Powdery Mildew: Fungicides for Its Management and Advances in Molecular Detection of Markers Associated with Resistance

by Andrea Kunova, Cristina Pizzatti, Marco Saracchi, Matias Pasquali and Paolo Cortesi

Microorganisms 2021, 9(7), 1541; https://doi.org/10.3390/microorganisms9071541 - 20 Jul 2021

Cited by 30 | Viewed by 6128

Abstract

Grapevine powdery mildew is a principal fungal disease of grapevine worldwide. Even though it usually does not cause plant death directly, heavy infections can lead to extensive yield losses, and even low levels of the disease can negatively affect the quality of the wine. Therefore, intensive spraying programs are commonly applied to control the disease, which often leads to the emergence and spread of powdery mildew strains resistant to different fungicides. In this review, we describe major fungicide classes used for grapevine powdery mildew management and the most common single nucleotide mutations in target genes known to confer resistance to different classes of fungicides. We searched the current literature to review the development of novel molecular methods for quick detection and monitoring of resistance to commonly used single-site fungicides against Erysiphe necator. We analyze and compare the developed methods. From our investigation it became evident that this research topic has been strongly neglected and we hope that effective molecular methods will be developed also for resistance monitoring in biotroph pathogens. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

24 pages, 8882 KiB

Open AccessReview

Control of Fungal Diseases in Mushroom Crops while Dealing with Fungicide Resistance: A Review

by Francisco J. Gea, María J. Navarro, Milagrosa Santos, Fernando Diánez and Jaime Carrasco

Microorganisms 2021, 9(3), 585; https://doi.org/10.3390/microorganisms9030585 - 12 Mar 2021

Cited by 52 | Viewed by 11684

Abstract

Mycoparasites cause heavy losses in commercial mushroom farms worldwide. The negative impact of fungal diseases such as dry bubble (Lecanicillium fungicola), cobweb (Cladobotryum spp.), wet bubble (Mycogone perniciosa), and green mold (Trichoderma spp.) constrains yield and harvest quality while reducing the cropping surface or damaging basidiomes. Currently, in order to fight fungal diseases, preventive measurements consist of applying intensive cleaning during cropping and by the end of the crop cycle, together with the application of selective active substances with proved fungicidal action. Notwithstanding the foregoing, the redundant application of the same fungicides has been conducted to the occurrence of resistant strains, hence, reviewing reported evidence of resistance occurrence and introducing unconventional treatments is worthy to pave the way towards the design of integrated disease management (IDM) programs. This work reviews aspects concerning chemical control, reduced sensitivity to fungicides, and additional control methods, including genomic resources for data mining, to cope with mycoparasites in the mushroom industry. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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19 pages, 1039 KiB

Open AccessReview

Non-Target Site Mechanisms of Fungicide Resistance in Crop Pathogens: A Review

by Mengjun Hu and Shuning Chen

Microorganisms 2021, 9(3), 502; https://doi.org/10.3390/microorganisms9030502 - 27 Feb 2021

Cited by 46 | Viewed by 7014

Abstract

The rapid emergence of resistance in plant pathogens to the limited number of chemical classes of fungicides challenges sustainability and profitability of crop production worldwide. Understanding mechanisms underlying fungicide resistance facilitates monitoring of resistant populations at large-scale, and can guide and accelerate the development of novel fungicides. A majority of modern fungicides act to disrupt a biochemical function via binding a specific target protein in the pathway. While target-site based mechanisms such as alternation and overexpression of target genes have been commonly found to confer resistance across many fungal species, it is not uncommon to encounter resistant phenotypes without altered or overexpressed target sites. However, such non-target site mechanisms are relatively understudied, due in part to the complexity of the fungal genome network. This type of resistance can oftentimes be transient and noninheritable, further hindering research efforts. In this review, we focused on crop pathogens and summarized reported mechanisms of resistance that are otherwise related to target-sites, including increased activity of efflux pumps, metabolic circumvention, detoxification, standing genetic variations, regulation of stress response pathways, and single nucleotide polymorphisms (SNPs) or mutations. In addition, novel mechanisms of drug resistance recently characterized in human pathogens are reviewed in the context of nontarget-directed resistance. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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18 pages, 4924 KiB

Open AccessReview

Fungicide Resistance Evolution and Detection in Plant Pathogens: Plasmopara viticola as a Case Study

by Federico Massi, Stefano F. F. Torriani, Lorenzo Borghi and Silvia L. Toffolatti

Microorganisms 2021, 9(1), 119; https://doi.org/10.3390/microorganisms9010119 - 6 Jan 2021

Cited by 86 | Viewed by 9812

Abstract

The use of single-site fungicides to control plant pathogens in the agroecosystem can be associated with an increased selection of resistance. The evolution of resistance represents one of the biggest challenges in disease control. In vineyards, frequent applications of fungicides are carried out every season for multiple years. The agronomic risk of developing fungicide resistance is, therefore, high. Plasmopara viticola, the causal agent of grapevine downy mildew, is a high risk pathogen associated with the development of fungicide resistance. P. viticola has developed resistance to most of the fungicide classes used and constitutes one of the most important threats for grapevine production. The goals of this review are to describe fungicide resistance evolution in P. viticola populations and how to conduct proper monitoring activities. Different methods have been developed for phenotyping and genotyping P. viticola for fungicide resistance and the different phases of resistance evolution and life cycles of the pathogen are discussed, to provide a full monitoring toolkit to limit the spread of resistance. A detailed revision of the available tools will help in shaping and harmonizing the monitoring activities between countries and organizations. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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34 pages, 4103 KiB

Open AccessReview

Fungicide Resistance in Powdery Mildew Fungi

by Alejandra Vielba-Fernández, Álvaro Polonio, Laura Ruiz-Jiménez, Antonio de Vicente, Alejandro Pérez-García and Dolores Fernández-Ortuño

Microorganisms 2020, 8(9), 1431; https://doi.org/10.3390/microorganisms8091431 - 17 Sep 2020

Cited by 84 | Viewed by 16765

Abstract

Powdery mildew fungi (Erysiphales) are among the most common and important plant fungal pathogens. These fungi are obligate biotrophic parasites that attack nearly 10,000 species of angiosperms, including major crops, such as cereals and grapes. Although cultural and biological practices may reduce the risk of infection by powdery mildew, they do not provide sufficient protection. Therefore, in practice, chemical control, including the use of fungicides from multiple chemical groups, is the most effective tool for managing powdery mildew. Unfortunately, the risk of resistance development is high because typical spray programs include multiple applications per season. In addition, some of the most economically destructive species of powdery mildew fungi are considered to be high-risk pathogens and are able to develop resistance to several chemical classes within a few years. This situation has decreased the efficacy of the major fungicide classes, such as sterol demethylation inhibitors, quinone outside inhibitors and succinate dehydrogenase inhibitors, that are employed against powdery mildews. In this review, we present cases of reduction in sensitivity, development of resistance and failure of control by fungicides that have been or are being used to manage powdery mildew. In addition, the molecular mechanisms underlying resistance to fungicides are also outlined. Finally, a number of recommendations are provided to decrease the probability of resistance development when fungicides are employed. Full article

(This article belongs to the Special Issue Fungicide Resistance in Plant Pathogens)

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