Special Issue "Fungicide Resistance in Plant Pathogens"

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

Deadline for manuscript submissions: 31 March 2021.

Special Issue Editors

Prof. Dr. Dolores Fernández-Ortu?o
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
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
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

Manuscript Submission Information

Manuscripts should be submitted online at www.dlhwdz.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All papers will be peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Microorganisms is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2000 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Published Papers (2 papers)

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Open AccessReview
Fungicide Resistance Evolution and Detection in Plant Pathogens: Plasmopara viticola as a Case Study
Microorganisms 2021, 9(1), 119; https://doi.org/10.3390/microorganisms9010119 - 06 Jan 2021
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 [...] Read more.
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)
Open AccessReview
Fungicide Resistance in Powdery Mildew Fungi
Microorganisms 2020, 8(9), 1431; https://doi.org/10.3390/microorganisms8091431 - 17 Sep 2020
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 [...] Read more.
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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Planned Papers

The below list represents only planned manuscripts. Some of these manuscripts have not been received by the Editorial Office yet. Papers submitted to MDPI journals are subject to peer-review.

Title: Nontarget-site Mechanisms of Fungicide Resistance in Crop Pathogens: A Review
Authors: Mengjun Hu 1 and Shuning Chen 2
Affiliation: 1 Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD 20742; 2 Key Laboratory of Integrated Pest Management in Crops, Ministry of Agriculture, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

The rapid emergence of resistance in plant pathogens to 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 may guide and accelerate development of novel fungicides. 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 in different fungi, it is not uncommon to encounter resistant phenotypes without alternated or overexpressed target-sites. However, such nontarget-site mechanisms are relatively understudied, due in part to the complexity of fungal genome network. This type of resistance can oftentimes be transient and noninheritable, further hindering research efforts. In this review, we summarized reported mechanisms of resistance that are otherwise related to target-sites, including increased activity of efflux pumps, metabolic circumvent, detoxification, standing genetic variations, and regulation of stress response pathways, with a focus on crop pathogens. In addition, novel mechanisms of drug resistance recently characterized in human pathogens are reviewed in the context of epigenetics.     

Title: Fungicide Resistance in Powdery Mildew Fungi
Authors: Alejandra Vielba-Fernández, Antonio de Vicente, Alejandro Pérez-García and Dolores Fernández-Ortuño
Affiliation: Departamento de Microbiología. Facultad de Ciencias. Universidad de Málaga, 29071 Málaga, Spain
Abstract: Powdery mildew is one of the most common and conspicuous diseases in the world. Although cultural and biological practices may reduce the infection risk, they do not provide enough protection. Therefore, chemical control remains the most effective way to manage powdery mildew; however, fungicide resistance risk is high because typical spray programs include multiple applications per season and some of the most economically important powdery mildew are considered as high risk pathogens. In this review will be included all the cases of decrease of sensitivity, development of resistance and control failure to the chemical groups that have been or are being used for powdery mildew control. 

Title: Field evaluation of the risk of Podosphaera xanthii developing resistance to QoI fungicide ZJ0712
Author: Jianqiang Miao
Affiliation: Department of Plant Pathology, College of Plant Protection, China Agricultural University, Beijing, China.
Abstract: Greenhouse-grown cucumbers were monitored over two successive growth seasons to investigate the effects of successive application of ZJ0712, a new QoI fungicide, on the development of resistance in cucumber powdery mildew caused by Podosphaera xanthii. Resistant isolates were detected after seven successive applications even when the fungicide showed higher than 80% control efficiency. Seven stable ZJ0712-resistant P. xanthii isolates were isolated. The typical QoI-resistance-related amino acid substitutions F129L were not detected in any of the seven resistant isolates and the typical point mutation G143A conferring resistance to Qo-inhibitors in many fungal pathogens were not observed in all resistant isolates.

Title: Carbendazim and pyrimethanil resistance shift in Botrytis cinerea from tomato in China and the characterization of resistant isolates
Authors: Can Zhang1, Xili Liu 1,2*
1 Department of Plant Pathology, China Agricultural University, Beijing 100193, China; 2 State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling 712100, China
Gray mold caused by Botrytis cinerea is one of the most important diseases in tomato. It can be controlled effectively by the benzimidazole fungicide carbendazim and methionine synthesis inhibitor pyrimethanil. For resistance monitoring, 115 B. cinerea isolates were collected between 2008 and 2009, and 467 B. cinerea isolates were collected between 2015 and 2017 in China. The resistance frequency and resistance level of B. cinerea to carbendazim and pyrimethanil both increased in recent years. Moreover, most of the resistant isolates showed no significant fitness penalty. These results will be helpful for the management of B. cinerea in the field.

Title: Rapid and reliable method for detecting the C239S mutation in the β-tubulin of Phytophthora sojae, which confers resistance to zoxamide
Authors: Meng Cai 1,2, Weizhen Wang 2, Qin Peng 2, Brett Tyler 3, Xili Liu 2,*
Affiliations: 1 Key Laboratory of Pesticide and Chemical Biology of Ministry of Education, College of Chemistry, Central China Normal University, Wuhan 430079, China; 2 Department of Plant Pathology, China Agricultural University, Beijing 100193, China; 3 Department of Botany & Plant Pathology, Oregon State University, Corvallis 97330, USA
Abstract: Zoxamide is one of the two β-tubulin inhibitors available for oomycete pathogens. Our previous research demonstrated that the single point mutation C239S in β-tubulin of Phytophthora sojae significantly increase the EC50 to zoxamide. In the current study, CRISPR/Cas9 technology was utilized in P. sojae and Phytophthora capsici, validating the role of the mutation in zoxamide resistance. Two molecular assays were constructed for rapid detection of the C239S mutation in P. sojae isolates in less than 24 hours, which can effectively detect zoxamide resistance in field and provide farmers an advanced warning to make quick changes in disease control management.

Title: DMI-fungicide resistance in Venturia nashicola, the causal agent of Asian pear scab – How reliable are fungicide sensitivity tests on culture?
Authors: Ishii, H. 1,2, Nishimura, K. 2, Kikuhara, K. 3, and Yamaoka, Y. 2
Affiliation: 1 National Institute for Agro-Environmental Sciences, Tsukuba, Ibaraki, Japan; 2 University of Tsukuba, Tsukuba, Ibaraki, Japan; 3 Fukuoka Agriculture and Forestry Research Center, Chikushino, Fukuoka, Japan
Abstract: Scab, caused by Venturia nashicola, is one of the most important diseases of Asian pears. The pathogen isolates resistant to DMI fungicides are widely distributed in the fungal populations. Testing for DMI sensitivity of isolates based on mycelial growth on fungicide-amended culture medium is not very reliable due to instability of resistance, so resistance is generally assessed by inoculation tests conducted on potted pear trees sprayed with fungicides. Various mutations have been found in CYP51 gene from resistant isolates which encodes the fungicide-targeting sterol demethylase. However, as other mechanisms, e.g. overexpression of CYP51 gene, may also involve in DMI resistance, development of molecular diagnostic methods seems to be difficult.

Title: Characterization of Prochloraz Resistance in Fusarium fujikuroi from Heilongjiang Province in China
Author: Jianqiang Miao
Affiliation: China Agricultural University, Beijing, China
Abstract: The current study monitored the development of Fusarium fujikuroi resistance to prochloraz in Heilongjiang province of China and analyzed the fitness of F. fujikuroi isolates with different resistance levels. The results indicated that most of the 95 F. fujikuroi isolates collected from Heilongjiang province were resistant to prochloraz and the resistance frequency reached 93.6%. The fitness of twenty-one F. fujikuroi isolates with different resistance levels were investigated. Results showed that partial prochloraz-resistant F. fujikuroi isolates showed excellent fitness. No cross-resistance was found between prochloraz and phenamacril, ipconazole, tebuconazole, carbendazim or fluopyram.

Title: Analysis of the field fludioxonil- resistance risk and the molecular basis in Botrytis cinereal from Shanghai province in China
Author: Jianqiang Miao
Affiliation: China Agricultural University, Beijing, China
Abstract: Botrytis cinere isolates were collected from different districts of Shanghai province in 2015-2017, and their sensitivity to fludioxonil was determined. As a result, a total of 65 out of 187 field isolates (34.75%) were found to be resistant to fludioxonil, with 36 isolates (19.25%) showing high resistance and 29 isolates (15.50%) showing moderate resistance. Some of these highly resistant isolates also developed resistance to fungicides of other modes of action, indicating combined resistance of B. cinerea has emerged in Shanghai province. Biological characteristics investigation showed that the fitness of highly resistant isolates is lower than that of sensitive ones. The potential target protein Bos1 was compared between highly resistant and sensitive isolates, and different resistance-related mutations were identified, including I365S, I365N, Q369P/N373S, and N373S.

Title: Fungicide resistance in mushroom cultivation and management strategies: A review
Author: Francisco J. Gea-Alegría 1, María J. Navarro 1, Mila Santos 2, Fernando Diánez 2 and Jaime Carrasco 3
Affiliation: Centro de Investigación, Experimentación y Servicios del Champiñón, 16220 Quintanar del Rey, Cuenca, Spain; Departamento de Agronomía, Escuela Politécnica Superior, Universidad de Almería, 04120 Almería, Spain; Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1, UK
Abstract: Cultivated button mushroom, Agaricus bisporus, is susceptible to a range of fungal diseases such as dry bubble (Lecanicillium fungicola), wet bubble (Mycogone perniciosa) and cobweb (Cladobotryum spp.), that impact negatively on the crop yield and quality. Methods to control these diseases currently include strict hygiene measures and the application of fungicides. However, the use of fungicides is limited by official regulations and because the crop itself is a fungus. Therefore, it is required to use only fungicides with proven selectivity to the parasite in order to prevent mushroom damage. This work reviews aspects concerning the chemical control, reduced sensitivity to fungicides, IPM programs and alternative control methods to cope with mycoparasites in the mushroom industry.

Title: Fungicide resistance evolution in plant pathogens: Plasmopara viticola as a case study
Author: Federico Massi 1, Stefano F.F. Torriani 2, Silvia Laura Toffolatti 1*
Affiliation: 1 Dipartimento di Scienze Agrarie e Ambientali, Università degli Studi di Milano, via Celoria 2, 20133 Milano, Italy. 2 Syngenta Crop Protection Münchwilen AG, Stein, Switzerland
Abstract: Resistance evolution represents one of the biggest problems to ensure disease control in many crops. Plasmopara viticola, the most important pathogen of grapevine, has a great evolutionary capacity and has been able to develop resistance against many fungicide classes. This review aims at evaluating how the use of chemicals has led to the selection of fungicide resistance in pathogen populations and which are the available tools for monitoring its evolution. Reviewing all available monitoring tools can help shaping a global and unified vision of resistance monitoring and management. Different resistance evolutionary phases and life cycle of the pathogen will be discussed with the aim to provide guidelines to contribute limiting the spread of resistance.

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