Evolutionary analysis of herbivorous insects in natural and agricultural environments

Herbivorous insects offer a remarkable example of the biological diversity that formed the foundation for Darwin's theory of evolution by natural selection. The ability of insects to evolve resistance rapidly to insecticides and host‐plant resistance present a continual challenge for pest management. This paper considers the manner in which genetic constraints, host‐plant availability and trade‐offs affect the evolution of herbivorous insects in natural and agricultural environments, and the extent to which lessons learned from studying natural systems may be applied to improve insect resistance management in agricultural systems. Studies on the genetic architecture of adaptation by herbivores to host plants and to insecticides are reviewed. The genetic basis of resistance is an important component of simulation models that predict the evolution of resistance. These models often assume monogenic resistance, but available data suggest that this assumption may be overly narrow and that modeling of resistance as oligogenic or polygenic may be more appropriate. As omics (e.g. genomics and proteomics) technologies become more accessible, a better understanding of the genetic basis of resistance will be possible. Trade‐offs often accompany adaptations by herbivores. Trade‐offs arise when the benefit of a trait, such as the ability to feed on a novel host plant or to survive in the presence of an insecticide, is counterbalanced by fitness costs that decrease fitness in the absence of the selective agent. For resistance to insecticides, and resistance to insecticidal transgenic crops in particular, fitness costs may act as an evolutionary constraint and delay or prevent the evolution of resistance. An important observation is that certain ecological factors such as host plants and entomopathogens can magnify fitness costs, which is termed ecological negative cross‐resistance. The application of omics technologies may allow for more efficient identification of factors that will impose ecological negative cross‐resistance, thereby bolstering insect resistance management. Copyright © 2009 Society of Chemical Industry     

植物病原真菌对杀菌剂抗性的研究进展

科学施用杀菌剂是植物病害综合治理的重要措施之一, 然而由于杀菌剂的长期使用, 病菌抗药性问题逐渐加重, 严重影响药剂的防治效果和使用寿命。近年来, 随着分子生物学技术的快速发展, 人们对杀菌剂抗性机制有了更深入的理解, 并开发出了病菌抗药基因型快速检测的方法。本文总结了植物病原真菌对苯并咪唑类杀菌剂(BZD)、肌球蛋白合成抑制剂、甾醇脱甲基抑制剂(DMI)、QoI类抑制剂、琥珀酸脱氢酶抑制剂（SDHI）和二甲酰亚胺类杀菌剂(DC)的抗药性现状与抗性机制。在此基础上, 介绍了聚合酶链反应(PCR)、限制性片段长度多态性(RFLP)、等位基因特异性PCR和环介导等温扩增(LAMP)技术在杀菌剂抗性快速检测方面的研究进展。此外, 对抗药性治理对策进行了讨论和展望。     

The fungicide-resistance problem

Mutation to resistance is more likely to occur to systemic fungicides than to conventional fungicides. The possibilities to obtain systemic fungicides, to which fungi will not readily become resistant, are discussed. A high potential for development of fungicide resistance does, however, not always imply that problems will arise in practice. If fungicide resistance is accompanied with reduced pathogenicity and fitness, the build-up of a resistant population will be hampered or prevented. Of importance are also the type of disease and the selection pressure exerted by the fungicide. The latter may be influenced by the management of fungicide application.     

Target and non-target site mechanisms of fungicide resistance and their implications for the management of crop pathogens

Fungicides are indispensable for high-quality crops, but the rapid emergence and evolution of fungicide resistance have become the most important issues in modern agriculture. Hence, the sustainability and profitability of agricultural production have been challenged due to the limited number of fungicide chemical classes. Resistance to site-specific fungicides has principally been linked to target and non-target site mechanisms. These mechanisms change the structure or expression level, affecting fungicide efficacy and resulting in different and varying resistance levels. This review provides background information about fungicide resistance mechanisms and their implications for developing anti-resistance strategies in plant pathogens. Here, our purpose was to review changes at the target and non-target sites of quinone outside inhibitor (QoI) fungicides, methyl-benzimidazole carbamate (MBC) fungicides, demethylation inhibitor (DMI) fungicides, and succinate dehydrogenase inhibitor (SDHI) fungicides and to evaluate if they may also be associated with a fitness cost on crop pathogen populations. The current knowledge suggests that understanding fungicide resistance mechanisms can facilitate resistance monitoring and assist in developing anti-resistance strategies and new fungicide molecules to help solve this issue. © 2023 Society of Chemical Industry.     

植物病原菌对杀菌剂抗性风险评估

植物病原菌对杀菌剂的抗性风险由基本风险和治理风险组成。杀菌剂使用之前或之初可根据 人工诱变、药剂选择或驯化实验、田间野生敏感菌株敏感性变异、抗药菌株的生物及遗传特 征、杀菌剂作用方式等进行基本抗药风险预测；杀菌剂使用数年之后可根据人工诱变、药剂 选择或驯化、田间药效与抗药性发生、抗药菌株的生物及遗传特征、杀菌剂作用方式与使用 对策等已有资料进行抗药风险评估。目前已有4种方法用于抗药风险评估。由杀菌剂与病害 共同决定的基本抗药风险可分成低、中和高度。基本抗性风险高的药剂合理使用可延缓田间 抗药性发生，中度基本抗性风险药剂不合理使用也可引发田间抗药性发生和药效明显降低。     

QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola

BACKGROUND: QoI fungicides or quinone outside inhibitors (also called strobilurins) have been widely used to control agriculturally important fungal pathogens since their introduction in 1996. Strobilurins block the respiration pathway by inhibiting the cytochrome bc1 complex in mitochondria. Several plant pathogenic fungi have developed field resistance. The first QoI resistance in Mycosphaerella graminicola (Fuckel) Schroter was detected retrospectively in UK in 2001 at a low frequency in QoI-treated plots. During the following seasons, resistance reached high frequencies across northern Europe. The aim of this study was to identify the main evolutionary forces driving the rapid emergence and spread of QoI resistance in M. graminicola populations.RESULTS: The G143A mutation causing QoI resistance was first detected during 2002 in all tested populations and in eight distinct mtDNA sequence haplotypes. By 2004, 24 different mtDNA haplotypes contained the G143A mutation. Phylogenetic analysis showed that strobilurin resistance was acquired independently through at least four recurrent mutations at the same site of cytochrome b. Estimates of directional migration rates showed that the majority of gene flow in Europe had occurred in a west-to-east direction.CONCLUSION: This study demonstrated that recurring mutations independently introduced the QoI resistance allele into different genetic and geographic backgrounds. The resistant haplotypes then increased in frequency owing to the strong fungicide selection and spread eastward through wind dispersal of ascospores.     

The genetic basis of classification of fungicides according to resistance risk1

In order to render a chemical ineffective, target organisms must possess appropriate genetic variability. Depending on whether plant pathogenic fungi can meet this requirement, our agricultural fungicides can be classified into three groups characterized as follows. 1) Major changes in sensitivity result from single-gene mutations. Such major genes are apparently present in all sensitive species. Risk of control failure is high or moderate, depending on the effect of resistance mutations on fitness. 2) Single-gene mutations have small effects on sensitivity. Positive interaction between several mutant genes often leads to a stepwise increase in resistance, but usually at an increasing cost in terms of fitness. Resistance risk is low to moderate. 3) Ability for mutational modification of sensitivity never demonstrated, so that appropriate variability is apparently unavailable and low, if any, resistance risk is involved. The paper examines what evidence is available for the classification of each important agricultural fungicide into one of the above groups and what are the implications of this classification on disease control strategies.     

植物病原菌抗药性及其抗性治理策略

随着现代高活性的选择性杀菌剂的研发和广泛使用,病原菌的抗药性问题日趋严重,这已成为植物病害化学保护领域最受关注的问题之一。本文阐释了抗药性相关术语的定义,概述了病原菌的抗药性现状,并从自然选择和诱导突变两种学说的角度分析了抗药性产生的原因。进一步分析了抗药性群体流行与病原菌自身特点、杀菌剂类型和作用机制等影响因子密切相关,综述了抗药性风险评估、抗药性机制、抗药性进化以及抗药性常规和分子检测方法等内容。最后,提出了抗药性治理的目标和策略,即根据抗药病原群体形成的主要影响因素,针对性地设计抗药性治理短期和长期策略,特别是需进一步加强对新药剂和新防治对象开展抗药性风险评估、制定抗药性管理策略、建立再评价机制等。综上,明确植物病原菌抗药性发生发展特点并制定科学合理的抗性治理策略,对进一步开展植物病害的科学防控具有重要的参考价值。     

实时荧光定量PCR在植物病害流行学中的应用

实时荧光定量PCR广泛应用于植物病理学研究的各个领域。近年来已开始应用于植物病害流行学的定量研究中,本文对近年来实时荧光定量PCR技术在病菌初始菌源的定量分析、病害流行动态的监测、寄主抗病性的快速鉴定和植物病原菌的抗药性监测等方面的应用进行了综述。     

Do some IPM concepts contribute to the development of fungicide resistance? Lessons learned from the apple scab pathosystem in the United States

One goal of integrated pest management (IPM) as it is currently practiced is an overall reduction in fungicide use in the management of plant disease. Repeated and long‐term success of the early broad‐spectrum fungicides led to optimism about the capabilities of fungicides, but to an underestimation of the risk of fungicide resistance within agriculture. In 1913, Paul Ehrlich recognized that it was best to ‘hit hard and hit early’ to prevent microbes from evolving resistance to treatment. This tenet conflicts with the fungicide reduction strategies that have been widely promoted over the past 40 years as integral to IPM. The authors hypothesize that the approaches used to implement IPM have contributed to fungicide resistance problems and may still be driving that process in apple scab management and in IPM requests for proposals. This paper also proposes that IPM as it is currently practiced for plant diseases of perennial systems has been based on the wrong model, and that conceptual shifts in thinking are needed to address the problem of fungicide resistance. © 2013 Society of Chemical Industry     

The dose rate debate: does the risk of fungicide resistance increase or decrease with dose?

This paper reviews the evidence relating to the question: does the risk of fungicide resistance increase or decrease with dose? The development of fungicide resistance progresses through three key phases. During the ‘emergence phase’ the resistant strain has to arise through mutation and invasion. During the subsequent ‘selection phase’, the resistant strain is present in the pathogen population and the fraction of the pathogen population carrying the resistance increases due to the selection pressure caused by the fungicide. During the final phase of ‘adjustment’, the dose or choice of fungicide may need to be changed to maintain effective control over a pathogen population where resistance has developed to intermediate levels. Emergence phase: no experimental publications and only one model study report on the emergence phase, and we conclude that work in this area is needed. Selection phase: all the published experimental work, and virtually all model studies, relate to the selection phase. Seven peer reviewed and four non‐peer reviewed publications report experimental evidence. All show increased selection for fungicide resistance with increased fungicide dose, except for one peer reviewed publication that does not detect any selection irrespective of dose and one conference proceedings publication which claims evidence for increased selection at a lower dose. In the mathematical models published, no evidence has been found that a lower dose could lead to a higher risk of fungicide resistance selection. We discuss areas of the dose rate debate that need further study. These include further work on pathogen‐fungicide combinations where the pathogen develops partial resistance to the fungicide and work on the emergence phase.     

木霉在植物病害生物防治中的应用及作用机制

木霉是植物病害生物防治中应用和研究非常广泛的一类生防真菌。本文阐述了木霉在多种植物病害防治上的应用及防治效果,并概括了木霉在生防过程中对植物病原物的生防机制,包括竞争、重寄生、抗生作用等,以及木霉与植物互作中对植物促生和诱导植物抗性的机制。目前,世界上含木霉的商品化制剂已超过250种,在不同国家地区都取得了良好的防治效果,更多的优秀生防木霉菌株也在通过野生菌株筛选或遗传改良等方式开发。木霉生物防治及机制研究对推广生物防治和减少化学农药有重要意义。     

Challenges facing arthropod biological control: identifying traits for genetic improvement of predators in protected crops

Biological control is an efficient pest control method but there are still limitations that are hindering its wider adoption. Genetic improvement of biological control agents (BCAs) can help to overcome these constraints, but the choice of key attributes for better performance that need to be selected is still an open question. Several characteristics have been suggested but the harsh reality is that selective breeding of BCAs has received a lot of attention but resulted in very little progress. Identifying the appropriate traits to be prioritized may be the first step to reverse this situation. In our opinion, the best way is to look at the factors limiting the performance of key BCAs, especially generalist predators (pesticide compatibility, prey‐density dependence, non‐suitable crops, and extreme environmental conditions), and according to these challenges, to choose the attributes that would allow BCAs to overcome those limitations. The benefits of selection for higher resistance to toxins, whether artificially applied (pesticides) or plant produced (plant defenses); increased fitness when feeding on non‐prey food (supplemented or plant‐derived); and better adaptation to extreme temperature and humidity are discussed. In conclusion, genetic improvement of BCAs can bring about new opportunities to biocontrol industry and users to enhance biocontrol resilience. © 2020 Society of Chemical Industry     

Triazole fungicides and the selection of resistance to medical triazoles in the opportunistic mould Aspergillus fumigatus

Azole resistance is an emerging problem in the opportunistic mould Aspergillus fumigatus. The triazoles are the most important agents for the management of Aspergillus diseases in humans. Selection for acquired resistance may occur in the hospital setting through exposure to high doses of azoles during azole therapy, but evidence is accumulating that A. fumigatus may become resistant to medical triazoles through environmental exposure to fungicides. The recovery of A. fumigatus isolates resistant to the medical triazoles from azole‐naive patients as well as from the environment strongly indicates an environmental route of resistance selection. Molecule alignment studies have identified five fungicides that share a very similar molecule structure with the medical triazoles, and thus may have selected for mechanisms that confer resistance to both groups of compounds. It is important to explore further the presumed fungicide‐driven route of resistance selection in order to implement effective preventive measures as the prevalence of azole resistance in A. fumigatus continues to increase and causes major challenges in the management of azole‐resistant Aspergillus diseases. Copyright © 2012 Society of Chemical Industry     

Alternative oxidase reduces the sensitivity of Mycosphaerella graminicola to QOI fungicides

Forty-six (1.5%) of nearly 3000 isolates of Mycosphaerella graminicola assayed in vitro were resistant to the QOI fungicide azoxystrobin, but on sub-culturing only ten remained resistant. Cross-resistance extended to other QOIs, but varied between different isolates. In planta the resistant isolates were not well controlled, especially at lower azoxystrobin dose rates. Propyl gallate, an inhibitor of alternative oxidase, potentiated the activity of azoxystrobin in vitro so that resistance was no longer observed. The growth of resistant strains in the presence of azoxystrobin led to alternative oxidase activation. This increased flexibility in respiration allows resistant strains to survive in the presence of a QOI fungicide. Under these conditions, selection for target-site mutations can occur. Using QOIs preventatively reduces the risk of resistance since the alternative oxidase cannot by itself generate all the energy needed for germination and early infection.     

多因子联合诱导系统的构建及对黄瓜白粉病防治试验

由多个不同的抗病诱导因子组成植物抗病诱导系统的1个子系统。每个因子都是这个系统中的1个要素。系统的性质不但取决于系统中的要素,还取决于要素的结构。合理的配伍可以使要素与要素之间、要素与系统之间的关系得以优化,使系统的功能得以强化。把筛选得到的多个不同的抗病诱导因子进行配伍,组合成新的"诱导组合体",其诱导效应比单一因子显著提高;用不同的"诱导组合体"进行"相继诱导"和"循环诱导",则进一步提高诱导效应,对黄瓜白粉病的田间防治效果达到78.16%,高于常规杀菌剂的防治效果。     

Adaptation to fungicides in Monilinia fructicola isolates with different fungicide resistance phenotypes

The ability to develop fungicide resistance was assessed in Monilinia fructicola isolates with different fungicide sensitivity phenotypes by adapting mycelium and conidia to increasing concentrations of selective fungicides and UV mutagenesis. Results showed that adaptation to Quinone outside inhibitor (QoI) fungicide azoxystrobin and sterol demethylation inhibitor (DMI) fungicide propiconazole was more effective in conidial-transfer experiments compared to mycelial-transfer experiments. DMI-resistant (DMI-R) isolates adapted to significantly higher doses of azoxystrobin in both, mycelial- and conidial-transfer experiments compared to benzimidazole-resistant (BZI-R) and sensitive (S) isolates. Adaptation to propiconazole in conidial-transfer experiments was accelerated in BZI-R isolates when a stable, nonlethal dose of 50 microg/ml thiophanate-methyl was added to the selection medium. One of two azoxystrobin-resistant mutants from DMI-R isolates did not show any fitness penalties; the other isolate expired before further tests could be carried out. The viable mutant caused larger lesions on detached peach fruit sprayed with azoxystrobin compared to the parental isolate. The azoxystrobin sensitivity of the viable mutant returned to baseline levels after the mutant was transferred to unamended medium. However, azoxystrobin resistance recovered quicker in the mutant compared to the corresponding parental isolate after renewed subculturing on medium amended with 0.2 and 1 microg/ml azoxystrobin; only the mutant but not the parental isolate was able to adapt to 5 microg/ml azoxystrobin. In UV mutagenesis experiments, the DMI-R isolates produced significantly more mutants compared to S isolates. All of the UV-induced mutants showed stable fungicide resistance with little fitness penalty. This study indicates the potential for QoI fungicide resistance development in M. fructicola in the absence of a mutagen and provides evidence for increased mutability and predisposition to accelerated adaptation to azoxystrobin in M. fructicola isolates resistant to DMI fungicides.     

Pervasive fungicide resistance in Botrytis from strawberry in Norway: Identification of the grey mould pathogen and mutations

Control of grey mould, caused by Botrytis spp., is a major challenge in open field strawberry production. Botrytis was isolated from plant parts collected from 19 perennial strawberry fields with suspected fungicide resistance in the Agder region of Norway in 2016. Resistance to boscalid, pyraclostrobin and fenhexamid was high and found in 89.1%, 86.0% and 65.4% of conidia samples, respectively. Multiple fungicide resistance was common; 69.6% of conidia samples exhibited resistance to three or more fungicides. Botrytis group S and B. cinerea sensu stricto isolates were obtained from 19 and 16 fields, respectively. The sdhB, cytb, erg27 and mrr1 genes of a selection of isolates were examined for the presence of mutations known to confer fungicide resistance to boscalid, pyraclostrobin, fenhexamid and pyrimethanil plus fludioxonil, respectively. Allele-specific PCR assays were developed for efficient detection of resistance-conferring mutations in cytb. Among B. cinerea isolates, 84.7%, 86.3% and 61.3% had resistance-conferring mutations in sdhB, cytb and erg27, respectively. A triplet deletion in mrr1, resulting in ΔL497, commonly associated with the multidrug resistance phenotype MDR1h, was detected in 29.2% of Botrytis group S isolates. High frequencies of resistance to several fungicides were also detected in Botrytis from both imported and domestically produced strawberry transplants. Fungicide resistance frequencies were not different among fields grouped by level of grey mould problem assessed by growers, indicating factors other than fungicide resistance contributed to control failure, a fact that has important implications for future management of grey mould.     

Dose and number of applications that maximize fungicide effective life exemplified by Zymoseptoria tritici on wheat – a model analysis

Two key decisions that need to be taken about a fungicide treatment programme are (i) the number of applications that should be used per crop growing season, and (ii) the dosage that should be used in each application. There are two opposing considerations, with control efficacy improved by a higher number of applications and higher dose, and resistance management improved by a lower number of applications and lower dose. Resistance management aims to prolong the effective life of the fungicide, defined as the time between its introduction onto the market for use on the target pathogen, and the moment when effective control is lost due to a build‐up of fungicide resistance. Thus, the question is whether there are optimal combinations of dose rate and number of applications that both provide effective control and lead to a longer effective life. In this paper, it is shown how a range of spray programmes can be compared and optimal programmes selected. This is explored with Zymoseptoria tritici on wheat and a quinone outside inhibitor (QoI) fungicide. For this pathogen–fungicide combination, a single treatment provided effective control under the simulated disease pressure, but only if the application timing was optimal and the dose was close to the maximum permitted. Programmes with three applications were generally not optimal as they exerted too much selection for resistance. Two‐application fungicide programmes balanced effective control with reasonable flexibility of dose and application timing, and low resistance selection, leading to long effective lives of the fungicide.