Genetics‐based methods for agricultural insect pest management

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双翅目害虫性别分离技术的研究进展及展望

在过去的几十年中,昆虫不育技术(sterile insect technique, SIT)已被用于防治农业害虫和人类健康相关的病媒害虫。相较于传统的农药控制策略,昆虫不育技术具有物种特异性和环境友好型等特点。通过释放不育雄虫的昆虫不育技术的主要障碍是在大规模饲养阶段将雄性与雌性分离,从而提高这些防治方法的成本效率,并防止释放携带和传播疾病的雌性群体。目前大多数针对双翅目害虫的遗传防治策略没有进行性别分离,少数害虫性别分离方法是基于蛹的大小或者雌雄蛹羽化时间差异进行人工识别和机械识别分离。双翅目昆虫性别决定及分化分子机制多种多样,其性别决定主要信号差异巨大,其多种性别决定基因已用于性别分离系统的开发。性比失衡性别分离策略通过破坏性别决定途径关键基因的表达获得雄性偏向后代,雌性条件性致死分离策略利用性别决定关键基因的雌雄选择性剪接差异实现性别分离,这两种性别分离策略目前正在害虫不育防治中接受大规模饲养应用评估,而基于双翅目昆虫雌雄性二态和基因标记发展的可视化性别分离策略也已成功实现多种害虫的性别分离。我们对性比失衡分离策略、雌性条件性致死分离策略和可视化性别分离策略在双翅目害虫中的研究进展进行了综述,重点评估了这些方法在雄虫大规模饲养和释放的应用潜力,以期在更完善的性别分离技术支持下为害虫防治研究取得更多突破性进展。     

Novel strategies targeting pathogen transmission reduction in insect vectors: Tsetse-transmitted trypanosomiasis control

Insect vectors are essential for the transmission of important human diseases such as malaria, leishmaniasis, Chagas and sleeping sickness. Insects are also responsible for the transmission of agricultural diseases that affect livestock and crops. Traditionally, control of the vector populations has been an effective disease management strategy. Recently, vector control strategies have been fortified by research in insect biology and in insect–pathogen interactions as well as by the development of transgenic technologies. In addition to insect population reduction methods, disease control via selective elimination of pathogens in insects can now be explored. Here we explore the tsetse vectors of African trypanosomes and describe the application of recent knowledge gained in their symbiotic, reproductive and vectorial biology to develop novel disease control strategies.     

Feasibility,limitation and possible solutions of RNAi‐based technology for insect pest control

Abstract Numerous studies indicate that target gene silencing by RNA interference (RNAi) could lead to insect death. This phenomenon has been considered as a potential strategy for insect pest control, and it is termed RNAi‐mediated crop protection. However, there are many limitations using RNAi‐based technology for pest control, with the effectiveness target gene selection and reliable double‐strand RNA (dsRNA) delivery being two of the major challenges. With respect to target gene selection, at present, the use of homologous genes and genome‐scale high‐throughput screening are the main strategies adopted by researchers. Once the target gene is identified, dsRNA can be delivered by micro‐injection or by feeding as a dietary component. However, micro‐injection, which is the most common method, can only be used in laboratory experiments. Expression of dsRNAs directed against insect genes in transgenic plants and spraying dsRNA reagents have been shown to induce RNAi effects on target insects. Hence, RNAi‐mediated crop protection has been considered as a potential new‐generation technology for pest control, or as a complementary method of existing pest control strategies; however, further development to improve the efficacy of protection and range of species affected is necessary. In this review, we have summarized current research on RNAi‐based technology for pest insect management. Current progress has proven that RNAi technology has the potential to be a tool for designing a new generation of insect control measures. To accelerate its practical application in crop protection, further study on dsRNA uptake mechanisms based on the knowledge of insect physiology and biochemistry is needed.     

昆虫种群的遗传调控

昆虫种群的遗传调控是利用昆虫自身生长发育的关键基因,采用性别控制开关,通过遗传转化使雄虫成为携带导致后代雌虫发育异常或雌性不育的遗传控制复合体（性别开关元件和靶标基因的复合体）．昆虫种群遗传调控是一种基于不育技术的昆虫种群控制系统,具有种类特异、环境友好和便捷高效等特点．目前为止,已经由早期的通过辐射不育方法发展到释放携带显性致死基因昆虫的方法,并在多种昆虫中获得成功．本文综述了昆虫种群遗传调控的发展历程,介绍了昆虫种群遗传调控相关的理论与方法,包括特异的调控元件、致死或缺陷基因和遗传转化体系的应用,并列举了几种昆虫种群遗传调控的实例,最后对于昆虫种群遗传调控系统中存在的问题以及可能的发展方向进行了展望．     

Patterns of virulence and benevolence in insect‐borne pathogens of plants

Direct and indirect interactions between insect‐borne pathogens and their host plants are reviewed in the context of theoretical analyses of the evolution of virulence. Unlike earlier theories, which maintained that parasites should evolve to be harmless or even beneficial to their hosts, recent models predict that coevolution between pathogen and host may lead to virulence or avirulence, depending on the pathogen transmission system. The studies reviewed here support the hypothesis that virulence can be advantageous for insect‐borne pathogens of plants. Virulent pathogens may be transmitted more readily by vector insects and are likely to induce stronger disease symptoms, thereby potentially making the plant more attractive to vectors. In contrast, the transmission advantage of virulence for seed‐transmitted pathogens is lower and the costs of virulence are high. Pathogens may sometimes benefit plants via indirect interactions that arise through relationships with other organisms. Evidence for the effects of insect‐borne pathogens on plant competition, herbivory, and parasitism also is reviewed, but few studies have measured the outcome of both direct and indirect interactions. Benefits of pathogen infection that accrue to plants from indirect interactions may sometimes outweigh the direct detrimental effects of virulence.     

A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore

Host plant chemical composition critically shapes the performance of insect herbivores feeding on them. Some insects have become specialized on plant secondary metabolites, and even use them to their own advantage such as defense against predators. However, infection by plant pathogens can seriously alter the interaction between herbivores and their host plants. We tested whether the effects of the plant secondary metabolites, iridoid glycosides (IGs), on the performance and immune response of an insect herbivore are modulated by a plant pathogen. We used the IG‐specialized Glanville fritillary butterfly Melitaea cinxia, its host plant Plantago lanceolata, and the naturally occurring plant pathogen, powdery mildew Podosphaera plantaginis, as model system. Pre‐diapause larvae were fed on P. lanceolata host plants selected to contain either high or low IGs, in the presence or absence of powdery mildew. Larval performance was measured by growth rate, survival until diapause, and by investment in immunity. We assessed immunity after a bacterial challenge in terms of phenoloxidase (PO) activity and the expression of seven pre‐selected insect immune genes (qPCR). We found that the beneficial effects of constitutive leaf IGs, that improved larval growth, were significantly reduced by mildew infection. Moreover, mildew presence downregulated one component of larval immune response (PO activity), suggesting a physiological cost of investment in immunity under suboptimal conditions. Yet, feeding on mildew‐infected leaves caused an upregulation of two immune genes, lysozyme and prophenoloxidase. Our findings indicate that a plant pathogen can significantly modulate the effects of secondary metabolites on the growth of an insect herbivore. Furthermore, we show that a plant pathogen can induce contrasting effects on insect immune function. We suspect that the activation of the immune system toward a plant pathogen infection may be maladaptive, but the actual infectivity on the larvae should be tested.     

Protease inhibitors:recent advancement in its usage as a potential biocontrol agent for insect pest management

Plant derived protease inhibitors(PIs)are a promising defensin for crop im-provement and insect pest management.Although agronomist made significant efforts in utilizing PIs for managing insect pests.the potentials of PIs are still obscured.Insect ability to compensate nutrient starvation induced by dietary PI feeding using different strategies,that is,overexpression of PI-sensitive protease,expression of PI-insensitive proteases,degradation of PI,has made this innumerable collection of PIs worthless.A practical challenge for agronomist is to identify potent PI candidates,to limit insect compensatory responses and to elucidate insect compensatory and resistance mechanisms activated upon herbivory.This knowledge could be further efficiently utilized to identify potential targets for RNAi-mediated pest control.These vital genes of insects could be functionally anno-tated using the advanced gene-editing technique,CRISPR/Cas9.Contemporary research is exploiting different in silico and modern molecular biology techniques to utilize PIs in controlling insect pests efficiently.This review is structured to update recent advancements in this field,along with is chronological background.     

Genetic elimination of field-cage populations of Mediterranean fruit flies

The Mediterranean fruit fly (medfly, Ceratitis capitata Wiedemann) is a pest of over 300 fruits, vegetables and nuts. The sterile insect technique (SIT) is a control measure used to reduce the reproductive potential of populations through the mass release of sterilized male insects that mate with wild females. However, SIT flies can display poor field performance, due to the effects of mass-rearing and of the irradiation process used for sterilization. The development of female-lethal RIDL (release of insects carrying a dominant lethal) strains for medfly can overcome many of the problems of SIT associated with irradiation. Here, we present life-history characterizations for two medfly RIDL strains, OX3864A and OX3647Q. Our results show (i) full functionality of RIDL, (ii) equivalency of RIDL and wild-type strains for life-history characteristics, and (iii) a high level of sexual competitiveness against both wild-type and wild-derived males. We also present the first proof-of-principle experiment on the use of RIDL to eliminate medfly populations. Weekly releases of OX3864A males into stable populations of wild-type medfly caused a successive decline in numbers, leading to eradication. The results show that genetic control can provide an effective alternative to SIT for the control of pest insects.     

Use of habitat odour by host‐seeking insects

Locating suitable feeding or oviposition sites is essential for insect survival. Understanding how insects achieve this is crucial, not only for understanding the ecology and evolution of insect–host interactions, but also for the development of sustainable pest‐control strategies that exploit insects' host‐seeking behaviours. Volatile chemical cues are used by foraging insects to locate and recognise potential hosts but in nature these resources usually are patchily distributed, making chance encounters with host odour plumes rare over distances greater than tens of metres. The majority of studies on insect host‐seeking have focussed on short‐range orientation to easily detectable cues and it is only recently that we have begun to understand how insects overcome this challenge. Recent advances show that insects from a wide range of feeding guilds make use of ‘habitat cues’, volatile chemical cues released over a relatively large area that indicate a locale where more specific host cues are most likely to be found. Habitat cues differ from host cues in that they tend to be released in larger quantities, are more easily detectable over longer distances, and may lack specificity, yet provide an effective way for insects to maximise their chances of subsequently encountering specific host cues. This review brings together recent advances in this area, discussing key examples and similarities in strategies used by haematophagous insects, soil‐dwelling insects and insects that forage around plants. We also propose and provide evidence for a new theory that general and non‐host plant volatiles can be used by foraging herbivores to locate patches of vegetation at a distance in the absence of more specific host cues, explaining some of the many discrepancies between laboratory and field trials that attempt to make use of plant‐derived repellents for controlling insect pests.     

Multiple guests in a single host: interactions across symbiotic and phytopathogenic bacteria in phloem‐feeding vectors – a review

Some pathogenic phloem‐limited bacteria are a major threat for worldwide agriculture due to the heavy economic losses caused to many high‐value crops. These disease agents – phytoplasmas, spiroplasmas, liberibacters, and Arsenophonus‐like bacteria – are transmitted from plant to plant by phloem‐feeding Hemiptera vectors. The associations established among pathogens and vectors result in a complex network of interactions involving also the whole microbial community harboured by the insect host. Interactions among bacteria may be beneficial, competitive, or detrimental for the involved microorganisms, and can dramatically affect the insect vector competence and consequently the spread of diseases. Interference is observed among pathogen strains competing to invade the same vector specimen, causing selective acquisition or transmission. Insect bacterial endosymbionts are another pivotal element of interactions between vectors and phytopathogens, because of their central role in insect life cycles. Some symbionts, either obligate or facultative, were shown to have antagonistic effects on the colonization by plant pathogens, by producing antimicrobial substances, by stimulating the production of antimicrobial substances by insects, or by competing for host infection. In other cases, the mutual exclusion between symbiont and pathogen suggests a possible detrimental influence on phytopathogens displayed by symbiotic bacteria; conversely, examples of microbes enhancing pathogen load are available as well. Whether and how bacterial exchanges occurring in vectors affect the relationship between insects, plants, and phytopathogens is still unresolved, leaving room for many open questions concerning the significance of particular traits of these multitrophic interactions. Such complex interplays may have a serious impact on pathogen spread and control, potentially driving new strategies for the containment of important diseases.     

遗传不育技术在蚊媒疾病防控中的应用

疟疾、登革热等重大传染性蚊媒疾病严重危害人类健康,且目前缺乏有效的药物和疫苗,防治埃及伊蚊、冈比亚按蚊等媒介昆虫是控制和消除这些疾病的有效手段。化学杀虫剂的大规模使用在一定程度上控制了疾病的传播,但其抗药性和环境污染等问题也随之而来。分子生物学的飞速发展为昆虫不育技术(SIT)的更新及害虫防治提供了新的策略,由此发展起来的以释放携带显性致死基因昆虫(RIDL)为代表的一系列遗传不育技术为蚊虫种群防控提供了更加有效的选择。本文概述了遗传技术在蚊虫防控中的应用进展,包括蚊虫遗传防治的历史和策略,阐述了RIDL技术体系的原理,同时介绍了相关遗传控制品系和已经开展的田间释放研究,展示了遗传修饰不育技术在蚊媒疾病防治中的巨大潜力。     

Insect declines and agroecosystems: does light pollution matter?

Drastic declines in insect populations, ‘Ecological Armageddon’, have recently gained increased attention in the scientific community, and are commonly considered to be the consequence of large‐scale factors such as land‐use changes, use of pesticides, climate change and habitat fragmentation. Artificial light at night (ALAN), a pervasive global change that strongly impacts insects, remains, however, infrequently recognised as a potential contributor to the observed declines. Here, we provide a summary of recent evidence of impacts of ALAN on insects and discuss how these impacts can drive declines in insect populations in light‐polluted areas. ALAN can increase overall environmental pressure on insect populations, and this is particularly important in agroecosystems where insect communities provide important ecosystem services (such as natural pest control, pollination, conservation of soil structure and fertility and nutrient cycling), and are already under considerable environmental pressure. We discuss how changes in insect populations driven by ALAN and ALAN itself may hinder these services to influence crop production and biodiversity in agricultural landscapes. Understanding the contribution of ALAN and other factors to the decline of insects is an important step towards mitigation and the recovery of the insect fauna in our landscapes. In future studies, the role of increased nocturnal illumination also needs to be examined as a possible causal factor of insect declines in the ongoing ‘Ecological Armageddon’, along with the more commonly examined factors. Given the large scale of agricultural land use and the potential of ALAN to indirectly and directly impact crop production and biodiversity, a better understanding of effects of ALAN in agroecosystems is urgently needed.     

Perception of insect feeding by plants

The recognition of phytophagous insects by plants induces a set of very specific responses aimed at deterring tissue consumption and reprogramming metabolism and development of the plant to tolerate the herbivore. The recognition of insects by plants requires the plant’s ability to perceive chemical cues generated by the insects and to distinguish a particular pattern of tissue disruption. Relatively little is known about the molecular basis of insect perception by plants and the signalling mechanisms directly associated with this perception. Importantly, the insect feeding behaviour (piercing‐sucking versus chewing) is a decisive determinant of the plant’s defence response, and the mechanisms used to perceive insects from different feeding guilds may be distinct. During insect feeding, components of the saliva of chewing or piercing‐sucking insects come into contact with plant cells, and elicitors or effectors present in this insect‐derived fluid are perceived by plant cells to initiate the activation of specific signalling cascades. Although receptor–ligand interactions controlling insect perception have yet not been molecularly described, a significant number of regulatory components acting downstream of receptors and involved in the activation of defence responses against insects has been reported. Some of these regulators mediate changes in the phytohormone network, while others directly control gene expression or the redox state of the cell. These processes are central in the orchestration of plant defence responses against insects.     

昆虫抗药性分子机制研究的新进展

昆虫抗性机制的研究对于抗性监测、治理及新农药的研制具有重要意义。在过去几十年中,人们对与昆虫杀虫剂抗性有关的昆虫行为、生理代谢活动以及作用靶标等进行了广泛的研究。已经证实,昆虫的抗药性与行为改变、生理功能改变、解毒功能增强以及靶标不敏感性有关。近年来,随着分子生物学以及昆虫基因组学的发展,昆虫抗药性的分子机理有了突破性进展,已发现并克隆了一些靶标基因,与抗药性相关的基因突变也得到广泛验证。本文综述了昆虫的抗药性机理在分子生物学上的研究最新进展,重点阐述了与昆虫抗性相关基因的扩增、表达及基因结构的改变等相关内容。     

Precocious Mexican fruit fly methoprene‐fed males inhibit female receptivity and perform sexually as mature males

The sterile insect technique (SIT) has been used successfully for the control of fruit flies. The efficiency of this technique can be significantly reduced when sterile released insects are exposed to adverse conditions and predators, as a great number of sterile insects die before reaching sexual maturity and thus fail to mate with wild females. Treatments with juvenile hormone (JH) analogues such as methoprene (M) significantly reduce the time to reach sexual maturity by sterile Anastrepha ludens (Loew) (Diptera: Tephritidae) males. In this study, we compared the sexual performance of non‐treated sexually mature males with young males that had been sexually accelerated with M. Furthermore, we compared the ability of M‐fed males in inhibiting female remating compared with sexually mature males. Results showed that at 5 days M‐fed males had lower mating success than mature males; however, 6‐day‐old (0.1%) M‐fed males had the same amount of matings as mature 13‐day‐old males. Young 5‐ to 10‐day‐old M‐fed males also had similar number of matings as mature non‐treated 12‐ to 17‐day‐old males. There were no differences in copula duration between treatments. Moreover, there were no differences between the fertility, fecundity or refractory period of females mated with either young male fed M or normal sexually mature males. These results indicated that young males that were sexually accelerated with M have the same sexual performance as non‐treated sexually mature males. Implications of using M as a pre‐release treatment for A. ludens controlled through SIT are discussed.     

Evaluation of partial sterility in mating performance and reproduction of the West Indian sweetpotato weevil,Euscepes postfasciatus

The sterile insect technique (SIT) is based on population and behavioral ecology and is widely used to suppress or eradicate target pest insect populations. The effectiveness of SIT depends on the ability of the released sterile males to mate with and inseminate wild females. The use of gamma‐radiation to induce sterility is, however, associated with negative impacts not only on reproductive cells but also on somatic cells. Consequently, irradiation for sterilization diminishes mating performance over time. In this study, we evaluated the balance between the irradiation dose and both fertility and mating propensity in Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae) for 22 days following irradiation. The mating propensity of males irradiated with a 150‐Gy dose, as currently used to induce complete sterility of E. postfasciatus in the SIT program in Okinawa Prefecture, was equal to that of non‐irradiated weevils for up to 6 days, and the mating propensity of males irradiated with a dose of 125 Gy was equal to that of non‐irradiated weevils for twice this period (12 days). The fertilization ability of weevils irradiated with a dose of 125 Gy was reduced by 4.6% in males and 0.6% in females, compared to the potential fertilization ability. We also discuss the possibility of the application of partially sterilized insects in eradication programs.     

论我国昆虫多样性的保护与利用

本文论述了保护昆虫多样性的意义、我国昆虫多样性的基本特点及面临的问题、昆虫多样性的保护战略和利用对策。文中强调指出,昆虫是生物界的一个主要类群,在我国,需要防治的害虫大约只占全部昆虫种类数的1%,其余种类对人类都是有益或者是中性的,它们不仅可以作为显花植物的传粉者、为人类提供食物和各种工业原料,而且可以作为许多害虫或杂草的天敌,以及用于环境净化和科学研究。我国由于地域辽阔,生境复杂,因此,昆虫种类极为丰富,珍稀物种及有益昆虫较多。然而,由于受到人类活动的干扰,我国昆虫多样性面临着生境遭到破坏,物种濒于灭绝,天敌大量减少等问题。为了有效地保护和利用我国的昆虫资源,作者提出了一些战略和对策。     

Swarming and mating activity of Anopheles gambiae mosquitoes in semi‐field enclosures

Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) is the major Afro‐tropical vector of malaria. Novel strategies proposed for the elimination and eradication of this mosquito vector are based on the use of genetic approaches, such as the sterile insect technique (SIT). These approaches rely on the ability of released males to mate with wild females, and depend on the application of effective protocols to assess the swarming and mating behaviours of laboratory‐reared insects prior to their release. The present study evaluated whether large semi‐field enclosures can be utilized to study the ability of males from a laboratory colony to respond to natural environmental stimuli and initiate normal mating behaviour. Laboratory‐reared males exhibited spatiotemporally consistent swarming behaviour within the study enclosures. Swarm initiation, peak and termination time closely tracked sunset. Comparable insemination rates were observed in females captured in copula in the semi‐field cages relative to females in small laboratory cages. Oviposition rates after blood feeding were also similar to those observed in laboratory settings. The data suggest that outdoor enclosures are suitable for studying swarming and mating in laboratory‐bred males in field‐like settings, providing an important reference for future studies aimed at assessing the comparative mating ability of strains for SIT and other vector control strategies.