Aphid Management in Crop Systems: Current Strategies and Future Perspectives

Abstract

Aphids are major agricultural pests worldwide, causing crop damage both through direct piercing-sucking feeding and the transmission of plant viruses. Their multistage life cycle, unique developmental physiology, plasticity in developing pesticide resistance, and multifaceted interactions with host plants and bacterial endosymbionts make effective control particularly challenging. In this review, we summarize the current toolbox available for aphid control across major crop systems, including chemical pesticides, biological agents, plant resistance, cultural practices, biorational control, and emerging strategies such as RNA interference (RNAi) and symbiosis-targeted approaches. Rather than providing an exhaustive survey of the literature, we draw on conceptual and illustrative studies to critically evaluate the strengths and limitations of each control strategy. Finally, we outline future directions for aphid control, highlighting the potential of modern technologies, such as artificial intelligence (AI), synthetic biology, data-driven analytics, and CRISPR-based genome editing, to expand and improve existing control options.

1. Introduction

1.1. Agricultural Significance of Aphids

Aphids are among the most damaging insect pests, causing significant yield loss for agricultural and economic crops annually across the world [1]. Aphids damage plants through direct feeding, indirect plant virus transmission, and fungal pathogen promotion. Direct feeding by aphids on plant phloem sap can reduce plant growth and cause mottled and curled leaves, yellowing and browning, wilting, low yields, and ultimately death [2,3]. Heavily infested young plant seedlings may die, and mature plants may fail to blossom and develop abnormal fruits, such as twisted pods and impaired seed development in legumes [4]. Beyond feeding, aphids can rapidly proliferate to cover leaf surfaces and exude honeydew, which covers plant stomatal openings and promotes black sooty mold growth on the leaf surface, therefore blocking photosynthesis, transpiration, and respiration [5]. Furthermore, honeydew accumulation can reduce fungicide efficacy by obstructing chemical absorption [1]. More severely, aphids are efficient vectors of numerous plant viruses, causing significant damage to various crops [6,7,8,9]. The green peach aphid, Myzus persicae, alone can transmit over 100 different plant viruses [10].

1.2. Why Aphid Control Remains Problematic?

Aphids represent one of the most challenging groups of agricultural pests due to their unique biology, ecology, and interactions with plants, microbes, and viruses. Several key traits contribute to their persistence and difficulty in control.

Rapid Reproduction Through Parthenogenesis and Telescoping Development: Parthenogenesis through telescoping development allows aphids to reproduce rapidly and expand their populations. Parthenogenesis, asexual reproduction without mating that produces live nymphs, and telescoping development, where developing embryos already contain the next generation, enable exponential population growth within a very short period [11,12]. With parthenogenesis and telescoping development, each adult aphid can produce hundreds of offspring during the growing season.

Ecological Versatility and Broad Host Range: Aphids exploit nearly every part of their host plants, from leaves and stems to flowers and roots [13,14,15]. Many species are polyphagous, feeding on a wide array of plant species and adapting to diverse environments. This broad host range not only enhances their survival but also increases their efficiency as vectors of plant viruses [16,17].

Pronounced Phenotypic Plasticity: Aphids exhibit striking phenotypic plasticity. When environmental conditions become unfavorable, they produce winged morphs capable of long-distance dispersal, facilitating colonization of new hosts and habitats [18]. Some species also display variation in body color, which may influence their ecological interactions with natural enemies, consequently their mortality [19]. It has been shown that, in the pea aphid Acyrthosiphon pisum, the predator ladybird beetle Coccinella septempunctata preys more red morphs than green ones, whereas the parasitoid wasp Aphidius ervi preferentially oviposits into green rather than red morphs [20,21].

Genetic Plasticity and Metabolic Adaptability: In addition to phenotypic plasticity, aphids display extensive plasticity at the genetic level, e.g., gene duplication. These duplications can buffer against the loss of RNA interference (RNAi) efficacy or pesticide target-sites sensitivity [22,23], and allow overproduction of detoxification enzymes such as cytochrome P450s, esterases (E4 and FE4), and others, thereby enhancing their resilience against chemical control strategies [23,24].

Intimate Associations with Bacterial Endosymbionts: Aphids are tightly linked with bacterial endosymbionts, including both primary (obligate) and secondary (facultative) symbionts, that shape their survival and adaptability. The obligate bacterial endosymbiont, Buchnera aphidicola (Proteobacteria: Gammaproteobacteria: Enterobacteriaceae), supplies essential amino acids and vitamins absent from plant sap to host aphids [25]. In addition, facultative symbionts, commonly inherited vertically but occasionally horizontally, confer diverse benefits, including protection against natural enemies and fungal pathogens, tolerance of extreme temperatures, and expanded host range [26,27]. Specific symbiont infections or coinfections can alter aphid body color, which provides significant ecological and evolutionary implications. For example, the facultative endosymbiont Rickettsiella viridis has been shown to change aphid body color from red to green by increasing the production of blue-green polycyclic quinones [28], and this color shift can be influenced by coinfection with another symbiont, Hamiltonella defensa [29].

Highly Efficient Transmission of Plant Viruses: Aphids are the most important vectors of plant viruses worldwide. The success of virus transmission is facilitated by several key adaptations in aphids. Their needlelike stylets enable piercing-sucking of plant phloem sap, facilitating efficient acquisition of virus [30]. Some plant viruses can promote aphid wing formation through various mechanisms [31], including direct interference with aphid wing plasticity pathways (e.g., Cucumber mosaic virus and its satellite virus in M. persicae) [32] or alteration of the host plant quality that increases aphid density (e.g., Pea enation mosaic virus in A. pisum) [33]. The wing induction promotes aphid migration for colonizing new hosts, meanwhile increasing aphid efficiencies in dispersing viruses over long distance [31]. Moreover, some transmitted viruses compromise plant defenses, creating conditions that favor further aphid colonization and feeding [34]. For example, the Cucumber mosaic virus 2b can inhibit host plant jasmonic acid biosynthetic pathways, leading to improved performance of M. persicae [35].

Extensive and Widespread Insecticide Resistance: Aphids are among the most resistant insects to pesticides. The widespread and repeated use of insecticides has selected for resistant aphid populations across multiple continents. Insecticide resistance has been reported in different aphid species against major chemical insecticide groups, including pyrethroids, neonicotinoids, butenolides, organophosphates, and carbamates, across diverse agricultural systems [36,37]. For instance, pyrethroid resistance has emerged in the soybean aphid Aphis glycines in North America, while resistance to flupyradifurone and neonicotinoids has been documented in M. persicae across Europe, the United States, and Asia. Similarly, resistance to organophosphates and carbamates has been reported in cereal aphids such as Rhopalosiphum padi in China [38,39,40,41]. This chemical resistance further complicates aphid management and highlights the limitations of relying solely on chemical insecticides for aphid control.

2. Current Control Strategies and Challenges

Current management of aphid infestations in field or greenhouse relies on an integrated approach that includes, but is not limited to, synthetic chemical pesticides, biological agents, plant resistance, cultural practices, biorational compounds, and RNAi. While each of these strategies contributes to reducing aphid populations, significant challenges and limitations remain.

2.1. Synthetic Chemical Control

Chemical pesticides remain the most widely used strategy due to their rapid action and effectiveness. Broad-spectrum synthetic pesticides, including fast-acting contact neurotoxins, pyrethroids, and acetylcholinesterase inhibitors (carbamates and organophosphates), as well as systemically acting compounds such as neonicotinoids and butenolides, have historically provided effective control of aphid populations by causing high mortality [42,43,44]. Despite efforts to develop more selective and less persistent insecticides, broad-spectrum pesticides are still heavily relied upon in agriculture. However, this continued reliance on chemical pesticides masks substantial and increasingly evident limitations in their field performance and long-term sustainability.

First, the effectiveness of chemical pesticides is highly context-dependent, varying substantially among aphid species and cropping systems. For example, imidacloprid effectively reduced survival and fecundity in Sitobion avenae, R. padi, and Schizaphis graminum, but showed little effect against Metopolophium dirhodum [45]. Similarly, while acetamiprid reduced Myzus mumecola populations on apricot trees by 98.7%, other tested insecticides were largely ineffective [43]. Laboratory studies also demonstrated that flonicamid significantly decreased longevity and fecundity in cotton aphids, Aphis gossypii, and that these effects persisted into the next generation [46].

More importantly, the overuse and repeated application of these synthetic chemicals have imposed strong selection pressures on aphid populations, leading to widespread increased resistance across almost all major insecticide modes of action (MoA) [47]. Aphids can develop resistance to pesticides through various mechanisms, including target-site insensitivity, increased detoxification enzymes, and resistance-associated genes [37]. For example, a long-term study in Minnesota in the United States found that soybean aphids A. glycines gradually developed resistance to lambda-cyhalothrin, while remaining susceptible to chlorpyrifos [48]. Likewise, M. persicae from peach orchards showed high levels of resistance to omethoate, abamectin, and pyrethroids; and increased resistance has been associated with enhanced metabolic detoxification mechanisms through cytochrome P450 activities [49]. Importantly, resistance can be reversible when pesticide selection pressure is removed. For example, M. persicae populations regained susceptibility to imidacloprid and sulfoxaflor after at least one year without exposure [49]. However, these reversions are highly dependent on the pesticides’ MoA and may not occur universally.

Beyond resistance, chemical pesticides pose risks to non-target organisms and broader ecosystems. For example, in soybean fields, sulfoxaflor and lambda-cyhalothrin provided similar levels of control efficacy against A. glycines, but sulfoxaflor was less disruptive to beneficial insects, such as lady beetles [50]. Application methods also influence both pesticide efficacy and their ecological impact on non-targeted organisms. While most chemical pesticides were applied through foliar spray, seed treatment with imidacloprid has been shown to be more effective against wheat aphids [45]. In addition, sulfoxaflor applied through drip irrigation provided cost-effective and long-lasting control of A. gossypii, while reducing toxicity to predators compared to foliar spray [51].

Efforts have been made to increase chemical pesticide efficiency and avoid resistance development in aphids. The first approach is to rotate or combine different MoA pesticides. Field trials in Ethiopia demonstrated that dimethoate, imidacloprid, and lambda-cyhalothrin, applied in combination, can effectively reduce wheat aphid populations [52]. Pesticide rotation in the order of carbosulfan, diafenthiuron, furathiocarb, and deltamethrin has been shown to be more effective in controlling A. gossypii compared to sole or mixture applications of insecticides [53]. Even simply cessation of pesticide use may restore pest susceptibility in some cases, but the time required varies by species and compound [49,54]. Second, it is essential to continuously develop novel compounds, including plant-derived natural products, with new MoAs. For instance, recent evaluations of new insecticides against A. gossypii on Bt cotton showed high efficacy for clothianidin, diafenthiuron, and thiamethoxam (>88% reduction), while lambda-cyhalothrin was comparatively ineffective [55]. Similarly, Tabet et al. (2023) reported success with acetamiprid in apricot orchards, while Jiang et al. (2019) demonstrated prolonged aphid control using sulfoxaflor through drip irrigation [43,51]. However, the pace of pesticide development must keep ahead of the rapid resistance development in aphids, such as high levels of imidacloprid resistance, which has already been observed in M. persicae in cabbage fields in China [49]. To ensure our advantages over aphid resistance, more efforts are needed to deeply understand the mechanisms of resistance development. Advances in molecular biology provide opportunities to identify resistance mechanisms and design more targeted interventions. For example, M. persicae nicotianae has adapted to tobacco’s nicotine through large-scale genome duplications, transposable element insertions, serial mutations, and regulatory changes [56]. Such insights may inform the development of inhibitors, RNAi approaches, or synergists that suppress resistance pathways and restore pesticide efficacy.

2.2. Biological Control

In addition to chemical control, biological control strategies have been widely applied in aphid management, including microbial biopesticides (like entomopathogenic fungi) [57], predators [58,59,60], and parasitoids [61,62]. These agents provide environmentally friendly alternatives that can reduce dependence on synthetic insecticides. Based on how agents are sourced and managed, biological control can be classified into three categories: classical (introduction and long-term establishment of exotic agents), augmentative (periodic release of mass-reared agents), and conservation (enhancement of existing natural enemies).

Classical Biological Control: The classical approach introduces exotic natural enemies against aphids with the goal of long-term establishment and sustained population suppression. An iconic example is the parasitoid Aphelinus mali, which was introduced sequentially across multiple regions to control the invasive woolly apple aphid Eriosoma lanigerum. Although widely established, its effectiveness varied among regions [63]. Similarly, the introduction of Aphidius spp. and other parasitoids targeting cereal aphids in South America led to the establishment and near-complete biological control of S. avenae and M. dirhodum within approximately a decade [64]. In another classical program, the entomopathogenic fungus Neozygites fresenii was introduced to control the cotton aphid A. gossypii in California, where it initiated epizootics and persisted within aphid populations, suggesting strong potential for long-term suppression [65].

Augmentative Biological Control: Many predatory species are commercially available for aphid management. These include dipterans such as European species of hoverflies, Eupeodes corollae and Sphaerophoria rueppellii [66,67], neuropterans such as lacewings, Micromus angulatus, Chrysoperla agilis, and Chrysoperla mutata [59,68], and coccinellidae lady beetles, such as C. septempunctata [60,69,70]. These predators are typically generalists capable of attacking multiple aphid species across different cropping systems, with demonstrated effectiveness under both greenhouse and field conditions. For example, E. corollae larvae actively prey on aphid pests, and the release of E. corollae in greenhouses significantly reduced A. gossypii populations on tomato, melon, and strawberry crops [71].

Parasitoid wasps also play a crucial role in aphid management by reducing their reproduction and population growth. Commercially available species include A. ervi (Hemiptera: Braconidae), which is highly effective against the pea aphid A. pisum under laboratory conditions [72] and Aphelinus spp. for the control of tea aphid Toxoptera aurantii under both laboratory and field conditions [73]. Other parasitoid wasps, such as Aphidius matricariae, Praon gallicum, P. unicum, P. humulaphidis, Ephedrus californicus, Diaeretiella rapae, and Monoctonus paulensis, also contribute significantly to natural aphid population control under greenhouse and field settings [74].

Fungal pathogens, the most studied microbial biopesticides, infect and control aphids through direct cuticle penetration and internal proliferation. Several species have been commercialized, including Lecanicillium spp., Beauveria bassiana, Isaria fumosorosea, and Metarhizium anisopliae. The entomopathogenic fungus Lecanicillium lecanii strain 41185 can achieve nearly 100% mortality in M. persicae and A. gossypii under optimal conditions [75,76]. Field trials of a newly emerging fungus, Verticillium lecanii, against M. persicae can achieve 52.17% mortality by 10 days after spraying [77]. In addition to fungal pathogens, bacterial biopesticides have also been developed for aphid control. For example, several strains of epiphytic bacterium Pseudomonas syringae have been shown under laboratory conditions to cause mortality in multiple aphid species, including A. pisum, M. persicae, A. gossypii, A. rumicis, and R. padi [78]. Many viruses can also infect and kill aphids, including M. persicae densovirus (MpDV), A. pisum virus (APV), A. glycine virus (ApGlV), and Aphid lethal paralysis virus (ALPV) [79]. For instance, a high incidence of ALPV has been associated with a dramatic decline in R. padi populations in wheat fields [80]. Beyond the use of intact microorganisms as biopesticides, bioactive compounds derived from those agents can also be developed as biorational pesticides for aphid control (See more details under Section 2.5).

Despite their environmental benefits, both classical and augmentative biological controls are far from universally effective. Their performance can be constrained by environmental conditions (e.g., humidity and temperature), challenges in mass production of predators or parasitoids, and difficulties in maintaining biological quality during large-scale rearing, and limited post-release establishment of the natural enemies, which reduces long-term sustainability [81]. These challenges limit the broader adoption of biological control in commercial agriculture. Even when agent–aphid associations occur and persist, unintended ecological consequences may arise, such as impacts on non-target organisms, genetic interactions with local populations, or interference with existing natural enemy communities through competition or intraguild predation [82].

Conservation Biological Control: Modern technologies, such as the CRISPR/Cas9 genome editing system, offer promising tools to modify host plant traits to better support aphid colonies, either for industrial-scale mass production of biological agents or as “banker plants” for sustaining predators and parasitoids in the field. For example, a CRISPR-edited Nicotiana benthamiana mutant line lacking Acyl-sugar acyl-transferase 2 (ASAT2) can significantly attract and promote M. persicae population in the laboratory [83] and have been shown to be effective in attracting aphids and predators in the natural setting [84]. Such plants could be used as a host for both mass-rearing and in-field sustainability of biological control agents.

In addition to improving the quality of the biological agents, a deeper understanding of species diversity and ecological interactions can further improve the effectiveness of their application. For example, the presence of the ant, Tapinoma ibericum, has been shown to significantly reduce the efficiency of natural enemies, including A. colemani, and the ladybird Scymnus sp. in greenhouse settings [85]. Similarly, ant activities can also reduce fungal infections on aphids, such as Pandora neoaphidis infection for milkweed aphid Aphis asclepiadis, by removing or grooming infected aphids [86].

Microbiota in the agro-ecosystem represent a valuable resource for identifying beneficial agents for aphid management. For example, the soil fungal root symbiont, Trichoderma harzianum (strain T22), has been shown to increase the attraction of the parasitoid A. ervi when it co-exists with aphid attack [87]. Other Trichoderma species, including Trichoderma harzianum and T. atroviride, have been used against the potato aphid M. euphorbiae [87,88]. When applied as seed treatments, these fungi can promote plant resistance by directly upregulating defense-related genes such as proteinase inhibitors, or genes involved in the production of volatile phenylpropanoids and terpenoids, which in turn trigger oriented flights of the parasitoid A. ervi toward Trichoderma-treated plants [87,88]. Harnessing beneficial microbes in the rhizosphere and phyllosphere could expand the toolkit for aphid biological control.

2.3. Plant Resistance for Aphid Control

Unlike other control strategies that rely on external inputs of chemicals, biological agents, or labor, exploiting intrinsic plant resistance offers a cost-effective and sustainable approach to aphid management. Plant resistance mechanisms include antibiosis (directly reducing aphid survival and reproduction), antixenosis (deterring aphids from feeding and colonizing), and tolerance (minimizing damage without directly affecting aphid performance). These mechanisms are regulated by a combination of physical, chemical, and genetic factors.

Plant physical defenses include trichomes (hairy, tough, or sticky), waxy leaf surfaces, and tough cell walls, which can prevent aphids from settling and feeding. In Sorghum bicolor, the sugarcane aphid Melanaphis sacchari preferentially colonizes and performs better on varieties lacking visible epicuticular wax [89]. Similarly, in peas, Pisum sativum, varieties with reduced surface wax significantly lower A. pisum populations compared to those with normal wax [90]. Structural components of the cell wall, such as lignin, pectin, and callose, also play a key role in aphid resistance [91]. Cotton cultivars with higher lignin content exhibit significantly greater resistance to aphids than susceptible cultivars [92].

Plant chemical defenses involve a wide range of secondary metabolites, including acylsugars, benzoxazinoids, and other compounds (See more details under Section 2.5). In N. benthamiana, disruption of acylsugar production significantly compromises resistance to M. persicae [83] and aphids prefer to colonize acylsugar-deficient plants under field conditions [84]. Similar acylsugar-mediated aphid resistance has been observed in other Solanaceae plants, including tomatoes, and against other pests, including thrips and whiteflies [93]. Benzoxazinoid biosynthesis has been extensively studied in wheat Triticum turgidum and in maize Zea mays, where it contributes to resistance against aphids such as S. avenae, R. padi, and S. graminum [94,95].

At the genetic level, plants deploy multiple resistance mechanisms against aphids, including R (resistance) genes, proteinase inhibitors, and pattern recognition receptors (PRRs), etc. Aphid feeding can trigger plant pattern-triggered immunity (PTI), which recruits a variety of PRRs to activate defense responses [96]. In addition to PTI, plants can activate effector-triggered immunity (ETI) through R genes that recognize aphid salivary effectors. Conventional R genes often encode nucleotide-binding leucine-rich repeat (NLR) proteins. Identified examples include Meu-1 in tomato, Vat in melon, Rag in soybean, RAP1 in Medicago, Gb3 in wheat, and Sl1 in Arabidopsis, which confer resistance to aphid species such as M. euphorbiae, A. gossypii, A. glycines, A. pisum, S. graminum, and M. persicae, respectively [97,98,99]. With advances in genomic and transcriptomic annotation, additional resistance genes beyond conventional R genes continue to be identified. For example, Dn genes in wheat confer resistance to the Russian wheat aphid, D. noxia, and are valuable targets for breeding programs [100]. Serine proteinase inhibitors identified in N. benthamiana contribute to resistance against M. persicae [101]. Furthermore, novel resistance genes have been reported in cowpea, Vigna unguiculata, against Aphis craccivora [102].

2.4. Cultural Control

Cultural control techniques are a fundamental component of Integrated Pest Management (IPM) programs and play a crucial role in sustainable aphid management. Popular practices include proper irrigation and fertilizer application, row spacing, seeding rates, manipulation of planting and harvest timing, intercropping or mixed cropping, tillage, crop rotation, and sanitation [103]. A growing body of research demonstrates that such approaches can significantly reduce aphid populations.

Intercropping is a widely studied strategy that provides multiple benefits—enhanced biodiversity, improved soil fertility, optimized resource use, and pest suppression—making it valuable for sustainable agriculture [104]. Depending on the crop system, intercropping can be implemented in various forms: row intercropping (e.g., cowpea/maize), strip intercropping (e.g., maize/beans, wheat/pea), relay intercropping (e.g., soybean/maize), mixed intercropping (e.g., grasses/legumes), and alternate intercropping [104]. Mixed intercropping of field beans with spring wheat or barley significantly reduced populations of the black bean aphid, A. fabae [105]. Pea/wheat mixtures lowered A. pisum densities compared to monocultures [106]. Similarly, cowpea/maize intercropping enhanced the efficacy of the biopesticide M. anisopliae (ICIPE62) against A. craccivora [107]. In addition to intercropping cash crops, cover crops and non-crop vegetation can also be integrated with target crops to enhance aphid control. In plum orchards, the use of oat as a cover crop has been shown to reduce plum aphid populations [108]. In pear orchards, inter-row ground covers with herbaceous non-cash plants significantly reduced aphid numbers, largely through supporting higher diversity and abundance of natural enemies [109]. Organic mulches have also been shown to be effective in reducing aphid populations. For example, triticale/vetch, grass/clover, grass silage, and straw mulch have been reported to significantly reduce aphid landing, thereby decreasing virus transmission in potato cultivation [110]. In addition to intercropping within crop rows, companion planting with aromatic herbs or flowering borders can function as “trap crops” or repellents, diverting aphids away from cash crops. For instance, planting rapeseed as a companion crop in sweet pepper fields significantly reduced M. persicae populations [111]. Furthermore, the establishment of native wildflower borders has been shown to promote the abundance and diversity of natural enemies by providing alternative prey as hosts or floral resources. In blueberry orchards, wildflower borders significantly reduced pest populations, including aphids [112], and similar effects have been consistently observed across diverse agricultural landscapes [113].

While these cultural systems have demonstrated effectiveness against aphids, their success depends on a nuanced understanding of crop diversity, habitat complexity, and within-field species interactions [114]. For example, the presence of whiteflies has been shown to reduce aphid predation by shared generalist predators in the field, suggesting that aphids and whiteflies may compete as prey for the same natural enemies [114]. Such interactions can create trade-offs in pest suppression when using generalist natural enemies. Moreover, although diversifying habitats may successfully attract beneficial insects, attraction does not necessarily translate into successful colonization or sustained control of target aphid populations [115].

To improve efficacy, cultural practices can be combined with other control strategies. For example, cultural practices can enhance the sustainability of biological control agents. Strip intercropping broccoli or lettuce with alyssum, Lobularia maritima, attracts natural enemies such as hoverflies for aphid suppression [115]. Manipulating nitrogen levels can also enhance plant defenses against aphids while improving yields. Moderate nitrogen application has been shown to promote plant growth while suppressing cotton aphid populations, whereas both excessive and insufficient nitrogen levels can favor aphid proliferation in Bt cotton fields [116]. Additionally, intercropping canola with nitrogen-fixing crops (e.g., faba bean or field pea) has been shown to suppress cabbage aphids, potentially due to enhanced nitrogen availability and its effects on plant defense and nutrition [117]. Theoretically, multi-crop intercropping systems could suppress multiple co-occurring pests simultaneously. For example, aphid and whitefly populations have been shown to negatively correlate with increased levels of crop diversity and habitat richness [114]. However, such systems must be balanced against practical challenges, including labor and harvest costs.

Push–pull strategies have also been developed in intercropping systems to enhance the effectiveness of cultural control. In these systems, aphids are repelled (“pushed”) from crops using deterrent cues while they are either attracted (“pulled”) away from crops or natural enemies are attracted (“pulled”) into the field. For example, volatiles from garlic (diallyl disulfide) or onion (propyl disulfide) have been shown to deter cotton aphids, while simultaneously increasing predator populations when these plants are intercropped in cotton fields [118]. Similar effects can be achieved by integrating the release of purified semiochemicals. In wheat-pea strip systems, applying E-β-farnesene (EBF, aphid alarm pheromone) or methyl salicylate (MeSA, a plant volatile) significantly increases the abundance of natural enemies like lady beetles, lacewings, and hoverflies. Meanwhile, this synergistic strategy enhances aphid suppression, reducing populations of R. padi, A. pisum, S. avenae, M. dirhodum, and S. graminum [119]. In addition, while EBF repels aphids, compounds such as (Z)-3-Hexenol can be used to attract species like M. dirhodum and S. avenae away from crop fields [120]. However, the broader application and effectiveness of push–pull strategies depend on the availability and optimization of suitable companion crops and semiochemicals, which can be further advanced through birational control approaches.

2.5. Biorational Control

As alternatives to conventional pesticides, biorational control strategies offer environmentally friendly and target-specific approaches to aphid management, primarily consisting of semiochemicals and chemical biopesticides. Semiochemicals, behavior-modifying compounds involved in communication between organisms, are most commonly discussed as alarm pheromones and plant-derived volatiles in the context of aphid control [121,122]. Chemical biopesticides, by contrast, are typically sourced from plants, microbes, or minerals and act directly on aphid physiology [123,124,125]. In aphid management, semiochemicals contribute to antixenosis resistance by deterring aphid feeding or host-seeking through volatile emissions, whereas chemical biopesticides are more closely associated with antibiosis resistance, acting as ingested toxins or metabolic inhibitors that reduce aphid survival, development, or reproduction [91].

Plant constitutive volatile emissions play multifaceted roles in plant–aphid interactions, functioning as chemical cues that influence insect behavior, ecological interactions, and defense outcomes. Constitutive volatiles can serve as orientation cues for aphids and support their host-location behavior [126]. Some are investigated as potential attractants for trap cropping or behavioral manipulation, while others, particularly those emitted from non-host plants, act as natural repellents, discouraging aphid settling [127,128]. In addition to such direct effects on aphids, floral volatiles derived from the phenylpropanoid pathway are also recognized for their role in indirect plant defense. These compounds can function as foraging cues for aphid natural enemies, such as parasitoids and predators, thereby enhancing biological control through natural enemy recruitment [129]. Furthermore, volatile compounds derived from plant essential oils, especially when present at saturating levels in the ambient air, can act as contact or fumigant toxins, exerting antibiosis effects that impair aphid survival, reproduction, or physiology [130,131,132].

In contrast to constitutive emissions, induced plant volatiles are dynamically produced in response to biotic stress and contribute to both direct and indirect defenses against aphids. One well-studied category is herbivore-induced plant volatiles (HIPVs), which are released in response to aphid feeding or probing and typically include green leaf volatiles (GLVs), terpenes, and other short-chain molecules. Specific HIPVs can function as prey- or host-associated cues for natural enemies of aphids, including predators and parasitoids, thereby enhancing indirect plant defense [133,134,135]. In addition, aphid stylet penetration and herbivory often activate salicylic acid (SA) and other signaling pathways [136] and concurrently induces multiple non-volatile biosynthetic pathways that alter biosynthesis for flavonoids, phenolics, and glucosinolates, which typically suppress aphid growth and fecundity [137,138,139,140]. In addition to herbivore-induced changes, virus infection can alter plant volatile profiles, likely through interference with plant primary and secondary metabolisms, thereby influencing aphid behavior. While the effects vary across virus species, emerging evidence suggests that virus-induced volatiles generally repel viruliferous aphids, encouraging their dispersal, while attracting non-viruliferous aphids [141,142,143]. These patterns imply that virus-induced changes in plant volatiles may reflect adaptive strategies that optimize viral transmission, though the underlying mechanisms and ecological consequences remain areas of active investigation.

In developing effective biorational strategies, it is essential to consider the coevolutionary dynamics between aphids and their host plants. Aphids have evolved diverse mechanisms to cope with plant specialized metabolites such as benzoxazinoids, alkaloids, and glucosinolates. The adaptations may include behavioral avoidance by experience [144], enhanced detoxification via enzyme systems [145,146], or the deployment of specific salivary effectors that modulate plant defense signaling [147]. In some cases, aphids can even selectively sequester or tolerate toxic compounds, turning plant defenses to their own advantage [148,149]. The evolutionary responses highlight the complexity of the plant-aphid arms race and underscore the importance of understanding both resistance traits and aphid counter-adaptations when designing sustainable control strategies [150]. Additionally, as mentioned above, virus-induced changes in plant volatile profiles may alter aphid behavior in ways that either inhibit or promote virus spread. While repellent volatiles are often seen as favorable for aphid deterrence, their role in stimulating aphid dispersal raises important questions about their unintended consequences, particularly for the transmission of persistent and non-persistent viruses. Addressing these knowledge gaps, especially the dual ecological outcomes of repellency, will be critical for advancing biorational aphid control in ways that are both ecologically informed and evolutionarily resilient.

Natural compounds remain significant and promising resources for identifying chemical biopesticides to control aphids. Traditional studies on the discovery of these semiochemicals and chemical biopesticides have been highly hypothesis-driven, typically relying on controlled laboratory experiments with limited variables/effects and small sample sizes. While informative, such approaches often exclude subtle or context-dependent interactions, which can lead to the exclusion of key compounds or specific combinations of compounds that contribute to aphid resistance. With the advancement of precision agriculture, data-driven approaches can be explored to promote the discovery of insect behavior-modifying compounds for further development of pest control strategies.

2.6. RNAi for Aphid Control

RNA interference (RNAi), a highly specific and powerful post-transcriptional gene silencing technology, was first discovered when double-stranded RNA (dsRNA) was introduced into the nematode Caenorhabditis elegans [151]. RNAi is a conserved evolutionary mechanism of gene regulation in eukaryotic organisms [152]. In natural environments, species constantly exchange long non-coding dsRNAs, and uptake of dsRNA can effectively regulate gene expression in recipient organisms, a process termed environmental RNA interference (eRNAi) [153]. In insects, ingestion of dsRNA can trigger RNAi responses that silence essential genes required for growth, development, survival, reproduction, and so on [154]. Therefore, RNAi has been intensively explored as a research tool to characterize gene functions, as well as potential agricultural pest control strategies. Recently, RNAi has been advanced to commercialization to be applied in the field. The first commercialized RNAi crop, SmartStax PRO maize, was approved in 2017 in the United States to control the western corn rootworm, Diabrotica virgifera virgifera [155]. Most recently, sprayable RNAi formulations have advanced toward commercial use (Calantha^TM) to control the Colorado potato beetle, Leptinotarsa decemlineata, in field applications [156].

Although RNAi-based pest control was initially explored in beetles and moths, extensive research has since focused on aphids. Target genes in aphids with a variety of functions have been tested using RNAi, including those in metabolic and developmental pathways, e.g., cuticular proteins in M. persicae [157] and zinc finger protein in S. avenae [158], salivary effectors that repress defenses in plants (e.g., Mp55, C002, SmDSR33) [159,160,161], essential genes in metabolism (e.g., arginine kinase) [162], developmental genes (e.g., hunchback) [160], and horizontally transferred genes [163].

Delivery strategies for RNAi have been designed and explored for the purposes of gene function annotation and application-oriented use. The advantages and disadvantages of each of these methods have been summarized in Chung et al. (2021) [164]. Those strategies included strategies directly applied to insect pests, for example, oral feeding through artificial diets, direct microinjection, topical applications directly on aphids, nanoparticle-mediated delivery, and insect symbiont-mediated delivery. For example, oral delivery of dsRNA targeting the gut aquaporin gene (AQP1) in pea aphids A. pisum can reach a complete mortality in laboratory settings [165]. In soybean aphids, A. glycines, a nanocarrier-mediated dsRNA spray applied to seedlings achieved up to 78.5% mortality under laboratory conditions [166]. In addition to direct application on insects, plant-mediated strategies include plant foliar sprays, plant root-soaking, trunk injection, Agrobacterium infiltration, virus-induced gene silencing (VIGS), and transgenic RNAi plants. Spray-induced gene silencing (SIGS) using aerosolized siRNA-nanoparticle complexes effectively knocked down genes and reduced aphid fitness in A. glycines [167]. Silencing the ABCG4 gene in M. persicae using VIGS reduced wing formation by up to 70%, and the few wings that did develop were smaller, limiting flight capacity [168]. Conversely, silencing the WRKY53 gene in wheat increased susceptibility to the Russian wheat aphid, Diuraphis noxia [169], highlighting the dual potential of VIGS in resistance screening. Transgenic approaches have been developed for more durable field applications. Transgenic wheat expressing dsRNA against the essential aphid salivary gene SmDSR33 disrupted feeding and reduced survival and reproduction [161]. In tomato, RNAi constructs targeting Acetylcholinesterase 1 (Ace1) in M. persicae also decreased survival and fecundity [170]. Notably, some transgenic approaches provide multigenerational persistence: silencing the salivary sheath protein (SHP) in S. avenae impaired feeding, development, and reproduction, with effects lasting for up to seven generations even after removal from transgenic plants [171].

While RNAi is fast advancing as a powerful tool to use in the field, concerns remain on its consistency, efficiency, particularly in Hemiptera, including aphids, and its potential off-target effects. For example, oral delivery of dsRNA targeting the gut aquaporin gene (AQP1) in A. pisum produced variable results across 83 pea aphid genotypes, ranging from no effect to complete mortality [165]. As those dsRNAs persist in the environment, especially through plant-mediated deliveries, and can even pass along to the upper trophic level as predators consuming the targeted pests [163], safety evaluation of off-target effects on beneficial insects or animals is critical in terms of field and long-term applications. To improve consistency, efficiency, and avoid potential off-targets, future efforts need to be taken to optimize dsRNA design and careful target selection with precision. Target selection and dsRNA fragment design remain critical for efficient RNAi. In addition, with expanding genomic resources, it is increasingly possible to identify aphid genes that are both highly effective for control and have minimal sequence similarity to non-target organisms, thereby reducing ecological risks.

While traditional long dsRNAs and siRNAs have been widely used, microRNAs (miRNAs)—naturally expressed regulators within interacting genomes—offer a novel strategy, named miRNA-induced gene silencing [172]. MiRNAs have been implicated as important in aphids, including interactions with their endosymbiont [173,174], interactions with the host plant [175,176], and the development of wing dimorphism [177], immune system [178]. Therefore, engineered miRNAs, as biopesticides or gene-edited crops, could be harnessed to disrupt these key aspects of aphid biology to achieve sustainable aphid management.

2.7. Targeting Symbiosis for Aphid Control

Endosymbionts provide aphids with critical survival advantages, including nutritional supplementation, stress tolerance, and protection against natural enemies, making the disruption of these associations a promising strategy for aphid management. For instance, horizontally transferred genes such as AmiD and LdcA1, which are essential for peptidoglycan remodeling and maintaining the aphid–Buchnera symbiosis, have been successfully targeted. Knockdown of these genes significantly reduced Buchnera abundance and activity, leading to impaired aphid growth and performance [179]. Similarly, recent work has revealed aphid miR-3024, a host-encoded microRNA that modulates symbiont-derived nutrient exchange, as a key regulator of the interaction between aphids and their secondary symbiont Serratia symbiotica. Overexpression of miR-3024 in host plants suppressed the aphid MRP4 gene, which encodes a transporter of vitamin B6 (VB6) from Serratia to the aphid, ultimately resulting in aphid mortality [174]. Interrupting secondary symbionts could help to increase the efficiency of biological agents, as many secondary symbionts provide aphid protection against predators. To date, nine facultative (secondary) symbionts have been widely documented within aphids, including S. symbiotica, Spiroplasma, Regiella insecticola, H. defensa, Rickettsia, Arsenophonus, Wolbachia, Fukatsuia symbiotica, and R. viridis [180]. Among those symbionts, Serratia and Rickettsia have been shown to confer heat tolerance to aphids [181,182]. The defensive bacterial symbiont, H. defensa, provides protection against parasitoid wasps through a bacteriophage (APSE) that encodes a cytolethal distending toxin B (cdtB) [183]. Although the underlying mechanisms are not fully understood, R. insecticola has been shown to confer resistance to several fungal entomopathogens (e.g., P. neoaphidis and Metarhizium brunneum), likely by limiting fungal penetration and amplification in the aphid body [184,185].

In addition to disrupting symbiotic relationships, symbionts themselves can be engineered as delivery vectors for RNAi-based pest control [186,187]. However, the genetic manipulation of aphid symbionts is often constrained by the difficulty of establishing in vitro cultures, as many possess reduced genomes and depend heavily on their host environment. Despite these challenges, several facultative symbionts have been successfully cultured axenically, including S. symbiotica, H. defensa, and F. symbiotica [188,189,190,191]. Notably, F. symbiotica not only thrives in axenic conditions but can also be reinfected into host aphids and stably maintained across multiple generations [189]. The ability to genetically manipulate these cultured symbionts provides a valuable platform for symbiont-mediated paratransgenic biotechnologies, such as the expression and dissemination of RNAi agents for aphid control [189,192].

3. Future Perspectives

Future aphid management is likely to rely increasingly on the integration of digital, molecular, and engineering approaches, shifting control strategies from reactive responses toward more predictive and targeted interventions. Innovations in precision agriculture, data-driven analytics, synthetic biology, and genome editing offer new opportunities to refine chemical, biological, cultural, and biorational approaches while reducing ecological costs and resistance risks.

Precision Agriculture for Chemical, Biological, and Cultural Control: Artificial intelligence (AI), particularly here as precision agriculture, is a fast-developing technology that can be integrated into almost all aspects of aphid management. AI-based precision agriculture includes aphid population scouting through image- or sensor-based systems, population forecasting to guide pesticide decision-making, and precision pesticide application enabled by AI-assisted mapping of aphid distributions combined with agricultural engineering solutions such as drone spraying, laser-guided spraying, and automated robotic spraying [193]. Image-based monitoring can help understand aphid abundances, diversity, as well as associated viral loads that impact damage to the host plant, while providing insights into how climate change impacts aphid population dynamics. Recent advances in AI further improve the automation for aphid identification and classification. While imaging conditions, image composition, and species-level discrimination remain challenging for automated aphid identification, a few machine learning programs have been developed for aphid classification. For example, classical machine learning algorithms have been used to identify and count aphids from sticky boards [194]. Deep learning methods were used to classify R. padi populations to recognize different life stages [195]. A neural architecture search tool implemented in Google AutoML Vision was able to distinguish three different aphid species, A. craccivora, A. pisum, and Megoura crassicauda, from plant images [196]. Lighting and background variability challenges have been resolved using the Visual Geometry Group with 16 convolutional layers (VGG-16) network architecture on imaging aphids from lemon tree plants [197]. Similarly, a VGG-13 architecture combined with a transfer learning system was used to quantify M. persicae nymphs and adults on leaves [198]. Those approaches reached high accuracies (81–97%) based on application conditions. Such technologies can improve pesticide efficacy while reducing pesticide usage, thereby enhancing sustainability by slowing the development of pesticide resistance as well as minimizing negative effects to beneficial insects. Beyond increasing efficiency and accuracy of identifying target aphid species in specific crop systems, the development of AI tools capable of distinguishing pest and non-pest aphid species and characterizing the overall insect community, including both pests and beneficial insects, would enable assessment of pest-to-beneficial ratios and identification of alternative food resources for natural enemies, thereby supporting more informed and ecologically sustainable pest management decisions.

Data-driven Discovery, Synthetic Biology, and Trait Engineering in Biorational Control: In recent years, the integration of meta-omics technologies and analytics, machine learning, and AI has been increasingly transforming how researchers identify and optimize semiochemicals for insect control [199,200]. By linking large-scale metabolomic data to specific aphid behaviors (e.g., settling, feeding, reproduction, or dispersal) at defined life stages, advanced machine learning algorithms might offer the potential to uncover fine-scale patterns between chemical structures and behavioral responses. Predictive modeling further enables the prioritization of candidate compounds for functional validation, significantly enhancing the efficiency and precision of discovery pipelines. However, the reliability of these approaches depends critically on the quality of input data, particularly aphid performance metrics, while poorly measured or inconsistent aphid data can compromise model outputs. Ensuring robust and standardized insect phenotyping is undoubtedly essential for realizing the full potential of data-driven biorational discovery.

Advances in synthetic biology and plant metabolic engineering are enabling susceptible crops to produce defensive compounds such as semiochemicals and chemical biopesticides. A well-documented strategy involves the heterologous expression of EβF synthase genes in plants such as Arabidopsis, tobacco, and chrysanthemum, enabling emission of the aphid alarm pheromone EβF, which repels M. persicae and A. gossypii while attracting natural enemies like D. rapae and Chrysopa septempunctata [201,202,203]. However, low yields of EβF remain a common challenge in sesquiterpene engineering, often attributed to limitations in precursor availability, enzyme activity, and intracellular targeting [204,205]. Meanwhile, ants are known to use EβF as a cue to locate aphid colonies [206]. Therefore, the in planta expression of EβF should be carefully evaluated to determine how it influences the behaviors of ant species in the presence of aphids and natural enemies. In addition, monoterpene engineering has shown comparable potential, underscoring terpene biosynthesis as a flexible platform for developing multitrophic aphid resistance. Genes encoding synthases for compounds such as linalool, 1,8-cineole, limonene, and carveol have been expressed in Arabidopsis, tobacco, and N. benthamiana, resulting in monoterpene emissions that deter M. persicae and A. gossypii, and attract beneficial predators like Harmonia axyridis and parasitoids such as D. rapae [204,207,208]. Some of these pathways also induce changes in plant morphology and signaling, including increased trichome density and elevated hormone levels, further reinforcing aphid resistance [208]. As the field advances, tissue-specific metabolic engineering is emerging as a promising strategy to fine-tune plant defenses against aphids. A compelling example involves epidermis-specific engineering in tomato, where heterologous expression of sesquiterpene synthases from wild tomato enabled localized production of defensive sesquiterpene blends. These epidermal defenses significantly reduced the survival and fecundity of M. euphorbiae, offering a targeted approach for aphid management [209].

Genome Editing for Genetic Control: Combining RNAi with CRISPR/Cas or other genome-editing approaches in either crops or insect genomes may broaden RNAi applications across diverse agricultural systems. CRISPR genome-editing has been used to engineer aphid host plants to help understand the interactions between host plants and aphids, such as plant secretion of acylsugars [83], serine proteinases [101], sugar transporter VST1 in watermelon [210], as well as high-throughput CRISPR library screening for aphid resistance [211].

Genome editing through CRISPR on aphids remains challenging, largely due to the fact that their parthenogenetic reproduction limits the genetic segregation and stable inheritance of induced mutations. However, a successful protocol has been reported through inducing male aphids for egg production, followed by gRNA injection into the egg for screening mutations [212]. A further refined CRISPR protocol, direct parental CRISPR (DIPA-CRISPR), successfully created Laccase2 knockout aphids and proved its essential role in overwintering egg adaptation [213]. Together, these two current protocols enabled the generation of mutant aphids for functional gene characterizations, although further methodological development will be required to adapt CRISPR-based approaches for practical aphid control.

Other Control Methods: Artificial high-voltage electrostatic fields (HVEFs) have also been explored for aphid management. Direct exposure of S. avenae to an HVEF of 4 kV/cm for 20 min significantly prolonged developmental time and reduced adult longevity [214].

4. In Summary

Future aphid management in crop systems will rely on integrated approaches for sustainable control. Chemical control remains a primary tool, but its effectiveness depends on rotating pesticides with different modes of action, optimizing application methods, and developing new compounds to overcome resistance while minimizing non-target impacts. Biological control using predators, parasitoids, and microbial biopesticides can reduce aphid populations sustainably, though mass-rearing and post-release persistence remain challenges that may be addressed with host or banker plant technologies. Cultural practices, including intercropping, cover crops, crop rotation, and habitat diversification, can suppress aphid populations and enhance natural enemy activity, especially when combined with semiochemical-based approaches. Molecular tools such as RNA interference (RNAi) offer precise gene silencing, while targeting aphid symbioses or engineering facultative symbionts provides additional innovative strategies. Emerging precision agriculture, data-driven analytics, synthetic biology, and genome-editing tools will not only enhance existing control strategies, such as biorational approaches and plant resistance, but also enable the development of novel strategies that expand the toolkit for aphid management. Integrating these strategies offers a durable, species-specific, and environmentally friendly framework for aphid management across diverse cropping systems.