Molecular Entomology 2024, Vol.15 http://emtoscipublisher.com/index.php/me © 2024 EmtoSci Publisher, registered at the publishing platform that is operated by Sophia Publishing Group, founded in British Columbia of Canada. All Rights Reserved.
Molecular Entomology 2024, Vol.15 http://emtoscipublisher.com/index.php/me © 2024 EmtoSci Publisher, registered at the publishing platform that is operated by Sophia Publishing Group, founded in British Columbia of Canada. All Rights Reserved. Publisher EmtoSci Publisher Editedby Editorial Team of Molecular Entomology Email: edit@me.emtoscipublisher.com Website: http://emtoscipublisher.com/index.php/me Address: 11388 Stevenston Hwy, PO Box 96016, Richmond, V7A 5J5, British Columbia Canada Molecular Entomology (ISSN 1925-198X) is an open access, peer reviewed journal published online by EmtoSci Publisher. The journal is committed to publishing and disseminating all the latest and outstanding research articles, letters and reviews in all areas of molecular entomology. The range of topics including genome structure of insects, gene expression and their function analysis, molecular evolution, molecular ecology, molecular genetics, insect physiology and biochemistry and other topical advisory subjects. Meanwhile we also publish the articles related to basic research, such as anatomy, morphology and taxonomy, which are fundamental to molecular technique’s innovation and development. All the articles published in Molecular Entomology are Open Access, and are distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. EmtoSci Publisher uses CrossCheck service to identify academic plagiarism through the world’s leading plagiarism prevention tool, iParadigms, and to protect the original authors’ copyrights. EmtoSci Publisher is an international Open Access publisher specializing in insect science, and entomology-related research registered at the publishing platform that is operated by Sophia Publishing Group (SPG), founded in British Columbia of Canada.
Molecular Entomology (online), 2024, Vol.15, No.5 ISSN 1925-198X http://emtoscipublisher.com/index.php/me © 2024 EmtoSci Publisher, registered at the publishing platform that is operated by Sophia Publishing Group, founded in British Columbia of Canada. All Rights Reserved. Latest Content Aphids as Vectors of Plant Viruses: Mechanisms of Transmission and Host Interaction Yunping Huang, Jia Xuan Molecular Entomology, 2024, Vol. 15, No. 5, 170-178 Role of Biopesticides in Integrated Pest Management for Maize Xian Zhang, Guifen Wang Molecular Entomology, 2024, Vol. 15, No. 5, 179-191 Genetic Insights intoSitophilus oryzae: Implications for Pest Management in Rice Guanli Fu Molecular Entomology, 2024, Vol. 15, No. 5, 192-199 Management Strategies Against Cotton Bollworms in Genetically Modified Crops Hui Lu, Jun Li Molecular Entomology, 2024, Vol. 15, No. 5, 200-208 Precision Pest Management: IoT and Remote Sensing in Tea Plant Protection Yali Deng, Haomin Chen Molecular Entomology, 2024, Vol. 15, No. 5, 209-220
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 170 Review Article Open Access Aphids as Vectors of Plant Viruses: Mechanisms of Transmission and Host Interaction Yunping Huang, Jia Xuan Institute of Life Science, Jiyang College of Zhejiang A and F University, Zhuji, 311800, Zhejiang, China Corresponding email: jia.xuan@jicat.org Molecular Entomology, 2024, Vol.15, No.5 doi: 10.5376/me.2024.15.0021 Received: 03 Sep., 2024 Accepted: 05 Oct., 2024 Published: 16 Oct., 2024 Copyright © 2024 Huang and Xuan, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Huang Y.P., and Xuan J., 2024, Aphids as vectors of plant viruses: mechanisms of transmission and host interaction, Molecular Entomology, 15(5): 170-178 (doi: 10.5376/me.2024.15.0021) Abstract This study systematically reviews the mechanisms by which aphids act as vectors for plant viruses and their interactions with host plants. By synthesizing recent findings on the molecular and ecological aspects of aphid-transmitted plant viruses, this study explores the significant roles of aphid biology, morphology, and endosymbionts in virus transmission. Plant viruses can manipulate host plant physiology to enhance transmission efficiency, with changes including virus-induced impacts on host metabolism and gene expression, thereby altering aphid behavior and increasing transmission effectiveness. This study also reveals that aphids exhibit complex behavioral and physiological adaptations in virus transmission. Understanding the interactions between aphids, viruses, and host plants is crucial for developing effective management strategies to mitigate the global agricultural impact of aphid-transmitted plant viruses. Keywords Aphids; Plant viruses; Virus transmission; Host interaction; Pest management 1 Introduction Aphids are among the most destructive insect pests affecting agricultural crops globally. These small, sap-sucking insects are notorious for their ability to cause direct damage to plants through their feeding behavior, which depletes essential nutrients and weakens plant structures. Aphids possess piercing-sucking mouthparts that facilitate their feeding on phloem sap, leading to significant yield losses in various crops, including potatoes, citrus, and hemp (Xu and Gray, 2020; Pitt et al., 2022). Additionally, aphids are vectors for numerous plant viruses, which further exacerbate their impact on agriculture. For instance, the green peach aphid (Myzus persicae) and the potato aphid (Macrosiphum euphorbiae) are known to transmit several economically important viruses to potato crops, resulting in severe yield reductions and loss of tuber quality. Understanding the mechanisms of virus transmission by aphids is crucial for developing effective management strategies to mitigate their impact on agriculture. Aphids transmit plant viruses through various modes, including non-persistent, semi-persistent, and persistent (circulative and non-circulative) transmission (Jayasinghe et al., 2021). The interaction between aphids, plant viruses, and host plants is complex and involves multiple factors, including aphid biology, virus characteristics, and plant responses (Gadhave et al., 2020; Ray and Casteel, 2022). For example, the transmission efficiency of viruses like Potato Virus Y (PVY) can be influenced by the feeding behavior of aphids, which is affected by both the virus and the host plant suitability (Pitt et al., 2022). Moreover, plant viruses can manipulate host plant physiology to enhance their transmission by aphid vectors, as seen in the case of Turnip Yellows Virus (TuYV), which alters the plant's nutritive content and defense mechanisms to benefit both the virus and the aphid vector (Krieger et al., 2023). Recent studies have also highlighted the role of insect-specific viruses and symbiotic bacteria in influencing aphid behavior and virus transmission. For instance, the Aphis citricidus Picorna Virus (AcPV) affects the stylet penetration activity of the brown citrus aphid, facilitating its transmission (An et al., 2023). Similarly, the presence of symbiotic bacteria like Serratia symbiotica in aphids can aid in suppressing plant defenses, thereby enhancing aphid feeding and virus transmission (Skaljac et al., 2019). These findings underscore the importance of a holistic understanding of the interactions between aphids, plant viruses, and host plants to devise sustainable pest management strategies.
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 171 This study integrates current knowledge on the mechanisms by which aphids transmit viruses and their interactions with host plants, examining the latest advancements in this field, including the role of aphid biology and morphology in virus transmission, the impact of viral infection on aphid feeding behavior, and the molecular interactions among plant viruses, aphids, and host plants, to provide a comprehensive understanding of factors influencing aphid-mediated virus transmission, with the goal of identifying potential targets for developing sustainable management strategies to mitigate the impact of aphid-transmitted viruses on global agriculture. 2 Mechanisms of Virus Transmission by Aphids 2.1 Non-persistent transmission Non-persistent transmission involves viruses that are acquired and transmitted by aphids within a short period, typically during brief probing of the plant epidermis. These viruses do not circulate within the aphid's body but are retained in the stylets. For instance, the Papaya Ringspot Virus (PRSV) is transmitted in a non-persistent manner by the melon aphid (Aphis gossypii). PRSV-infected plants enhance the fitness and feeding behavior of A. gossypii, likely through nutrient enrichment, which in turn facilitates virus transmission (Gadhave et al., 2019). Potyviruses, the largest group of plant-infecting RNA viruses, are also predominantly transmitted non-persistently by aphids, influencing aphid behavior and host plant biochemistry to enhance transmission efficiency (Gadhave et al., 2020). 2.2 Semi-persistent transmission In semi-persistent transmission, viruses are retained in the foregut or salivary glands of the aphid but do not circulate within the insect's body. These viruses can be retained for a longer period compared to non-persistent viruses. The transmission process involves specific interactions between the virus capsid and retention sites in the vector. For example, Non-Circulative, Semi-Persistent (NCSP) viruses have evolved mechanisms to bind to specific sites in the aphid's foregut, facilitating prolonged retention and transmission. This mode of transmission is influenced by the vector's feeding behavior and the plant's response to virus infection, which can alter vector attraction and feeding patterns (Zhou et al., 2018). 2.3 Persistent transmission Persistent transmission involves viruses that circulate within the aphid's body, moving from the gut to the hemolymph and eventually to the salivary glands. These viruses can be retained for the lifetime of the aphid. For instance, the Turnip Yellows Virus (TuYV) is transmitted persistently by aphids in a circulative, non-propagative manner. TuYV infection alters the host plant's metabolic composition, reducing defense responses and enhancing the plant's suitability as a feeding site, which promotes higher transmission efficiency (Chesnais et al., 2022; Krieger et al., 2023). Persistent viruses manipulate plant traits to create a more favorable environment for aphid feeding and virus transmission over extended periods (Shi et al., 2021). 2.4 Circulative and non-circulative pathways Viruses transmitted by aphids can follow either circulative or non-circulative pathways. In the circulative pathway, viruses enter the aphid's gut, circulate through the hemolymph, and reach the salivary glands, as seen with TuYV (Krieger et al., 2023). In contrast, non-circulative viruses, such as potyviruses, are retained in the stylets or foregut and do not enter the hemolymph. The mode of transmission (circulative or non-circulative) significantly influences the virus-vector-plant interactions, with circulative viruses often inducing more profound changes in plant physiology to enhance vector attraction and feeding (Chesnais et al., 2022). 2.5 Factors influencing transmission efficiency Several factors influence the efficiency of virus transmission by aphids, including the virus's ability to manipulate host plant traits, the vector's feeding behavior, and the presence of endosymbionts. For example, the presence of the endosymbiont Buchnera aphidicola in aphids can modulate the volatile profile of host plants, affecting aphid feeding preferences and virus transmission dynamics (Shi et al., 2021). Additionally, virus-induced changes in plant defense responses and nutrient profiles can either enhance or deter aphid feeding, thereby influencing transmission efficiency (Gadhave et al., 2019; Shi et al., 2021; Krieger et al., 2023). Understanding these complex interactions is crucial for developing effective strategies to manage aphid-transmitted plant viruses.
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 172 3 Host Interaction and Virus Acquisition 3.1 Aphid feeding behavior and stylet penetration Aphid feeding behavior and stylet penetration are critical for the transmission of plant viruses. The Electrical Penetration Graph (EPG) technique has been utilized to study the feeding behavior of aphids, revealing that virus infection can alter aphid feeding patterns. For instance, cannabis aphids (Phorodon cannabis) demonstrated different feeding behaviors on hemp and potato, which influenced the transmission efficiency of Potato Virus Y (PVY) (Pitt et al., 2022). Additionally, the presence of insect-specific viruses, such as Aphis citricidus Picorna Virus (AcPV), can affect the stylet penetration activity of aphids, thereby facilitating virus transmission (An et al., 2023). These findings highlight the complex interactions between aphids, their feeding behavior, and virus transmission. 3.2 Virus-vector interactions at the cellular level At the cellular level, virus-vector interactions involve intricate mechanisms that facilitate virus acquisition and transmission (Figure 1) (Catto et al., 2022). Plant viruses can manipulate host plant physiology to enhance their transmission by vectors. For example, the Turnip Yellows Virus (TuYV) alters the metabolic composition of infected plants, which benefits both the aphid vector and the virus transmission (Krieger et al., 2023). Furthermore, the presence of endosymbionts like Buchnera aphidicola in aphids can modulate virus transmission by affecting the volatile profile of host plants, leading to changes in aphid feeding preferences (Shi et al., 2021). These cellular-level interactions underscore the co-evolutionary dynamics between plant viruses, aphids, and host plants. 3.3 Host plant responses to aphid-virus infections Host plants exhibit various responses to aphid-virus infections, which can influence virus transmission. Transcriptome profiling of Arabidopsis thaliana and Camelina sativa infected with different viruses revealed virus- and host-specific gene expression changes that impact aphid behavior and virus transmission (Chesnais et al., 2022). Additionally, the presence of plant lectins can reduce virus transmission by interfering with the virus-aphid interaction. For instance, feeding aphids with Pisum Sativum Lectin (PSL) significantly reduced the transmission efficiency of barley yellow dwarf virus and potato virus Y (Francis et al., 2020). These host plant responses play a crucial role in the overall dynamics of aphid-virus interactions. 3.4 Evolutionary adaptations of aphids in virus transmission Aphids have evolved various adaptations to enhance their efficiency as virus vectors. These adaptations include changes in feeding behavior, stylet penetration, and interactions with host plants and endosymbionts. For example, the melon aphid (Aphis gossypii) shows increased performance and arrestment on Papaya Ringspot Virus (PRSV)-infected plants due to enhanced nutrient profiles, which in turn promotes virus transmission (Gadhave et al., 2020). Additionally, the co-evolution of aphids and plant viruses has led to the development of mutualistic interactions, where both the virus and the vector benefit from the interaction (Ray and Casteel, 2022). These evolutionary adaptations highlight the complex and dynamic nature of aphid-virus interactions. 4 Molecular Mechanisms Underlying Virus Transmission 4.1 Role of viral proteins in facilitating aphid-mediated transmission Viral proteins play a crucial role in facilitating the transmission of plant viruses by aphids. For instance, the interaction between viral proteins and aphid proteins is essential for the efficient transmission of viruses like the Potato Leafroll Virus (PLRV). Studies have identified several aphid proteins that interact with PLRV, including an orthologue of the human innate immunity protein complement Component 1 Q Subcomponent-Binding Protein (C1QBP). This protein partially co-localizes with PLRV in the cytoplasmic puncta and along the periphery of aphid gut epithelial cells, indicating its role in the acquisition and transmission efficiency of PLRV by Myzus persicae (DeBlasio et al., 2021). Additionally, the identification of cuticular proteins such as Stylin-01 in aphid mouthparts has provided insights into the mechanisms of noncirculative virus transmission. Stylin-01 has been shown to be involved in the transmission of the Cauliflower Mosaic Virus (CaMV) by binding to the virus in the acrostyle of aphid stylets (Webster et al., 2018).
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 173 Figure 1 Schematic diagram explaining the interactions between plant viruses and their vectors with respect to different transmission modes viz., non-persistent, semi-persistent, persistent non-propagative, and persistent-propagative (Adopted from Catto et al., 2022) Image caption: (A) Non-persistent viruses, such as Cucumber Mosaic Virus (CMV), are acquired by aphids from the epidermal cells of infected plants and retained at the tip of its stylet (acrostyle) at the distal end of the common (food/salivary) duct. (B) Semi-persistent viruses, such as Tomato Chlorosis Virus (ToCV), are phloem-limited in infected plants, and the virus attaches to the binding site at the vector’s foregut with the help of the minor Capsid Protein (CPm). (C) Persistent non-propagative viruses, such as Tomato Yellow Leaf Curl Virus (TYLCV), are also phloem-limited and are retained in the midgut upon acquisition. Through receptor-mediated endocytosis, the virus traverses the midgut barrier into hemolymph where the endosymbiont protein GroEL interacts with the virion. The virus from the hemolymph reaches primary salivary glands mediated again via species-specific receptors. (D) Thrips acquire persistent propagative viruses, such as Tomato Spotted Wilt Virus (TSWV), from epidermal cells of infected plants. Gn/Gc protein supports virus entry into midgut cells, where replication of the virus occurs. The virus TSWV enters Primary Salivary Glands (PSG) from MG1 through Tubular Salivary Glands (TSG) (Adopted from Catto et al., 2022) 4.2 Aphid genomic and transcriptomic insights into virus transmission Genomic and transcriptomic analyses have revealed significant insights into the molecular interactions between aphids and plant viruses. For example, transcriptome profiling of Arabidopsis thaliana and Camelina sativa plants infected with Turnip Yellows Virus (TuYV) or CaMV and infested with Myzus persicae aphids has shown virusand host-specific differences in gene expression patterns. These differences are linked to the mode of virus transmission and the severity of symptoms, which in turn affect aphid behavior and fecundity (Chesnais et al., 2022). Furthermore, a review of transcriptional responses in various insect vectors, including aphids, has cataloged differential gene expression related to virus reception, cell entry, tissue tropism, and vector immune responses. This understanding can aid in identifying candidate genes for targeted management approaches using RNAi or CRISPR editing (Catto et al., 2022). 4.3 Virus-induced alterations in aphid behavior and physiology Plant viruses can induce significant alterations in aphid behavior and physiology to enhance their transmission. For instance, the Turnip Yellows Virus (TuYV) has been shown to alter the metabolic composition of infected plants, which in turn benefits the aphid vector and increases virus transmission efficiency. The virus infection alleviates gene deregulations induced by aphids in non-infected plants, leading to changes in the plant's nutritive
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 174 content and defense reactions (Krieger et al., 2023). Similarly, the Papaya Ringspot Virus (PRSV) has been found to enhance the fitness of its vector, the melon aphid (Aphis gossypii), by increasing the concentrations of essential amino acids and soluble carbohydrates in the host plant. This results in increased aphid arrestment and long-term feeding on PRSV-infected plants, thereby promoting virus transmission (Gadhave et al., 2019). Additionally, the interaction between plant viruses and aphid vectors often involves mutualistic relationships where both the virus and the vector benefit from the interaction. Viral and vector effectors target conserved mechanisms of plant immunity, manipulating host physiology to facilitate successful colonization and transmission (Ray and Casteel, 2022). 5 Case Study 5.1 Specific case of aphid-mediated virus transmission in crop plants Aphids are notorious vectors of plant viruses, significantly impacting crop production worldwide. One notable example is the transmission of the Turnip Yellows Virus (TuYV) by aphids in Arabidopsis thaliana. This virus is transmitted in a circulative and non-propagative manner, meaning the virus circulates within the aphid but does not replicate within it. Research has shown that TuYV infection can alleviate the gene deregulations induced by aphid infestation, thereby promoting virus transmission. The virus alters the plant's metabolic composition, making it more conducive for aphid feeding and increasing transmission efficiency (Figure 2) (Krieger et al., 2023). Another significant case involves the transmission of Potato Virus Y (PVY) by the cannabis aphid (Phorodon cannabis). This aphid species has been shown to efficiently transmit PVY to both hemp and potato plants, with varying transmission rates depending on the host plant (Pitt et al., 2022). Figure 2 Experimental set-up for the high-throughput transcriptomic and metabolomic analyses (Adopted from Krieger et al., 2023) Image caption: Arabidopsis plants were inoculated with Turnip Yellows Virus (TuYV)-viruliferous (upper panel) or nonviruliferous (lower panel) Myzus persicaeaphids. After 3 weeks, the two batches of plants were infested with 30 nonviruliferous aphids for 6 or 72 h before harvesting (samples 3 to 4 and 5 to 6, respectively). Plants that were not infested with aphids were similarly processed (samples 1 and 2) (Adopted from Krieger et al., 2023) 5.2 Analysis of virus spread dynamics in a real-world scenario The dynamics of virus spread in real-world agricultural settings are complex and influenced by multiple factors, including aphid behavior, plant-virus interactions, and environmental conditions. For instance, the spread of non-persistent viruses like PVY is heavily influenced by the feeding behavior of aphids. Studies using the Electrical Penetration Graph (EPG) technique have shown that viruliferous aphids (those carrying the virus)
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 175 exhibit different feeding behaviors compared to non-viruliferous aphids, which can affect virus transmission rates. Viruliferous aphids tend to spend less time ingesting phloem, potentially leading to increased dispersal and virus spread (Pitt et al., 2022). Additionally, epidemiological models have demonstrated that agronomic practices such as fertilization, irrigation, and pesticide application can significantly impact the spread of non-persistent viruses. For example, fertilization and irrigation can either reduce or increase virus spread depending on whether the interference between resident and transient aphids is direct or indirect (Zaffaroni et al., 2021). 5.3 Impact on crop yield and agricultural practices The impact of plant viruses on crop yields can be severe, leading to significant reductions in both quantity and quality of the produce (Zhan, 2024). The impact of aphid-mediated virus transmission on crop yield and agricultural practices is profound. Viruses like TuYV and PVY can cause significant yield losses, necessitating the development of effective management strategies. For instance, the presence of TuYV in Arabidopsis thaliana has been shown to alter the plant's nutritive content and defense mechanisms, making it more susceptible to aphid infestation and virus transmission (Krieger et al., 2023). Similarly, the efficient transmission of PVY by cannabis aphids can lead to substantial yield losses in both hemp and potato crops (Pitt et al., 2022). To mitigate these impacts, various strategies have been proposed, including the use of plant lectins to reduce virus transmission efficiency. Feeding aphids with specific plant lectins has been shown to significantly reduce the transmission of viruses like Barley Yellow Dwarf Virus and Potato Virus Y, offering a potential alternative approach for crop protection (Francis et al., 2020). Additionally, understanding the interactions between aphids, viruses, and plant hosts at the molecular level can inform the development of targeted pest management strategies, such as the use of chemical inhibitors to disrupt key protein-protein interactions involved in virus transmission (DeBlasio et al., 2021). 6 Strategies for Managing Aphid-Mediated Virus Transmission 6.1 Biological control methods Biological control methods involve the use of natural predators, parasitoids, and pathogens to manage aphid populations and reduce virus transmission. One promising approach is the use of entomopathogenic fungi, such as Beauveria bassiana, which has shown effectiveness in reducing virus transmission rates. For instance, endophytic colonization of melon plants with B. bassiana significantly reduced the transmission rates of Cucumber Mosaic Virus (CMV) and Cucurbit Aphid-Borne Yellows Virus (CABYV) by 21.9% and 24.4%, respectively (González-Mas et al., 2019). Additionally, the manipulation of aphid endosymbionts, such as Buchnera aphidicola, can alter aphid behavior and reduce virus transmission. For example, CMV infection reduces B. aphidicola abundance in aphids, leading to a shift in feeding preference from infected to healthy plants, thereby potentially reducing the spread of the virus (Shi et al., 2021). 6.2 Chemical control and integrated pest management (IPM) Chemical control methods, including the use of insecticides, are commonly employed to manage aphid populations. However, the indiscriminate use of pesticides can lead to resistance development and non-target effects. Integrated Pest Management (IPM) strategies combine chemical control with other methods to achieve sustainable pest management. For example, the application of pesticides can be optimized by understanding the interactions between resident and transient aphids. An epidemiological model showed that pesticide application could counterintuitively increase the spread of non-persistent viruses if not properly managed, highlighting the importance of integrating ecological principles into pest management strategies (Zaffaroni et al., 2021). Additionally, the use of selective insecticides that target specific aphid species while preserving natural enemies can enhance the effectiveness of IPM programs. 6.3 Breeding virus-resistant plant varieties Breeding virus-resistant plant varieties is a long-term strategy to manage aphid-mediated virus transmission. Resistant varieties can reduce the incidence of virus infections and limit the spread of viruses by aphids. Advances in understanding the molecular mechanisms of plant-virus-vector interactions have facilitated the development of resistant varieties. For instance, the identification of plant transcription factors and protein degradation pathways
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 176 targeted by virus and vector effectors can inform breeding programs aimed at enhancing plant resistance (Ray and Casteel, 2022). Additionally, the manipulation of plant nutrient profiles to deter aphid feeding and reduce virus transmission has shown promise. For example, PRSV-infected plants exhibited increased concentrations of essential amino acids and soluble carbohydrates, which enhanced the fitness of the melon aphid, suggesting that altering plant nutrient profiles could be a potential strategy for breeding resistant varieties (Gadhave et al., 2019). 6.4 Future directions in aphid management for virus control Future research in aphid management for virus control should focus on a multidisciplinary approach that integrates biological, chemical, and genetic strategies. Understanding the complex interactions between aphids, viruses, and host plants at the molecular level can inform the development of targeted control methods. For instance, the use of effector-mediated interactions to manipulate host plant physiology and enhance resistance to both aphids and viruses is a promising area of research (Ray and Casteel, 2022). Additionally, the development of ecological models that incorporate environmental factors and microbial communities can improve our understanding of disease dynamics and inform the deployment of microbiome-targeted pest management tactics (Enders and Hefley, 2023). Finally, exploring the potential of novel biotechnological approaches, such as RNA interference (RNAi) and gene editing, to disrupt virus transmission pathways in aphids could provide new avenues for sustainable pest management. 7 Concluding Remarks Aphids are significant vectors of plant viruses, and their interactions with both the viruses they transmit and the host plants they infest are complex and multifaceted. Recent research has highlighted the role of effector proteins in mediating these interactions, with both viruses and aphids using effectors to manipulate host plant physiology to their advantage. Studies have shown that plant viruses can alter the host plant's metabolic and gene expression profiles to facilitate their transmission by aphids. For instance, the Turnip Yellows Virus (TuYV) can alleviate aphid-induced stress responses in Arabidopsis thaliana, thereby enhancing its own transmission. Additionally, the transmission efficiency of potyviruses, the largest group of plant-infecting RNA viruses, is influenced by various factors including aphid behavior and host plant biochemistry. Aphid biology and morphology also play crucial roles in virus transmission, with different transmission modes (persistent, circulative, non-circulative) being affected by these factors. Furthermore, the presence of endosymbionts in aphids can modulate virus transmission by altering the volatile profiles of host plants, thereby influencing aphid feeding behavior. Understanding the mechanisms of aphid-mediated virus transmission has significant implications for crop protection and virus control. The ability of viruses to manipulate host plant responses to benefit their transmission suggests that targeting these molecular interactions could be a viable strategy for controlling virus spread. For example, the use of plant lectins to interfere with virus transmission by aphids has shown promise, as lectins can bind to viral glycoproteins and reduce transmission efficiency. Additionally, manipulating the nutrient profile of host plants to make them less favorable for aphid vectors could reduce virus transmission rates. The role of endosymbionts in modulating virus transmission also opens up new avenues for pest management, such as targeting symbionts to disrupt the transmission process. Overall, integrating these insights into pest management strategies could lead to more effective and sustainable approaches to controlling aphid-transmitted plant viruses. Future research should focus on further elucidating the molecular mechanisms underlying aphid-virus-host plant interactions. This includes identifying specific effector proteins involved in these interactions and understanding their roles in manipulating host plant physiology. Additionally, more studies are needed to explore the impact of different environmental factors on virus transmission dynamics, particularly in the context of climate change. The role of microbial communities within aphids and their influence on virus transmission also warrants further investigation, as this could lead to novel microbiome-targeted pest management strategies. Moreover, the development of multi-omics approaches to study these complex interactions at a systems level could provide deeper insights into the co-evolutionary dynamics between aphids, viruses, and host plants. Finally, translating these findings into practical applications for crop protection will require interdisciplinary collaboration between molecular biologists, entomologists, plant pathologists, and agronomists.
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 177 Acknowledgments We would like to thank Professor Wang for his support and assistance throughout this manuscript, which greatly clarified the direction of the study. We also appreciate the valuable comments and suggestions from the reviewers, which have been instrumental in improving this study. Conflict of Interest Disclosure The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest. References An X., Gu Q., Wang J., Chang T., Zhang W., Wang J., and Niu J., 2023, Insect-specific RNA virus affects the stylet penetration activity of brown citrus aphid (Aphis citricidus) to facilitate its transmission, Insect Science, 31(1): 255-270. https://doi.org/10.1111/1744-7917.13242 Catto M., Mugerwa H., Myers B., Pandey S., Dutta B., and Srinivasan R., 2022, A review on transcriptional responses of interactions between insect vectors and plant viruses, Cells, 11(4): 693. https://doi.org/10.3390/cells11040693 Chesnais Q., Golyaev V., Velt A., Rustenholz C., Brault V., Pooggin M., and Drucker M., 2022, Comparative plant transcriptome profiling of Arabidopsis thaliana Col-0 and Camelina sativa var. Celine infested with Myzus persicae aphids acquiring circulative and noncirculative viruses reveals virus- and plant-specific alterations relevant to aphid feeding behavior and transmission, Microbiology Spectrum, 10(4): e00136-22. https://doi.org/10.1128/spectrum.00136-22 DeBlasio S., Wilson J., Tamborindeguy C., Johnson R., Pinheiro P., MacCoss M., Gray S., and Heck M., 2021, Affinity purification-mass spectrometry identifies a novel interaction between a polerovirus and a conserved innate immunity aphid protein that regulates transmission efficiency, Journal of Proteome Research, 20(6): 3365-3387. https://doi.org/10.1021/acs.jproteome.1c00313 Enders L., and Hefley T., 2023, Modeling host-microbiome interactions to improve mechanistic understanding of aphid vectored plant pathogens, Frontiers in Ecology and Evolution, 11: 1251165. https://doi.org/10.3389/fevo.2023.1251165 Francis F., Chen J., Yong L., and Bosquée E., 2020, Aphid feeding on plant lectins falling virus transmission rates: a multicase study, Journal of Economic Entomology, 113: 1635-1639. https://doi.org/10.1093/jee/toaa104 Gadhave K., Dutta B., Coolong T., and Srinivasan R., 2019, A non-persistent aphid-transmitted Potyvirus differentially alters the vector and non-vector biology through host plant quality manipulation, Scientific Reports, 9(1): 2503. https://doi.org/10.1038/s41598-019-39256-5 Gadhave K., Gautam S., Rasmussen D., and Srinivasan R., 2020, Aphid transmission of potyvirus: the largest plant-infecting RNA virus genus, Viruses, 12(7): 773. https://doi.org/10.3390/v12070773 González-Mas N., Quesada-Moraga E., Plaza M., Fereres A., and Moreno A., 2019, Changes in feeding behaviour are not related to the reduction in the transmission rate of plant viruses byAphis gossypii (Homoptera: Aphididae) to melon plants colonized by Beauveria bassiana (Ascomycota: Hypocreales), Biological Control, 130: 95-103. https://doi.org/10.1016/J.BIOCONTROL.2018.11.001 Jayasinghe W., Akhter M., Nakahara K., and Maruthi M., 2021, Effect of aphid biology and morphology on plant virus transmission, Pest Management Science, 78(2): 416-427. https://doi.org/10.1002/ps.6629 Krieger C., Halter D., Baltenweck R., Cognat V., Boissinot S., Maia-Grondard A., Erdinger M., Bogaert F., Pichon E., Hugueney P., Brault V., and Ziegler-Graff V., 2023, An aphid-transmitted virus reduces the host plant response to its vector to promote its transmission, Phytopathology, 113(9): 1745-1760. https://doi.org/10.1094/PHYTO-12-22-0454-FI Pitt W., Kairy L., Villa E., Nalam V., and Nachappa P., 2022, Virus infection and host plant suitability affect feeding behaviors of cannabis aphid (Hemiptera: Aphididae), a newly described vector of potato virus Y, Environmental Entomology, 51: 322-331. https://doi.org/10.1093/ee/nvac001 Ray S., and Casteel C., 2022, Effector-mediated plant-virus-vector interactions, The Plant Cell, 34: 1514-1531. https://doi.org/10.1093/plcell/koac058 Shi X., Yan S., Zhang C., Zheng L., Zhang Z., Sun S., Gao Y., Tan X., Zhang D., and Zhou X., 2021, Aphid endosymbiont facilitates virus transmission by modulating the volatile profile of host plants, BMC Plant Biology, 21: 1-8. https://doi.org/10.1186/s12870-021-02838-5 Skaljac M., Vogel H., Wielsch N., Mihajlovic S., and Vilcinskas A., 2019, Transmission of a protease-secreting bacterial symbiont among pea aphids via host plants, Frontiers in Physiology, 10: 438. https://doi.org/10.3389/fphys.2019.00438
Molecular Entomology 2024, Vol.15, No.5, 170-178 http://emtoscipublisher.com/index.php/me 178 Webster C., Pichon E., Munster M., Monsion B., Deshoux M., Gargani D., Calevro F., Jiménez J., Moreno A., Krenz B., Thompson J., Perry K., Fereres A., Blanc S., and Uzest M., 2018, Identification of plant virus receptor candidates in the stylets of their aphid vectors, Journal of Virology, 92(14): e00432-18. https://doi.org/10.1128/JVI.00432-18 Xu Y., and Gray S., 2020, Aphids and their transmitted potato viruses: a continuous challenges in potato crops, Journal of Integrative Agriculture, 19: 367-375. https://doi.org/10.1016/s2095-3119(19)62842-x Zaffaroni M., Rimbaud L., Mailleret L., Cunniffe N., and Bevacqua D., 2021, Modelling interference between vectors of non-persistently transmitted plant viruses to identify effective control strategies, PLoS Computational Biology, 17(12): e1009727. https://doi.org/10.1371/journal.pcbi.1009727 Zhan C.Y., 2024, The role of viruses in sugarcane yield reduction: a case study on Sugarcane yellow leaf virus, Molecular Pathogens, 15(3): 119-128. https://doi.org/10.5376/mp.2024.15.0012 Zhou J., Drucker M., and Ng J., 2018, Direct and indirect influences of virus-insect vector-plant interactions on non-circulative, semi-persistent virus transmission, Current Opinion in Virology, 33: 129-136. https://doi.org/10.1016/j.coviro.2018.08.004
Molecular Entomology 2024, Vol.15, No.5, 179-191 http://emtoscipublisher.com/index.php/me 179 Research Insight Open Access Role of Biopesticides in Integrated Pest Management for Maize Xian Zhang, Guifen Wang Hainan Key Laboratory of Crop Molecular Breeding, Sanya, 572000, China Corresponding email: guifang.wang@hitar.org Molecular Entomology, 2024, Vol.15, No.5 doi: 10.5376/me.2024.15.0022 Received: 05 Sep., 2024 Accepted: 06 Oct., 2024 Published: 17 Oct., 2024 Copyright © 2024 Zhang and Wang, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Zhang X., and Wang G.F., 2024, Role of biopesticides in integrated pest management for maize, Molecular Entomology, 15(5): 179-191 (doi: 10.5376/me.2024.15.0022) Abstract Biopesticides play a crucial role in the Integrated Pest Management (IPM) of maize, offering an environmentally sustainable alternative to chemical pesticides. This study assesses the efficacy, benefits, and challenges of using biopesticides in maize pest management. Key biopesticides, including microbial agents such as Bacillus thuringiensis and botanical extracts like neem, have demonstrated significant effectiveness in controlling major pests, particularly the fall armyworm (Spodoptera frugiperda). This study highlights advancements in biopesticide formulation, including encapsulation technologies and genetic modifications, which have enhanced the stability and application of these agents in varying environmental conditions. Additionally, the integration of biopesticides with precision agriculture and other IPM components has proven to optimize pest control while reducing the ecological footprint of maize farming. Despite their potential, challenges such as production costs, regulatory barriers, and pest resistance are limiting factors for wider adoption. The review concludes by discussing future directions in research and policy needed to accelerate the global use of biopesticides in maize IPM, contributing to more sustainable agricultural practices. Keywords Biopesticides; Integrated Pest Management; Maize; Sustainable Agriculture; Fall Armyworm 1 Introduction Maize (Zea mays L.) is one of the most widely cultivated crops globally, playing a crucial role in food security and economic stability. However, maize cultivation faces numerous challenges, particularly pest infestations that affect the crop at various growth stages, including pests like the fall armyworm (Spodoptera frugiperda) and corn rootworm (Diabrotica spp.). These pests not only significantly reduce yields but also increase production costs. While chemical pesticides have been used to manage these pests, they have led to environmental pollution and increased pest resistance, highlighting the urgent need for more sustainable pest management solutions (Gassmann and Clifton, 2017). Integrated Pest Management (IPM) is a sustainable pest control strategy that combines biological, physical, and chemical methods to reduce reliance on chemical pesticides while protecting the environment. Biopesticides, as a key component of IPM, are gaining popularity due to their natural, environmentally friendly properties and minimal impact on non-target organisms. In maize cultivation, microbial biopesticides like Bacillus thuringiensis and Entomopathogenic fungi such as Metarhizium rileyi have proven effective in pest control. Additionally, botanical pesticides (e.g., neem) and biochemical pesticides (e.g., pheromones) have been widely adopted in IPM systems for maize (Mnif and Ghribi, 2015; Parajuli et al., 2022). This study explores the role of biopesticides in integrated pest management for maize, evaluating the efficacy of different biopesticide types and their environmental and economic impacts on pest control, revealing challenges in the commercialization and widespread application of microbial, botanical, and biochemical pesticides in maize pest management, with the aim of providing recommendations and solutions for sustainable agriculture development. 1 Types of Biopesticides Used in Maize Cultivation 1.1 Microbial biopesticides Microbial biopesticides are derived from living organisms, such as bacteria, fungi, and viruses, that are pathogenic to pests. Among the most well-known microbial biopesticides is Bacillus thuringiensis (Bt), a bacterium that
Molecular Entomology 2024, Vol.15, No.5, 179-191 http://emtoscipublisher.com/index.php/me 180 produces toxins lethal to various insect pests. In maize cultivation, Bt has been used extensively to manage lepidopteran pests, particularly corn borers. When ingested by pests, the Bt toxin disrupts the midgut lining, leading to paralysis and death. The specificity of Bt makes it an ideal candidate for integrated pest management (IPM), as it targets specific pests while leaving beneficial insects unharmed (Mnif and Ghribi, 2015). Another important microbial biopesticide used in maize is Metarhizium rileyi, a fungus that infects pests like the fall armyworm (Spodoptera frugiperda). Metarhizium species are known for their ability to parasitize a wide range of insect pests, making them a powerful tool in maize IPM. Studies have shown that formulations of Metarhizium rileyi remain stable under various environmental conditions, with high efficacy in reducing pest populations. The fungus infects pests through direct contact, penetrating their exoskeleton and proliferating within, leading to death (Grijalba et al., 2018). In addition to Bacillus thuringiensis and Metarhizium rileyi, other microbial agents such as entomopathogenic nematodes and viruses are also used as biopesticides in maize cultivation. These organisms attack pest larvae or adult insects, disrupting their development and leading to reduced pest populations. The widespread adoption of microbial biopesticides in maize cultivation is driven by their low toxicity to humans and animals, as well as their ability to decompose rapidly, minimizing environmental impact (Lengai and Muthomi, 2018). 1.2 Botanical biopesticides Botanical biopesticides are derived from plant extracts and are widely used in pest management due to their natural origin and lower environmental impact compared to synthetic chemicals. Neem (Azadirachta indica) is one of the most extensively studied and used botanical pesticides in maize cultivation. Neem contains several active compounds, including azadirachtin, which acts as an insect growth regulator and feeding deterrent. It is particularly effective against pests such as aphids, leafhoppers, and corn borers. Neem-based biopesticides are safe for non-target organisms and break down quickly in the environment, making them ideal for sustainable agriculture (Lengai and Muthomi, 2018). Another well-known botanical biopesticide is pyrethrum, which is derived from the flowers of Chrysanthemum species. Pyrethrins, the active ingredients in pyrethrum, are potent insect neurotoxins that cause paralysis and death in a wide range of pests, including those affecting maize. Pyrethrum is used in maize cultivation as a contact insecticide and is favored for its rapid action against pests like the European corn borer (Ostrinia nubilalis). Its low toxicity to mammals and birds further enhances its appeal in integrated pest management strategies (Kumar et al., 2021). Botanical biopesticides are also derived from a variety of other plant sources, such as garlic, pepper, and eucalyptus. These plants contain natural compounds that repel or inhibit the growth of pests. For instance, garlic extract has been used as a repellent against insects like aphids and mites in maize fields. The use of botanical pesticides, while offering a more eco-friendly alternative to chemical pesticides, also faces challenges such as inconsistent efficacy and the need for frequent application due to rapid degradation in the environment (Parajuli et al., 2022). 1.3 Biochemical biopesticides Biochemical biopesticides include naturally occurring substances that control pests through mechanisms other than direct toxicity. Pheromones, one of the most commonly used biochemical biopesticides, play a crucial role in pest control by disrupting the mating behavior of pests. In maize cultivation, pheromone traps are used to control pests like the European corn borer (Ostrinia nubilalis) by confusing male moths and preventing them from locating females, thus reducing reproduction rates and subsequent pest infestations. This method is species-specific, minimizing harm to non-target organisms (Lengai and Muthomi, 2018). In addition to pheromones, other biochemical biopesticides include plant growth regulators and insect growth regulators (IGRs). IGRs work by interfering with the normal development of insect pests, preventing them from reaching adulthood and reproducing. In maize IPM programs, IGRs are used to manage pest populations such as
Molecular Entomology 2024, Vol.15, No.5, 179-191 http://emtoscipublisher.com/index.php/me 181 the corn rootworm, significantly reducing their impact on crop yields. These biochemicals are environmentally safe and effective at low doses, making them attractive alternatives to conventional pesticides (Kumar et al., 2021). Another category of biochemical biopesticides is plant-derived Volatile Organic Compounds (VOCs), which can repel or inhibit pests. For example, VOCs from certain fungi or plants are used to protect stored maize from pests such as the maize weevil (Sitophilus zeamais). These compounds have shown significant potential in controlling pest populations while being non-toxic to humans and beneficial insects. Although biochemical biopesticides are highly specific and environmentally friendly, their use is often limited by high production costs and the need for advanced delivery systems (Herrera et al., 2015). 1.4 Insect-resistant transgenic maize as a biopesticide Insect-resistant transgenic maize, such as Bt maize, is a form of biopesticide that involves the insertion of genes fromBacillus thuringiensis into the maize genome. This enables the plant to produce insecticidal proteins that target specific pests like the European corn borer and the corn rootworm. The introduction of Bt maize in the 1990s revolutionized pest control in maize cultivation by reducing the need for external pesticide applications. The insecticidal proteins produced by Bt maize disrupt the digestive system of target pests, causing paralysis and death while being harmless to humans and most non-target organisms (Osman et al., 2015). Bt maize has been highly effective in reducing pest populations and protecting maize crops from significant damage. However, the long-term use of transgenic crops has led to concerns about pest resistance. Some insect populations, such as the corn rootworm, have developed resistance to the Bt toxins, diminishing the effectiveness of transgenic crops over time. To counteract this, newer varieties of transgenic maize have been developed that express multiple Bt toxins or combine Bt traits with other pest management strategies to delay resistance development (Gassmann and Clifton, 2017). Transgenic maize also offers benefits beyond pest control, such as reducing the environmental impact of chemical pesticide use and lowering production costs for farmers. By incorporating biopesticidal traits directly into the crop, the need for chemical pesticide applications is significantly reduced. However, the adoption of transgenic crops is met with regulatory and market challenges in some regions, where concerns over genetically modified organisms (GMOs) persist. Despite these challenges, Bt maize continues to be a cornerstone of modern maize IPM programs and offers significant potential for the future of sustainable agriculture (Nyangau et al., 2020). 2 Mechanisms of Action 2.1 How microbial biopesticides affect pest populations Microbial biopesticides are derived from organisms such as bacteria, fungi, and viruses, and their mode of action involves various biological mechanisms. For instance, Bacillus thuringiensis (Bt) produces toxins that disrupt the gut of lepidopteran pests like the corn borer, leading to their death. These toxins are highly specific, only affecting certain insect species while being harmless to humans and non-target organisms (Kulkarni, 2015). Another mechanism involves fungal biopesticides, such as Metarhizium rileyi, which penetrate the insect's cuticle and proliferate inside the host, eventually causing the pest to die. This fungus has shown high efficacy against pests like the fall armyworm, a major threat to maize crops (Grijalba et al., 2018). These microbial biopesticides can also work by inducing systemic resistance in plants, helping crops to better defend themselves against future pest attacks.Some microbial biopesticides, particularly bacteria, compete with pests for resources such as nutrients or space, reducing the ability of harmful organisms to establish themselves on the plant. For example, some strains of beneficial bacteria produce antimicrobial substances that inhibit the growth of harmful pathogens or compete for iron by producing siderophores, making the environment less favorable for pest growth (Roca-Couso et al., 2021). 2.2 Mode of action of botanical biopesticides Botanical biopesticides, derived from plant extracts, affect pests through multiple pathways. Neem (Azadirachta
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