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Biology and Molecular Mechanisms of Plant-Aphid Interactions

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A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Molecular Biology and Genomics".

Deadline for manuscript submissions: 15 February 2025 | Viewed by 11698

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Dr. Yinghua Huang

E-Mail Website1 Website2
Guest Editor

1. United States Department of Agriculture-Agricultural Research Service (USDA-ARS), Plant Science Research Laboratory, Stillwater, OK 74075, USA
2. Department of Plant Biology, Ecology, and Evolution, Oklahoma State University, Stillwater, OK 74078, USA
Interests: aphid; crop protection; crop science; DNA marker; genomics; plant biotechnology; plant genetics; plant-aphid interaction; plant resistance; QTL mapping
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Dear Colleagues,

Aphids are key pests of crop plants throughout the world because they pose serious threats to crop production. As phloem-feeding insects, aphids suck plant juices and secrete sticky “honeydew”, causing serious damage to the host plants. Fortunately, some plants often can withstand aphid feeding with no adverse effect. These plants can mount a successful defense using their natural genetics or alter the ways they interact with aphids; thus, host plant resistance has been used for effective aphid control in many crops. Interactions between plants and aphids happens in parallel or as coevolution, leading to the development of their new relationship, under which aphids must evolve innovative ways to feed and colonize on their hosts, whereas plants must develop novel compounds, express special gene(s) or modify the regulatory mechanisms to defend against aphids. The mechanisms of plant defense against aphids are complicated, highly dynamic, and wide-ranging and involve direct and indirect defenses. Recent studies of plant-aphid interactions by comparing transcriptomic, proteomic, and metabolomic data led to identification of key genes, proteins, and chemical compounds derived from the plant-aphid interactions, which offer new insight into the molecular mechanisms of plant defense against aphids. The Special Issue welcomes papers on various aspects of plant-aphid interactions, particularly on molecular mechanisms.

Dr. Yinghua Huang
Guest Editor

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Keywords

aphids
genetics
host plant defense
defense mechanism
molecular response
phytohormone
plant-aphid interaction
plant immunity
plant resistance

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Published Papers (9 papers)

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Research

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13 pages, 3254 KiB

Open AccessArticle

Seed Coating with Thiamethoxam-Induced Plant Volatiles Mediates the Olfactory Behavior of Sitobion miscanthi

by Jiacong Sun, Yonggang Liu, Shaodan Fei, Yixuan Wang, Jinglong Liu and Haiying Zhang

Insects 2024, 15(10), 810; https://doi.org/10.3390/insects15100810 - 16 Oct 2024

Viewed by 902

Abstract

Pesticides can induce target plants to release odors that are attractive or repellent to their herbivore insects. But, to date, the activity of volatile organic compounds (VOCs), singly or as mixtures, which play a crucial role in the olfactory behavior of herbivore insects, remains unclear. The objective of our research was to investigate the impact of thiamethoxam (TMX), a pesticide, on the emission of odors by wheat plants, and how these odors influence the behavior of grain aphids (Sitobion miscanthi). S. miscanthi showed a greater repellent response to the volatiles emitted by Thx-induced plants compared to those emitted by uncoated plants. Using gas chromatography–mass spectrometry (GCMS), we discovered that TMX greatly induced the release of VOCs in wheat plants. For instance, the levels of Bornyl acetate, 2-Oxepanone, Methyl acrylate, Cyclohexene, α-Pinene, and 1-Nonanol in coated wheat plants were significantly higher as compared to uncoated wheat plants. Moreover, varying concentrations also had an impact on the olfactory behavior of S. miscanthi. For instance, Cyclohexene exhibited clear attractiveness to aphids at concentrations of 100 μL/mL, whereas it displayed evident repellent properties at concentrations of 1 μL/mL and 10 μL/mL. These new findings demonstrate how TMX-induced VOCs affect the behavior of S. miscanthi and could help in developing innovative approaches to manage aphids by manipulating the emission of plant volatiles. Furthermore, these findings can also be utilized to evaluate substances that either attract or repel aphids, with the aim of implementing early monitoring and environmentally friendly methods to manage aphids, while simultaneously impeding the spread of viruses. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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18 pages, 3885 KiB

Open AccessArticle

De Novo Transcriptome Profiling of Mustard Aphid (Lipaphis erysimi) and Differential Expression of Transcripts Associated with Feeding and Non-Feeding Conditions and Developmental Stages

by Rubina Chongtham, Manvi Sharma, Rohit Nandan Shukla, Gopal Joshi, Amar Kumar, Shailendra Goel, Manu Agarwal and Arun Jagannath

Insects 2024, 15(9), 682; https://doi.org/10.3390/insects15090682 - 9 Sep 2024

Viewed by 893

Abstract

Lipaphis erysimi is a specialist aphid of the Indian subcontinent that causes significant yield losses in oilseed Brassicas. Several aphid genes have been used as preferred targets in RNAi-based transgenic plants for aphid resistance. In order to enhance the repertoire of potential target genes for aphid control and to identify the genes associated with aphid feeding and development, we performed a two-way comparative study of differential gene expression profiles between (i) feeding and non-feeding adults and (ii) adult and nymph developmental stages of L. erysimi. De novo RNA-seq of aphids using Illumina technology generated a final transcriptome comprising 52,652 transcripts. Potential transcripts for host selection, detoxification, salivary proteins and effectors, molecular chaperones and developmental genes were identified. Differential gene expression studies identified variations in the expression of 1502 transcripts between feeding and non-feeding adults and 906 transcripts between nymphs and adults. These data were used to identify novel target genes for RNAi-based aphid control and facilitate further studies on the molecular basis of aphid feeding and development. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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14 pages, 1486 KiB

Open AccessArticle

Identification and Evaluation of qRT-PCR Reference Genes in Melanaphis sacchari

by Kunliang Zou, Tonghan Wang, Minghui Guan, Yang Liu, Jieqin Li, Yanlong Liu, Junli Du and Degong Wu

Insects 2024, 15(7), 522; https://doi.org/10.3390/insects15070522 - 11 Jul 2024

Viewed by 817

Abstract

Appropriate reference genes must be selected for accurate qRT-PCR data to conduct a thorough gene expression analysis in the sorghum aphid (Melanaphis sacchari, Hemiptera, Aphididae). This approach will establish a foundation for gene expression analysis and determines the efficacy of RNA interference in the sorghum aphid. Nine potential reference genes, including Actin, 18S, GAPDH, RPL7, EF-1α, EF-1β, 28S, HSP70, and TATA, were assessed under various experimental conditions to gauge their suitability based on qRT-PCR Ct values. The stability of these candidate reference genes in diverse experimental setups was analyzed employing several techniques, including the ΔCt comparative method, geNorm, Normfinder, BestKeeper, and RefFinder. The findings revealed that the quantity of ideal reference genes ascertained by the geNorm method for diverse experimental conditions remained consistent. For the developmental stages of the sorghum aphid, RPL7 and 18S proved to be the most dependable reference genes, whereas GAPDH and EF-1β were recommended as the most stable reference genes for different tissues. In experiments involving wing dimorphism, EF-1α and GAPDH were identified as the optimal reference gene pair. Under varying temperatures, EF-1α and EF-1β were found to be the most dependable gene pair. For studies focusing on insecticide susceptibility, 18S and TATA emerged as the most stable candidate reference genes. Across all experimental conditions, EF-1α and EF-1β was the optimal combination of reference genes in the sorghum aphid. This research has pinpointed stable reference genes that can be utilized across various treatments, thereby enhancing gene expression studies and functional genomics research on the sorghum aphid. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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10 pages, 3052 KiB

Open AccessArticle

Binding Analysis of Sf-SR-C MAM Domain and Sf-FGFR Ectodomain to Vip3Aa

by Chenghai Wang, Min Li, Xiling Chen, Shilong Fan and Jun Lan

Insects 2024, 15(6), 428; https://doi.org/10.3390/insects15060428 - 6 Jun 2024

Viewed by 796

Abstract

Bacillus thuringiensis Vip3Aa has been widely used in transgenic crops to resist the erosion of insects. The Scavenger Receptor-C (SR-C) and Fibroblast Growth Factor Receptor (FGFR) of Spodoptera frugiperda (Sf-SR-C and Sf-FGFR) have formerly been identified as the cell receptors of Vip3Aa. However, the interaction mechanism of Vip3Aa binding to Sf-SR-C or Sf-FGFR is still unknown. Here, we purified the MAM domain of Sf-SR-C (Sf-MAM) and the Sf-FGFR ectodomain expressed extracellularly by Sf9 cells. We then solved the crystal structure of the Sf-MAM domain. Structure docking analysis of the Sf-MAM and Vip3Aa C-terminal domain (CTD) excluded the possibility of the two proteins binding. A further surface plasmon resonance (SPR) assay also revealed that the Sf-MAM and Sf-FGFR ectodomain could not bind to the Vip3Aa protein. Our results have raised the urgency of determining the authentic cell receptor for Vip3Aa. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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12 pages, 1476 KiB

Open AccessEditor’s ChoiceArticle

The Characterization of Melanaphis sacchari Microbiota and Antibiotic Treatment Effect on Insects

by Beatriz Xoconostle-Cázares, José Abrahán Ramírez-Pool, Leandro Alberto Núñez-Muñoz, Berenice Calderón-Pérez, Brenda Yazmín Vargas-Hernández, Rafael Bujanos-Muñiz and Roberto Ruiz-Medrano

Insects 2023, 14(10), 807; https://doi.org/10.3390/insects14100807 - 11 Oct 2023

Cited by 2 | Viewed by 1702

Abstract

Insects are under constant selective pressure, which has resulted in adaptations to novel niches such as crops. This is the case of the pest Melanaphis sacchari, the sugarcane aphid, native to Africa and currently spreading worldwide. The aphid undergoes successful parthenogenesis, causing important damage to a variety of crops and leading to important economic losses for farmers. A natural M. sacchari population grown in sorghum was studied to identify its microbiome through the sequencing of its 16S rDNA metagenome. A high proportion of Proteobacteria, followed by Firmicutes, Bacteroidetes, and Actinobacteria, was observed. We also detected Wolbachia, which correlates with the asexual reproduction of its host. M. sacchari was challenged in a bioassay with the antibiotics oxytetracycline and streptomycin, resulting in a dose-dependent decay of its survival rate. The possibility of controlling this pest by altering its microbiota is proposed. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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15 pages, 1526 KiB

Open AccessArticle

A Method for Identification of Biotype-Specific Salivary Effector Candidates of Aphid

by Duoqi Wang, Qinglan Yang, Xiaoyue Hu, Biao Liu and Yongmo Wang

Insects 2023, 14(9), 760; https://doi.org/10.3390/insects14090760 - 13 Sep 2023

Cited by 4 | Viewed by 1888

Abstract

Polyphagous aphids often consist of host-specialized biotypes that perform poorly in non-native hosts. The underlying mechanisms remain unknown. Host-specialized biotypes may express biotype-specific salivary effectors or elicitors that determine aphid hosts. Here, we tried three strategies to identify possible effectors in Malvaceae- (MA) and Cucurbitaceae-specialized (CU) biotypes of the cotton-melon aphid Aphis gossypii Glover. The whole-aphid RNA-seq identified 765 differentially expressed genes (DEGs), and 139 of them were possible effectors; aphid-head RNA-seq identified 523 DEGs were identified, and 98 of them were possible effectors. The homologous genes of published aphid effectors were not differentially expressed between CU and MA. Next, quantitative proteomic analyses of saliva identified 177 possible proteins, and 44 of them were different proteins. However, none of the genes of the 44 proteins were differentially expressed, reflecting the discrepancy between transcriptome and proteome data. Finally, we searched for DEGs of the 177 salivary proteins in the aphid-head transcriptomes, and the salivary proteins with expression differences were regarded as effector candidates. Through this strategy, 11 effector candidates were identified, and their expression differences were all confirmed by RT-qPCR. The combinatorial analysis has great potential to identify biotype-specific effector candidates in aphids and other sap-sucking insects. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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14 pages, 2674 KiB

Open AccessArticle

Different Tea Germplasms Distinctly Influence the Adaptability of Toxoptera aurantii (Hemiptera: Aphididae)

by Changhao Lu, Ni Shen, Wenbin Jiang, Bi Xie, Runa Zhao, Guolan Zhou, Degang Zhao, Yingqin He and Wenlong Chen

Insects 2023, 14(8), 695; https://doi.org/10.3390/insects14080695 - 7 Aug 2023

Cited by 4 | Viewed by 1351

Abstract

Aphids are typical phloem-sucking insect pests. A good understanding regarding their feeding behavior and population dynamics are critical for evaluating host adaptation and screening of aphid-resistant resources. Herein, the adaptability of Toxoptera aurantii (Boyer) (Hemiptera: Aphididae) to different hosts was evaluated via electropenetrography and an age-stage, two-sex life table on six tea germplasms: Zikui (ZK), Zhongcha108 (ZC108), Zhongcha111 (ZC111), Qianmei419 (QM419), Meitan5 (MT5), and Fudingdabaicha (FD). Our findings revealed that the feeding activities of T. aurantii differed considerably among the host plants. T. aurantii exhibited significantly more pathway activities on ZK and FD than on the other hosts. However, the duration of feeding of T. aurantii on ZK phloem considerably decreased compared with those of the other germplasms. Life parameters indicated that T. aurantii exhibited the highest intrinsic rate of increase (r), net reproductive rate (R₀), and finite rate of increase (λ) on MT5, and the maximum values of total longevity and oviposition period were recorded on FD; these variables were reduced significantly on ZK. The results of our study demonstrate that T. aurantii can successfully survive on the six tea germplasms; however, ZK was less suitable for T. aurantii and should be considered as a potential source of resistance in breeding and Integrated Pest Management. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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16 pages, 3249 KiB

Open AccessArticle

Multifunctionality of Jasmonic Acid Accumulation during Aphid Infestation in Altering the Plant Physiological Traits That Suppress the Plant Defenses in Wheat Cultivar XN979

by Xia Yan, Shicai Xu, Jiao Guo, Jiazhen Hu, Dejia He, Li Jia, Huanzhang Shang, Guangwei Li and Kun Luo

Insects 2023, 14(7), 622; https://doi.org/10.3390/insects14070622 - 11 Jul 2023

Cited by 4 | Viewed by 1510

Abstract

Crop plants have coevolved phytohormone-mediated defenses to combat and/or repel their colonizers. The present study determined the effects of jasmonic acid (JA) accumulation during aphid infestation on the preference and performance of Sitobion miscanthi Takahashi (Hemiptera: Aphididae), and its potential role in fine-tuning hormone-dependent responses in XN979 wheat cultivar seedlings was evaluated via the transcriptional profiles of marker genes related to JA- and salicylic acid (SA)-dependent responses. The preference experiment and the life table data reveal that direct foliage spraying of 2.5 mM methyl jasmonate (MeJA) exhibited weak negative or positive effects on the preferential selection and the population dynamics and oviposition parameters of S. miscanthi. The transcription level of phytohormone biosynthesis genes shows that foliage spraying of MeJA significantly upregulated the marker genes in the JA biosynthesis pathway while downregulating the SA pathway. In addition, either MeJA treatment or previous aphid infestation significantly induced upregulated transcription of the genes involved in the JA- and SA-dependent defense responses, and the transcription level of the tryptophan decarboxylase (TaTDC) gene, which facilitates the conversion of L-tryptophan to tryptamine, was rapidly upregulated after the treatments as well. The main products of tryptamine conversion could play a crucial role in suppressing SA-dependent defense responses. These results will provide more experimental evidence to enable understanding of the antagonistic interaction between hormone signaling processes in cereals under aphid infestation. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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Review

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29 pages, 1406 KiB

Open AccessReview

Molecular Interactions Between Plants and Aphids: Recent Advances and Future Perspectives

by Sunil Kumaraswamy and Yinghua Huang

Insects 2024, 15(12), 935; https://doi.org/10.3390/insects15120935 - 28 Nov 2024

Viewed by 605

Abstract

Aphids are small, notorious insect pests that negatively impact plant health and agricultural productivity through direct damage, such as sap-sucking, and indirectly as vectors of plant viruses. Plants respond to aphid feeding with a variety of molecular mechanisms to mitigate damage. These responses are diverse and highly dynamic, functioning either independently or in combination. Understanding plant–aphid interactions is crucial for revealing the full range of plant defenses against aphids. When aphids infest, plants detect the damage via specific receptor proteins, initiating a signaling cascade that activates defense mechanisms. These defenses include a complex interaction of phytohormones that trigger defense pathways, secondary metabolites that deter aphid feeding and reproduction, lectins and protease inhibitors that disrupt aphid physiology, and elicitors that activate further defense responses. Meanwhile, aphids counteract plant defenses with salivary effectors and proteins that suppress plant defenses, aiding in their successful colonization. This review offers a detailed overview of the molecular mechanisms involved in plant–aphid interactions, emphasizing both established and emerging plant defense strategies. Its uniqueness lies in synthesizing the recent progress made in plant defense responses to aphids, along with aphids’ countermeasures to evade such defenses. By consolidating current knowledge, this review provides key insights for developing sustainable strategies to achieve crop protection and minimize dependence on chemical pesticides. Full article

(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)

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