Next Article in Journal
Oviposition Competition Between Zeugodacus cucurbitae and Bactrocera dorsalis Adults in Five Hosts
Previous Article in Journal
Wolbachia Screening in Aedes aegypti and Culex pipiens Mosquitoes from Madeira Island, Portugal
Previous Article in Special Issue
Potential Involvement of Buchnera aphidicola (Enterobacteriales, Enterobacteriaceae) in Biotype Differentiation of Sitobion avenae (Hemiptera: Aphididae)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 16
Issue 4
10.3390/insects16040417
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Pre-Crop Chemical Control Has No Effects on Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) Endosymbiotic Bacterial Diversity Along an Industrial Maize Management

by
Artúr Botond Csorba
1,*,
Kálmán Szanyi
2,
Szabolcs Szanyi
2,
Gábor Tarcali
2,
Adalbert Balog
1,* and
Antal Nagy
2,*
1
Department of Horticulture, Faculty of Technical and Human Sciences, Sapientia Hungarian University of Transylvania, Aleea Sighișoarei 2, Târgu Mureș, 540485 Corunca, Romania
2
Faculty of the Agricultural and Food Sciences and Environmental Management, Institute of Plant Protection, University of Debrecen, Böszörményi Str. 138, 4032 Debrecen, Hungary
*
Authors to whom correspondence should be addressed.
Insects 2025, 16(4), 417; https://doi.org/10.3390/insects16040417
Submission received: 13 February 2025 / Revised: 20 March 2025 / Accepted: 10 April 2025 / Published: 15 April 2025
(This article belongs to the Special Issue Biology and Molecular Mechanisms of Plant-Aphid Interactions)
Browse Figures
Versions Notes

Simple Summary

In the present study, the endosymbiotic bacterial species diversity was assessed in a conventionally managed maize (Zea mays) field, that represents more than 90% of the Central European maize crops. Because no insecticide treatment is allowed legally in Europe to control corn leaf aphids (Rhopalosiphum maidis) in industrial maize crops, the only method is the assessment of the pre-crop treatment effects on corn leaf aphids endosymbionts that confers adaptation to host. This is also important because in the last five years, the corn leaf aphid population is increasing; therefore, alternative methods must be considered as no treatments before harvest are allowed in accordance with the European Green Deal. In our study, the primary symbionts Buchnera aphidicola as well as a few facultative species (Serratia symbiotica, Wolbachia spp.) dominate corn leaf aphid communities in all sites and between generations. No effect of pre-crop pesticide treatment on endosymbionts was detected.

Abstract

During this research, the corn leaf aphids endosymbiotic bacterial diversity was tested in the same crop systems (monoculture industrial maize as grain for livestock) and the same soil type (Chernozem) when pre-crop pesticide management was used. Bacterial symbionts were analyzed using Illumina systems, and the Silva 16S NR99 V138.2 database was used to assign bacterial taxa on genus and species levels. The presence of the obligate endosymbiont B. aphidicola has been clearly detected in all cases, and in all samples but its abundance varied between samples inside crops, but not between crops and generations. The facultative symbionts S. symbiotica and Wolbachia spp. frequency varied between generations, and increased at generation II; however, differences were not significant. We concluded that the pre-crop pesticide application has no effect on corn leaf aphids bacterial symbionts, so the indirect pesticide application on aphids adaptation is low or nonexistent.

1. Introduction

Aphids (Hemiptera: Aphididae) are one of the most important agricultural pests that cause significant damage due to their feeding on phloem sap, which leads to plant discoloration and deformation. In addition to the direct damage they cause, aphids also serve as vectors for numerous plant viruses of considerable economic importance [1,2].
The management of aphid populations has traditionally been reliant on the application of various classes of insecticides, including pyrethroids, neonicotinoids, carbamates, and organophosphates [3,4]. However, the persistent and widespread use of these chemical control measures over several decades has led to the emergence of resistance in aphid populations, rendering them less susceptible to many of the commonly used insecticidal classes [5,6,7].
The impact of the organophosphorus insecticide, fenitrothion (abbreviated as MEP), on the microbial communities within soils, both with and without a history of insecticide application was examined. The findings indicate that the application of MEP did not result in a significant alteration to the total bacterial population in the soil. However, it was observed to cause a notable reduction in microbial diversity [8]. Furthermore, the application of MEP led to a substantial increase in the relative abundance of MEP-degrading bacteria, particularly those belonging to the genus Burkholderia, an endosymbiotic microorganism capable of being acquired from the soil [8,9].
In another study, the bacterial communities present within Aphis gossypii, functioning as intracellular symbionts, were analyzed in both naturally occurring and pesticide-treated populations. The results revealed that the composition of the bacterial communities remained stable across all four pesticide-treated samples and most pesticides indicated no influence on the composition of bacterial communities [10].
In the case of fungicide application, the existing hypotheses suggest that certain fungicides possessing antibacterial properties may suppress bacterial endosymbionts within aphids, which play a crucial role in their survival. A study conducted by Evatt Chirgwin et al. [11] investigated this phenomenon and found that the fungicide chlorothalonil did not exert an immediate effect on aphid survival. However, both strobilurin-based fungicides, pyraclostrobin and trifloxystrobin, led to a reduction in aphid survival following 48 h of exposure. Additionally, trifloxystrobin was observed to negatively impact the lifespan and reproductive output of the F1 generation, whereas pyraclostrobin did not exhibit similar effects on these parameters. Despite these findings, none of the fungicides tested were found to consistently influence the population density of the bacterial endosymbionts Buchnera or Rickettsiella within whole aphid specimens [11].
Previous studies investigating the application of herbicides have emphasized that oxyfluorfen exhibits high persistence and limited mobility in soil. The estimated half-life of oxyfluorfen in soil ranges from 30 to 103 days, depending on the applied dosage and varying levels of precipitation [12]. Given its moderate to high persistence in soil, the potential for environmental contamination with oxyfluorfen is notably increased [13]. Furthermore, recent findings demonstrated that glyphosate treatment led to a significant reduction in the abundance and gene copy number of Staphylococcus, while concurrently increasing the abundance and gene copy number of Enterobacter in Harmonia axyridis [14].
Studies have provided evidence suggesting that symbiotic bacteria (both primary and secondary) may play a significant role in pesticide resistance, primarily due to their capacity to degrade or detoxify various pesticides [15,16]. Riportus pedestris has developed resistance to fenitrothion through its symbiont Burkholderia [16], while Plutella xylostella has been shown to degrade indoxacarb with the assistance of Bacillus cereus [17]. In the case of Bactrocera dorsalis, the gut symbiont Citrobacter plays a key role in the degradation of trichlorfon [15]. Moreover, an increased abundance of Rickettsia symbionts in Bemisia tabaci, coupled with a reduced presence of Porteira and Hamiltonella, is correlated with enhanced resistance to thiomethoxam [18].
In aphid populations, exposure to pesticides has been shown to influence the composition of the associated bacterial communities. However, the precise role that these bacterial communities may have in facilitating pesticide resistance remains an area that requires further investigation and a deeper understanding [10].
In the case of Aphis gossypii, it has been demonstrated that the yellow morphs of the melon aphid, exhibit significantly higher levels of resistance to commonly used pesticides such as imidacloprid and sulfoxaflor, when compared to the green morphs. The yellow morphs had a higher density of primary symbiont Buchnera compared to the green morphs, which can describe a possible relationship between the density of symbiont and pesticide resistance. No significant difference in resistance was observed between the two morphs when exposed to the pesticide avermectin [19].
Facultative (or secondary) symbionts, such as S. symbiotica, H. defensa, R. insecticola, Spiroplasma, and Rickettsia, can have a detrimental impact on aphid survival and reproduction. However, the extent of this effect appears to be contingent upon both the specific strain of the host and symbiont, as well as the presence or absence of stress factors [20,21]. It has been revealed that aphid lines positive for Serratia species were notably more susceptible to insecticide exposure compared to their non-infected counterparts which can be associated with the above-mentioned trade-off [22].
A study investigating the susceptibility of aphids to various insecticides revealed that Sitobion miscanthi, harboring Hamiltonella defensa exhibited an increased vulnerability to lower concentrations of insecticide, in contrast to their uninfected counterparts [23]. Sphingomonas, known for its detoxification capabilities, may present a potential mechanism by which insect pests can metabolize imidacloprid, was demonstrated in this study [24]. Wolbachia and Rickettsia, both prevalent facultative symbionts in insects, are not only implicated in phenomena such as male killing and parthenogenesis, but they have also been linked to the development of insecticide resistance [25,26]. In the case of the pea aphid, Acyrthosiphon pisum, the presence of Rickettsia was found to exert influence on several key components of host fitness, including aspects such as body weight and fecundity [27]. In Serratia species, it has been observed that these bacteria may harbor plasmids encoding specific enzymes, such as hydrolases, which are believed to be directly involved in the degradation of insecticides [28,29].
The goal of this study was to test the corn leaf aphids endosymbiotic bacterial diversity in the same crop systems (monoculture industrial maize as grain for livestock) and same soil type (Chernozem) when only the pre-crop management differed and used as control. These types of fields represent more than 90% of the Central European maize crops. No previous analyses were made in order to test aphid symbionts under a conventionally management regime, where the pre-crop fields were treated with pesticides. Because no insecticide treatment is allowed legally in Europe to control corn leaf aphids in industrial maize crops, the only methods are to assess the pre-crop (pea in our case) treatment effects on corn leaf aphids endosymbionts.

2. Materials and Methods

2.1. Study Area and Sampling Methods of Corn Leaf Aphids

Maize is the largest cash crop in Europe and Hungary. The average corn yield in 2020 was approximately 8.5 million tons and the area dedicated to corn cultivation fluctuated between 778,000 and 906,000 hectares from 2022 to 2024 [30]. In our study, a comprehensive open field aphid assessment and sampling were performed during a 2024 vegetation period, in Eastern and Central Hungary, using four maize fields, all managed under an intensive regime where grain for livestock was produced. The soil type Chernozem was also similar in all fields (Figure 1). From four fields, three (D-A-S2, D-A-S3, D-A-S4) were monoculture for 3–4 years, and one field (D-A-S1) was used as control, where pea was the previous year’s culture and herbicide and insecticide treatments were used during the whole year of production (Table 1).
Inside each of the four fields, two smaller similar plots were defined and sampled. Aphids were collected from maize plants inside these smaller plots to minimize the possible effects of field margins, and the same method of sampling was used in all sites. Apterous viviparous females were searched for inside the colonies, choosing ten maize plants per smaller plot. Inside each colony, the adult and the first instar aphid nymphs (five individuals/plant) were collected and stored in 0.5 mL Eppendorf tubes containing 99% ethanol prior to DNA analysis. The first sampling data were collected on 25 June 2024 and the second on 10 August 2024. In this way, two generations were sampled and analyzed.

2.2. Bacterial Symbionts Identification and Bioinformatics Assessments

Aphids bacterial symbionts were analyzed using Illumina systems. From each sample, both adults and the first instar larvae were separately analyzed. In this way, we were able to obtain symbionts from two generations (D1, D2). Illumina PE reads trimmed with cutadapt V3.5 [31]. Untrimmed reads were discarded from the analysis. Sequence level error estimation, filtering, merging, and taxonomy assignment were completed with DADA2 workflow V1.22 [32]. Silva 16S NR99 V138.2 database was used to assign taxa on the species level [33].

2.3. Data Analyses

The community composition of the most frequent bacterial symbionts for each aphid colony and site was analyzed by sites and generations (D1, D2) separately. Charts generated with phyloseq V1.38 [34] and polished with ggplot2 V3.5.1 [35] were made and analyzed, and graphical presentation were completed in an R V4.1.2 environment [36]. Alignment of all bacterial genetic sequences was performed using ClustalW, and the results were visualized in EMPeror [37]. Bacterial symbionts frequency (the most dominant 10 taxa) were presented as bar charts. Non-metric multidimensional scaling (NMDS) based on Chao1, Shannon and Simpson diversity were then performed and presented as boxplots. This was performed to compare symbionts diversity by sites and by generations. PERMANOVA analysis of the sample diversities between the groups (sites and generations) was performed in an R V4.1.2 environment [36].
Principal component analyses (PCoA) were used to test the effect of sites and generations on bacterial symbionts abundances for each maize field, where locations (sites) and generations were considered as main components and endosymbiont species diversity as variables. Data analyses and visualization were made using the computer program PAST 4.02. (https://past.en.lo4d.com/windows, accessed on 25 January 2025).

3. Results

A high infestation rate of all maize fields with corn leaf aphids was detected during the period of June and August. In certain cases the infestation was 100%, which means that each maize plant had at least one relatively high aphid colony (Figure 1).
All sites and samples were dominated by the obligate endosymbiont B. aphidicola, this was followed by S. symbiotica; however, both Buchnera and Serratia frequency and diversity varied between sites and generations (Figure 2A and Figure 3A). The third most frequent symbiont was the Wolbachia spp., its frequency and diversity also varied between sites and generations. The facultative symbiont H. defensa was only present in site 2, while other bacterial taxa frequency (non-symbionts) such as Acinetobacter, Klebsiella, and Pantoea were also higher in some plots and samples (Figure 2A and Figure 3A). Alpha diversity analyses of endosymbionts did not show significant differences between sites nor between generations (Figure 2B and Figure 3B).
Principal component analyses revealed that sites and generations had low effects on corn leaf aphid bacterial symbionts distributions, and the endosymbiont species diversity as variables determined more than 70% of their distributions (Figure 4A,B).
Permanova analysis of the sample diversities between sites (DS1–DS4) and generations (D1 and D2) did not revealed significant differences (Table 2 and Table 3).

4. Discussion

In the present study, the population density and diversity of the endosymbiotic bacterial species were assessed in a conventionally managed maize field. These types of fields represent more than 90% of the Central European maize crops. No previous analyses were made in order to test aphid symbionts under a conventionally management regime, where the pre-crop fields were treated with pesticides. Because no insecticide treatment is allowed legally in Europe to control corn leaf aphids in industrial maize crops, the only methods were to assess the pre-crop (pea in our case) treatment effects on corn leaf aphids endosymbionts.
As previous studies mentioned that bacterial endosymbionts are responsible for adaptation, it remains unclear if pesticide applications (even if these are indirect treatments) might or might not have effects on aphids’ population diversity. This question is also important because in the last five years, the corn leaf aphid population has been increasing all over in Europe, and no insecticide application has been made or is under consideration in the EU. It can also be mentioned that in the case of further expansion of this species, alternative methods must be considered as no treatments before harvest will be allowed in accordance with the European Green Deal. In our concrete cases, the primary symbionts Buchnera as well as a few facultative species (Serratia, Wolbachia) dominate corn leaf aphid communities in all sites and between generations.
The presence of the obligate endosymbiont B. aphidicola has been clearly detected in all cases, but its abundance varied between samples inside crops, but not between crops and generations. This abundance can be explained because this obligate endosymbiont is required for the survival of aphids and provides essential amino acids that are rare in their phloem sap diet [38].
Other similar studies have also revealed that other novel symbiont can be inherited in aphids body, that physically replace B. aphidicola (here in Geopemphigus genus), the host may acquire additional symbiont species to adequately provided the essential functions, or even replace the old symbionts with new ones [39]. This change in endosymbionts was previously observed within the tribe Cerataphidini (subfamily Hormaphidinae) [40,41].
The other dominant symbiont was the S. symbiotica, which is well known to be involved in defense against heat and potentially in aphid nutrition. In our study, S. symbiotica was present in all sites, both in treated and untreated; however, its frequency highly varied between generations, in generation 1 (D1) from 10 samples only five times were present, and two times in higher abundances, while in generation 2 (D2) from 10 samples nine times were detected, from which seven times in higher abundances. Previous studies also reported that S. symbiotica protected pea aphids, A. pisum, from heat stress (in both directions) by regulating the aphid metabolome [42]. In our cases the high frequency in generation 2, during the summer period can be an explanation, that S. symbiotica indeed conferred adaptation against heat stress, this was clearly detected in aphids new generation abundances during July and August.
The facultative endosymbiont Wolbachia spp. was also present in all sites but also in higher frequency in generation 2 (D2). The presence of Wolbachia spp. was first reported by Gómez-Valero et al. (2004) in cedar bark aphid (Cinara cedri cedri Mimeur, 1936) [43], and it was also detected that Wolbachia increased the prevalence of asexual lineages in the aphids. It was also demonstrated that Wolbachia spp. can protect aphids (and other arthropods) against fungal pathogens and abiotic stress factors (extreme heat and cold) [44]. Our previous research testing corn leaf aphids symbionts diversity under different climate conditions also revealed that Wolbachia spp. was not only present in large-scale field corn crops under warm climates but also under colder conditions, which clearly demonstrates that Wolbachia has an important role in the thermal adaptation of corn leaf aphid (authors paper under review).
The endosymbiont Hemiltonella defensa, was also detected, but only in one field and in two samples, its role is to protect aphid hosts from parasitoid wasps (in our cases probably against Aphidius ervi) and minimizes aphid mortality due to parasitoid attack [45]. It was also demonstrated that the parasitoid wasp A. ervi is less attracted to plants infested with aphids harboring H. defensa [46].

5. Conclusions

In conclusion, we demonstrate for the first time that along a large geographic area and cropping system, the pre-crop pesticide application has no effect on corn leaf aphids bacterial symbionts, so the indirect pesticide application on aphids adaptation is low or inexistent. Earlier studies have demonstrated that several other as fertilizer input, winter temperature, tillage systems but also biodiversity changes as well as different soil management and environmental factors could also influence the expansion of aphids.
As no directed insecticide control as yet exists and is allowed in European maize fields against corn leaf aphids, whereas more than ten synthetic pesticides are available in the USA to combat this pest, before using these compounds (which are all neurotoxins), the effect of symbionts on the distribution and abundance of this aphid species should be considered.

Author Contributions

Conceptualization, A.B.C., A.B., A.N., S.S., K.S. and G.T.; methodology, A.B.C., A.B., A.N., S.S. and K.S.; software, A.B.C., A.B., A.N., S.S. and K.S.; validation, A.B.C., A.B., A.N., S.S., K.S. and G.T.; formal analysis, A.B.C. and A.B.; investigation, A.B., S.S. and A.N.; resources, A.B. and A.N.; data curation, A.B.C. and A.B.; writing—original draft preparation, A.B.C., A.B., A.N., S.S., G.T. and K.S.; writing—review and editing, A.B.C., A.B., A.N., G.T. and S.S.; visualization, A.B.C. and A.B.; supervision, A.B.C. and A.B.; project administration, A.B.; funding acquisition, A.B. All authors have read and agreed to the published version of the manuscript.

Funding

The work was founded by the UEFISCDI Romania, project PN-III-P4-PCE-2021-0543.

Data Availability Statement

The datasets used and/or analyzed during the current study available at figshare: https://figshare.com/articles/dataset/Corn_Leaf_aphid_symbionts_genetic_analyses/25027973, accessed on 31 January 2025.

Acknowledgments

The authors are grateful to all farm managers who helped in the various scientific assessments and supported our field research. Supported by the University of Debrecen Scientific Research Bridging Fund (DETKA) and University of Debrecen Program for Scientific Publication.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. James, C.K.N.; Perry, K.L. Transmission of Plant Viruses by Aphid Vectors. Mol. Plant Pathol. 2004, 5, 505–511. [Google Scholar] [CrossRef]
  2. Stevens, M.; Lacomme, C. Transmission of Plant Viruses. In Aphids as Crop Pests; van Emden, H.F., Harrington, R., Eds.; CABI: Wallingford, UK, 2017; pp. 323–361. [Google Scholar]
  3. Bass, C.; Puinean, A.M.; Zimmer, C.T.; Denholm, I.; Field, L.M.; Foster, S.P.; Gutbrod, O.; Nauen, R.; Slater, R.; Williamson, M.S. The Evolution of Insecticide Resistance in the Peach Potato Aphid, Myzus persicae. Insect Biochem. Mol. Biol. 2014, 51, 41–51. [Google Scholar] [CrossRef]
  4. Geiger, F.; Bengtsson, J.; Berendse, F.; Weisser, W.W.; Emmerson, M.; Morales, M.B.; Ceryngier, P.; Liira, J.; Tscharntke, T.; Winqvist, C.; et al. Persistent Negative Effects of Pesticides on Biodiversity and Biological Control Potential on European Farmland. Basic. Appl. Ecol. 2010, 11, 97–105. [Google Scholar] [CrossRef]
  5. Bass, C.; Denholm, I.; Williamson, M.S.; Nauen, R. The Global Status of Insect Resistance to Neonicotinoid Insecticides. Pestic. Biochem. Physiol. 2015, 121, 78–87. [Google Scholar] [CrossRef]
  6. Herron, G.A.; Wilson, L.J. Can Resistance Management Strategies Recover Insecticide Susceptibility in Pests?: A Case Study with Cotton Aphid Aphis gossypii (Aphididae: Hemiptera) in Australian Cotton: Resistance Management of Aphis gossypii. Austral Entomol. 2017, 56, 1–13. [Google Scholar] [CrossRef]
  7. Sparks, T.C.; Nauen, R. IRAC: Mode of Action Classification and Insecticide Resistance Management. Pestic. Biochem. Physiol. 2015, 121, 122–128. [Google Scholar] [CrossRef]
  8. Itoh, H.; Navarro, R.; Takeshita, K.; Tago, K.; Hayatsu, M.; Hori, T.; Kikuchi, Y. Bacterial Population Succession and Adaptation Affected by Insecticide Application and Soil Spraying History. Front. Microbiol. 2014, 5, 457. [Google Scholar] [CrossRef]
  9. Kim, J.-Y.; Jung, M.; Lee, D.-H. Characterization of Burkholderia Bacteria Clade Compositions in Soil and Riptortus pedestris (Hemiptera: Alydidae) in South Korea. J. Asia-Pac. Entomol. 2022, 25, 101976. [Google Scholar] [CrossRef]
  10. Zhang, S.; Luo, J.; Wang, L.; Zhang, L.; Zhu, X.; Jiang, W.; Cui, J. Bacterial Communities in Natural versus Pesticide-Treated Aphis gossypii Populations in North China. Microbiologyopen 2019, 8, e00652. [Google Scholar] [CrossRef]
  11. Chirgwin, E.; Yang, Q.; Umina, P.A.; Gill, A.; Soleimannejad, S.; Gu, X.; Ross, P.; Hoffmann, A.A. Fungicides Have Transgenerational Effects on Rhopalosiphum padi but Not Their Endosymbionts. Pest Manag. Sci. 2022, 78, 4709–4718. [Google Scholar] [CrossRef]
  12. Frank, R.; Stephen Clegg, B.; Ritcey, G. Disappearance of Oxyfluorfen (Goal) from Onions and Organic Soils. Bull. Environ. Contam. Toxicol. 1991, 46, 485–491. [Google Scholar] [CrossRef]
  13. Yen, J.-H.; Sheu, W.-S.; Wang, Y.-S. Dissipation of the Herbicide Oxyfluorfen in Subtropical Soils and Its Potential to Contaminate Groundwater. Ecotoxicol. Environ. Saf. 2003, 54, 151–156. [Google Scholar] [CrossRef]
  14. Gao, X.; Hu, F.; Zhang, S.; Luo, J.; Zhu, X.; Wang, L.; Zhang, K.; Li, D.; Ji, J.; Niu, L.; et al. Glyphosate Exposure Disturbs the Bacterial Endosymbiont Community and Reduces Body Weight of the Predatory Ladybird Beetle Harmonia axyridis (Coleoptera: Coccinellidae). Sci. Total Environ. 2021, 790, 147847. [Google Scholar] [CrossRef]
  15. Cheng, D.; Guo, Z.; Riegler, M.; Xi, Z.; Liang, G.; Xu, Y. Gut Symbiont Enhances Insecticide Resistance in a Significant Pest, the Oriental Fruit Fly Bactrocera dorsalis (Hendel). Microbiome 2017, 5, 13. [Google Scholar] [CrossRef]
  16. Kikuchi, Y.; Hayatsu, M.; Hosokawa, T.; Nagayama, A.; Tago, K.; Fukatsu, T. Symbiont-Mediated Insecticide Resistance. Proc. Natl. Acad. Sci. USA 2012, 109, 8618–8622. [Google Scholar] [CrossRef]
  17. Ramya, S.L.; Venkatesan, T.; Srinivasa Murthy, K.; Jalali, S.K.; Verghese, A. Detection of Carboxylesterase and Esterase Activity in Culturable Gut Bacterial Flora Isolated from Diamondback Moth, Plutella xylostella (Linnaeus), from India and Its Possible Role in Indoxacarb Degradation. Braz. J. Microbiol. 2016, 47, 327–336. [Google Scholar] [CrossRef]
  18. Pan, H.P.; Chu, D.; Liu, B.M.; Xie, W.; Wang, S.L.; Wu, Q.J.; Xu, B.Y.; Zhang, Y.J. Relative Amount of Symbionts in Insect Hosts Changes with Host-Plant Adaptation and Insecticide Resistance. Environ. Entomol. 2013, 42, 74–78. [Google Scholar] [CrossRef]
  19. Guo, S.-K.; Gong, Y.-J.; Chen, J.-C.; Shi, P.; Cao, L.-J.; Yang, Q.; Hoffmann, A.A.; Wei, S.-J. Increased Density of Endosymbiotic Buchnera Related to Pesticide Resistance in Yellow Morph of Melon Aphid. J. Pest. Sci. 2020, 93, 1281–1294. [Google Scholar] [CrossRef]
  20. Laughton, A.M.; Fan, M.H.; Gerardo, N.M. The Combined Effects of Bacterial Symbionts and Aging on Life History Traits in the Pea Aphid, Acyrthosiphon pisum. Appl. Environ. Microbiol. 2014, 80, 470–477. [Google Scholar] [CrossRef]
  21. Simon, J.-C.; Boutin, S.; Tsuchida, T.; Koga, R.; Le Gallic, J.-F.; Frantz, A.; Outreman, Y.; Fukatsu, T. Facultative Symbiont Infections Affect Aphid Reproduction. PLoS ONE 2011, 6, e21831. [Google Scholar] [CrossRef]
  22. Skaljac, M.; Kirfel, P.; Grotmann, J.; Vilcinskas, A. Fitness Costs of Infection with Serratia symbiotica Are Associated with Greater Susceptibility to Insecticides in the Pea Aphid Acyrthosiphon pisum: Serratia symbiotica Correlates with Susceptibility to Insecticides in Pea Aphid. Pest Manag. Sci. 2018, 74, 1829–1836. [Google Scholar] [CrossRef]
  23. Li, Q.; Sun, J.; Qin, Y.; Fan, J.; Zhang, Y.; Tan, X.; Hou, M.; Chen, J. Reduced Insecticide Susceptibility of the Wheat Aphid Sitobion miscanthi after Infection by the Secondary Bacterial Symbiont Hamiltonella Defensa. Pest Manag. Sci. 2021, 77, 1936–1944. [Google Scholar] [CrossRef]
  24. Lv, N.; Li, R.; Cheng, S.; Zhang, L.; Liang, P.; Gao, X. The Gut Symbiont Sphingomonas Mediates Imidacloprid Resistance in the Important Agricultural Insect Pest Aphis gossypii Glover. BMC Biol. 2023, 21, 86. [Google Scholar] [CrossRef]
  25. Hagimori, T.; Abe, Y.; Date, S.; Miura, K. The First Finding of a Rickettsia Bacterium Associated with Parthenogenesis Induction Among Insects. Curr. Microbiol. 2006, 52, 97–101. [Google Scholar] [CrossRef]
  26. Kontsedalov, S.; Zchori-Fein, E.; Chiel, E.; Gottlieb, Y.; Inbar, M.; Ghanim, M. The Presence of Rickettsia is Associated with Increased Susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to Insecticides. Pest Manag. Sci. 2008, 64, 789–792. [Google Scholar] [CrossRef]
  27. Sakurai, M.; Koga, R.; Tsuchida, T.; Meng, X.-Y.; Fukatsu, T. Rickettsia Symbiont in the Pea Aphid Acyrthosiphon pisum: Novel Cellular Tropism, Effect on Host Fitness, and Interaction with the Essential Symbiont Buchnera. Appl. Environ. Microbiol. 2005, 71, 4069–4075. [Google Scholar] [CrossRef]
  28. Singh, B.K. Organophosphorus-Degrading Bacteria: Ecology and Industrial Applications. Nat. Rev. Microbiol. 2009, 7, 156–164. [Google Scholar] [CrossRef]
  29. Pakala, S.B.; Gorla, P.; Pinjari, A.B.; Krovidi, R.K.; Baru, R.; Yanamandra, M.; Merrick, M.; Siddavattam, D. Biodegradation of Methyl Parathion and P-Nitrophenol: Evidence for the Presence of a p-Nitrophenol 2-Hydroxylase in a Gram-Negative Serratia sp. Strain DS001. Appl. Microbiol. Biotechnol. 2007, 73, 1452–1462. [Google Scholar] [CrossRef]
  30. FAOStat. Available online: https://www.fao.org/faostat/en/#compare (accessed on 26 July 2022).
  31. Martin, M. Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads. EMBnet J. 2011, 17, 10. [Google Scholar] [CrossRef]
  32. Callahan, B.J.; McMurdie, P.J.; Rosen, M.J.; Han, A.W.; Johnson, A.J.A.; Holmes, S.P. DADA2: High-Resolution Sample Inference from Illumina Amplicon Data. Nat. Methods 2016, 13, 581–583. [Google Scholar] [CrossRef]
  33. Quast, C.; Pruesse, E.; Yilmaz, P.; Gerken, J.; Schweer, T.; Yarza, P.; Peplies, J.; Glöckner, F.O. The SILVA Ribosomal RNA Gene Database Project: Improved Data Processing and Web-Based Tools. Nucleic Acids Res. 2012, 41, D590–D596. [Google Scholar] [CrossRef] [PubMed]
  34. McMurdie, P.J.; Holmes, S. Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE 2013, 8, e61217. [Google Scholar] [CrossRef]
  35. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Use R!), 2nd ed.; Springer International Publishing: Cham, Switzerland, 2016; ISBN 978-3-319-24275-0. [Google Scholar]
  36. R Core Team. R: A Language and Environment for Statistical Computing [Computer Software]; R Foundation for Statistical Computing: Vienna, Austria, 2021. [Google Scholar]
  37. Vázquez-Baeza, Y.; Pirrung, M.; Gonzalez, A.; Knight, R. EMPeror: A Tool for Visualizing High-Throughput Microbial Community Data. Gigascience 2013, 2, 2047-217X-2-16. [Google Scholar] [CrossRef]
  38. Shigenobu, S.; Watanabe, H.; Hattori, M.; Sakaki, Y.; Ishikawa, H. Genome Sequence of the Endocellular Bacterial Symbiont of Aphids buchnera sp. APS. Nature 2000, 407, 81–86. [Google Scholar] [CrossRef]
  39. Chong, R.A.; Moran, N.A. Evolutionary Loss and Replacement of Buchnera, the Obligate Endosymbiont of Aphids. ISME J. 2018, 12, 898–908. [Google Scholar] [CrossRef]
  40. Nováková, E.; Hypša, V.; Klein, J.; Foottit, R.G.; von Dohlen, C.D.; Moran, N.A. Reconstructing the Phylogeny of Aphids (Hemiptera: Aphididae) Using DNA of the Obligate Symbiont Buchnera aphidicola. Mol. Phylogenet Evol. 2013, 68, 42–54. [Google Scholar] [CrossRef]
  41. Wegierek, P.; Michalik, A.; Wieczorek, K.; Kanturski, M.; Kobiałka, M.; Śliwa, K.; Szklarzewicz, T. Buchnera aphidicola of the Birch Blister Aphid, Hamamelistes betulinus (Horváth, 1896) (Insecta, Hemiptera, Aphididae: Hormaphidinae): Molecular Characterization, Transmission between Generations and Its Geographic Significance. Acta Zoologica 2017, 98, 412–421. [Google Scholar] [CrossRef]
  42. Xu, S.; Chen, J.; Qin, M.; Jiang, L.; Qiao, G. Geography-Dependent Symbiont Communities in Two Oligophagous Aphid Species. FEMS Microbiol. Ecol. 2021, 97, fiab132. [Google Scholar] [CrossRef]
  43. Gómez-Valero, L.; Soriano-Navarro, M.; Pérez-Brocal, V.; Heddi, A.; Moya, A.; García-Verdugo, J.M.; Latorre, A. Coexistence of Wolbachia with Buchnera aphidicola and a Secondary Symbiont in the Aphid Cinara cedri. J. Bacteriol. 2004, 186, 6626–6633. [Google Scholar] [CrossRef]
  44. Iturbe-Ormaetxe, I.; Walker, T.; O’Neill, S.L. Wolbachia and the Biological Control of Mosquito-borne Disease. EMBO Rep. 2011, 12, 508–518. [Google Scholar] [CrossRef]
  45. Rothacher, L.; Ferrer-Suay, M.; Vorburger, C. Bacterial Endosymbionts Protect Aphids in the Field and Alter Parasitoid Community Composition. Ecology 2016, 97, 1712–1723. [Google Scholar] [CrossRef]
  46. Frago, E.; Mala, M.; Weldegergis, B.T.; Yang, C.; McLean, A.; Godfray, H.C.J.; Gols, R.; Dicke, M. Symbionts Protect Aphids from Parasitic Wasps by Attenuating Herbivore-Induced Plant Volatiles. Nat. Commun. 2017, 8, 1860. [Google Scholar] [CrossRef]
Insects 16 00417 g001
Figure 1. Field collection and genetic analyses of corn leaf aphids under conventionally managed maize fields.
Figure 1. Field collection and genetic analyses of corn leaf aphids under conventionally managed maize fields.
Insects 16 00417 g001
Insects 16 00417 g002
Figure 2. The community composition of the most frequent bacterial symbionts for each aphid colony inside the sites (A) and alpha diversity analyses by sites (B).
Figure 2. The community composition of the most frequent bacterial symbionts for each aphid colony inside the sites (A) and alpha diversity analyses by sites (B).
Insects 16 00417 g002
Insects 16 00417 g003
Figure 3. The community composition of the most frequent bacterial symbionts for each aphid colony between generations (A) and alpha diversity analyses by generations (B).
Figure 3. The community composition of the most frequent bacterial symbionts for each aphid colony between generations (A) and alpha diversity analyses by generations (B).
Insects 16 00417 g003
Insects 16 00417 g004
Figure 4. Principal component analyses (PCoA) by sites (A) and generations (B), where locations (sites) and generations were considered as the main components and endosymbiont species diversity as variables.
Figure 4. Principal component analyses (PCoA) by sites (A) and generations (B), where locations (sites) and generations were considered as the main components and endosymbiont species diversity as variables.
Insects 16 00417 g004
Table 1. Different treatments used in the experiment.
Table 1. Different treatments used in the experiment.
Commercial NameActive IngredientDosageTime
Basagran 480 SLbentazone 480 g/L2 L/ha3 May 2023
Tropotox XTMCPB 400 g/L2 L/ha3 May 2023
Judolambda-cyhalothrin 5 g/L and pirimicarb 100 g/L1.2 L/ha15 May 2023
Amistar SCazoxystrobin 250 g/L1 L/ha20 May 2023
Adengo 465 SCizoxaflutole 225 g/L, thiencarbazone-methyl 90 g/L and cyprosulfamide 150 g/L0.4 L/ha22 April 2024
Table 2. PERMANOVA analysis of the sample diversities between Groups DS1 and DS2 (A), Groups DS1 and DS3 (B), Groups DS1 and DS4 (C), Groups DS2 and DS3 (D), Groups DS2 and DS4 (E) and Groups DS3 and DS4 (F), in a site sample feature.
Table 2. PERMANOVA analysis of the sample diversities between Groups DS1 and DS2 (A), Groups DS1 and DS3 (B), Groups DS1 and DS4 (C), Groups DS2 and DS3 (D), Groups DS2 and DS4 (E) and Groups DS3 and DS4 (F), in a site sample feature.
ADfSumsOfSqsMeanSqsF.ModelR2Pr(>F)
Soil Type10.180.180.560.050.41
Residuals103.170.31NA0.94NA
Total113.36NANA1.00NA
BDfSumsOfSqsMeanSqsF.ModelR2Pr(>F)
Soil Type10.130.130.430.050.60
Residuals82.460.30NA0.94NA
Total92.60NANA1.00NA
CDfSumsOfSqsMeanSqsF.ModelR2Pr(>F)
Soil Type10.290.290.870.090.38
Residuals82.670.33NA0.90NA
Total92.96NANA1.00NA
DDfSumsOfSqsMeanSqsF.ModelR2Pr(>F)
Soil Type10.050.050.150.010.89
Residuals82.700.33NA0.98NA
Total92.75NANA1.00NA
EDfSumsOfSqsMeanSqsF.ModelR2Pr(>F)
Soil Type10.160.160.450.050.63
Residuals82.900.36NA0.94NA
Total93.07NANA1.00NA
FDfSumsOfSqsMeanSqsF.ModelR2Pr(>F)
Soil Type10.200.200.540.080.52
Residuals62.190.36NA0.91NA
Total72.39NANA1.00NA
Table 3. PERMANOVA analysis of the sample diversities between generations D1 and D2 in a time sample feature.
Table 3. PERMANOVA analysis of the sample diversities between generations D1 and D2 in a time sample feature.
DfSumsOfSqsMeanSqsF.ModelR2Pr(>F)
Time11.091.094.130.180.02
Residuals184.780.26NA0.81NA
Total195.88NANA1.00NA
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Csorba, A.B.; Szanyi, K.; Szanyi, S.; Tarcali, G.; Balog, A.; Nagy, A. Pre-Crop Chemical Control Has No Effects on Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) Endosymbiotic Bacterial Diversity Along an Industrial Maize Management. Insects 2025, 16, 417. https://doi.org/10.3390/insects16040417

AMA Style

Csorba AB, Szanyi K, Szanyi S, Tarcali G, Balog A, Nagy A. Pre-Crop Chemical Control Has No Effects on Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) Endosymbiotic Bacterial Diversity Along an Industrial Maize Management. Insects. 2025; 16(4):417. https://doi.org/10.3390/insects16040417

Chicago/Turabian Style

Csorba, Artúr Botond, Kálmán Szanyi, Szabolcs Szanyi, Gábor Tarcali, Adalbert Balog, and Antal Nagy. 2025. "Pre-Crop Chemical Control Has No Effects on Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) Endosymbiotic Bacterial Diversity Along an Industrial Maize Management" Insects 16, no. 4: 417. https://doi.org/10.3390/insects16040417

APA Style

Csorba, A. B., Szanyi, K., Szanyi, S., Tarcali, G., Balog, A., & Nagy, A. (2025). Pre-Crop Chemical Control Has No Effects on Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) Endosymbiotic Bacterial Diversity Along an Industrial Maize Management. Insects, 16(4), 417. https://doi.org/10.3390/insects16040417

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop