Field-Evolved Sulfoxaflor Resistance of Three Wheat Aphid Species in China

Sulfoxaflor belongs to a new class of insecticides which are effective against many sap-feeding pests. Sitobion miscanthi, Rhopalosiphum padi, and Metopolophium dirhodum are the predominant pests coexisting on wheat plants. It is unknown whether these aphid species have developed resistance to sulfoxaflor. Here, the susceptibilities of three wheat aphid species from different regions of China to sulfoxaflor were evaluated. The results showed that two S. miscanthi, one R. padi, and two M. dirhodum field populations were highly resistant to sulfoxaflor. Additionally, 13 S. miscanthi, 9 R. padi, and 4 M. dirhodum field populations were moderately resistant to sulfoxaflor. Analysis of differences in toxicity showed that the susceptibility levels of R. padi in 9 of 20 regions, M. dirhodum in 5 of 9 regions, and M. dirhodum in 3 of 9 regions to sulfoxaflor were greater than those of S. miscanthi, S. miscanthi, and R. padi in the same regions, respectively. Thus, each wheat aphid species has field populations that are highly sulfoxaflor resistant. The R. padi and M. dirhodum populations were more susceptible to sulfoxaflor than those of S. miscanthi. These findings provide new insights into insecticide resistance development and rational sulfoxaflor use.

The Sensitivity of Field Populations of Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) to Seven Insecticides in Northern China

Insect pests are primarily controlled by insecticides. However, the sensitivity decreases and insecticide resistance is problematic for the effective management of agriculturally important insects, including Metopolophium dirhodum, which is an aphid that commonly feeds on cereals. The insecticide sensitivity status and potential resistance of M. dirhodum field populations remain relatively unknown. In this study, the susceptibility of 19 M. dirhodum populations from seven provinces in Northern China to neonicotinoids, pyrethroids, organophosphates, and a macrolide (abamectin) was determined in 2017–2019. The results indicated that two populations were highly resistant to thiamethoxam, with a relative resistance ratio (RLR) of 134.03 and 103.03, whereas one population was highly resistant to beta-cypermethrin (RLR of 121.42). On the basis of the RLR, the tested M. dirhodum populations ranging from susceptible to showing moderate levels of resistance to imidacloprid (RLR of 1.50 to 57.29), omethoate (RLR of 1.07 to 18.73), and abamectin (RLR of 1.10 to 25.89), but they were ranging from susceptible to showing tolerance or low levels of resistance to bifenthrin (RLR of 1.14 to 6.02) and chlorpyrifos (RLR of 1.11 to 7.59). Furthermore, a pair-wise correlation analysis revealed a significant correlation between the median lethal concentrations (LC50) for beta-cypermethrin and thiamethoxam, reflecting the cross-resistance between these two insecticides. The data obtained in our study provide timely information about aphid insecticide sensitivity, which may be used to delay the evolution of M. dirhodum insecticide resistance in Northern China.

Identifying aphid resistance in the ancestral wheat Triticum monococcum under field conditions

Wheat is an economically, socially, and nutritionally important crop, however, aphid infestation can often reduce wheat yield through feeding and virus transmission. Through field phenotyping, we investigated aphid resistance in ancestral wheat Triticum monococcum (L.). Aphid (Rhopalosiphum padi (L.), Sitobion avenae (F.) and Metopolophium dirhodum (Wlk.)) populations and natural enemy presence (parasitised mummified aphids, ladybird adults and larvae and lacewing eggs and larvae) on two naturally susceptible wheat varieties, Triticum aestivum (L.) var. Solstice and T. monococcum MDR037, and three potentially resistant genotypes T. monococcum MDR657, MDR045 and MDR049 were monitored across three years of field trials. Triticum monococcum MDR045 and MDR049 had smaller aphid populations, whereas MDR657 showed no resistance. Overall, natural enemy presence was positively correlated with aphid populations; however, MDR049 had similar natural enemy presence to MDR037 which is susceptible to aphid infestation. It is hypothesised that alongside reducing aphid population growth, MDR049 also confers indirect resistance by attracting natural enemies. The observed resistance to aphids in MDR045 and MDR049 has strong potential for introgression into commercial wheat varieties, which could have an important role in Integrated Pest Management strategies to reduce aphid populations and virus transmission.

RNA Sequencing Analysis of Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) Reveals the Mechanism Underlying Insecticide Resistance

Xinjiang (XJ) and Ningxia (NX) provinces are important agricultural regions in western China. Aphids are one kind of the most devastating pests in both the provinces. Aphids are typical phloem-feeding insects distributed worldwide and can severely damage crops. In this study, two representative Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) populations were collected from the typical agricultural regions of XJ and NX, respectively for a high-throughput transcriptome sequencing analysis. A total of 5,265 differentially expressed genes (DEGs) were identified. The functional annotation of DEGs and the identification of enriched pathways indicated many of the DEGs are involved in processes related to energy metabolism, development, and insecticide resistance. Furthermore, an investigation of insecticide toxicity revealed the NX population is more resistant to insecticide treatments than the XJ population. Thus, the transcriptome data generated in present study can be used for functional gene characterization relevant to aphid development, metabolism, environmental adaptation, and insecticide resistance.

Susceptibility of Four Species of Aphids in Wheat to Seven Insecticides and Its Relationship to Detoxifying Enzymes

Sitobion avenae (Fabricius), Rhopalosiphum padi (Linnaeus), Schizaphis graminum (Rondani), and Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) are important pests of wheat and other cereals worldwide. In this study, the susceptibilities of four wheat aphid species to seven insecticides were assessed. Furthermore, the activities of carboxylesterase (CarE), glutathione S-transferase (GSTs), and cytochrome P450 monooxygenase (P450s) were determined in imidacloprid treated and untreated aphids. The results showed that the susceptibilities of four wheat aphid species to tested insecticides are different and M. dirhodum has shown higher tolerance to most insecticides. Relatively higher CarE and GST activities were observed in M. dirhodum, and P450s activities increased significantly in response to imidacloprid treatment. Moreover, susceptibility to imidacloprid were increased by the oxidase inhibitor piperonyl butoxide in M. dirhodum (20-fold). The results we have obtained imply that P450s may play an important role in imidacloprid metabolic process in M. dirhodum. We suggest that a highly species-specific approach is essential for managing M. dirhodum.

Selection and validation of experimental condition-specific reference genes for qRT-PCR in Metopolophium dirhodum (Walker) (Hemiptera: Aphididae)

Metopolophium dirhodum (Walker) (Hemiptera: Aphididae) is one of the most common aphid pests of winter cereals. To facilitate accurate gene expression analyses with qRT-PCR assays, the expression stability of candidate reference genes under specific experimental conditions must be verified before they can be used to normalize target gene expression levels. In this study, 10 candidate reference genes in M. dirhodum were analyzed by qRT-PCR under various experimental conditions. Their expression stability was evaluated with delta Ct, BestKeeper, geNorm, and NormFinder methods, and the final stability ranking was determined with RefFinder. The results indicate that the most appropriate sets of internal controls were SDHB and RPL8 across geographic population; RPL8, Actin, and GAPDH across developmental stage; SDHB and NADH across body part; RPL8 and Actin across wing dimorphism and temperature; RPL4 and EF1A across starvation stress; AK and RPL4 across insecticide treatments; RPL8 and NADH across antibiotic treatments; RPL8, RPL4, Actin, and NADH across all samples. The results of this study provide useful insights for establishing a standardized qRT-PCR procedure for M. dirhodum and may be relevant for identifying appropriate reference genes for molecular analyses of related insects.

Antibiosis to Metopolophium dirhodum (Homoptera: Aphididae) in Spring Wheat and Emmer Cultivars

Yield losses caused by pests, including aphids, can be substantial in cereals. Breeding for resistance against aphids is therefore desirable for enhancing the economic and environmental sustainability of cereal production. The aim of our study was to reveal the degree of antibiosis against Metopolophium dirhodum (Walker) (Homoptera: Aphididae), in four cultivars of spring wheat, Triticum aestivum L. (‘Alicia’, ‘Odeta’, ‘Libertina’, ‘Astrid’), and two cultivars of emmer, Triticum turgidum ssp. dicoccum (Schrank ex Schübler) Thell. (‘Rudico’, ‘Tapiruz’) (both Poales: Poaceae) under controlled laboratory conditions. Using age-stage, two-sex life table, we quantified responses of M. dirhodum to each cultivar and to project population growth. The spring wheat and emmer cultivars varied in their suitability to M. dirhodum. The cultivar most susceptible to M. dirhodum was the emmer cultivar ‘Rudico’; the projected population size of M. dirhodum on this cultivar was one order of magnitude larger than those on other cultivars. The most resistant cultivar was the spring wheat cultivar ‘Libertina’. Since emmer is commonly used as a gene source for breeding T. aestivum, we advocate that care be taken to avoid the transmission of genes responsible for suitability to aphids from emmer to T. aestivum.