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. 2024 Dec 11;25(24):13298.
doi: 10.3390/ijms252413298.

Transcriptome Analysis Unveils Molecular Mechanisms of Acaricide Resistance in Two-Spotted Spider Mite Populations on Hops

Sonu Koirala B K  1 , Gaurab Bhattarai  2 , Adekunle W Adesanya  3   4 , Timothy W Moural  1 , Laura C Lavine  3 , Douglas B Walsh  3   4 , Fang Zhu  1   5
Affiliations

Transcriptome Analysis Unveils Molecular Mechanisms of Acaricide Resistance in Two-Spotted Spider Mite Populations on Hops

Sonu Koirala B K et al. Int J Mol Sci. .

Abstract

Broad-spectrum crop protection technologies, such as abamectin and bifenthrin, are globally relied upon to curb the existential threats from economic crop pests such as the generalist herbivore Tetranychus urticae Koch (TSSM). However, the rising cost of discovering and registering new acaricides, particularly for specialty crops, along with the increasing risk of pesticide resistance development, underscores the urgent need to preserve the efficacy of currently registered acaricides. This study examined the overall genetic mechanism underlying adaptation to abamectin and bifenthrin in T. urticae populations from commercial hop fields in the Pacific Northwestern region of the USA. A transcriptomic study was conducted using four populations (susceptible, abamectin-resistant, and two bifenthrin-resistant populations). Differential gene expression analysis revealed a notable disparity, with significantly more downregulated genes than upregulated genes in both resistant populations. Gene ontology enrichment analysis revealed a striking consistency among all three resistant populations, with downregulated genes predominately associated with chitin metabolism. In contrast, upregulated genes in the resistant populations were linked to biological processes, such as peptidase activity and oxidoreductase activity. Proteolytic activity by peptidase enzymes in abamectin- and bifenthrin-resistant TSSM populations may suggest their involvement in acaricide metabolism. These findings provide valuable insights into the molecular mechanisms underlying acaricide resistance in the TSSM. This knowledge can be utilized to develop innovative pesticides and molecular diagnostic tools for effectively monitoring and managing resistant TSSM populations.

Keywords: RNA sequencing; acaricide resistance; metabolic detoxification; two-spotted spider mite.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Principal component analysis (PCA) of variance-stabilization-transformed (vst) normalized gene expression values in all three biological replicates of acaricide-resistant and -susceptible TSSM populations. The first (PC1) and second (PC2) principal components explain 69% and 14% of the total variance observed for gene expression, respectively. Each colored dot represents a biological replicate. SUS: susceptible; ABA_1X: abamectin-resistant; BIF_1X and BIF_100X: bifenthrin-resistant.
Figure 2
Figure 2
Volcano plots showing differentially expressed genes (|log2fold change| ≥ 1.5) in (A) abamectin- and (B,C) bifenthrin-resistant two-spotted spider mite (TSSM) populations. Orange and blue dots represent upregulated (log2fold change ≥ 1.5) and downregulated (log2fold change ≤ −1.5) genes (FDR-adjusted p-value < 0.05), respectively. SUS: susceptible; ABA_1X: abamectin-resistant; BIF_1X and BIF_100X: bifenthrin-resistant.
Figure 3
Figure 3
Venn diagrams showing (A) all differentially expressed (both up- and downregulated), (B) only upregulated, and (C) only downregulated common and unique genes among three acaricide-resistant two-spotted spider mite (TSSM) populations: ABA_1X, BIF_1X, and BIF_100X, respectively. ABA_1X: abamectin-resistant; BIF_1X and BIF_100X: bifenthrin-resistant.
Figure 4
Figure 4
The ontological relationship of up- and downregulated genes in three acaricide-resistant populations. The gene ontology is presented as biological processes (BPs) (top), molecular functions (MFs) (middle), and cellular components (bottom), and the color scales represent the number of differentially expressed genes in the corresponding gene ontology. Up- and downregulated genes were selected based on the following criteria: |log2fold change| > 1.5 and Benjamini–Hochberg (BH)-adjusted p-values < 0.05.
Figure 5
Figure 5
log2fold change in genes belonging to various detoxification gene classes in abamectin (ABA_1X)- and bifenthrin (BIF_1X and BIF_100X)-resistant TSSM populations. The value “-” indicates that the gene does not meet the statistical criteria to be called differentially expressed in this study (|log2fold| ≥ 1.5 and Benjamin–Hochberg-adjusted contrast p-value ≤ 0.05). The color intensity in each gene category indicates the level of gene expression, with darker shades representing more |log2fold| changes. Dark blue indicates greater downregulation, while dark orange denotes higher upregulation. ABA_1X: abamectin-resistant; BIF_1X and BIF_100X: bifenthrin-resistant.
Figure 6
Figure 6
Percentage of (A,C,E) single-nucleotide polymorphisms (SNPs) with all consequences and (B,D,F) consequences in coding regions in the ABA_1X, BIF_1X, and BIF_100X TSSM populations, respectively. SNPs were identified in resistant populations in reference to the homozygous genotype of the susceptible TSSM population. N: number of variants. ABA_1X: abamectin-resistant; BIF_1X and BIF_100X: bifenthrin-resistant.
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