Abstract
Aphids are economically important insect pests of crops worldwide. Despite resistant varieties being available, resistance is continuously challenged and eventually broken down, posing a threat to food security. In the current study, the epigenome of two related Russian wheat aphid (Diuraphis noxia, Kurdjumov) biotypes (i.e., SA1 and SAM) that differ in virulence was investigated to elucidate its role in virulence in this species. Whole genome bisulfite sequencing covered a total of 6,846,597,083 cytosine bases for SA1 and 7,397,965,699 cytosine bases for SAM, respectively, of which a total of 70,861,462 bases (SA1) and 74, 073,939 bases (SAM) were methylated, representing 1.126 ± 0.321% (SA1) and 1.105 ± 0.295% (SAM) methylation in their genomes. The sequence reads were analyzed for contexts of DNA methylation and the results revealed that RWA has methylation in all contexts (CpG, CHG and CHH), with the majority of methylation within the CpG context (± 5.19%), while the other contexts show much lower levels of methylation (CHG − ± 0.27%; CHH − ± 0.34%). The top strand was slightly (0.02%) more methylated than the bottom strand. Of the 35,493 genes that mapped, we also analyzed the contexts of methylation of each of these and found that the CpG methylation was much higher in genic regions than in intergenic regions. The CHG and CHH levels did not differ between genic and intergenic regions. The exonic regions of genes were more methylated (±0.56%) than the intronic regions. We also measured the 5mC and 5hmC levels between the aphid biotypes, and found little difference in 5mC levels between the biotypes, but much higher levels of 5hmC in the virulent SAM. RWA had two homologs of each of the DNA methyltransferases 1 (DNMT1a and DNMT1b) and DNMT3s (DNMT3a and DNMT3b), but only a single DNMT2, with only the expression of DNMT3 that differed significantly between the two RWA biotypes. RWA has a single ortholog of Ten eleven translocase (DnTET) in the genome. Feeding studies show that the more virulent RWA biotype SAM upregulate DnDNMT3 and DnTET in response to wheat expressing antibiosis and antixenosis.
Highlights
Diuraphis noxia (Kurdjumov, Hemiptera: Aphididae—or Russian wheat aphid, RWA) biotypes are morphologically similar, yet display vast differences in their capacity to damage wheat cultivars upon feeding (Botha, 2013)
In 2012, Gong et al investigated the methylation of four genes encoding salivary gland proteins in RWA biotypes US1 and US2, and found these genes to be differentially methylated in the different biotypes
We identified differentially expressed (DE) genes between biotypes SA1 and SAM using edgeR (Robinson et al, 2010) based on gene-level expected counts estimated by RSEM
Summary
Diuraphis noxia (Kurdjumov, Hemiptera: Aphididae—or Russian wheat aphid, RWA) biotypes are morphologically similar, yet display vast differences in their capacity to damage wheat cultivars upon feeding (i.e., their virulence) (Botha, 2013). Insects have a variety of combinations of the DNMT genes, with some lineages having lost one (e.g., Bombyx mori and Triboleum castaneum) or two (e.g., Drosophila melanogaster and Anopheles gambiae) classes of DNMTs, and others having multiple homologs (e.g., Apis mellifera, Nasonia vitripennis, and Acyrthosiphon pisum) within a certain DNMT class (Kunert et al, 2003; Marhold et al, 2004; Walsh et al, 2010; Xiang et al, 2010; Glastad et al, 2011; Feliciello et al, 2013) Despite their important function in DNA methylation, knowledge of RWA DNMTs is still lacking. To quantify global methylation (5mC) and demethylation (5hmC) in the South African biotypes with shared genealogy; and thirdly, to characterize the DNA methyltransferases (DNMTs) and ten-eleven translocase enzymelike (TET) genes and expression in these aphids, to relate these observations to the reported difference in virulence levels of the South African RWA biotypes SA1 and SAM
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