Host plant adaptation in the polyphagous whitefly, Trialeurodes vaporariorum, is associated with transcriptional plasticity and altered sensitivity to insecticides

- Host plant adaptation in the polyphagous whitefly, Trialeurodes vaporariorum , is.
- vaporariorum upon transfer to a range of different host plants revealed profound differences in the transcriptional response to more or less challenging hosts.
- Remarkably, these changes in gene expression were associated with significant shifts in the tolerance of host-adapted T..
- Full list of author information is available at the end of the article.
- urticae [12] character- isation of the expression levels of all the genes in the gen- ome of an insect when on different host plants can provide unique insights into the mechanisms underlying host-dependent changes in insecticide sensitivity.
- While the genomes of two different species of the B.
- The latter closely matches the genome size (615 MB) of the other sequenced whitefly species, B.
- The com- pleteness of the gene space in the assembled genome was assessed using the Benchmarking Universal Single-Copy Orthologues (BUSCO) and Core Eukaryotic genes mapping approach (CEGMA) pipelines.
- BUSCO analysis identified 90.8, 92 and 93.5% of the Eukaryota, Insecta and Arthropoda test gene sets respectively as complete in the assembly (Add- itional file 4: Figure S2B).
- Furthermore, 94% of CEGMA core Eukaryotic genes (including both complete and partial genes) were present in the assembled genome (Additional file 6:.
- Approximately 30% of the rapidly evolving genes gained in T.
- Curation and phylogeny of genes involved in detoxification of natural and synthetic xenobiotics Because of our interests in the mechanisms underpinning adaptation of T.
- A total of 80 cytochrome P450s were identified in the T.
- Phylogenetic comparison of the CYPome of T.
- However, significant differences in the CYPomes of the species are observed in the CYP3 and CYP4 clades.
- A similar pattern was observed in the CYP4 clade with the CYP3133 family, which is unique to the two whitefly species, comprising 19 genes and 7 subfamiles in B.
- The net effect of the differences in the two clans sums to 17 additional CYP3 P450 genes and 31 CYP4 genes in B.
- tabaci are highly polyphagous so this disparity in P450 gene content is somewhat surprising, however, similar numbers of P450 genes are observed in the genomes of the generalist aphid M.
- In the case of GSTs a total of 26 genes were collated from the T.
- A total of 31 CCEs (4 novel) were identified in the T..
- Phylogeny (Add- itional file 14: Figure S4A) assigned 14 of the T..
- In many of the clades (C, D, F and A) close to 1:1 orthology between the two species is observed.
- However, significant differences in the two species are observed in the B and G clades with many more ABC transporter genes observed in B.
- tabaci in the G clade and more genes in the B clade in T.
- tabaci where several ABC transporter genes of the G clade were implicated in re- sistance to neonicotinoids [30]..
- Comparison of the UGT gene family of T.
- However cur- ation and naming (UGT nomenclature committee) of UGT genes in the two species revealed many of the pre- viously proposed UGTs of B.
- the UGT344 family of the pea aphid A.
- In the case of the natural insecticide nicotine only the tobacco- reared line exhibited a significant reduction in tolerance to this compound..
- a Maximum likelihood phylogeny of the CYPome of B.
- c Bar chart indicating numbers of P450s significantly over/under-expressed in the above populations.
- response was observed for the nightshade-reared lines with 4304 and 2974 genes identified as DE in the tomato and tobacco-reared lines compared to the control line on bean.
- vaporariorum lines, with an intermediate number of genes (2069) DE in the compari- son with the cucumber-reared line.
- The magnitude of the transcriptional response of T.
- vaporariorum to the different host plants is consistent with the profile of the defensive secondary metabolites they produce.
- identified in the RNAseq comparisons involving the cu- cumber or pumpkin-reared lines (Additional file 19: Fig- ure S7).
- This likely reflects the DE of genes involved in regulating the large scale transcrip- tional changes observed in the tomato-reared compari- son (see below) and parallels the findings of previous research on host-plant adaptation of the polyphagous butterfly, Polygonia c-album [9].
- Interestingly, the same terms were enriched in the genes classed as rapidly evolving in T.
- observed marked differences in the expression of P450 genes between the whitefly lines adapted to novel host plants (Fig.
- A total of 11, 18 and 28 P450 genes were DE in the cucumber-, tobacco- and tomato-reared T.
- CYP6EA1 a mem- ber of the CYP3 clade (overexpressed 5.0–9.2-fold) and CYP306A1 (overexpressed 3.3–2.4-fold).
- 20-fold in the cucumber-reared line but is not overexpressed in the pumpkin reared line, despite this both of these lines show the same.
- Finally, the high ex- pression of CYP6DP2 in the tomato-reared line is not associated with tolerance to chlorantraniliprole (Fig.
- tabaci, the overex- pression of CYP6CM2–4 in the tobacco-reared line rep- resent potential candidates to explain the tolerance of this line to nicotine (Fig.
- In the case of GSTs two genes were upregulated in the cucumber-reared line (g10036 and g13867), however, both of these were also overexpressed at similar levels in both night-shade reared lines (Additional file 13: Figure S3B and Additional file 18: Tables S16, S20).
- This sug- gests that while they may play a role in host plant adap- tation they play no role in the enhanced tolerance of the cucumber-reared line to chlorantraniliprole, or the toler- ance of the nightshade-reared lines to pymetrozine or imidacloprid (Fig.
- In addition to these two genes, one further GST (g5077) was upregulated exclusively in the nightshade-reared plants (overexpressed 2.7- and 2.3- fold in the tobacco- and tomato-reared lines) (Add- itional file 18: Table S20).
- No additional GSTs were overexpressed exclusively (or at significantly higher levels) in the tobacco-reared lines that might contribute to the tolerance of this line to nicotine..
- g17172 also belongs to clade A, however, comparison of its pattern of expression in the three T.
- vaporariorum lines with the sensitivity of these lines to insecticides suggests it is unlikely to confer toler- ance to any of the compounds tested..
- Much more marked changes were observed in the ex- pression of genes encoding UGTs, with 11 UGT genes upregulated in the cucumber-reared line and 9 upregu- lated in both nightshade-reared plants (Additional file 16:.
- The four UGT genes (UGT352P5, UGT356E1, UGT352P2 and UGT358B1) exclusively upregulated (2.3–4.5-fold) in the cucumber-reared line are potential candidates for a role in the marked tolerance of this line to chlorantraniliprole.
- The two UGTs (g12287 and g2864) exclusively overexpressed in the nightshade reared lines are potential candidate genes for a role in the tolerance of these lines to insecticides, particularly g12287 which was overexpressed >.
- Four genes (g11125, g11231, g5414 and g3563) were moderately (up to 5.4-fold) overex- pressed in the cucumber-feeding line.
- Three of the ABC transporter genes overexpressed in the cucumber-reared line (g11231, g5414 and g3563) also be- long to this clade and thus are potential candidates for the increased tolerance to chlorantraniliprole.
- Both genes sig- nificantly upregulated in the tobacco-reared line (g11231 and g5415) were also upregulated in the tomato-reared line, and so are unlikely to be responsible for the tolerance of this line to nicotine (Fig.
- Analysis of the transcriptomes of the T.
- These included marked changes in the expression of genes encoding cathepsin B cysteine proteases and cuticular proteins, both of which have been previously implicated in insect adjustment to new host plants [24].
- In the case of cathepsin B prote- ases the tomato, tobacco and cucumber reared lines all had >.
- In the cucumber- reared line all but one of the 14 cathepsin B genes DE was upregulated (2.1- to 14.6-fold), however, in both the tobacco and tomato reared lines a higher number of.
- In the case of genes encoding structural components of the insect cuticle 15 sequences were identified as over-expressed in the nightshade-reared T.
- host plants was suggested by the over-expression of 56 transcription factors in the tomato- and tobacco-reared lines, representing 5.1% of all DE genes (Add- itional file 18: Table S20).
- P450s of the CYP6CM1 subfamily confer tolerance to plant-derived, but not synthetic, insecticides.
- vaporariorum were all overexpressed in the tobacco-reared line which exhibited tolerance to both nicotine and imidacloprid (Add- itional file 20: Figure S8).
- In insecticide bioassays none of the three lines showed tolerance to the neonicotinoid imi- dacloprid (Fig.
- In contrast, in bioassays with nicotine a trend of increased tolerance of the three transgenic lines to this compound was observed when compared to the control.
- Comparison of gene superfamilies most commonly involved in the detoxification, transport and excretion of xenobiotics with those of the tobacco whitefly B..
- a key role in the striking ability of such species to utilise a di- verse range of plants as hosts.
- Sequencing, assembly and annotation of the T..
- Four hundred fifty mixed sex adults of the resulting.
- b Percentage mortality of the same strains when exposed to a single high concentration (30,000 ppm) of nicotine.
- The completeness of the gene space in the assembled genome was assessed by BUSCO (Benchmarking univer- sal single-copy orthologs) –v3.0.2 [67] and CEGMA (Core Eukaryotic genes mapping approach) –v2.5.0 [68].
- implemented in the BRAKER pipeline using RNA-seq alignments as evidence.
- This is a simple fossil calibra- tion for the most common recent ancestor of the three families.
- Clean reads were aligned to the genome using HISAT2 v and gene expression estimated using the htseq-count tool implemented in the HTSeq package [88].
- Analysis of the T.
- (B) Summary of Benchmarking Universal Single-Copy Orthologs (BUSCO) analysis of the T.
- (C) Functional annotation of the T.
- Summary of gene annotation of the T..
- Number of P450, GST, CCE, UGT and ABC genes in the genomes of five insect species..
- (B) Relative expression (log2fold) of the full length GSTs from 4 T.
- (B) Relative expression (log2fold) of the full length CCEs from 4 T.
- (B) Relative expression (log2fold) of the full length ABCs from 4 T.
- (B) Relative expression (log2fold) of the full length UGTs from 4 T.
- Gene ontology analysis of genes differentially expressed in the tobacco and tomato-reared lines of T..
- The funding bodies were not involved in the design of the study, data collection, interpretation of data, or in writing the manuscript..
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