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Learning-induced gene expression in the heads of two Nasonia species that differ in long-term memory formation.

Hoedjes KM, Smid HM, Schijlen EG, Vet LE, van Vugt JJ - BMC Genomics (2015)

Bottom Line: We determined conditioning-induced DE compared to naïve controls for both species.Several candidate genes that may regulate differences in LTM have been identified.This transcriptome analysis is a valuable resource for future in-depth studies to elucidate the role of candidate genes and antisense transcription in natural variation in LTM formation.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Entomology, Plant Sciences Group, Wageningen University, P.O. box 8031, 6700AP, Wageningen, The Netherlands. katja.hoedjes@unil.ch.

ABSTRACT

Background: Cellular processes underlying memory formation are evolutionary conserved, but natural variation in memory dynamics between animal species or populations is common. The genetic basis of this fascinating phenomenon is poorly understood. Closely related species of Nasonia parasitic wasps differ in long-term memory (LTM) formation: N. vitripennis will form transcription-dependent LTM after a single conditioning trial, whereas the closely-related species N. giraulti will not. Genes that were differentially expressed (DE) after conditioning in N. vitripennis, but not in N. giraulti, were identified as candidate genes that may regulate LTM formation.

Results: RNA was collected from heads of both species before and immediately, 4 or 24 hours after conditioning, with 3 replicates per time point. It was sequenced strand-specifically, which allows distinguishing sense from antisense transcripts and improves the quality of expression analyses. We determined conditioning-induced DE compared to naïve controls for both species. These expression patterns were then analysed with GO enrichment analyses for each species and time point, which demonstrated an enrichment of signalling-related genes immediately after conditioning in N. vitripennis only. Analyses of known LTM genes and genes with an opposing expression pattern between the two species revealed additional candidate genes for the difference in LTM formation. These include genes from various signalling cascades, including several members of the Ras and PI3 kinase signalling pathways, and glutamate receptors. Interestingly, several other known LTM genes were exclusively differentially expressed in N. giraulti, which may indicate an LTM-inhibitory mechanism. Among the DE transcripts were also antisense transcripts. Furthermore, antisense transcripts aligning to a number of known memory genes were detected, which may have a role in regulating these genes.

Conclusion: This study is the first to describe and compare expression patterns of both protein-coding and antisense transcripts, at different time points after conditioning, of two closely related animal species that differ in LTM formation. Several candidate genes that may regulate differences in LTM have been identified. This transcriptome analysis is a valuable resource for future in-depth studies to elucidate the role of candidate genes and antisense transcription in natural variation in LTM formation.

No MeSH data available.


The numbers of shared and unique protein-coding transcripts observed in the entire transcriptomes(left)and among differentially expressed(DE)transcripts(right)ofN. vitripennisandN. giraultiare shown.
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Fig3: The numbers of shared and unique protein-coding transcripts observed in the entire transcriptomes(left)and among differentially expressed(DE)transcripts(right)ofN. vitripennisandN. giraultiare shown.

Mentions: The protein-coding transcripts of N. vitripennis and N. giraulti that had a hit to the N. vitripennis proteome were compared amongst each other to assess differences in gene expression between the two species. The majority of the transcripts of N. vitripennis and N. giraulti, 86.1% and 82.9% of the transcriptomes respectively, was observed in both species, which indicates a high level of similarity in transcripts expressed in the brains of both species. However, only 37.8% and 39.0% of the DE transcripts of N. vitripennis and N. giraulti, respectively, were differentially expressed in both species (Figure 3). This result suggests that there are substantial differences in conditioning-induced differential gene expression in N. vitripennis and N. giraulti. Results from analyses on DE transcripts are presented in the following paragraphs. Information on transcripts includes the Drosophila gene name (when available).Figure 3


Learning-induced gene expression in the heads of two Nasonia species that differ in long-term memory formation.

Hoedjes KM, Smid HM, Schijlen EG, Vet LE, van Vugt JJ - BMC Genomics (2015)

The numbers of shared and unique protein-coding transcripts observed in the entire transcriptomes(left)and among differentially expressed(DE)transcripts(right)ofN. vitripennisandN. giraultiare shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4440501&req=5

Fig3: The numbers of shared and unique protein-coding transcripts observed in the entire transcriptomes(left)and among differentially expressed(DE)transcripts(right)ofN. vitripennisandN. giraultiare shown.
Mentions: The protein-coding transcripts of N. vitripennis and N. giraulti that had a hit to the N. vitripennis proteome were compared amongst each other to assess differences in gene expression between the two species. The majority of the transcripts of N. vitripennis and N. giraulti, 86.1% and 82.9% of the transcriptomes respectively, was observed in both species, which indicates a high level of similarity in transcripts expressed in the brains of both species. However, only 37.8% and 39.0% of the DE transcripts of N. vitripennis and N. giraulti, respectively, were differentially expressed in both species (Figure 3). This result suggests that there are substantial differences in conditioning-induced differential gene expression in N. vitripennis and N. giraulti. Results from analyses on DE transcripts are presented in the following paragraphs. Information on transcripts includes the Drosophila gene name (when available).Figure 3

Bottom Line: We determined conditioning-induced DE compared to naïve controls for both species.Several candidate genes that may regulate differences in LTM have been identified.This transcriptome analysis is a valuable resource for future in-depth studies to elucidate the role of candidate genes and antisense transcription in natural variation in LTM formation.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Entomology, Plant Sciences Group, Wageningen University, P.O. box 8031, 6700AP, Wageningen, The Netherlands. katja.hoedjes@unil.ch.

ABSTRACT

Background: Cellular processes underlying memory formation are evolutionary conserved, but natural variation in memory dynamics between animal species or populations is common. The genetic basis of this fascinating phenomenon is poorly understood. Closely related species of Nasonia parasitic wasps differ in long-term memory (LTM) formation: N. vitripennis will form transcription-dependent LTM after a single conditioning trial, whereas the closely-related species N. giraulti will not. Genes that were differentially expressed (DE) after conditioning in N. vitripennis, but not in N. giraulti, were identified as candidate genes that may regulate LTM formation.

Results: RNA was collected from heads of both species before and immediately, 4 or 24 hours after conditioning, with 3 replicates per time point. It was sequenced strand-specifically, which allows distinguishing sense from antisense transcripts and improves the quality of expression analyses. We determined conditioning-induced DE compared to naïve controls for both species. These expression patterns were then analysed with GO enrichment analyses for each species and time point, which demonstrated an enrichment of signalling-related genes immediately after conditioning in N. vitripennis only. Analyses of known LTM genes and genes with an opposing expression pattern between the two species revealed additional candidate genes for the difference in LTM formation. These include genes from various signalling cascades, including several members of the Ras and PI3 kinase signalling pathways, and glutamate receptors. Interestingly, several other known LTM genes were exclusively differentially expressed in N. giraulti, which may indicate an LTM-inhibitory mechanism. Among the DE transcripts were also antisense transcripts. Furthermore, antisense transcripts aligning to a number of known memory genes were detected, which may have a role in regulating these genes.

Conclusion: This study is the first to describe and compare expression patterns of both protein-coding and antisense transcripts, at different time points after conditioning, of two closely related animal species that differ in LTM formation. Several candidate genes that may regulate differences in LTM have been identified. This transcriptome analysis is a valuable resource for future in-depth studies to elucidate the role of candidate genes and antisense transcription in natural variation in LTM formation.

No MeSH data available.