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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 proportion of‘protein-coding(sense)’,‘antisense’, ‘long non-coding RNA’and‘unknown’is shown for(a)N. vitripennistotal transcriptome(30223 transcripts),(b)N. giraultitotal transcriptome(29641 transcripts),(c)N. vitripennisdifferentially expressed(DE)transcripts(2458 transcripts),and(d)N. giraultiDE transcripts(2220 transcripts)(DE compared to unconditioned expression).
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Fig1: The proportion of‘protein-coding(sense)’,‘antisense’, ‘long non-coding RNA’and‘unknown’is shown for(a)N. vitripennistotal transcriptome(30223 transcripts),(b)N. giraultitotal transcriptome(29641 transcripts),(c)N. vitripennisdifferentially expressed(DE)transcripts(2458 transcripts),and(d)N. giraultiDE transcripts(2220 transcripts)(DE compared to unconditioned expression).

Mentions: The percentages and average length of protein-coding (sense) transcripts, antisense transcripts, long non-coding RNA (lncRNA) and unknown transcripts are shown in Table 1 and Figure 1 (a-b). The head transcriptome of N. giraulti had a larger number of protein-coding transcripts than that of N. vitripennis, whereas it had half the amount of antisense transcripts. Also the fraction of lncRNA of N. giraulti was lower than that of N. vitripennis. A small portion of the lncRNA and unknown (i.e. misassembled or misassigned) transcripts contains a putative ORF, suggesting these might be (unknown) protein-coding genes.Table 1


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 proportion of‘protein-coding(sense)’,‘antisense’, ‘long non-coding RNA’and‘unknown’is shown for(a)N. vitripennistotal transcriptome(30223 transcripts),(b)N. giraultitotal transcriptome(29641 transcripts),(c)N. vitripennisdifferentially expressed(DE)transcripts(2458 transcripts),and(d)N. giraultiDE transcripts(2220 transcripts)(DE compared to unconditioned expression).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: The proportion of‘protein-coding(sense)’,‘antisense’, ‘long non-coding RNA’and‘unknown’is shown for(a)N. vitripennistotal transcriptome(30223 transcripts),(b)N. giraultitotal transcriptome(29641 transcripts),(c)N. vitripennisdifferentially expressed(DE)transcripts(2458 transcripts),and(d)N. giraultiDE transcripts(2220 transcripts)(DE compared to unconditioned expression).
Mentions: The percentages and average length of protein-coding (sense) transcripts, antisense transcripts, long non-coding RNA (lncRNA) and unknown transcripts are shown in Table 1 and Figure 1 (a-b). The head transcriptome of N. giraulti had a larger number of protein-coding transcripts than that of N. vitripennis, whereas it had half the amount of antisense transcripts. Also the fraction of lncRNA of N. giraulti was lower than that of N. vitripennis. A small portion of the lncRNA and unknown (i.e. misassembled or misassigned) transcripts contains a putative ORF, suggesting these might be (unknown) protein-coding genes.Table 1

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.