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, 10 (12), 883-901

Core Transcriptional Signatures of Phase Change in the Migratory Locust

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Core Transcriptional Signatures of Phase Change in the Migratory Locust

Pengcheng Yang et al. Protein Cell.

Erratum in

Abstract

Phenotypic plasticity plays fundamental roles in successful adaptation of animals in response to environmental variations. Here, to reveal the transcriptome reprogramming in locust phase change, a typical phenotypic plasticity, we conducted a comprehensive analysis of multiple phase-related transcriptomic datasets of the migratory locust. We defined PhaseCore genes according to their contribution to phase differentiation by the adjustment for confounding principal components analysis algorithm (AC-PCA). Compared with other genes, PhaseCore genes predicted phase status with over 87.5% accuracy and displayed more unique gene attributes including the faster evolution rate, higher CpG content and higher specific expression level. Then, we identified 20 transcription factors (TFs) named PhaseCoreTF genes that are associated with the regulation of PhaseCore genes. Finally, we experimentally verified the regulatory roles of three representative TFs (Hr4, Hr46, and grh) in phase change by RNAi. Our findings revealed that core transcriptional signatures are involved in the global regulation of locust phase changes, suggesting a potential common mechanism underlying phenotypic plasticity in insects. The expression and network data are accessible in an online resource called LocustMine (http://www.locustmine.org:8080/locustmine).

Keywords: RNA interference; phenotypic plasticity; transcriptional regulatory network.

Figures

Figure 1
Figure 1
PhaseCore gene identification. (A) Experimental design of this study. Left: developmental stages from eggs to adults. Scale bars = 5 mm. Middle: various tissues, including three tissues from adult locust (fat body, hemolymph, and antenna), and five tissues from the fourth instar nymphs (antenna, brain, thoracic ganglia, wing, and pronotum). Right: the time courses of phase change (i.e., gregarization and solitarization) with two brain and thoracic ganglia tissues at six time points (0, 4, 8, 16, 32, and 64 h). (B) Samples from gregarious (G) and solitary locusts (S), and CS and IG locusts classified using the AC-PCA method for developmental, tissue, and time course datasets. One circle represents one sample. Blue represents typical or crowded solitary locusts, and red represents typical or isolated gregarious locusts. (C) Scatterplots and Pearson’s correlation (marked in red) of pairs of the PC1 values from the three datasets. Lines were fitted using least-squares linear regression. (D) Accuracy distribution of leave-one-out cross validation (LOO-CV) and cross-dataset validation (CDV) for the three datasets using Borda gene list. Only the top 15,000 genes were considered. These genes were divided into 15 bins with 1,000 genes in each bin. The accuracy was calculated for each bin
Figure 2
Figure 2
The attributes and functions of PhaseCore genes. PhaseCore genes displayed extreme gene attributes (A–H). The PhaseCore gene sets were the top 1,700 genes in the Borda gene list (i.e., the far-left column in (A–H)). PhaseCore genes displayed (A) higher percentage of PRGs, (B) higher specific expression level, (C) lower network connectivity in the co-expression network, (D) faster evolution rate, (E) higher CpG o/e, (F) lower methylation level, (G) lower percentage of genes with known function and (H) higher percentage of DEGs from two experiments with three replicates. (I) Selected enriched functional classes of PhaseCore genes at two cutoff: 10% and 5%. Red represents the degree of the enrichment. b. binding; p. process; m. metabolic; c. compound
Figure 3
Figure 3
Identification and regulational functions of PhaseCoreTF genes. (A) Barplot of locust TF families with >10 members. (B) Schema of transcriptional regulatory network (TRN) reconstruction. (C) Whole genome TRN. The red nodes represent the PhaseCore genes or PhaseCore TF genes, which were connected by green lines. The labelled nodes were 20 PhaseCore TF genes. (D) PhaseCoreTF regulating GO terms enriched in PhaseCore genes. (E) Venn diagram displaying the overlap among the DEGs from Brain_Hou dataset and PhaseCore genes. (F) Network presentation of PhaseCoreTF regulating PhaseCore genes. Ellipse nodes are TF genes, rectangle nodes are target genes. Nodes in red or green represent highly or lowly expressed in gregarious locust, and gray represents non-DEGs
Figure 4
Figure 4
Hr4, Hr46, andgrhregulating locust phase behavior. (A) Expression levels of three TF genes after RNA interference (RNAi). (B) and (C) Behavioral changes induced by RNAi of Hr4 (B), grh and Hr46 (C). The red arrows denote the median Pgreg values. Pgreg = 1 indicates full gregarious behavior, and Pgreg = 0 indicates fully solitary behavior. (D) and (E) Total distance moved (TDM) 48h after injection of dsRNA of Hr4, grh and Hr46. (F and G) Total duration of movement (TDMV) 48 h after injection of dsRNA of Hr4, grh and Hr46. *P < 0.05, **P < 0.01 by Mann-Whitney test
Figure 5
Figure 5
RNA-seq revealed combinatorial regulations amongHr4, Hr46andgrh. (A) Venn diagram displaying the overlap among the three RNAi DEG lists and PhaseCore genes. (B) Venn diagram displaying the overlap among the DEGs from RNAi and target genes. Two target gene sets were used: the target genes through ensembling TF-Target pairs of total TF genes (TarTotal), and ensembling TF-target pairs of each TF gene (TarEach) (see MATERIALS AND METHODS). The hypergeometric test P value was calculated for these two target gene sets. (C) Bar chart that illustrates two sets intersections among four DEG lists in a matrix layout. The matrix of solid and empty circles at the bottom illustrates the “presence” (solid green) or “absence” (empty) of the gene sets in each intersection. The number to the right of the matrix indicates gene set size. The colored bars on the top of the matrix represent the intersection sizes, with the color intensity showing the P value significance. The DEGs in normal brain tissues were derived from Brain_Hou dataset. (D) Network of the DEGs from the RNAi of Hr4, Hr46, and grh. PhaseCore genes of the time course data with functional annotation are displayed. Red circles indicate TFs, and the green rectangles indicate no TFs. The edges with dashed lines indicate DEGs after RNAi, and the edges with solid lines indicate that the connections were supported by RNAi DEGs and target prediction
Figure 6
Figure 6
LocustMine use case. (A) LocustMine homepage. (A1) Quick visit to subsections, including BLAST and JBrowse. (A2) Enter a gene name to access the Gene page report. (A3) Enter a list of genes to perform GO and pathway enrichments. (A4) Take a tour will direct to a new page of LocustMine documentation. (A5) Popular template queries can be found here and under the Templates button at the top of the page. (B–I) Illustrate the report page of gene Hr4 (http://locustmine.org:8080/locustmine/gene:LOCMI17305). (B) Header of gene report page, including quick link to several subsections. (C) Gene function, including gene ontology and pathways. (D) Interactions from PPI, co-expression and TF-Target. (E) Gene models and proteins. (F) Homology information. (G) Gene expression values from 52 samples. (H) Gene lists containing Hr4. (I) Links to the orthologues in other Mines. (J–M) Enrichment analysis for gene list T-IG-32h-VS-T-IG-C-up. The demo case could be accessed from the link: http://locustmine.org:8080/locustmine/bagDetails.do?scope=all&bagName=T-IG-32h-VS-T-IG-C-up. (J) Under Lists on the LocustMine homepage, users can manually enter or upload a list of genes for analysis. Here, we use the the public list T-IG-32h-VS-T-IG-C-up as example. (K) Screenshot of gene information of the list. (L) Gene ontology and protein domain enrichment. (M) Pathway enrichment and Gene Sets enrichment

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