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Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta).

ABSTRACT: Vitellogenin has been proposed to regulate division of labor and social organization in social insects. The red imported fire ant (Solenopsis invicta) harbors four distinct, adjacent vitellogenin genes (Vg1, Vg2, Vg3, and Vg4). Contrary to honey bees that have a single Vg ortholog as well as potentially fertile nurses, and to other ant species that lay trophic eggs, S. invicta workers completely lack ovaries or the ability to lay eggs. This provides a unique model to investigate whether Vg duplication in S. invicta was followed by subfunctionalization to acquire non-reproductive functions and whether Vg was co-opted to regulate behavior within the worker caste. To investigate these questions, we compared the expression patterns of S. invicta Vg genes among workers from different morphological subcastes or performing different tasks. RT-qPCRs revealed higher relative expression of Vg1 in major workers compared to both medium and minor workers, and of Vg2 in major workers when compared to minor workers. Relative expression of Vg1 was also higher in carbohydrate foragers when compared to nurses and protein foragers. By contrast, the level of expression of Vg2, Vg3, and Vg4 were not significantly different among the workers performing the specific tasks. Additionally, we analyzed the relationship between the expression of the Vg genes and S-hydroprene, a juvenile hormone analog. No changes in Vg expression were recorded in workers 12 h after application of the analog. Our results suggest that in S. invicta the Vg gene underwent subfunctionalization after duplication to new functions based on the expression bias observed in these data. This may suggest an alternative and still unknown function for Vg in the workers that needs to be investigated further.

SUBMITTER: Hawkings C

PROVIDER: S-EPMC5978388 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta).

Hawkings Chloe C Tamborindeguy Cecilia C

PeerJ 20180528

Vitellogenin has been proposed to regulate division of labor and social organization in social insects. The red imported fire ant (Solenopsis invicta) harbors four distinct, adjacent vitellogenin genes (Vg1, Vg2, Vg3, and Vg4). Contrary to honey bees that have a single Vg ortholog as well as potentially fertile nurses, and to other ant species that lay trophic eggs, S. invicta workers completely lack ovaries or the ability to lay eggs. This provides a unique model to investigate wh ...[more]

PMID: 29868280

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Project description:BackgroundAdvances in sequencing and analysis tools have facilitated discovery of many new viruses from invertebrates, including ants. Solenopsis invicta is an invasive ant that has quickly spread worldwide causing significant ecological and economic impacts. Its virome has begun to be characterized pertaining to potential use of viruses as natural enemies. Although the S. invicta virome is the best characterized among ants, most studies have been performed in its native range, with less information from invaded areas.MethodsUsing a metatranscriptome approach, we further identified and molecularly characterized virus sequences associated with S. invicta, in two introduced areas, U.S and Taiwan. The data set used here was obtained from different stages (larvae, pupa, and adults) of S. invicta life cycle. Publicly available RNA sequences from GenBank's Sequence Read Archive were downloaded and de novo assembled using CLC Genomics Workbench 20.0.1. Contigs were compared against the non-redundant protein sequences and those showing similarity to viral sequences were further analyzed.ResultsWe characterized five putative new viruses associated with S. invicta transcriptomes. Sequence comparisons revealed extensive divergence across ORFs and genomic regions with most of them sharing less than 40% amino acid identity with those closest homologous sequences previously characterized. The first negative-sense single-stranded RNA virus genomic sequences included in the orders Bunyavirales and Mononegavirales are reported. In addition, two positive single-strand virus genome sequences and one single strand DNA virus genome sequence were also identified. While the presence of a putative tenuivirus associated with S. invicta was previously suggested to be a contamination, here we characterized and present strong evidence that Solenopsis invicta virus 14 (SINV-14) is a tenui-like virus that has a long-term association with the ant. Furthermore, based on virus sequence abundance compared to housekeeping genes, phylogenetic relationships, and completeness of viral coding sequences, our results suggest that four of five virus sequences reported, those being SINV-14, SINV-15, SINV-16 and SINV-17, may be associated to viruses actively replicating in the ant S. invicta.ConclusionsThe present study expands our knowledge about viral diversity associated with S. invicta in introduced areas with potential to be used as biological control agents, which will require further biological characterization.

Project description:Purpose: We aimed to provide a basis for the adaptive mechanism and a rich resource for the discovery and identification of novel genes involved in the cold and heat stress response in Solenopsis invicta. retinal transcriptome profiling (RNA-seq) to microarray and quantitative reverse transcription polymerase chain reaction (qRT–PCR) methods and to evaluate protocols for optimal high-throughput data analysis Methods: Solenopsis invicta was reared at lab condition, and incubated at 4 different temperature for 24h (10, 20, 30 and 40℃). RNA was extracted using Trizol reagent and Illumina sequencing was performed at Macrogen. Illumina short reads were quality-filtered and Illumina-based de novo transcriptome assembly was performed. Differential Gene Expression Analysis was studied for different tempearture conditions. Results: Totally 99,085 unigenes was obtained which at least 19,154 were annotated with gene descriptions, gene ontology terms, and metabolic pathways. 86 GO functional sub-groups and 23 EggNOG terms resulted. DEGs with log2FC≥10 were screened and were compared at different temperatures. We found 203, 48 and 66 specific DEGs co-regulated at 10, 20 and 40℃, respectively compare with 30℃. Comparing transcriptome profiles for differential gene expression resulted various DE proteins and genes, including cytochrome P450, NADH dehydrogenase subunit 1, cuticle protein and HSP which have previously been reported to be involved in cold and high temperature resistance. GO analysis revealed that antioxidant activity up-regulated under high temperature stress. Conclusions: we compared the transcriptomes of S. invicta under high- and low-temperature stresses using RNA-Seq technology based on the high-throughput sequencing. Comparative transcriptome analysis identified many genes and a large number of changes were discovered in metabolic pathway through the GO and KEGG enrichment analysis. Our data will facilitate further molecular investigations and genomic research. Many high- and low-temperature significantly up-regulated genes were first identified in this study. These newly found genes may be important and necessary to RIFA overwintering and its behavior for adaptation in new environment as well as quarantine area.

Dataset Information

Expression analysis of vitellogenins in the workers of the red imported fire ant (Solenopsis invicta).

Publications

Expression analysis of vitellogenins in the workers of the red imported fire ant (<i>Solenopsis invicta</i>).

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