Chromosome-level genome assembly of Chinese water Scorpion Ranatra chinensis (Heteroptera: Nepidae).

Heteroptera (the true bugs), one of the most diverse lineages of insects, diversified in feeding strategies and living habitats, and thus become an ideal lineage for studies on adaptive evolution. Chinese water scorpion Ranatra chinensis (Heteroptera: Nepidae) is a predaceous bug living in lentic water systems, representing an ideal model for studying habitat transition and adaptation to water environment. However, genetic studies on this water bug remain limited. Here, we obtained a chromosome-level genome of R. chinensis using PacBio HiFi long reads and Hi-C sequencing reads. The total assembly size of genome is 867.89 Mb, with a scaffold N50 length of 26.48 Mb and the GC content of 39.50%. All contigs were assembled into 23 pseudo-chromosomes (N = 19 A + X1X2X3X4), and we predicted 18,424 protein-coding genes in this genome. This study will provide valuable genomic resources for future studies on the biology, water adaptation, and genome evolution of water bugs.

An orthology-based methodology as a complementary approach to retrieve evolutionarily conserved A-to-I RNA editing sites.

Adar-mediated adenosine-to-inosine (A-to-I) mRNA editing is a conserved mechanism that exerts diverse regulatory functions during the development, evolution, and adaptation of metazoans. The accurate detection of RNA editing sites helps us understand their biological significance. In this work, with an improved genome assembly of honeybee (Apis mellifera), we used a new orthology-based methodology to complement the traditional pipeline of (de novo) RNA editing detection. Compared to the outcome of traditional pipeline, we retrieved many novel editing sites in CDS that are deeply conserved between honeybee and other distantly related insects. The newly retrieved sites were missed by the traditional de novo identification due to the stringent criteria for controlling false-positive rate. Caste-specific editing sites are identified, including an Ile>Met auto-recoding site in Adar. This recoding was even conserved between honeybee and bumblebee, suggesting its putative regulatory role in shaping the phenotypic plasticity of eusocial Hymenoptera. In summary, we proposed a complementary approach to the traditional pipeline and retrieved several previously unnoticed CDS editing sites. From both technical and biological aspects, our works facilitate future researches on finding the functional editing sites and advance our understanding on the connection between RNA editing and the great phenotypic diversity of organisms.

RetSat stabilizes mitotic chromosome segregation in pluripotent stem cells.

BACKGROUND: Chromosome stability is crucial for homeostasis of pluripotent stem cells (PSCs) and early-stage embryonic development. Chromosomal defects may raise carcinogenic risks in regenerative medicine when using PSCs as original materials. However, the detailed mechanism regarding PSCs chromosome stability maintenance is not fully understood. METHODS: Mouse embryonic stem cells (line D3) and human embryonic stem cells (line H9) were cultured under standard conditions. To confirm the loading of RetSat protein on mitotic chromosomes of PSCs, immunostaining was performed in PSCs spontaneous differentiation assay and iPSC reprogramming assay from mouse embryonic fibroblasts (MEFs), respectively. In addition, qPCR, immunoprecipitation, LC-MS/MS and immunoblotting were used to study the expression of RetSat, and interactions of RetSat with cohesin/condensin components. RNA sequencing and teratoma formation assay was conducted to evaluate the carcinogenic risk of mouse embryonic stem cells with RetSat deletion. RESULTS: We reported a PSC high-expressing gene, RetSat, plays key roles in chromosome stabilization. We identified RetSat protein localizing onto mitotic chromosomes specifically in stemness positive cells such as embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSCs). We found dramatic chromosome instability, e.g. chromosome bridging, lagging and interphase micronuclei in mouse and human ESCs when down regulating RetSat. RetSat knock-out mouse ESCs upregulated cancer associated gene pathways, and displayed higher tumorigenic capacities in teratoma formation assay. Mechanistically, we confirmed that RetSat interacts with cohesin/condensin components Smc1a and Nudcd2. RetSat deletion impaired the chromosome loading dosage of Smc1a, Smc3 and Nudcd2. CONCLUSIONS: In summary, we reported RetSat to be a key stabilizer of chromosome condensation in pluripotent stem cells. This highlights the crucial roles of RetSat in early-stage embryonic development, and potential value of RetSat as an effective biomarker for assessing the quality of pluripotent stem cells.

Comparative genomic analyses on assassin bug Rhynocoris fuscipes (Hemiptera: Reduviidae) reveal genetic bases governing the diet-shift.

Genetic basis underlying the biodiversity and phenotypic plasticity are fascinating questions in evolutionary biology. Such molecular diversity can be achieved at multi-omics levels. Here, we sequenced the first chromosome-level genome of assassin bug Rhynocoris fuscipes, a polyphagous generalist predator for biological control of agroecosystems. Compared to non-predatory true bugs Apolygus lucorum and Riptortus pedestris, the R. fuscipes-specific genes were enriched in diet-related genes (e.g., serine proteinase, cytochrome P450) which had higher expression level and more exons than non-diet genes. Extensive A-to-I RNA editing was identified in all three species and showed enrichment in genes associated with diet in R. fuscipes, diversifying the transcriptome. An extended analysis between five predaceous and 27 phytophagous hemipteran species revealed an expansion of diet-related genes in R. fuscipes. Our findings bridge the gap between genotype and phenotype, and also advance our understanding on genetic and epigenetic bases governing the diet shifts in ture bugs.

Learning from the Codon Table: Convergent Recoding Provides Novel Understanding on the Evolution of A-to-I RNA Editing.

Adenosine-to-inosine (A-to-I) RNA editing recodes the genetic information. Apart from diversifying the proteome, another tempting advantage of RNA recoding is to correct deleterious DNA mutation and restore ancestral allele. Solid evidences for beneficial restorative editing are very rare in animals. By searching for "convergent recoding" under a phylogenetic context, we proposed this term for judging the potential restorative functions of particular editing site. For the well-known mammalian Gln>Arg (Q>R) recoding site, its ancestral state in vertebrate genomes was the pre-editing Gln, and all 470 available mammalian genomes strictly avoid other three equivalent ways to achieve Arg in protein. The absence of convergent recoding from His>Arg, or synonymous mutations on Gln codons, could be attributed to the strong maintenance on editing motif and structure, but the absence of direct A-to-G mutation is extremely unexpected. With similar ideas, we found cases of convergent recoding in Drosophila genus, reducing the possibility of their restorative function. In summary, we defined an interesting scenario of convergent recoding, the occurrence of which could be used as preliminary judgements for whether a recoding site has a sole restorative role. Our work provides novel insights to the natural selection and evolution of RNA editing.

Conserved A-to-I RNA editing with non-conserved recoding expands the candidates of functional editing sites.

Adenosine-to-inosine (A-to-I) RNA editing recodes the genome and confers flexibility for the organisms to adapt to the environment. It is believed that RNA recoding sites are well suited for facilitating adaptive evolution by increasing the proteomic diversity in a temporal-spatial manner. The function and essentiality of a few conserved recoding sites are recognized. However, the experimentally discovered functional sites only make up a small corner of the total sites, and there is still the need to expand the repertoire of such functional sites with bioinformatic approaches. In this study, we define a new category of RNA editing sites termed 'conserved editing with non-conserved recoding' and systematically identify such sites in Drosophila editomes, figuring out their selection pressure and signals of adaptation at inter-species and intra-species levels. Surprisingly, conserved editing sites with non-conserved recoding are not suppressed and are even slightly overrepresented in Drosophila. DNA mutations leading to such cases are also favoured during evolution, suggesting that the function of those recoding events in different species might be diverged, specialized, and maintained. Finally, structural prediction suggests that such recoding in potassium channel Shab might increase ion permeability and compensate the effect of low temperature. In conclusion, conserved editing with non-conserved recoding might be functional as well. Our study provides novel aspects in considering the adaptive evolution of RNA editing sites and meanwhile expands the candidates of functional recoding sites for future validation.

Does coevolution in refugia drive mimicry in bumble bees? Insights from a South Asian mimicry group.

Müllerian mimicry was proposed to be an example of a coevolved mutualism promoted by population isolation in glacial refugia. This, however, has not been well supported in butterfly models. Here, we use genomic data to test this theory while examining the population genetics behind mimetic diversification in a pair of co-mimetic bumble bees, Bombus breviceps Smith and Bombus trifasciatus Smith. In both lineages, populations were structured by geography but not as much by color pattern, suggesting sharing of color alleles across regions of restricted gene flow and formation of mimicry complexes in the absence of genetic differentiation. Demographic analyses showed mismatches between historical effective population size changes and glacial cycles, and niche modeling revealed only mild habitat retraction during glaciation. Moreover, mimetic subpopulations of the same color form in the two lineages only in some cases exhibit similar population history and genetic divergence. Therefore, the current study supports a more complex history in this comimicry than a simple refugium-coevolution model.

Melanasterasinica He & Burckhardt, sp. nov., a new psylloid species (Hemiptera, Psylloidea, Liviidae) from China developing on Grewia sp. (Malvaceae).

Melanasterasinica He & Burckhardt, sp. nov., a new psylloid species developing on Grewia sp., is described from Hainan, China. It is the first Melanastera species reported from Asia and China, and the second species from the Old World. While New World species of Melanastera are mostly associated with the plant families Melastomataceae and Annonaceae, the two Old World species develop on the malvaceous Grewia, a host otherwise used in psylloids by two Haplaphalara species. The new species is described, diagnosed and illustrated, and its host plant and biogeographic ranges are discussed.

Phylogeographic Pattern of the Assassin Bug Sycanus bifidus Inferred from Mitochondrial Genomes and Nuclear Genes.

The assassin bug Sycanus bifidus has a wide distribution across southern China. This study explored its distribution and evolution by analyzing mitochondrial and nuclear ribosomal RNA genes, revealing how Pleistocene climate and geological changes shaped its phylogeography. We identified two main clades, A and B, that diverged in the Middle Pleistocene. Hainan Island's populations form a unique group within Clade A, suggesting that the Qiongzhou Strait served as a dispersal corridor during glaciation. Rising sea levels likely separated the Hainan population afterward. Ecological niche modeling showed that both populations have been viable since the last interglacial period, with demographic analyses indicating possible expansions during the Middle and Late Pleistocene, driven by favorable climates. This study highlights the significant effects of Pleistocene sea-level and climatic changes on the distribution and evolution of S. bifidus in China.

A review on recent taxonomic updates of gut bacteria associated with social bees, with a curated genomic reference database.

Honeybees and bumblebees play a crucial role as essential pollinators. The special gut microbiome of social bees is a key factor in determining the overall fitness and health of the host. Although bees harbor relatively simple microbial communities at the genus level, recent studies have unveiled significant genetic divergence and variations in gene content within each bacterial genus. However, a comprehensive and refined genomics-based taxonomic database specific to social bee gut microbiomes remains lacking. Here, we first provided an overview of the current knowledge on the distribution and function of social bee gut bacteria, as well as the factors that influence the gut population dynamics. We then consolidated all available genomes of the gut bacteria of social bees and refined the species-level taxonomy, by constructing a maximum-likelihood core genome phylogeny and calculating genome-wide pairwise average nucleotide identity. On the basis of the refined species taxonomy, we constructed a curated genomic reference database, named the bee gut microbe genome sequence database (BGM-GDb). To evaluate the species-profiling performance of the curated BGM-GDb, we retrieved a series of bee gut metagenomic data and inferred the species-level composition using metagenomic intra-species diversity analysis system (MIDAS), and then compared the results with those obtained from a prebuilt MIDAS database. We found that compared with the default database, the BGM-GDb excelled in aligned read counts and bacterial richness. Overall, this high-resolution and precise genomic reference database will facilitate research in understanding the gut community structure of social bees.

Meningioma achieves malignancy and erastin-induced ferroptosis resistance through FOXM1-AURKA-NRF2 axis.

The oncogene Aurora kinase A (AURKA) has been implicated in various tumor, yet its role in meningioma remains unexplored. Recent studies have suggested a potential link between AURKA and ferroptosis, although the underlying mechanisms are unclear. This study presented evidence of AURKA upregulation in high grade meningioma and its ability to enhance malignant characteristics. We identified AURKA as a suppressor of erastin-induced ferroptosis in meningioma. Mechanistically, AURKA directly interacted with and phosphorylated kelch-like ECH-associated protein 1 (KEAP1), thereby activating nuclear factor erythroid 2 related factor 2 (NFE2L2/NRF2) and target genes transcription. Additionally, forkhead box protein M1 (FOXM1) facilitated the transcription of AURKA. Suppression of AURKA, in conjunction with erastin, yields significant enhancements in the prognosis of a murine model of meningioma. Our study elucidates an unidentified mechanism by which AURKA governs ferroptosis, and strongly suggests that the combination of AURKA inhibition and ferroptosis-inducing agents could potentially provide therapeutic benefits for meningioma treatment.

The first A-to-I RNA editome of hemipteran species Coridius chinensis reveals overrepresented recoding and prevalent intron editing in early-diverging insects.

BACKGROUND: Metazoan adenosine-to-inosine (A-to-I) RNA editing resembles A-to-G mutation and increases proteomic diversity in a temporal-spatial manner, allowing organisms adapting to changeable environment. The RNA editomes in many major animal clades remain unexplored, hampering the understanding on the evolution and adaptation of this essential post-transcriptional modification. METHODS: We assembled the chromosome-level genome of Coridius chinensis belonging to Hemiptera, the fifth largest insect order where RNA editing has not been studied yet. We generated ten head RNA-Seq libraries with DNA-Seq from the matched individuals. RESULTS: We identified thousands of high-confidence RNA editing sites in C. chinensis. Overrepresentation of nonsynonymous editing was observed, but conserved recoding across different orders was very rare. Under cold stress, the global editing efficiency was down-regulated and the general transcriptional processes were shut down. Nevertheless, we found an interesting site with "conserved editing but non-conserved recoding" in potassium channel Shab which was significantly up-regulated in cold, serving as a candidate functional site in response to temperature stress. CONCLUSIONS: RNA editing in C. chinensis largely recodes the proteome. The first RNA editome in Hemiptera indicates independent origin of beneficial recoding during insect evolution, which advances our understanding on the evolution, conservation, and adaptation of RNA editing.

Comparative genomic analyses reveal evidence for adaptive A-to-I RNA editing in insect Adar gene.

Although A-to-I RNA editing leads to similar effects to A-to-G DNA mutation, nonsynonymous RNA editing (recoding) is believed to confer its adaptiveness by 'epigenetically' regulating proteomic diversity in a temporospatial manner, avoiding the pleiotropic effect of genomic mutations. Recent discoveries on the evolutionary trajectory of Ser>Gly auto-editing site in insect Adar gene demonstrated a selective advantage to having an editable codon compared to uneditable ones. However, apart from pure observations, quantitative approaches for justifying the adaptiveness of individual RNA editing sites are still lacking. We performed a comparative genomic analysis on 113 Diptera species, focusing on the Adar Ser>Gly auto-recoding site in Drosophila. We only found one species having a derived Gly at the corresponding site, and this occurrence was significantly lower than genome-wide random expectation. This suggests that the Adar Ser>Gly site is unlikely to be genomically replaced with G during evolution, and thus indicating the advantage of editable status over hardwired genomic alleles. Similar trends were observed for the conserved Ile>Met recoding in gene Syt1. In the light of evolution, we established a comparative genomic approach for quantitatively justifying the adaptiveness of individual editing sites. Priority should be given to such adaptive editing sites in future functional studies.

Review of the Genus Sycanus Amyot & Serville, 1843 (Heteroptera: Reduviidae: Harpactorinae), from China Based on DNA Barcoding and Morphological Evidence.

Due to the variability of body coloration and morphological similarity among closely related species, unresolved issues and debates still persist in the taxonomic study of the genus Sycanus from China. In this study, we conducted phylogenetic analyses and species delimitation for Sycanus in China based on a COI DNA barcoding dataset comprising 81 samples. The results revealed that all the samples could be classified into 12 species by integrating molecular analyses with morphological comparison. This paper provides a comprehensive systematic review of the Sycanus species found in China, including descriptions of three new species: S. taiwanensis Zhao & Cai sp. nov., S. flavicorius Li & Cai sp. nov., and S. hainanensis Wang & Cai sp. nov. Furthermore, it is proposed that S. croceovittatus Dohrn, 1859, S. leucomesus Walker, 1873, and S. villicus Stål, 1863, are three synonyms of S. bifidus (Fabricius, 1787); S. bicolor Hsiao, 1979, is a synonym of S. versicolor Dohrn, 1859; and S. hsiaoi Maldonado-Capriles, 1990, is a synonym of S. marginellus Putshkov, 1987. Additionally, brief biological information is provided for two species, S. falleni Stål, 1863, and S. croceus Hsiao, 1979.

Chromosome-level genome of the poultry shaft louse Menopon gallinae provides insight into the host-switching and adaptive evolution of parasitic lice.

BACKGROUND: Lice (Psocodea: Phthiraptera) are one important group of parasites that infects birds and mammals. It is believed that the ancestor of parasitic lice originated on the ancient avian host, and ancient mammals acquired these parasites via host-switching from birds. Here we present the first chromosome-level genome of Menopon gallinae in Amblycera (earliest diverging lineage of parasitic lice). We explore the transition of louse host-switching from birds to mammals at the genomic level by identifying numerous idiosyncratic genomic variations. RESULTS: The assembled genome is 155 Mb in length, with a contig N50 of 27.42 Mb. Hi-C scaffolding assigned 97% of the bases to 5 chromosomes. The genome of M. gallinae retains a basal insect repertoire of 11,950 protein-coding genes. By comparing the genomes of lice to those of multiple representative insects in other orders, we discovered that gene families of digestion, detoxification, and immunity-related are generally conserved between bird lice and mammal lice, while mammal lice have undergone a significant reduction in genes related to chemosensory systems and temperature. This suggests that mammal lice have lost some of these genes through the adaption to environment and temperatures after host-switching. Furthermore, 7 genes related to hematophagy were positively selected in mammal lice, suggesting their involvement in the hematophagous behavior. CONCLUSIONS: Our high-quality genome of M. gallinae provides a valuable resource for comparative genomic research in Phthiraptera and facilitates further studies on adaptive evolution of host-switching within parasitic lice.

Natural selection and genetic diversity maintenance in a parasitic wasp during continuous biological control application.

Aphidius gifuensis is a parasitoid wasp and primary endoparasitoid enemy of the peach potato aphid, Myzus persicae. Artificially reared, captive wasps of this species have been extensively and effectively used to control populations of aphids and limit crop loss. However, the consequences of large-scale releasing of captive A. gifuensis, such as genetic erosion and reduced fitness in wild populations of this species, remains unclear. Here, we sequence the genomes of 542 A. gifuensis individuals collected across China, including 265 wild and 277 human-intervened samples. Population genetic analyses on wild individuals recovered Yunnan populations as the ancestral group with the most complex genetic structure. We also find genetic signature of environmental adaptation during the dispersal of wild populations from Yunnan to other regions. While comparative genomic analyses of captive wasps revealed a decrease in genetic diversity during long-term rearing, population genomic analyses revealed signatures of natural selection by several biotic (host plants) or abiotic (climate) factors, which support maintenance of the gene pool of wild populations in spite of the introduction of captive wasps. Therefore, the impact of large-scale release is reduced. Our study suggests that A. gifuensis is a good system for exploring the genetic and evolutionary effects of mass rearing and release on species commonly used as biocontrol agents.

Narrowing down the candidates of beneficial A-to-I RNA editing by comparing the recoding sites with uneditable counterparts.

Adar-mediated adenosine-to-inosine (A-to-I) RNA editing mainly occurs in nucleus and diversifies the transcriptome in a flexible manner. It has been a challenging task to identify beneficial editing sites from the sea of total editing events. The functional Ser>Gly auto-recoding site in insect Adar gene has uneditable Ser codons in ancestral nodes, indicating the selective advantage to having an editable status. Here, we extended this case study to more metazoan species, and also looked for all Drosophila recoding events with potential uneditable synonymous codons. Interestingly, in D. melanogaster, the abundant nonsynonymous editing is enriched in the codons that have uneditable counterparts, but the Adar Ser>Gly case suggests that the editable orthologous codons in other species are not necessarily edited. The use of editable versus ancestral uneditable codon is a smart way to infer the selective advantage of RNA editing, and priority might be given to these editing sites for functional studies due to the feasibility to construct an uneditable allele. Our study proposes an idea to narrow down the candidates of beneficial recoding sites. Meanwhile, we stress that the matched transcriptomes are needed to verify the conservation of editing events during evolution.

O-GlcNAcylation of melanophilin enhances radiation resistance in glioblastoma via suppressing TRIM21 mediated ubiquitination.

The molecular mechanism of glioblastoma (GBM) radiation resistance remains poorly understood. The aim of this study was to elucidate the potential role of Melanophilin (MLPH) O-GlcNAcylation and the specific mechanism through which it regulates GBM radiotherapy resistance. We found that MLPH was significantly upregulated in recurrent GBM tumor tissues after ionizing radiation (IR). MLPH induced radiotherapy resistance in GBM cells and xenotransplanted human tumors through regulating the NF-κB pathway. MLPH was O-GlcNAcylated at the conserved serine 510, and radiation-resistant GBM cells showed higher levels of O-GlcNAcylation of MLPH. O-GlcNAcylation of MLPH protected its protein stability and tripartite motif containing 21(TRIM21) was identified as an E3 ubiquitin ligase promoting MLPH degradation whose interaction with MLPH was affected by O-GlcNAcylation. Our data demonstrate that MLPH exerts regulatory functions in GBM radiation resistance by promoting the NF-κB signaling pathway and that O-GlcNAcylation of MLPH both stabilizes and protects it from TRIM21-mediated ubiquitination. These results identify a potential mechanism of GBM radiation resistance and suggest a potential therapeutic strategy for GBM treatment.

Genetic Modification of a Hox Locus Drives Mimetic Color Pattern Variation in a Highly Polymorphic Bumble Bee.

Müllerian mimicry provides natural replicates ideal for exploring mechanisms underlying adaptive phenotypic divergence and convergence, yet the genetic mechanisms underlying mimetic variation remain largely unknown. The current study investigates the genetic basis of mimetic color pattern variation in a highly polymorphic bumble bee, Bombus breviceps (Hymenoptera, Apidae). In South Asia, this species and multiple comimetic species converge onto local Müllerian mimicry patterns by shifting the abdominal setal color from orange to black. Genetic crossing between the orange and black phenotypes suggested the color dimorphism being controlled by a single Mendelian locus, with the orange allele being dominant over black. Genome-wide association suggests that a locus at the intergenic region between 2 abdominal fate-determining Hox genes, abd-A and Abd-B, is associated with the color change. This locus is therefore in the same intergenic region but not the same exact locus as found to drive red black midabdominal variation in a distantly related bumble bee species, Bombus melanopygus. Gene expression analysis and RNA interferences suggest that differential expression of an intergenic long noncoding RNA between abd-A and Abd-B at the onset setal color differentiation may drive the orange black color variation by causing a homeotic shift late in development. Analysis of this same color locus in comimetic species reveals no sequence association with the same color shift, suggesting that mimetic convergence is achieved through distinct genetic routes. Our study establishes Hox regions as genomic hotspots for color pattern evolution in bumble bees and demonstrates how pleiotropic developmental loci can drive adaptive radiations in nature.