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Insights into the genomic evolution of insects from cricket genomes.

ABSTRACT: Most of our knowledge of insect genomes comes from Holometabolous species, which undergo complete metamorphosis and have genomes typically under 2 Gb with little signs of DNA methylation. In contrast, Hemimetabolous insects undergo the presumed ancestral process of incomplete metamorphosis, and have larger genomes with high levels of DNA methylation. Hemimetabolous species from the Orthopteran order (grasshoppers and crickets) have some of the largest known insect genomes. What drives the evolution of these unusual insect genome sizes, remains unknown. Here we report the sequencing, assembly and annotation of the 1.66-Gb genome of the Mediterranean field cricket Gryllus bimaculatus, and the annotation of the 1.60-Gb genome of the Hawaiian cricket Laupala kohalensis. We compare these two cricket genomes with those of 14 additional insects and find evidence that hemimetabolous genomes expanded due to transposable element activity. Based on the ratio of observed to expected CpG sites, we find higher conservation and stronger purifying selection of methylated genes than non-methylated genes. Finally, our analysis suggests an expansion of the pickpocket class V gene family in crickets, which we speculate might play a role in the evolution of cricket courtship, including their characteristic chirping.

SUBMITTER: Ylla G

PROVIDER: S-EPMC8203789 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Insights into the genomic evolution of insects from cricket genomes.

Ylla Guillem G Nakamura Taro T Itoh Takehiko T Kajitani Rei R Toyoda Atsushi A Tomonari Sayuri S Bando Tetsuya T Ishimaru Yoshiyasu Y Watanabe Takahito T Fuketa Masao M Matsuoka Yuji Y Barnett Austen A AA Noji Sumihare S Mito Taro T Extavour Cassandra G CG

Communications biology 20210614 1

Most of our knowledge of insect genomes comes from Holometabolous species, which undergo complete metamorphosis and have genomes typically under 2 Gb with little signs of DNA methylation. In contrast, Hemimetabolous insects undergo the presumed ancestral process of incomplete metamorphosis, and have larger genomes with high levels of DNA methylation. Hemimetabolous species from the Orthopteran order (grasshoppers and crickets) have some of the largest known insect genomes. What drives the evolut ...[more]

PMID: 34127782

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Project description:BACKGROUND:As the developmental costs of genomic tools decline, genomic approaches to non-model systems are becoming more feasible. Many of these systems may lack advanced genetic tools but are extremely valuable models in other biological fields. Here we report the development of expressed sequence tags (EST's) in an orthopteroid insect, a model for the study of neurobiology, speciation, and evolution. RESULTS:We report the sequencing of 14,502 EST's from clones derived from a nerve cord cDNA library, and the subsequent construction of a Gene Index from these sequences, from the Hawaiian trigonidiine cricket Laupala kohalensis. The Gene Index contains 8607 unique sequences comprised of 2575 tentative consensus (TC) sequences and 6032 singletons. For each of the unique sequences, an attempt was made to assign a provisional annotation and to categorize its function using a Gene Ontology-based classification through a sequence-based comparison to known proteins. In addition, a set of unique 70 base pair oligomers that can be used for DNA microarrays was developed. All Gene Index information is posted at the DFCI Gene Indices web page CONCLUSION:Orthopterans are models used to understand the neurophysiological basis of complex motor patterns such as flight and stridulation. The sequences presented in the cricket Gene Index will provide neurophysiologists with many genetic tools that have been largely absent in this field. The cricket Gene Index is one of only two gene indices to be developed in an evolutionary model system. Species within the genus Laupala have speciated recently, rapidly, and extensively. Therefore, the genes identified in the cricket Gene Index can be used to study the genomics of speciation. Furthermore, this gene index represents a significant EST resources for basal insects. As such, this resource is a valuable comparative tool for the understanding of invertebrate molecular evolution. The sequences presented here will provide much needed genomic resources for three distinct but overlapping fields of inquiry: neurobiology, speciation, and molecular evolution.

Project description:Aroideae is an important subfamily of the Araceae family and contains many plants with medicinal and edible value. It is difficult to identify and classify Aroideae species accurately on the basis of morphology alone because of their polymorphic phenotypic traits. The chloroplast genome (CPG) is useful for studying on plant taxonomy and phylogeny, and the analysis of codon usage bias (CUB) in CPGs provides further insights into the intricate phylogenetic relationships among Aroideae. The results showed that the codon third position of the chloroplast genome coding sequence in Aroideae was rich in A and T, with a GC content of 37.91%. The ENC-plot and PR2-plot revealed that the codon usage bias of Aroideae was influenced by multiple factors, with natural selection as the dominant factor. Thirteen to twenty optimal codons ending in A/T were identified in 61 Aroideae species. Additionally, the comparative analysis of CPGs revealed that two single copy regions and non-coding regions were variable in Aroideae. Eight highly divergent regions (Pi > 0.064) were identified (ndhF, rpl32, ccsA, ndhE, ndhG, ndhF-rpl32, ccsA-ndhD, and ndhE-ndhG) , in which ndhE have the potential to serve as a reliable DNA marker to discriminate chloroplasts in Aroideae subfamily. Furthermore, the maximum likelihood-based phylogenetic trees constructed from complete chloroplast genomes and protein-coding sequences presented similar topologies. Principal component clustering analysis based on relative synonymous codon usage values (RSCUs) revealed that Calla was clearly deviated from Montrichardia and Anubias, and that Alocasia was closer to Colocasieae than to Arisaemateae. These findings suggest that the use of RSCU for clustering analysis could offer new theoretical support for species classification and evolution. Our research could provide a theoretical foundation for the chloroplast genetic engineering, taxonomy, and phylogenetic relationships of Aroideae chloroplasts.

Project description:BackgroundOpsins are key proteins in animal photoreception. Together with a light-sensitive group, the chromophore, they form visual pigments which initiate the visual transduction cascade when photoactivated. The spectral absorption properties of visual pigments are mainly determined by their opsins, and thus opsins are crucial for understanding the adaptations of animal eyes. Studies on the phylogeny and expression pattern of opsins have received considerable attention, but our knowledge about insect visual opsins is still limited. Up to now, researchers have focused on holometabolous insects, while general conclusions require sampling from a broader range of taxa. We have therefore investigated visual opsins in the ocelli and compound eyes of the two-spotted cricket Gryllus bimaculatus, a hemimetabolous insect.ResultsPhylogenetic analyses place all identified cricket sequences within the three main visual opsin clades of insects. We assign three of these opsins to visual pigments found in the compound eyes with peak absorbances in the green (515 nm), blue (445 nm) and UV (332 nm) spectral range. Their expression pattern divides the retina into distinct regions: (1) the polarization-sensitive dorsal rim area with blue- and UV-opsin, (2) a newly-discovered ventral band of ommatidia with blue- and green-opsin and (3) the remainder of the compound eye with UV- and green-opsin. In addition, we provide evidence for two ocellar photopigments with peak absorbances in the green (511 nm) and UV (350 nm) spectral range, and with opsins that differ from those expressed in the compound eyes.ConclusionsOur data show that cricket eyes are spectrally more specialized than has previously been assumed, suggesting that similar adaptations in other insect species might have been overlooked. The arrangement of spectral receptor types within some ommatidia of the cricket compound eyes differs from the generally accepted pattern found in holometabolous insect taxa and awaits a functional explanation. From the opsin phylogeny, we conclude that gene duplications, which permitted differential opsin expression in insect ocelli and compound eyes, occurred independently in several insect lineages and are recent compared to the origin of the eyes themselves.

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Insights into the genomic evolution of insects from cricket genomes.

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Insights into the genomic evolution of insects from cricket genomes.

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