Improved genome assembly provides new insights into the environmental adaptation of the American cockroach, Periplaneta americana

The synanthropic pest and a model organism for entomological research, American cockroach, Periplaneta americana (Linnaeus), can survive in unfavorable environments for humans. To investigate the genetic mechanisms of success in environmental adaptation of P. americana, we de novo reassembled its wh...

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Veröffentlicht in:Archives of insect biochemistry and physiology 2022-12, Vol.111 (4), p.e21956-n/a
Hauptverfasser: Zheng, Xiaofeng, Wang, Lei, Liu, Yi, Yang, Zhen, Li, Fengjun, Yan, Lin, Shen, Yongmei, Yue, Bisong, Zhou, Chuang
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container_title Archives of insect biochemistry and physiology
container_volume 111
creator Zheng, Xiaofeng
Wang, Lei
Liu, Yi
Yang, Zhen
Li, Fengjun
Yan, Lin
Shen, Yongmei
Yue, Bisong
Zhou, Chuang
description The synanthropic pest and a model organism for entomological research, American cockroach, Periplaneta americana (Linnaeus), can survive in unfavorable environments for humans. To investigate the genetic mechanisms of success in environmental adaptation of P. americana, we de novo reassembled its whole genome based on next‐generation sequencing and PacBio sequencing. The final genome reassembly consisted of approximately 3.34 Gb with scaffold N50 of 465.51 Kb. The completeness (95.4%) of the complete genome was evaluated with single‐copy orthologous genes using BUSCO. We identified 18,618 protein‐coding genes, 16,443 (88.32%) of which were well supported by public protein databases. We identified 482.04 Mb (approximately 14.45%) repeat elements, 1,385,093 perfect microsatellites simple sequence repeats in P. americana genome, which was higher than other four Blattaria insects. Comparative genomics analysis revealed obvious expansion in the gene families associated with chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), which provided the necessary information for functional characterization of the chemosensory receptors of P. americana, with potential for new or refined applications of semiochemicals‐based control of this pest insect. Similarly, gene families (cytochrome P450s, carboxyl/choline esterases, and UDP‐glycosyl‐transferases) encoding receptors for bitter or toxic substances and detoxification enzymes were obviously expanded in P. americana, enabling its ability to detect and detoxify many toxins. Enrichment analysis of positively selected genes in P. americana revealed items associated with metabolic process and catalytic activity, which possibly contributed to the pesticide resistance of P. americana. We also analyzed the homologs to antimicrobial peptide genes reported in the Drosophila genome, and identified two attacins and seven defensins in P. americana. Our data and findings will substantially facilitate molecular studies in P. americana, including elucidation of detoxification mechanisms of xenobiotic, as well as development of new pest management strategies for the control of pests like P. americana. Gene families involved in chemoreception and detoxification in the Periplaneta americana and other four Blattaria insects. Highlights The whole genome of Periplaneta americana, an omnivorous scavenger, was de novo reassembled with size of 3.34
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To investigate the genetic mechanisms of success in environmental adaptation of P. americana, we de novo reassembled its whole genome based on next‐generation sequencing and PacBio sequencing. The final genome reassembly consisted of approximately 3.34 Gb with scaffold N50 of 465.51 Kb. The completeness (95.4%) of the complete genome was evaluated with single‐copy orthologous genes using BUSCO. We identified 18,618 protein‐coding genes, 16,443 (88.32%) of which were well supported by public protein databases. We identified 482.04 Mb (approximately 14.45%) repeat elements, 1,385,093 perfect microsatellites simple sequence repeats in P. americana genome, which was higher than other four Blattaria insects. Comparative genomics analysis revealed obvious expansion in the gene families associated with chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), which provided the necessary information for functional characterization of the chemosensory receptors of P. americana, with potential for new or refined applications of semiochemicals‐based control of this pest insect. Similarly, gene families (cytochrome P450s, carboxyl/choline esterases, and UDP‐glycosyl‐transferases) encoding receptors for bitter or toxic substances and detoxification enzymes were obviously expanded in P. americana, enabling its ability to detect and detoxify many toxins. Enrichment analysis of positively selected genes in P. americana revealed items associated with metabolic process and catalytic activity, which possibly contributed to the pesticide resistance of P. americana. We also analyzed the homologs to antimicrobial peptide genes reported in the Drosophila genome, and identified two attacins and seven defensins in P. americana. Our data and findings will substantially facilitate molecular studies in P. americana, including elucidation of detoxification mechanisms of xenobiotic, as well as development of new pest management strategies for the control of pests like P. americana. Gene families involved in chemoreception and detoxification in the Periplaneta americana and other four Blattaria insects. Highlights The whole genome of Periplaneta americana, an omnivorous scavenger, was de novo reassembled with size of 3.34 Gb and scaffold N50 of 465.51 Kb. Obvious expansions were observed in the gene families of chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), indicating potential adaptive strategies of P. americana for survival, reproduction, and social communication. The detoxification system (cytochrome P450s, carboxyl/choline esterases, and UDP‐glycosyl‐transferases) also showed significant expansion. Furthermore, positively selected genes were enriched to multiple pathways related to pesticide resistance, suggesting strong detoxification ability of P. americana. There were two attacins and seven defensins identified, probably responsible for the efficient immune system of P. americana.</description><identifier>ISSN: 0739-4462</identifier><identifier>EISSN: 1520-6327</identifier><identifier>DOI: 10.1002/arch.21956</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc</publisher><subject>Adaptation ; Antiinfectives and antibacterials ; Antimicrobial peptides ; Catalytic activity ; Chemical communication ; Chemical pest control ; Chemoreception ; Choline ; Cockroaches ; Coding ; Communications systems ; comparative genomics ; Cytochrome ; Cytochromes ; Defensins ; Detoxification ; environmental adaptation ; Esterases ; Gene families ; gene family expansion ; Gene sequencing ; Genes ; Genomes ; Genomics ; Glutamic acid receptors (ionotropic) ; Immune system ; Insecticide resistance ; Insects ; Membrane proteins ; Membranes ; Microsatellites ; Nucleotide sequence ; Odorant receptors ; Periplaneta americana ; Pest control ; Pesticide resistance ; Pesticides ; Pests ; positive selection ; Proteins ; Receptors ; Scaffolds ; Semiochemicals ; Simple sequence repeats ; Taste receptors ; Toxic substances ; Toxins</subject><ispartof>Archives of insect biochemistry and physiology, 2022-12, Vol.111 (4), p.e21956-n/a</ispartof><rights>2022 Wiley Periodicals LLC.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3346-75c1a981c1efc071e50a3f8cb6a6657c31dbc4b9e41e0af574b35f41dd52c9973</citedby><cites>FETCH-LOGICAL-c3346-75c1a981c1efc071e50a3f8cb6a6657c31dbc4b9e41e0af574b35f41dd52c9973</cites><orcidid>0000-0002-6163-2410</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Farch.21956$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Farch.21956$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,27922,27923,45572,45573</link.rule.ids></links><search><creatorcontrib>Zheng, Xiaofeng</creatorcontrib><creatorcontrib>Wang, Lei</creatorcontrib><creatorcontrib>Liu, Yi</creatorcontrib><creatorcontrib>Yang, Zhen</creatorcontrib><creatorcontrib>Li, Fengjun</creatorcontrib><creatorcontrib>Yan, Lin</creatorcontrib><creatorcontrib>Shen, Yongmei</creatorcontrib><creatorcontrib>Yue, Bisong</creatorcontrib><creatorcontrib>Zhou, Chuang</creatorcontrib><title>Improved genome assembly provides new insights into the environmental adaptation of the American cockroach, Periplaneta americana</title><title>Archives of insect biochemistry and physiology</title><description>The synanthropic pest and a model organism for entomological research, American cockroach, Periplaneta americana (Linnaeus), can survive in unfavorable environments for humans. To investigate the genetic mechanisms of success in environmental adaptation of P. americana, we de novo reassembled its whole genome based on next‐generation sequencing and PacBio sequencing. The final genome reassembly consisted of approximately 3.34 Gb with scaffold N50 of 465.51 Kb. The completeness (95.4%) of the complete genome was evaluated with single‐copy orthologous genes using BUSCO. We identified 18,618 protein‐coding genes, 16,443 (88.32%) of which were well supported by public protein databases. We identified 482.04 Mb (approximately 14.45%) repeat elements, 1,385,093 perfect microsatellites simple sequence repeats in P. americana genome, which was higher than other four Blattaria insects. Comparative genomics analysis revealed obvious expansion in the gene families associated with chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), which provided the necessary information for functional characterization of the chemosensory receptors of P. americana, with potential for new or refined applications of semiochemicals‐based control of this pest insect. Similarly, gene families (cytochrome P450s, carboxyl/choline esterases, and UDP‐glycosyl‐transferases) encoding receptors for bitter or toxic substances and detoxification enzymes were obviously expanded in P. americana, enabling its ability to detect and detoxify many toxins. Enrichment analysis of positively selected genes in P. americana revealed items associated with metabolic process and catalytic activity, which possibly contributed to the pesticide resistance of P. americana. We also analyzed the homologs to antimicrobial peptide genes reported in the Drosophila genome, and identified two attacins and seven defensins in P. americana. Our data and findings will substantially facilitate molecular studies in P. americana, including elucidation of detoxification mechanisms of xenobiotic, as well as development of new pest management strategies for the control of pests like P. americana. Gene families involved in chemoreception and detoxification in the Periplaneta americana and other four Blattaria insects. Highlights The whole genome of Periplaneta americana, an omnivorous scavenger, was de novo reassembled with size of 3.34 Gb and scaffold N50 of 465.51 Kb. Obvious expansions were observed in the gene families of chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), indicating potential adaptive strategies of P. americana for survival, reproduction, and social communication. The detoxification system (cytochrome P450s, carboxyl/choline esterases, and UDP‐glycosyl‐transferases) also showed significant expansion. Furthermore, positively selected genes were enriched to multiple pathways related to pesticide resistance, suggesting strong detoxification ability of P. americana. 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To investigate the genetic mechanisms of success in environmental adaptation of P. americana, we de novo reassembled its whole genome based on next‐generation sequencing and PacBio sequencing. The final genome reassembly consisted of approximately 3.34 Gb with scaffold N50 of 465.51 Kb. The completeness (95.4%) of the complete genome was evaluated with single‐copy orthologous genes using BUSCO. We identified 18,618 protein‐coding genes, 16,443 (88.32%) of which were well supported by public protein databases. We identified 482.04 Mb (approximately 14.45%) repeat elements, 1,385,093 perfect microsatellites simple sequence repeats in P. americana genome, which was higher than other four Blattaria insects. Comparative genomics analysis revealed obvious expansion in the gene families associated with chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), which provided the necessary information for functional characterization of the chemosensory receptors of P. americana, with potential for new or refined applications of semiochemicals‐based control of this pest insect. Similarly, gene families (cytochrome P450s, carboxyl/choline esterases, and UDP‐glycosyl‐transferases) encoding receptors for bitter or toxic substances and detoxification enzymes were obviously expanded in P. americana, enabling its ability to detect and detoxify many toxins. Enrichment analysis of positively selected genes in P. americana revealed items associated with metabolic process and catalytic activity, which possibly contributed to the pesticide resistance of P. americana. We also analyzed the homologs to antimicrobial peptide genes reported in the Drosophila genome, and identified two attacins and seven defensins in P. americana. Our data and findings will substantially facilitate molecular studies in P. americana, including elucidation of detoxification mechanisms of xenobiotic, as well as development of new pest management strategies for the control of pests like P. americana. Gene families involved in chemoreception and detoxification in the Periplaneta americana and other four Blattaria insects. Highlights The whole genome of Periplaneta americana, an omnivorous scavenger, was de novo reassembled with size of 3.34 Gb and scaffold N50 of 465.51 Kb. Obvious expansions were observed in the gene families of chemoreception (olfactory receptors, gustatory receptors, ionotropic glutamate receptors, chemosensory protein, and sensory neuron membrane protein), indicating potential adaptive strategies of P. americana for survival, reproduction, and social communication. The detoxification system (cytochrome P450s, carboxyl/choline esterases, and UDP‐glycosyl‐transferases) also showed significant expansion. Furthermore, positively selected genes were enriched to multiple pathways related to pesticide resistance, suggesting strong detoxification ability of P. americana. There were two attacins and seven defensins identified, probably responsible for the efficient immune system of P. americana.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1002/arch.21956</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-6163-2410</orcidid></addata></record>
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subjects Adaptation
Antiinfectives and antibacterials
Antimicrobial peptides
Catalytic activity
Chemical communication
Chemical pest control
Chemoreception
Choline
Cockroaches
Coding
Communications systems
comparative genomics
Cytochrome
Cytochromes
Defensins
Detoxification
environmental adaptation
Esterases
Gene families
gene family expansion
Gene sequencing
Genes
Genomes
Genomics
Glutamic acid receptors (ionotropic)
Immune system
Insecticide resistance
Insects
Membrane proteins
Membranes
Microsatellites
Nucleotide sequence
Odorant receptors
Periplaneta americana
Pest control
Pesticide resistance
Pesticides
Pests
positive selection
Proteins
Receptors
Scaffolds
Semiochemicals
Simple sequence repeats
Taste receptors
Toxic substances
Toxins
title Improved genome assembly provides new insights into the environmental adaptation of the American cockroach, Periplaneta americana
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