Genome assembly of the southern pine beetle (Dendroctonus frontalis Zimmerman) reveals the origins of gene content reduction in Dendroctonus

Megan Copeland, Shelby Landa, Adekola Oluwatosin Owoyemi, Michelle M. Jonika, James M. Alfieri, J. Spencer Johnston, Terrence Pradakshana Sylvester, Bethany R. Kyre, Zachary Hoover, Carl E. Hjelmen, Lynne K. Rieske, Heath Blackmon, Claudio Casola

Producción científica: Articlerevisión exhaustiva

1 Cita (Scopus)

Resumen

Dendroctonus frontalis also known as southern pine beetle (SPB), is the most damaging insect forest pest in the southeastern United States. Genomic data are important to provide information on pest biology and to identify molecular targets to develop improved pest management approaches. Here, we produced a chromosome-level genome assembly of SPB using long-read sequencing data. Synteny analyses confirmed the conservation of the core Coleopteran Stevens elements and validated the bona fide SPB X chromosome. Transcriptomic data were used to obtain 39 588 transcripts corresponding to 13 354 putative protein-coding loci. Comparative analyses of gene content across 14 beetles and three other insects revealed several losses of conserved genes in the Dendroctonus clade and gene gains in SPB and Dendroctonus that were enriched for loci encoding membrane proteins and extracellular matrix proteins. While lineage-specific gene losses contributed to the gene content reduction observed in Dendroctonus, we also showed that widespread misannotation of transposable elements represents an important cause of the apparent gene expansion in several non-Dendroctonus species. Our findings uncovered distinctive features of the SPB gene complement and disentangled the role of biological and annotation-related factors contributing to gene content variation across beetles.

Idioma originalEnglish
Número de artículo240755
PublicaciónRoyal Society Open Science
Volumen11
N.º12
DOI
EstadoPublished - dic 1 2024

Nota bibliográfica

Publisher Copyright:
© 2024 The Author(s).

Financiación

We thank the Eppley Foundation for Research, the Texas A&M AgriLife Research and the Texas A&M Forest Service for supporting this project. C.C. was supported by the USDA National Institute of Food and Agriculture project 1019860; H.B. was supported by the National Institute of General Medical Sciences at the National Institutes of Health R35GM138098. Acknowledgements. We are grateful to Brian T. Sullivan for assistance with collecting D. frontalis specimens. We thank four reviewers for their comments and insights. Ethics. This work did not require ethical approval from a human subject or animal welfare committee. Data accessibility. The Dendroctonus frontalis genome assembly sequence is available through the NCBI BioSample ID PRJNA1100959. Raw transcriptome sequencing reads are available through the SRA ID PRJNA1102401. Datasets and gene family analysis results are available through the following Figshare repository [75]. Supplementary material is available online [76]. Declaration of AI use. We have not used AI-assisted technologies in creating this article. Authors’ contributions. M.C.: data curation, formal analysis, visualization; S.L.: data curation, formal analysis, visualization; A.O.O.: data curation, formal analysis, visualization; M.M.J.: data curation, formal analysis, visualization; J.M.A.: data curation; J.S.J.: formal analysis; T.P.S.: formal analysis; B.R.K.: data curation; Z.H.: data curation; C.E.H.: data curation; L.K.R.: conceptualization, investigation, resources, writing—review and editing; H.B.: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, supervision, validation, visualization, writing—original draft, writing—review and editing; C.C.: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, supervision, validation, visualization, writing—original draft, writing—review and editing. All authors gave final approval for publication and agreed to be held accountable for the work performed therein. Conflict of interest declaration. We declare we have no competing interests. Funding. We thank the Eppley Foundation for Research, the Texas A&M AgriLife Research and the Texas A&M Forest Service for supporting this project. C.C. was supported by the USDA National Institute of Food and Agriculture project 1019860; H.B. was supported by the National Institute of General Medical Sciences at the National Institutes of Health R35GM138098. Acknowledgements. We are grateful to Brian T. Sullivan for assistance with collecting D. frontalis specimens. We thank four reviewers for their comments and insights.

FinanciadoresNúmero del financiador
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences
Texas Forest Service
Eppley Foundation for Research
College of Agriculture and Life Sciences, Texas A&M University
US Department of Agriculture National Institute of Food and Agriculture, Agriculture and Food Research Initiative1019860
National Institutes of Health (NIH)R35GM138098

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