Transposon dynamics in the emerging oilseed crop Thlaspi arvense

PLoS Genet. 2024 Jan 31;20(1):e1011141. doi: 10.1371/journal.pgen.1011141. eCollection 2024 Jan.

Abstract

Genome evolution is partly driven by the mobility of transposable elements (TEs) which often leads to deleterious effects, but their activity can also facilitate genetic novelty and catalyze local adaptation. We explored how the intraspecific diversity of TE polymorphisms might contribute to the broad geographic success and adaptive capacity of the emerging oil crop Thlaspi arvense (field pennycress). We classified the TE inventory based on a high-quality genome assembly, estimated the age of retrotransposon TE families and comprehensively assessed their mobilization potential. A survey of 280 accessions from 12 regions across the Northern hemisphere allowed us to quantify over 90,000 TE insertion polymorphisms (TIPs). Their distribution mirrored the genetic differentiation as measured by single nucleotide polymorphisms (SNPs). The number and types of mobile TE families vary substantially across populations, but there are also shared patterns common to all accessions. Ty3/Athila elements are the main drivers of TE diversity in T. arvense populations, while a single Ty1/Alesia lineage might be particularly important for transcriptome divergence. The number of retrotransposon TIPs is associated with variation at genes related to epigenetic regulation, including an apparent knockout mutation in BROMODOMAIN AND ATPase DOMAIN-CONTAINING PROTEIN 1 (BRAT1), while DNA transposons are associated with variation at the HSP19 heat shock protein gene. We propose that the high rate of mobilization activity can be harnessed for targeted gene expression diversification, which may ultimately present a toolbox for the potential use of transposition in breeding and domestication of T. arvense.

MeSH terms

  • DNA Transposable Elements / genetics
  • Epigenesis, Genetic
  • Evolution, Molecular
  • Genetic Drift
  • Humans
  • Nuclear Proteins / genetics
  • Plant Breeding
  • Retroelements / genetics
  • Thlaspi* / genetics
  • Thlaspi* / metabolism

Substances

  • Retroelements
  • DNA Transposable Elements
  • BRAT1 protein, human
  • Nuclear Proteins

Grants and funding

The study was supported by Marie Skłodowska Curie ETN EpiDiverse (EU Horizon 2020 Grant Agreement No. 764965; C.B., O.B., D.W.), the European Research Council (Grant Agreement No. 716823 “FEAR-SAP”; C.B.), the Novo Nordisk Foundation Novozymes Prize and the Max Planck Society (D.W.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.