The genomic ecosystem of transposable elements in maize

PLoS Genet. 2021 Oct 14;17(10):e1009768. doi: 10.1371/journal.pgen.1009768. eCollection 2021 Oct.

Abstract

Transposable elements (TEs) constitute the majority of flowering plant DNA, reflecting their tremendous success in subverting, avoiding, and surviving the defenses of their host genomes to ensure their selfish replication. More than 85% of the sequence of the maize genome can be ascribed to past transposition, providing a major contribution to the structure of the genome. Evidence from individual loci has informed our understanding of how transposition has shaped the genome, and a number of individual TE insertions have been causally linked to dramatic phenotypic changes. Genome-wide analyses in maize and other taxa have frequently represented TEs as a relatively homogeneous class of fragmentary relics of past transposition, obscuring their evolutionary history and interaction with their host genome. Using an updated annotation of structurally intact TEs in the maize reference genome, we investigate the family-level dynamics of TEs in maize. Integrating a variety of data, from descriptors of individual TEs like coding capacity, expression, and methylation, as well as similar features of the sequence they inserted into, we model the relationship between attributes of the genomic environment and the survival of TE copies and families. In contrast to the wholesale relegation of all TEs to a single category of junk DNA, these differences reveal a diversity of survival strategies of TE families. Together these generate a rich ecology of the genome, with each TE family representing the evolution of a distinct ecological niche. We conclude that while the impact of transposition is highly family- and context-dependent, a family-level understanding of the ecology of TEs in the genome can refine our ability to predict the role of TEs in generating genetic and phenotypic diversity.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • DNA Transposable Elements / genetics*
  • Ecosystem
  • Evolution, Molecular
  • Genome, Plant / genetics*
  • Genome-Wide Association Study / methods
  • Genomics / methods
  • Molecular Sequence Annotation / methods
  • Sequence Analysis, DNA / methods
  • Zea mays / genetics*

Substances

  • DNA Transposable Elements

Grants and funding

M.C.S. and J.R.-I. are supported by the National Science Foundation Plant Genome award 1238014. M.C.S. acknowledges support from the National Science Foundation Graduate Research Fellowship under Grant No. 1650042; J.R.-I. acknowledges support from the USDA Hatch project CA-D-PLS-2066-H. S.N.A. and N.M.S. are supported by a grant from USDA-NIFA (2016-67013-24747). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.