The Genomic Ecosystem of Transposable Elements in Maize

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. But 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 ecological and evolutionary 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 these attributes of the genomic environment and the survival of TE copies and families. Our analyses reveal a diversity of ecological strategies of TE families, each representing the evolution of a distinct ecological niche allowing survival of the TE family. In contrast to the wholesale relegation of all TEs to a single category of junk DNA, these differences generate a rich ecology of the genome, suggesting families of TEs that coexist in time and space compete and cooperate with each other. 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. transposable elements | ecology | maize Correspondence: mcstitzer@ucdavis.edu 'Lumping our beautiful collection of transposons into a single category is a crime' -Michael R. Freeling,

Gene capture by transposable elements leads to epigenetic conflict in maize

“…If gene fragments provide camouflage for TEs, one reasonable prediction is that they will exist within the genome for longer periods of time than free TEs. Using the inferred age of elements from a previous study 34 , we found that this is indeed the case (Figure 4a). The above differences were principally caused by Sirevirus elements, perhaps in part reflecting their higher proportion of free TEs.…”

“…To test the first idea, we used age estimates from terminal branch lengths of TE phylogenetic trees generated by Stitzer at al. (2019) 34 . We found that TEs with captured fragments are older than free TEs (mean of 0.134 vs. 0.066 million years, one-sided Mann-Whitney-Wilcoxon Test p<2.2e-16; Figure 4a), suggesting that they have remained intact within the genome for longer periods.…”

“…We converted the chromosomal coordinates of TEs from v2 to the most recent v4 genome version using the Assembly Converter tool available in http://www.gramene.org/ (accepted TEs had >80% of length converted), and then overlapped the v4 coordinates with the recent maize TE annotation available at https://mcstitzer.github.io/maize_TEs/ (accepted TEs had >80% overlap). In this way, we retrieved information on insertion age based on terminal branch lengths generated by Stitzer et al (2019) 34 .…”

“…The first is Pack-MULEs themselves. They commonly capture genes and therefore provide a rich template for study, but often have lower methylation levels than other TE families 29,34 , possibly because they preferentially insert near the 5' termini of genes 35 . This tendency may lessen the potential for intragenomic conflict with their donor genes.…”

Degradation of the repetitive genomic landscape in a close relative ofC. elegans

“…But at the same time, the range in repeat content among eukaryotic genomes is great, with some species having a scant number of repetitive elements (0.8% in one species of bdelloid rotifer (Nowell, et al * Correspondence: gavincw@uoregon.edu 2018)). And not only does the global repeat content among genomes vary-heterogeneity in repeat content both within and between chromosomes occurs (Rizzon, et al 2002;Stitzer, et al 2019). Furthermore, repeat density in genomes has been observed to covary with patterns of genomic diversity (Clark, et al 2007), recombination rate (Rizzon, et al 2002), gene density (Medstrand, et al 2002), chromatin state (Peng and Karpen 2008), centromeric regions (Plohl, et al 2014) and physical spatial position (Guelen, et al 2008).…”