Three Groups of Transposable Elements with Contrasting Copy Number Dynamics and Host Responses in the Maize (Zea mays ssp. mays) Genome

Abstract

Most angiosperm nuclear DNA is repetitive and derived from silenced transposable elements (TEs). TE silencing requires substantial resources from the plant host, including the production of small interfering RNAs (siRNAs). Thus, the interaction between TEs and siRNAs is a critical aspect of both the function and the evolution of plant genomes. Yet the co-evolutionary dynamics between these two entities remain poorly characterized. Here we studied the organization of TEs within the maize (Zea mays ssp mays) genome, documenting that TEs fall within three groups based on the class and copy numbers. These groups included DNA elements, low copy RNA elements and higher copy RNA elements. The three groups varied statistically in characteristics that included length, location, age, siRNA expression and 24∶22 nucleotide (nt) siRNA targeting ratios. In addition, the low copy retroelements encompassed a set of TEs that had previously been shown to decrease expression within a 24 nt siRNA biogenesis mutant (mop1). To investigate the evolutionary dynamics of the three groups, we estimated their abundance in two landraces, one with a genome similar in size to that of the maize reference and the other with a 30% larger genome. For all three accessions, we assessed TE abundance as well as 22 nt and 24 nt siRNA content within leaves. The high copy number retroelements are under targeted similarly by siRNAs among accessions, appear to be born of a rapid bust of activity, and may be currently transpositionally dead or limited. In contrast, the lower copy number group of retrolements are targeted more dynamically and have had a long and ongoing history of transposition in the maize genome.

A role for palindromic structures in the cis-region of maize Sirevirus LTRs in transposable element evolution and host epigenetic response

“…These observations were further supported by comparing the average number of siRNA species that mapped to each element of each family, which was first normalized by the family's average genome length to allow cross-family comparisons (Supplemental Table S2). Altogether, these findings corroborate previous evidence that siRNA targeting does not necessarily correlate with TE abundance (Barber et al 2012;Diez et al 2014).…”

“…We mapped the previously published leaf (Diez et al 2014), tassel (Zhang et al 2009), and immature ear (Nobuta et al 2008) siRNA libraries to the reference maize B73 genome and assessed mapping patterns for 21-nt, 22-nt, and 24-nt siRNAs separately. Each distinct siRNA sequence was termed "species," and its number of reads was termed "expression."…”

“…For example, some studies used only U_siRNAs, but mapping was conducted on TE exemplars (Gent et al 2013;Regulski et al 2013). In contrast, other studies randomly allocated M_siRNAs to a single genomic locus (Wang et al 2009;He et al 2013) or weighted each M_siRNA by its number of mapping locations (Barber et al 2012;Diez et al 2014). Recently, tools have been developed that appoint M_siRNAs to single loci based on the densities of U_siRNAs among all possible options (Axtell 2013b).…”

Accessible DNA and Relative Depletion of H3K9me2 at Maize Loci Undergoing RNA-Directed DNA Methylation

“…In maize, both 24-nucleotide siRNAs and CHH methylation are more abundant near genes than in the expanses of repetitive intergenic DNA, giving rise to the term CHH islands (Gent et al, 2013). In addition, 24-nucleotide siRNAs in maize are much more highly associated with DNA transposons, which tend to be close to genes, than with LTR retrotransposons, which make up most of the intergenic spaces (Gent et al, 2013;Diez et al, 2014). The results of our genome-level studies using BS-seq in maize mutants, chromatin immunoprecipitation (ChIP), and MNase digestion extend and quantify these observations and indicate that heterochromatin in the traditional sense is structurally distinct from chromatin engaged in RdDM.…”

“…RdDM is primarily associated with the repression of transposons, but it can indirectly affect gene expression through genomic imprinting (Vu et al, 2013) and paramutation (reviewed in Hollick, 2012). Multiple studies have suggested that RdDM is not a uniform feature of heterochromatin in plant genomes but is enriched in particular heterochromatic regions, including 5S ribosomal loci, long terminal repeats of retrotransposons, DNA transposons, and repetitive elements in general when close to genes (Onodera et al, 2005;Zheng et al, 2012;Zhong et al, 2012;Gent et al, 2013;Regulski et al, 2013;Stroud et al, 2013;Sun et al, 2013;Zemach et al, 2013;Diez et al, 2014;Wei et al, 2014). In Arabidopsis, methylation in long transposons near centromeres can be mediated by the DNA methyltransferase CMT2 without the involvement of RdDM (Zemach et al, 2013).…”