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.

Highlights

  • Most DNA within angiosperm genomes is repetitive, typically representing active transposable elements (TEs) or DNA derived from formerly active TEs

  • These doublestranded RNAs are cleaved by DICER complexes into 24 nucleotide fragments, and the 24 nt small interfering RNAs (siRNAs) are loaded onto an Argonaut complex, which migrates to a precise chromosomal location based on homology between the DNA-target and the 24 nt siRNA

  • The Unique TE (UTE) consisted of 1514 TEs that was built by filtering the exemplar database of 1526 TEs (TEdb) [16,22] to reduce cross-homologies between TE exemplars and thereby improve mapping resolution [17]

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Summary

Introduction

Most DNA within angiosperm genomes is repetitive, typically representing active transposable elements (TEs) or DNA derived from formerly active TEs. TE activity is attenuated by the plant host, which uses small interfering RNAs (siRNAs) to silence TEs both before and after transcription. TEs are first recognized by the host, probably via double-stranded RNAs that originate either as a consequence of a hairpin structure in the RNA or by complementary transcripts from different strands. These doublestranded RNAs are cleaved by DICER complexes into 24 nucleotide (nt) fragments, and the 24 nt siRNAs are loaded onto an Argonaut complex, which migrates to a precise chromosomal location based on homology between the DNA-target and the 24 nt siRNA. The Argonaut complex attracts methylation machinery, leading to de novo TE methylation and silencing

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