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

Abstract

Transposable elements (TEs) proliferate within the genome of their host, which responds by silencing them epigenetically. Much is known about the mechanisms of silencing in plants, particularly the role of siRNAs in guiding DNA methylation. In contrast, little is known about siRNA targeting patterns along the length of TEs, yet this information may provide crucial insights into the dynamics between hosts and TEs. By focusing on 6456 carefully annotated, full-length Sirevirus LTR retrotransposons in maize, we show that their silencing associates with underlying characteristics of the TE sequence and also uncover three features of the host-TE interaction. First, siRNA mapping varies among families and among elements, but particularly along the length of elements. Within the cis-regulatory portion of the LTRs, a complex palindrome-rich region acts as a hotspot of both siRNA matching and sequence evolution. These patterns are consistent across leaf, tassel, and immature ear libraries, but particularly emphasized for floral tissues and 21-to 22-nt siRNAs. Second, this region has the ability to form hairpins, making it a potential template for the production of miRNA-like, hairpin-derived small RNAs. Third, Sireviruses are targeted by siRNAs as a decreasing function of their age, but the oldest elements remain highly targeted, partially by siRNAs that cross-map to the youngest elements. We show that the targeting of older Sireviruses reflects their conserved palindromes. Altogether, we hypothesize that the palindromes aid the silencing of active elements and influence transposition potential, siRNA targeting levels, and ultimately the fate of an element within the genome.

Constant conflict between Gypsy LTR retrotransposons and CHH methylation within a stress‐adapted mangrove genome

“…S1). The low level of methylation in unclassified elements is consistent with previous observations (Bousios et al, 2016) that older TEs are typically methylated less densely than younger ones. New Phytologist CHH methylation is de novo DNA methylation that depends on the RdDM pathway (Zemach et al, 2013;McCue et al, 2015).…”

“…S1). The low level of methylation in unclassified elements is consistent with previous observations (Bousios et al ., ) that older TEs are typically methylated less densely than younger ones.…”

“…Our results also shed light on the factors that contribute to the process of epigenetic TE silencing. Palindromic structures in the maize Sirevirus LTRs can form hairpins that are processed into ‘primary’ siRNAs and aid in the silencing of active elements (Bousios et al ., ). Although we searched the LTRs of R. apiculata transposons for secondary RNA structures, we did not find any TE families prone to form hairpins.…”

“…We wondered why old Gypsy elements harbored a high siRNA density. Previous studies have suggested that the reactivation of silenced TEs can trigger trans-silencing of active relatives (Lisch, 2009;Bousios et al, 2016). It is possible that some old Gypsy elements became zombies and were retained as immunity memory in the R. apiculata genome.…”

Creating Order from Chaos: Epigenome Dynamics in Plants with Complex Genomes

“…These could include small quantities of small RNAs produced by elements themselves whose titer reaches some threshold as copy numbers increase (Marí-Ordóñez et al, 2013), preexisting pools of trans-acting small RNAs derived from previously silenced elements (Bousios et al, 2016), novel sense-antisense transcript combinations due to nested insertions (Lisch and Slotkin, 2011), or novel rearrangements such as is observed with Mu killer. There is also evidence for variation in chromatin marks at TEs of differing lengths (Zemach et al, 2013) or differing families (Eichten et al, 2012;Wang et al, 2015).…”