Recurrent evolution of heat-responsiveness in Brassicaceae COPIA elements

BACKGROUND: The mobilization of transposable elements (TEs) is suppressed by host genome defense mechanisms. Recent studies showed that the cis-regulatory region of Arabidopsis thaliana COPIA78/ONSEN retrotransposons contains heat-responsive elements (HREs), which cause their activation during heat stress. However, it remains unknown whether this is a common and potentially conserved trait and how it has evolved. RESULTS: We show that ONSEN, COPIA37, TERESTRA, and ROMANIAT5 are the major families of heat-responsive TEs in A. lyrata and A. thaliana. Heat-responsiveness of COPIA families is correlated with the presence of putative high affinity heat shock factor binding HREs within their long terminal repeats in seven Brassicaceae species. The strong HRE of ONSEN is conserved over millions of years and has evolved by duplication of a proto-HRE sequence, which was already present early in the evolution of the Brassicaceae. However, HREs of most families are species-specific, and in Boechera stricta, the ONSEN HRE accumulated mutations and lost heat-responsiveness. CONCLUSIONS: Gain of HREs does not always provide an ultimate selective advantage for TEs, but may increase the probability of their long-term survival during the co-evolution of hosts and genomic parasites. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-016-1072-3) contains supplementary material, which is available to authorized users.