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Expansion of a core regulon by transposable elements promotes Arabidopsis chemical diversity and pathogen defense.

ABSTRACT: Plants synthesize numerous ecologically specialized, lineage-specific metabolites through biosynthetic gene duplication and functional specialization. However, it remains unclear how duplicated genes are wired into existing regulatory networks. We show that the duplicated gene CYP82C2 has been recruited into the WRKY33 regulon and indole-3-carbonylnitrile (ICN) biosynthetic pathway through exaptation of a retroduplicated LINE retrotransposon (EPCOT3) into an enhancer. The stepwise development of a chromatin-accessible WRKY33-binding site on EPCOT3 has potentiated the regulatory neofunctionalization of CYP82C2 and the evolution of inducible defense metabolite 4-hydroxy-ICN in Arabidopsis thaliana. Although transposable elements (TEs) have long been recognized to have the potential to rewire regulatory networks, these results establish a more complete understanding of how duplicated genes and TEs contribute in concert to chemical diversity and pathogen defense.

SUBMITTER: Barco B

PROVIDER: S-EPMC6671987 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Expansion of a core regulon by transposable elements promotes Arabidopsis chemical diversity and pathogen defense.

Barco Brenden B Kim Yoseph Y Clay Nicole K NK

Nature communications 20190801 1

Plants synthesize numerous ecologically specialized, lineage-specific metabolites through biosynthetic gene duplication and functional specialization. However, it remains unclear how duplicated genes are wired into existing regulatory networks. We show that the duplicated gene CYP82C2 has been recruited into the WRKY33 regulon and indole-3-carbonylnitrile (ICN) biosynthetic pathway through exaptation of a retroduplicated LINE retrotransposon (EPCOT3) into an enhancer. The stepwise development of ...[more]

PMID: 31371717

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Project description:BACKGROUND:Transposition is disruptive in nature and, thus, it is imperative for host genomes to evolve mechanisms that suppress the activity of transposable elements (TEs). At the same time, transposition also provides diverse sequences that can be exapted by host genomes as functional elements. These notions form the basis of two competing hypotheses pertaining to the role of epigenetic modifications of TEs in eukaryotic genomes: the genome defense hypothesis and the exaptation hypothesis. To date, all available evidence points to the genome defense hypothesis as the best explanation for the biological role of TE epigenetic modifications. RESULTS:We evaluated several predictions generated by the genome defense hypothesis versus the exaptation hypothesis using recently characterized epigenetic histone modification data for the human genome. To this end, we mapped chromatin immunoprecipitation sequence tags from 38 histone modifications, characterized in CD4+ T cells, to the human genome and calculated their enrichment and depletion in all families of human TEs. We found that several of these families are significantly enriched or depleted for various histone modifications, both active and repressive. The enrichment of human TE families with active histone modifications is consistent with the exaptation hypothesis and stands in contrast to previous analyses that have found mammalian TEs to be exclusively repressively modified. Comparisons between TE families revealed that older families carry more histone modifications than younger ones, another observation consistent with the exaptation hypothesis. However, data from within family analyses on the relative ages of epigenetically modified elements are consistent with both the genome defense and exaptation hypotheses. Finally, TEs located proximal to genes carry more histone modifications than the ones that are distal to genes, as may be expected if epigenetically modified TEs help to regulate the expression of nearby host genes. CONCLUSIONS:With a few exceptions, most of our findings support the exaptation hypothesis for the role of TE epigenetic modifications when vetted against the genome defense hypothesis. The recruitment of epigenetic modifications may represent an additional mechanism by which TEs can contribute to the regulatory functions of their host genomes.

Project description:BackgroundMutator-like elements (MULEs) are a significant superfamily of DNA transposons on account of their: (i) great transpositional activity and propensity for insertion in or near gene sequences, (ii) their consequent high mutagenic capacity, and, (iii) their tendency to acquire host gene fragments. Consequently, MULEs are important genetic tools and represent a key study system for research into host-transposon interactions. Yet, while several studies have focused on the impacts of MULEs on crop and fungus genomes, their evolution remains poorly explored.ResultsWe perform comprehensive bioinformatic and phylogenetic analyses to address currently available MULE diversity and reconstruct evolution for the group. For this, we mine MULEs from online databases, and combine search results with available transposase sequences retrieved from previously published studies. Our analyses uncover two entirely new MULE clades that contain elements almost entirely restricted to arthropod hosts, considerably expanding the set of MULEs known from this group, suggesting that many additional MULEs may await discovery from further arthropod genomes. In several cases, close relationships occur between MULEs recovered from distantly related host organisms, suggesting that horizontal transfer events may have played an important role in the evolution of the group. However, it is apparent that MULEs from plants remain separate from MULEs identified from other host groups. MULE structure varies considerably across phylogeny, and TIR length is shown to vary greatly both within and between MULE groups. Our phylogeny suggests that MULE diversity is clustered in well-supported groups, typically according to host taxonomy. With reference to this, we make suggestions on how MULE diversity can be partitioned to provide a robust taxonomic framework.ConclusionsOur study represents a considerable advance in the understanding of MULE diversity, host range and evolution, and provides a taxonomic framework for the classification of further MULE elements that await discovery. Our findings also raise a number of questions relating to MULE biology, suggesting that this group will provide a rich avenue for future study.

Project description:BackgroundPlant genomes can respond rapidly to environmental changes and transposable elements (TEs) arise as important drivers contributing to genome dynamics. Although some elements were reported to be induced by various abiotic or biotic factors, there is a lack of general understanding on how environment influences the activity and diversity of TEs. Here, we combined common garden experiment with short-read sequencing to investigate genomic abundance and expression of 2245 consensus TE sequences (containing retrotransposons and DNA transposons) in an alpine environment in Arabidopsis arenosa. To disentangle general trends from local differentiation, we leveraged four foothill-alpine population pairs from different mountain regions. Seeds of each of the eight populations were raised under four treatments that differed in temperature and irradiance, two factors varying with elevation. RNA-seq analysis was performed on leaves of young plants to test for the effect of elevation and subsequently of temperature and irradiance on expression of TE sequences.ResultsGenomic abundance of the 2245 consensus TE sequences varied greatly between the mountain regions in line with neutral divergence among the regions, representing distinct genetic lineages of A. arenosa. Accounting for intraspecific variation in abundance, we found consistent transcriptomic response for some TE sequences across the different pairs of foothill-alpine populations suggesting parallelism in TE expression. In particular expression of retrotransposon LTR Copia (e.g. Ivana and Ale clades) and LTR Gypsy (e.g. Athila and CRM clades) but also non-LTR LINE or DNA transposon TIR MuDR consistently varied with elevation of origin. TE sequences responding specifically to temperature and irradiance belonged to the same classes as well as additional TE clades containing potentially stress-responsive elements (e.g. LTR Copia Sire and Tar, LTR Gypsy Reina).ConclusionsOur study demonstrated that the A. arenosa genome harbours a considerable diversity of TE sequences whose abundance and expression response varies across its native range. Some TE clades may contain transcriptionally active elements responding to a natural environmental gradient. This may further contribute to genetic variation between populations and may ultimately provide new regulatory mechanisms to face environmental challenges.

Dataset Information

Expansion of a core regulon by transposable elements promotes Arabidopsis chemical diversity and pathogen defense.

Publications

Expansion of a core regulon by transposable elements promotes Arabidopsis chemical diversity and pathogen defense.

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