A Gene Family Derived from Transposable Elements during Early Angiosperm Evolution Has Reproductive Fitness Benefits in Arabidopsis thaliana

Abstract

The benefits of ever-growing numbers of sequenced eukaryotic genomes will not be fully realized until we learn to decipher vast stretches of noncoding DNA, largely composed of transposable elements. Transposable elements persist through self-replication, but some genes once encoded by transposable elements have, through a process called molecular domestication, evolved new functions that increase fitness. Although they have conferred numerous adaptations, the number of such domesticated transposable element genes remains unknown, so their evolutionary and functional impact cannot be fully assessed. Systematic searches that exploit genomic signatures of natural selection have been employed to identify potential domesticated genes, but their predictions have yet to be experimentally verified. To this end, we investigated a family of domesticated genes called MUSTANG (MUG), identified in a previous bioinformatic search of plant genomes. We show that MUG genes are functional. Mutants of Arabidopsis thaliana MUG genes yield phenotypes with severely reduced plant fitness through decreased plant size, delayed flowering, abnormal development of floral organs, and markedly reduced fertility. MUG genes are present in all flowering plants, but not in any non-flowering plant lineages, such as gymnosperms, suggesting that the molecular domestication of MUG may have been an integral part of early angiosperm evolution. This study shows that systematic searches can be successful at identifying functional genetic elements in noncoding regions and demonstrates how to combine systematic searches with reverse genetics in a fruitful way to decipher eukaryotic genomes.

Transposable Elements: Powerful Contributors to Angiosperm Evolution and Diversity

“…Although not particularly common, exaptation can nevertheless have enormous impacts, such as the generation of adaptive immune system in jawed vertebrates (Schatz 2004) and of the mammalian placenta (Rawn and Cross 2008; Oliver and Greene 2012). A significant number of genes whose sequences are largely TE derived have now been reported in angiosperms (He et al 2000; Bundock and Hooykaas 2005; Cowan et al 2005; Muehlbauer et al 2006; Lin et al 2007; Roccaro et al 2007; Duan et al 2008; Joly-Lopez et al 2012; Knip et al 2012), but not in examined gymnosperms, indicating that TEs have made beneficial contributions specifically to the angiosperm gene repertoire. It is likely that further examples will be identified as more genomes are analyzed.…”

Mutator and MULE Transposons

“…Although the function of these genes has not been established, at least some of them appear to be negatively modulated by phytohormones and by auxin, and their expression shows some tissue specificity (152). Further, mutations in some combinations of these genes have defects in growth, flowering and reproduction (153). Finally, a third clade of MULE-related genes has been identified in rice.…”

Divergence of Drosophila melanogaster repeatomes in response to a sharp microclimate contrast in Evolution Canyon, Israel

“…Once relegated to junk DNA, today many repeat elements emerge as potent functional genetic units, providing inspiration for new research initiatives (1). Although traditionally viewed as selfish DNA, TEs are increasingly being recognized as agents of adaptive change and a rich source of evolutionary novelties, including hybrid dysgenesis (2), insecticide resistance (3), mammalian placenta (4), and vertebrate adaptive immune system (4), as well as flower development and plant fitness (5). Domesticated TEs can be repurposed to function as transcription factors, whereas others play various roles in heterochromatin formation, genome stability, centromere binding, chromosome segregation, meiotic recombination, TE silencing, programmed genome rearrangement, V(D)J recombination, and translational regulation (4,6).…”