Concerted Divergence after Gene Duplication in Polycomb Repressive Complexes

Abstract

Duplicated genes are a major contributor to genome evolution and phenotypic novelty. There are multiple possible evolutionary fates of duplicated genes. Here, we provide an example of concerted divergence of simultaneously duplicated genes whose products function in the same complex. We studied POLYCOMB REPRESSIVE COMPLEX2 (PRC2) in Brassicaceae. The VERNALIZATION (VRN)-PRC2 complex contains VRN2 and SWINGER (SWN), and both genes were duplicated during a whole-genome duplication to generate FERTILIZATION INDEPENDENT SEED2 (FIS2) and MEDEA (MEA), which function in the Brassicaceae-specific FIS-PRC2 complex that regulates seed development. We examined the expression of FIS2, MEA, and their paralogs, compared their cytosine and histone methylation patterns, and analyzed the sequence evolution of the genes. We found that FIS2 and MEA have reproductive-specific expression patterns that are correlated and derived from the broadly expressed VRN2 and SWN in outgroup species. In vegetative tissues of Arabidopsis (Arabidopsis thaliana), repressive methylation marks are enriched in FIS2 and MEA, whereas active marks are associated with their paralogs. We detected comparable accelerated amino acid substitution rates in FIS2 and MEA but not in their paralogs. We also show divergence patterns of the PRC2-associated VERNALIZATION5/VIN3-LIKE2 that are similar to FIS2 and MEA. These lines of evidence indicate that FIS2 and MEA have diverged in concert, resulting in functional divergence of the PRC2 complexes in Brassicaceae. This type of concerted divergence is a previously unreported fate of duplicated genes. In addition, the Brassicaceae-specific FIS-PRC2 complex modified the regulatory pathways in female gametophyte and seed development.

Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2

“…We investigated how Su(z)12 was recruited as a substrate of the N-end rule pathway specifically in the flowering plant lineage. VRN2 is proposed to have evolved following duplication of an ancient EMF2-like Su(z)12 gene 37,38 . Alignment of Arabidopsis EMF2 and VRN2 protein sequences shows that the MC-N-terminus of VRN2 is equivalent to an internal MC-dipeptide in the N-terminal cap region of EMF2 21 amino acid residues downstream of Met1 (Fig.…”

“…Here, we report that flowering plants have uniquely evolved a variant of the Su(z)12 PRC2 component—VRN2—that is regulated by the O 2 - and NO-sensitive branch of the Arg/N-end rule pathway. This proteolytic regulation is required to prevent ectopic accumulation of VRN2 outside of meristems in the absence of external stimuli such as cold or hypoxia, despite constitutive VRN2 mRNA expression 38 . We show that both submergence and cold-exposure promote VRN2 accumulation.…”

The maternally expressed polycomb group gene OsEMF2a is essential for endosperm cellularization and imprinting in rice

“…In Drosophila , polycomb repressive complex 2 (PRC2) is composed of four core polycomb group (PcG) proteins: WD40 protein p55, suppressor of zeste 12 (Su(z)12), enhancer of zeste, and extra sex combs ( Tonosaki and Kinoshita, 2015 ). Although PRC2 is conserved in eukaryotes, plants have multiplied the group members of each PcG family during evolution ( Furihata et al., 2016 ; Huang et al., 2017 ; Qiu et al., 2017 ). Due to their methyltransferase activity for the methylation of Lys27 in histone H3 (H3K27), PRC2 complexes are vital for plant development, as they modulate the epigenetic modification of chromatin ( Mozgova and Hennig, 2015 ).…”

Comparative genomics of StAR-related lipid transfer (START) domains across wild and cultivated rice

“…gain or loss of domains and in some cases domain rearrangements that occur in the new copy at the gene level which decides the adaptability of organisms to the challenging environments. This phenomenon has been reported among all the kingdoms of life due to dosage of the extra gene product, and its spatio-temporal expression changes [57–60].…”