Rapid Evolution of Genomic Imprinting in Two Species of the Brassicaceae

Abstract

Genomic imprinting is an epigenetic phenomenon occurring in mammals and flowering plants that causes genes to adopt a parent-of-origin-specific mode of expression. While the imprinting status of genes is well conserved in mammals, clear estimates for the degree of conservation were lacking in plants. We therefore analyzed the genome-wide imprinting status of Capsella rubella, which shared a common recent ancestor with Arabidopsis thaliana ∼10 to 14 million years ago. However, only ∼14% of maternally expressed genes (MEGs) and ∼29% of paternally expressed genes (PEGs) in C. rubella were commonly imprinted in both species, revealing that genomic imprinting is a rapidly evolving phenomenon in plants. Nevertheless, conserved PEGs exhibited signs of selection, suggesting that a subset of imprinted genes play an important functional role and are therefore maintained in plants. Like in Arabidopsis, PEGs in C. rubella are frequently associated with the presence of transposable elements that preferentially belong to helitron and MuDR families. Our data further reveal that MEGs and PEGs differ in their targeting by 24-nucleotide small RNAs and asymmetric DNA methylation, suggesting different mechanisms establishing DNA methylation at MEGs and PEGs.

Endosperm and Imprinting, Inextricably Linked

“…Transcriptomic studies have identified imprinted genes on a genome-wide scale in the cereals rice, maize, and sorghum (Sorghum bicolor) and in the dicots Arabidopsis, A. lyrata, Capsella rubella, and castor bean (Ricinus communis) Hsieh et al, 2011;Luo et al, 2011;Waters et al, 2011;Wolff et al, 2011;Zhang et al, 2011;Xin et al, 2013;Xu et al, 2014;Hatorangan et al, 2016;Klosinska et al, 2016;M. Zhang et al, 2016).…”

“…Thus, it is important to only compare imprinting among genes that can be confidently assessed for imprinting in both species (Klosinska et al, 2016). Two recent studies have compared imprinting between the closely related species Arabidopsis and C. rubella, and Arabidopsis and A. lyrata, which diverged from one another around 10 to 15 million years ago (Hatorangan et al, 2016;Klosinska et al, 2016). While one study characterized imprinting as rapid and the other characterized it as fairly conserved, in both comparisons imprinting of around 50% of genes was shared.…”

Genomic Imprinting Was Evolutionarily Conserved during Wheat Polyploidization

“…The paternally expressed auxin biosynthesis-related genes YUCCAs and Tryptophan aminotransferase related1 (TAR1) are rare examples of conserved imprinted genes present in rice, maize, and A. thaliana endosperm (Hsieh et al, 2011;Luo et al, 2011;Zhang et al, 2011;Chen et al, 2017). In addition, only 14% of MEGs and 29% of PEGs in C. rubella were commonly imprinted in A. thaliana (Hatorangan et al, 2016). However, 50% of imprinted genes were subsequently found to be conserved between A. lyrata and A. thaliana, which diverged ;13 MYA (Klosinska et al, 2016).…”

“…In addition, the proportion of commonly imprinted genes is also limited between C. rubella and A. thaliana (Hatorangan et al, 2016). However, extensive conservation of imprinted expression patterns was revealed between A. lyrata and A. thaliana (Klosinska et al, 2016).…”

“…However, the amount of overlap among imprinted genes of various plant species is limited (Waters et al, 2013;Pires and Grossniklaus, 2014;Hatorangan et al, 2016). For example, only 14% of MEGs and 29% of PEGs in Capsella rubella were commonly imprinted in A. thaliana (Hatorangan et al, 2016).…”