Exploring the evolution of the proteins of the plant nuclear envelope

Abstract

In this study, we explore the plasticity during evolution of proteins of the higher plant nuclear envelope (NE) from the most ancestral plant species to advanced angiosperms. The higher plant NE contains a functional Linker of Nucleoskeleton and Cytoskeleton (LINC) complex based on conserved Sad1-Unc84 (SUN) domain proteins and plant specific Klarsicht/Anc1/Syne homology (KASH) domain proteins. Recent evidence suggests the presence of a plant lamina underneath the inner membrane and various coiled-coil proteins have been hypothesized to be associated with it including Crowded Nuclei (CRWN; also termed LINC and NMCP), Nuclear Envelope Associated Protein (NEAP) protein families as well as the CRWN binding protein KAKU4. SUN domain proteins appear throughout with a key role for mid-SUN proteins suggested. Evolution of KASH domain proteins has resulted in increasing complexity, with some appearing in all species considered, while other KASH proteins are progressively gained during evolution. Failure to identify CRWN homologs in unicellular organisms included in the study and their presence in plants leads us to speculate that convergent evolution may have occurred in the formation of the lamina with each kingdom having new proteins such as the Lamin B receptor (LBR) and Lamin-Emerin-Man1 (LEM) domain proteins (animals) or NEAPs and KAKU4 (plants). Our data support a model in which increasing complexity at the nuclear envelope occurred through the plant lineage and suggest a key role for mid-SUN proteins as an early and essential component of the nuclear envelope.

Keywords: Chromatin; KASH domain; LINC complex; SUN domain; higher plant; nucleoskeleton; nucleus.

Figure 1.

Distribution of components of plant nuclear envelope in the plant kingdom. (A) Selected plant lineages used in this study from left to right: Unicells Algae (pink), Moss and Club Moss (red), Gymnosperm (orange), Basal Angisoperms (yellow), Monocots (green) and Eudicots (blue). Zeta epsilon and gamma WGDs are indicated as arrow heads respectively in black, gray and purple. (B) Distribution of the 9 protein families (rows) in the 20 species (columns). Absence (0) of a given protein is highlighted in light orange.

Figure 2.

Phylogenetic tree of Cter-SUN proteins and gene expression levels. Left: maximum likelihood tree of Cter-SUN protein homologues constructed from an alignment. Bootstrap values are presented. The color of the label shows the lineage of the plant. The gene label is constructed with the 3 letters from the species name (supplementary Table 4) and the gene name of the A. thaliana homologues. Right: red bar represents the value of the transcription level in seedlings expressed in RPKM, except for species indicated by *, the RNA-seq data was obtained from leaf tissue (Supplementary Table 2).

Figure 3.

Phylogenetic tree of mid-SUN proteins.

Figure 5.

Phylogenetic tree of SINE1, SINE2 homologues proteins.

Figure 4.

Phylogenetic tree of WIP proteins.

Figure 6.

Phylogenetic tree of CRWN proteins.

Figure 7.

Phylogenetic tree of NEAP proteins.

Figure 8.

Phylogenetic tree of KAKU4 proteins.