Dynamics and Adaptive Benefits of Protein Domain Emergence and Arrangements during Plant Genome Evolution

Abstract

Plant genomes are generally very large, mostly paleopolyploid, and have numerous gene duplicates and complex genomic features such as repeats and transposable elements. Many of these features have been hypothesized to enable plants, which cannot easily escape environmental challenges, to rapidly adapt. Another mechanism, which has recently been well described as a major facilitator of rapid adaptation in bacteria, animals, and fungi but not yet for plants, is modular rearrangement of protein-coding genes. Due to the high precision of profile-based methods, rearrangements can be well captured at the protein level by characterizing the emergence, loss, and rearrangements of protein domains, their structural, functional, and evolutionary building blocks. Here, we study the dynamics of domain rearrangements and explore their adaptive benefit in 27 plant and 3 algal genomes. We use a phylogenomic approach by which we can explain the formation of 88% of all arrangements by single-step events, such as fusion, fission, and terminal loss of domains. We find many domains are lost along every lineage, but at least 500 domains are novel, that is, they are unique to green plants and emerged more or less recently. These novel domains duplicate and rearrange more readily within their genomes than ancient domains and are overproportionally involved in stress response and developmental innovations. Novel domains more often affect regulatory proteins and show a higher degree of structural disorder than ancient domains. Whereas a relatively large and well-conserved core set of single-domain proteins exists, long multi-domain arrangements tend to be species-specific. We find that duplicated genes are more often involved in rearrangements. Although fission events typically impact metabolic proteins, fusion events often create new signaling proteins essential for environmental sensing. Taken together, the high volatility of single domains and complex arrangements in plant genomes demonstrate the importance of modularity for environmental adaptability of plants.

Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions

“…Strikingly, 48% of all P. patens loci are in Physcomitrella-only clusters (Figure 5), which independently supports an analysis based on protein domains where 52% of all P. patens genes have no Pfam domain [80]. Further filtering of these loci including BLASTP against GenPept and EST support indicates that ~22% (7169) of all loci in Physcomitrella-only clusters have no detectable homolog, while at least ~13% (4157) have no homolog but transcript evidence.…”

Nonsyntenic Genes Drive Highly Dynamic Complementation of Gene Expression in Maize Hybrids

“…In total, 49% (19,365) of all maize genes were assigned to subgenomes 1 or 2 . The remaining 51% likely emerged more recently, e.g., by modular rearrangement of protein encoding domains (Kersting et al, 2012), by the transposition of existing genes (Freeling et al, 2008), or by exon shuffling from helitrons and other transposons leading to fusion genes (Barbaglia et al, 2012). Among the 27,347 genes expressed in this study, 17,402 (64%) genes were assigned to one of the two subgenomes.…”

Evolution of Protein Domain Repeats in Metazoa

“…The justification for this is that retention rates after gene duplication, which affects the number of paralogs in a protein family, are highly variable between different protein families (Shiu et al 2006; Morel et al 2015). Significant and long deviations from the molecular clock hypothesis, however, are rare at the sequence level (Kumar 2005) and for domain rearrangements (Kersting et al 2012; Moore et al 2013). …”

“…Several studies have described changes in domain arrangements (i.e., the N- to C-terminal order of domains in a protein) and concluded that the dominating forces of rearrangement are duplication of protein coding genes, fusion and terminal domain losses (Apic et al 2003; Ye and Godzik 2004; Kummerfeld and Teichmann 2005; Weiner and Bornberg-Bauer 2006; Weiner et al 2006; Wang and Caetano-Anollés 2009; Zmasek and Godzik 2011, 2012; Forslund and Sonnhammer 2012; Moore et al 2013) whereas fissions and emergence of novel domains are rather rare (Kummerfeld and Teichmann 2005; Moore and Bornberg-Bauer 2012; Kersting et al 2012). In all of these studies, domain repeats have been treated as a single domain, i.e., repeat units have been computationally “collapsed” into a single unit for better handling.…”