A survey of lineage-specific genes in Triticeae reveals de novo gene evolution from genomic raw material

Abstract

Plant genomes typically contain ∼35,000 genes, almost all belonging to highly-conserved gene families. Only a small fraction are lineage-specific, which are found in only one or few closely related species. Little is known about how genes arise de novo in plant genomes and how often this occurs, however they are believed to be important for plants diversification and adaptation. We developed a pipeline to identify lineage-specific genes in Triticeae, using newly available genome assemblies of wheat, barley and rye. Applying a set of stringent criteria, we identified 5,942 candidate Triticeae-specific genes (TSGs), of which 2,337 were validated as protein-coding genes in wheat. Differential gene expression analyses revealed that stress-induced wheat TSGs are strongly enriched in secreted proteins. Some were previously described to be involved in Triticeae non-host resistance and cold adaptation. Additionally, we show that 1,079 TSGs have sequence homology to transposable elements (TEs), ∼68% of them deriving from regulatory non-coding regions of Gypsy retrotransposons. Most importantly, we demonstrate that these TSGs are enriched in transmembrane domains and are among the most highly expressed wheat genes overall. To summarize, we conclude that de novo gene formation is relatively rare and that Triticeae probably possess ∼779 lineage-specific genes per haploid genome. TSGs which respond to pathogen and environmental stresses, may be interesting candidates for future targeted resistance breeding in Triticeae. Finally, we propose that non-coding regions of TEs might provide important genetic raw material for the functional innovation of TM domains and the evolution of novel secreted proteins.

Chromosome-scale genome assembly of bread wheat’s wild relativeTriticum timopheevii

“…Completeness of the gene model prediction was also evaluated using BUSCO and produced a score of 99.7% (0.1% fragmented and 0.2% missing BUSCOs; Table S8). The number of HC gene models (70,365) is in the range of a tetraploid Triticeae species (34,000–43,000 high-confidence gene models per haploid genome) 92 .…”

Chromosome-scale assembly of the wild wheat relative Aegilops umbellulata

“…Completeness of the gene model prediction was evaluated using BUSCO and produced a score of 98.1% (0.3% fragmented and 1.6% missing BUSCOs). The number of predicted gene models (36,268) is in the range of a diploid Triticeae species (34,000-43,000 high-confidence gene models per haploid genome) 58 .…”

Accurate identification of de novo genes in plant genomes using machine learning algorithms

“…First unequivocally discovered in Drosophila (28, 29), de novo genes have been identified across several other groups of animals (23,(30)(31)(32)(33) and are well characterized in some model organisms, particularly Saccharomyces cerevisiae (21,(34)(35)(36)(37)(38). In plants, thousands of potential DNGs have been retrieved through computational surveys in Arabidopsis thaliana, Brassica rapa, poplar, rice, sweet orange and Triticeae (8,(10)(11)(12)(39)(40)(41)(42)(43)(44)(45)(46)(47).…”