The Ancient Salicoid Genome Duplication Event: A Platform for Reconstruction of De Novo Gene Evolution inPopulus trichocarpa

Abstract

Orphan genes are characteristic genomic features that have no detectable homology to genes in any other species and represent an important attribute of genome evolution as sources of novel genetic functions. Here, we identified 445 genes specific to Populus trichocarpa. Of these, we performed deeper reconstruction of 13 orphan genes to provide evidence of de novo gene evolution. Populus and its sister genera Salix are particularly well suited for the study of orphan gene evolution because of the Salicoid whole-genome duplication event (WGD) which resulted in highly syntenic sister chromosomal segments across the Salicaceae. We leveraged this genomic feature to reconstruct de novo gene evolution from inter-genera, inter-species, and intra-genomic perspectives by comparing the syntenic regions within the P. trichocarpa reference, then P. deltoides, and finally Salix purpurea. Furthermore, we demonstrated that 86.5% of the putative orphan genes had evidence of transcription. Additionally, we also utilized the Populus genome-wide association mapping panel (GWAS), a collection of 1,084 undomesticated P. trichocarpa genotypes to further determine putative regulatory networks of orphan genes using expression quantitative trait loci (eQTL) mapping. Functional enrichment of these eQTL subnetworks identified common biological themes associated with orphan genes such as response to stress and defense response. We also identify a putative cis-element for a de novo gene and leverage conserved synteny to describe evolution of a putative transcription factor binding site. Overall, 45% of orphan genes were captured in trans-eQTL networks.

Genome dynamics in mosses: Extensive synteny coexists with a highly dynamic gene space

“…Furthermore, collinear blocks were also syntenic, showing virtually no movement of collinear blocks among chromosomes. This level of collinearity and synteny represents a relatively rigid genome structure that is exceptional compared to the data available for highly collinear grass and angiosperm genomes with similar depth of divergence (74–80) and is in line with findings by (26). While gene order, gene content, and chromosomal position of collinear blocks are highly conserved, their orientation appears to be dynamic.…”

“…While the presence of lineage-specific genes is not surprising, their relative contribution to the gene space of each species is exceptionally large, reaching 20-30%. In comparison, gene space difference between highly contiguous angiosperm genomes with similar depth of divergence is less pronounced (17,80,(82)(83)(84)(85)(86)(87)(88)(89). For instance, the proportion of species-specific genes usually remains below 3-10% in most studies.…”

Expression quantitative trait loci mapping identified PtrXB38 as a key hub gene in adventitious root development in Populus

“…Whole‐genome resequencing and variant calling for the 917 P. trichocarpa Torr. & Gray individuals was performed as described previously (Yates et al ., 2021). The single nucleotide polymorphism (SNP) and indel dataset is available at http://bioenergycenter.org/besc/gwas/.…”

GWAS identifies candidate regulators of in planta regeneration in Populus trichocarpa

“…We analyzed the distribution of SNPs after resequencing of 406 additional genotypes by the DOE Joint Genome Institute. SNP calling was done at Oak Ridge National Laboratory (Yates et al ., 2021). There was a total of 40.4M SNPs prior to filtering for minor allele frequency (MAF) and additional quality criteria.…”