Spruce giga‐genomes: structurally similar yet distinctive with differentially expanding gene families and rapidly evolving genes

Abstract

SUMMARY Spruces (Picea spp.) are coniferous trees widespread in boreal and mountainous forests of the northern hemisphere, with large economic significance and enormous contributions to global carbon sequestration. Spruces harbor very large genomes with high repetitiveness, hampering their comparative analysis. Here, we present and compare the genomes of four different North American spruces: the genome assemblies for Engelmann spruce (Picea engelmannii) and Sitka spruce (Picea sitchensis) together with improved and more contiguous genome assemblies for white spruce (Picea glauca) and for a naturally occurring introgress of these three species known as interior spruce (P. engelmannii × glauca × sitchensis). The genomes were structurally similar, and a large part of scaffolds could be anchored to a genetic map. The composition of the interior spruce genome indicated asymmetric contributions from the three ancestral genomes. Phylogenetic analysis of the nuclear and organelle genomes revealed a topology indicative of ancient reticulation. Different patterns of expansion of gene families among genomes were observed and related with presumed diversifying ecological adaptations. We identified rapidly evolving genes that harbored high rates of non‐synonymous polymorphisms relative to synonymous ones, indicative of positive selection and its hitchhiking effects. These gene sets were mostly distinct between the genomes of ecologically contrasted species, and signatures of convergent balancing selection were detected. Stress and stimulus response was identified as the most frequent function assigned to expanding gene families and rapidly evolving genes. These two aspects of genomic evolution were complementary in their contribution to divergent evolution of presumed adaptive nature. These more contiguous spruce giga‐genome sequences should strengthen our understanding of conifer genome structure and evolution, as their comparison offers clues into the genetic basis of adaptation and ecology of conifers at the genomic level. They will also provide tools to better monitor natural genetic diversity and improve the management of conifer forests. The genomes of four closely related North American spruces indicate that their high similarity at the morphological level is paralleled by the high conservation of their physical genome structure. Yet, the evidence of divergent evolution is apparent in their rapidly evolving genomes, supported by differential expansion of key gene families and large sets of genes under positive selection, largely in relation to stimulus and environmental stress response.

Reference-free assembly of long-read transcriptome sequencing data with RNA-Bloom2

“…The Sitka spruce ( Picea sitchensis ) is a large, evergreen, and long-living conifer species native to the Pacific Northwest in North America. Although a 20 Gbp draft genome assembly is publicly available 26 , its scaffold N50 length is 56.8 kbp, which reflects the draft stage of this short-read genome assembly. In particular, the Sitka spruce’s alternative splicing pattern has not been fully investigated.…”

Conifers concentrate large numbers of NLR immune receptor genes on one chromosome

“…2012), which may suggest lower rates of gene diversification. On the other hand, conifers have suites of rapidly evolving genes (Gagalova et al 2022) and highly diversified gene families or sub-families (e.g., Bedon et al 2010; Stival Sena et al 2018; Van Ghelder et al 2019) both related to stimuli and stress response. Several comparative studies in conifers have shown high levels of intergeneric macro-synteny and macro-collinearity among Pinaceae taxa (Pavy et al 2012) (Pelgas et al 2006; Ritland et al 2011; Westbrook et al 2015) and clear chromosomal rearrangements when comparing Pinaceae and Cupressaceae (Moriguchi et al 2012, de Miguel et al 2015).…”

“…Liu et al 2019), we tested whether this is a Pinaceae family-wide phenomenon by examining publicly available genomic resources in other members of the family. To characterise the distribution of NLR genes in the speciose Picea genus, we deployed a high-density linkage map for P. abies (Bernhardsson et al 2019) and high-quality genome assemblies of P. glauca and P. sitchensis (Gagalova et al 2022). Although these assemblies do not have chromosome-level contiguity, they are suitably scaffolded into linkage groups corresponding to an updated version of the original P. glauca high-density linkage map (Pavy et al 2017).…”

“…In some species that lack such assemblies, high-density genetic maps are available to probe genome architecture (J.-J. Liu et al 2019; Bernhardsson et al 2019; Gagalova et al 2022). Together, these assembled genome sequences and genetic maps, along with diverse transcriptomes (e.g., Van Ghelder et al 2019) open the doors to more comprehensive analyses of resistance genes and their genomic architecture in conifer trees.…”

Genetic basis of growth reaction to drought stress differs in contrasting high‐latitude treeline ecotones of a widespread conifer

“…These SNPs showed good quality and minor allele frequency (MAF) of at least 6% in previous white spruce studies (Pavy et al, 2017). All selected SNPs were located in coding regions that have a higher probability of sequence conservation and were mapped to the reference maps of Pavy et al (2017) and Gagalova et al (2022). The sequences surrounding the SNPs (at least 75 bp) were blasted against the transcriptome of white spruce (Birol et al, 2013) and only sequences of SNPs with a full hit in the genome were retained.…”