A chromosome-level genome assembly and annotation of the desert horned lizard, Phrynosoma platyrhinos, provides insight into chromosomal rearrangements among reptiles

Abstract

Background: The increasing number of chromosome-level genome assemblies has advanced our knowledge and understanding of macroevolutionary processes. Here, we introduce the genome of the desert horned lizard, Phrynosoma platyrhinos, an iguanid lizard occupying extreme desert conditions of the American southwest. We conduct analysis of the chromosomal structure and composition of this species and compare these features across genomes of 12 other reptiles (5 species of lizards, 3 snakes, 3 turtles, and 1 bird).

Findings: The desert horned lizard genome was sequenced using Illumina paired-end reads and assembled and scaffolded using Dovetail Genomics Hi-C and Chicago long-range contact data. The resulting genome assembly has a total length of 1,901.85 Mb, scaffold N50 length of 273.213 Mb, and includes 5,294 scaffolds. The chromosome-level assembly is composed of 6 macrochromosomes and 11 microchromosomes. A total of 20,764 genes were annotated in the assembly. GC content and gene density are higher for microchromosomes than macrochromosomes, while repeat element distributions show the opposite trend. Pathway analyses provide preliminary evidence that microchromosome and macrochromosome gene content are functionally distinct. Synteny analysis indicates that large microchromosome blocks are conserved among closely related species, whereas macrochromosomes show evidence of frequent fusion and fission events among reptiles, even between closely related species.

Conclusions: Our results demonstrate dynamic karyotypic evolution across Reptilia, with frequent inferred splits, fusions, and rearrangements that have resulted in shuffling of chromosomal blocks between macrochromosomes and microchromosomes. Our analyses also provide new evidence for distinct gene content and chromosomal structure between microchromosomes and macrochromosomes within reptiles.

Keywords: Reptilia; gene content; macrochromosome; microchromosome; synteny.

Figure 1:

For each major clade, we list diploid chromosome numbers, macrochromosome numbers, and microchromosome numbers based on previous research [1]. The phylogeny was adapted from [2].

Figure 2:

The genome content of P. platyrhinos. The outer circle shows gene density on each chromosome, the middle circle shows repeat element density, and the inner one shows GC content. Each estimate is calculated per 1 million base pair window in each chromosome. “Ma” indicates macrochromosomes, and “mi,” microchromosomes. Two scaffolds for macrochromosome 3 are attached together (the black line) and 2 microchromosomes (mi6 and mi10) resulting from a single scaffold are showed separately and in size order with the rest of the microchromosomes.

Figure 3:

Synteny between P. platyrhinos and 12 reptilian taxa: 3 snakes (N. naja, T. elegans, and C. viridis), 5 lizards (A. carolinensis, L. agilis, Z. vivipara, P. muralis, and S. merianae), 3 turtles (T. scripta, G. evgoodei, and D. coriacea), and 1 bird (G. gallus). The cladogram shows the phylogenetic relationships among the sampled taxa [80] (2 scaffolds for macrochromosome 3 [3a and 3b] are concatenated in this figure).

Figure 4:

Effective number of chromosomes (C) assessed using the dominance analysis. Values close to 1 represent full dominance (homologies from a given P. platyrhinos chromosome are contained within a single chromosome/scaffold of another species). Values >1 mean a spread of homologies across multiple chromosomes/scaffolds.

Figure 5:

Summary of the effective number of chromosomes of P. platyrhinos in comparison with the 12 target species based on SR. (top) Mean (points) and SD (error bars) of SR for each chromosome among 12 species. Values close to 1 represent full dominance (homologies from a given P. platyrhinos chromosome are contained within a single chromosome/scaffold). Values >1 mean a spread of homologies across multiple chromosomes/scaffolds. (bottom) Cumulative SR for chromosomes of 12 reptilian species. The total amount of SR at greater phylogenetic distances is higher (cumulative SR ∼ 30 in turtles) and showing greater rearrangements and partitions of syntenic blocks in macrochromosomes than in microchromosomes.

Figure 6:

Synteny between P. platyrhinos potential microchromosomes (before assigning scaffolds to specific chromosomes) and the 12 reptilian genomes. The cladogram shows the phylogenetic relationships among the assessed taxa [80].