Genome structure-based Juglandaceae phylogenies contradict alignment-based phylogenies and substitution rates vary with DNA repair genes

Abstract

In lineages of allopolyploid origin, sets of homoeologous chromosomes may coexist that differ in gene content and syntenic structure. Presence or absence of genes and microsynteny along chromosomal blocks can serve to differentiate subgenomes and to infer phylogenies. We here apply genome-structural data to infer relationships in an ancient allopolyploid lineage, the walnut family (Juglandaceae), by using seven chromosome-level genomes, two of them newly assembled. Microsynteny and gene-content analyses yield identical topologies that place Platycarya with Engelhardia as did a 1980s morphological-cladistic study. DNA-alignment-based topologies here and in numerous earlier studies instead group Platycarya with Carya and Juglans, perhaps misled by past hybridization. All available data support a hybrid origin of Juglandaceae from extinct or unsampled progenitors nested within, or sister to, Myricaceae. Rhoiptelea chiliantha, sister to all other Juglandaceae, contains proportionally more DNA repair genes and appears to evolve at a rate 2.6- to 3.5-times slower than the remaining species.

Detection of Ghost Introgression from Phylogenomic Data Requires a Full-Likelihood Approach

“…An alternative approach may involve utilizing genome-structure information, such as gene order or content, which is more resistant to the effects of gene flow. Incorporating these features into the inference of species tree topologies could provide a promising avenue for overcoming this challenge (Zhao et al 2021;Ding et al 2023).…”

Distinct ancient structural polymorphisms control heterodichogamy in walnuts and hickories

“…We find that the divergence between G-locus haplotypes is comparable to the divergence between Juglans and Carya , indicating deep divergence of Juglans G-locus haplotypes, potentially occurring close in time to the split between Juglans and Carya ( ∼ 70 Myr). We used a molecular clock approach with substitution rates estimated from nonsynonymous coding regions in Juglans (Ding et al . 2023; Zhu et al .…”

“…We then calculated the divergence time as T = D XY / (2 µ ). Using two reported estimates of the substitution rate ( µ = 1.5 × 10 − 9 per bp per year (Ding et al . 2023), and 2.5 × 10 − 9 per bp per year (Zhu et al .…”

“…Published Cyclocarya resequencing data were obtained from Qu et al (2023). We used publicly available long-read genome assemblies of plants within Fagales generated by Zhu et al (2019); Marrano et al (2020); Fitz-Gibbon et al (2023); Zhang et al (2021); Lovell et al (2021); Zhang et al (2023); Ding et al (2023); Ning et al (2020); Li et al (2022); Zhang et al (2020); Sork et al (2022); Qu et al (2023); Cao et al (2023); Guzman-Torres et al (2023).…”

“…We adjusted the values of Dxy for multiple hits using the Jukes and Cantor (1969) distance. We then calculated the divergence time as T = Dxy/ (2 μ ), using a value of 1.5 × 10 − 9 per bp per year as an estimate of the substitution rate (Ding et al 2023). We note there is considerable uncertainty about the substitution rate, and hence about this estimated time.…”