Multiscale analysis of the randomization limits of the chromosomal gene organization between Lepidoptera and Diptera.

José M Ranz,Sarah J Bedford,Cei Abreu-Goodger,Ryan N Su,Pablo M González,Therese Markow

doi:10.1098/rspb.2021.2183

Abstract

How chromosome gene organization and gene content evolve among distantly related and structurally malleable genomes remains unresolved. This is particularly the case when considering different insect orders. We have compared the highly contiguous genome assemblies of the lepidopteran Danaus plexippus and the dipteran Drosophila melanogaster, which shared a common ancestor around 290 Ma. The gene content of 23 out of 30 D. plexippus chromosomes was significantly associated with one or two of the six chromosomal elements of the Drosophila genome, denoting common ancestry. Despite the phylogenetic distance, 9.6% of the 1-to-1 orthologues still reside within the same ancestral genome neighbourhood. Furthermore, the comparison D. plexippus–Bombyx mori indicated that the rates of chromosome repatterning are lower in Lepidoptera than in Diptera, although still within the same order of magnitude. Concordantly, 14 developmental gene clusters showed a higher tendency to retain full or partial clustering in D. plexippus, further supporting that the physical association between the SuperHox and NK clusters existed in the ancestral bilaterian. Our results illuminate the scope and limits of the evolution of the gene organization and content of the ancestral chromosomes to the Lepidoptera and Diptera while helping reconstruct portions of the genome in their most recent common ancestor.

Highlights

With the exception of neighbouring genes featuring coordinated gene expression through shared or long-range enhancers [1,2,3], gene order organization among distantly related metazoans is thought to be quasi-random as a result of chromosome structural mutations [4]
We examined the gene organization of 9 homeobox (Hox, NK, SuperHox, Irx, PRD-LIM and its subcomponent HRO, SINE/Six, and the Vsx and Uncx families) and 5 non-homeobox clusters (Wnt, Fox, Inexin, Runt, E(spl)/Brd) in D. plexippus, and when necessary in the silkmoth B. mori to inform on their differential dynamics of change
The extent to which the chromosomal gene content and organization has been remodelled during species divergence, among distantly related and structurally dynamic genomes, remains elusive due to limited contiguity of genome assemblies, suboptimal or entirely absent gene annotations, as well as non-reliable orthologues relationships

Summary

Introduction

With the exception of neighbouring genes featuring coordinated gene expression through shared or long-range enhancers [1,2,3], gene order organization among distantly related metazoans is thought to be quasi-random as a result of chromosome structural mutations [4]. No effort has been performed so far to (i) comprehensively investigate the relationship between the chromosomes between the Lepidoptera and the Diptera, (ii) determine the extent to which gene order randomization has taken place between the species orders, and (iii) reconstruct, even partially, the chromosome gene organization in their ancestor. To fill these gaps in knowledge, we used a recently generated high contiguity assembly and gene annotation for D. plexippus, as a representative of the Lepidoptera, as well as the inferred orthologous relationships between this species and D. melanogaster [26]. Our results demonstrate the potential of high-quality genomic resources in uncovering signatures of macro- and microsynteny, helping to reconstruct the genome in the ancestor of structurally dynamic genomes of distantly related species

Methods

Results

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Discussion