A FISH-based chromosome map for the European corn borer yields insights into ancient chromosomal fusions in the silkworm

Abstract

A significant feature of the genomes of Lepidoptera, butterflies and moths, is the high conservation of chromosome organization. Recent remarkable progress in genome sequencing of Lepidoptera has revealed that syntenic gene order is extensively conserved across phylogenetically distant species. The ancestral karyotype of Lepidoptera is thought to be n = 31; however, that of the most well-studied moth, Bombyx mori, is n = 28, and diverse studies suggest that three chromosomal fusion events occurred in this lineage. To identify the boundaries between predicted ancient fusions involving B. mori chromosomes 11, 23 and 24, we constructed fluorescence in situ hybridization (FISH)-based chromosome maps of the European corn borer, Ostrinia nubilalis (n = 31). We first determined a 511 Mb genomic sequence of the Asian corn borer, O. furnacalis, a congener of O. nubilalis, and isolated bacterial artificial chromosomes and fosmid clones that were expected to localize in candidate regions for the boundaries using these sequences. Combined with FISH and genetic analysis, we narrowed down the candidate regions to 40 kb-1.5 Mb, in strong agreement with a previous estimate based on the genome of a butterfly, Melitaea cinxia. The significant difference in the lengths of the candidate regions where no functional genes were observed may reflect the evolutionary time after fusion events.

Comparison of the genetic relationship between nine Cephalopod species based on cluster analysis of karyotype evolutionary distance

“…Fluorescence in situ hybridization (FISH), which enables visualization of target DNA sites on chromosomes through a signal display using probes, has been widely applied in chromosomal localization (Colomba et al 2002, Zhang et al 2007, Wang et al 2015, Escudero et al 2016) and gene mapping (Ishizuka et al 2016, Yasukochi et al 2016) for many years; however, there is only one report of its use in cephalopods, which was based on the localization of telomere sequence (Adachi et al 2014). In order to improve our understanding of cephalopod karyotypes, the development of chromosomal markers with higher resolution is needed to identify chromosome gene structure (Amar-Basulto et al 2011).…”

Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast-Asian wood white butterfly,Leptidea amurensis

“…Based on the occurrence across the lepidopteran phylogenetic tree, the modal chromosome number of n = 31 has been proposed as the ancestral number for Lepidoptera (Suomalainen, ; Lukhtanov, ). The putative ancestral karyotype is strongly supported by recent results of comparative chromosome mapping (Baxter et al ., ; Sahara et al ., ; Van't Hof et al ., ; Ahola et al ., ; Yasukochi et al ., ). Recent studies also suggest extensive conservation at the chromosomal level and evolutionary stability of whole lepidopteran genomic regions (Yasukochi et al ., , , ; Pringle et al ., ; Sahara et al ., , ; Van't Hof et al ., ; Ahola et al ., ).…”

Cryptic, extensive and non-random chromosome reorganization revealed by a butterfly chromonome

“…displays macrosynteny), regardless of haploid chromosome number. The degree of such synteny between species separated by up to 140 My is astounding as illustrated by recent chromosomal level genomic assemblies 7,13 , as well as previous studies of the sequence and structure of lepidopteran genomes [14][15][16][17] . This ability of Lepidoptera to accommodate such chromosomal rearrangements, yet maintain high levels of macro and microsynteny (i.e.…”

“…Butterflies and moths comprise nearly 10% of all described species 6 and inhabit diverse niches with varied life histories, yet they exhibit a striking similarity in their genome architecture despite 140 million generations 19 of divergence. The vast majority have a haploid chromosome number between 28 and 32 7,11,12 , and within chromosomes the gene content and order is remarkably similar among divergent species as adduced by three previous chromonomes 7,13 , BAC sequencing and chromosomal structure analyses 14,15 . Complicating this picture of conservation, haploid chromosome counts in species of Lepidoptera, as compared to all non-polyploid animals, exhibit the highest variance in number between species within a genus (n = 5 to 226 [16][17][18] ), the highest single count (n=226 9 ), and polymorphism in counts that do not affect fertility in crosses 3,19 .…”