A molecular cell biology toolkit for the study of meiosis in the silkworm <i>Bombyx mori</i>

Xiang, Youbin; Tsuchiya, Dai; Guo, Fei; Gardner, Jennifer M.; McCroskey, Scott; Price, Andrew; Tromer, Eelco C.; Walters, James R.; Lake, Cathleen M.; Hawley, R. Scott

doi:10.1093/g3journal/jkad058

Cited by 4 publications

(4 citation statements)

References 65 publications

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“…In that study, as well as a study in Drosophila melanogaster, folding, volume, and intermixing of CTs have been associated with condensin II 3,64 . Condensin II subunits are present in the B. mori genome 65,66 , and it would be interesting to evaluate whether the substantial degree of territoriality is caused by uniquely high activity of condensin II in B. mori. CT strength is also intriguing from an evolutionary point of view.…”

Section: Discussionmentioning

confidence: 99%

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Gil,

Navarrete,

Rosin

et al. 2023

Preprint

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The hallmarks of chromosome organization in multicellular eukaryotes are chromosome territories (CT), chromatin compartments, and different types of domains, including topologically associated domains (TADs). Yet, most of these concepts derive from analyses of organisms with monocentric chromosomes. Here we describe the 3D genome architecture of an organism with holocentric chromosomes, the silkwormBombyx mori. At the genome-wide scale,B. morichromosomes form highly separated territories and lack substantial trans contacts. As described in other eukaryotes,B. morichromosomes segregate into an active A and an inactive B compartment. Remarkably, we also identify a third compartment, Secluded »S», with a unique contact pattern. Compartment S shows strong enrichment of short-range contacts and depletion of long-range contacts. It hosts a unique combination of genetic and epigenetic features, localizes at the periphery of CTs and shows developmental plasticity. Biophysical modeling shows that formation of such secluded domains requires a new mechanism – a high density of extruded loops within them along with low level of extrusion and compartmentalization of A and B. Together with other evidence of loop extrusion in interphase, this suggests SMC-mediated loop extrusion in this insect. Overall, our analyses highlight the evolutionary plasticity of 3D genome organization driven by a new combination of known processes.

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Section: Discussionmentioning

confidence: 99%

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Gil,

Navarrete,

Rosin

et al. 2023

Preprint

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“…5). Further evidence to support the specialisa)on of these paralogues in moths is provided by transcriptomic data from B. mori larvae which detected enrichment of predicted eupyreneenriched Ccdc63 (LOC101738429) transcripts in larval testes, but not Ccdc63 (LOC101746125) transcripts predicted to be apyrene-enriched (higher expression in pupal testes) (22). This apyrene specialisa)on may be exclusive to moths, as the paralogous protein in the Monarch bu_erfly D. plexippus (LOC116774756) was found to be enriched in eupyrene sperm, rather than apyrene (10).…”

Section: Gene Duplica*on and Specialisa*on Has Produced Apyrene-and E...mentioning

confidence: 98%

“…13 somware (19) (Supplementary Methods). Resul)ng phylogene)c trees were then cross-referenced with our RNA-seq dataset and previously published proteomic and transcriptomic datasets (10,(20)(21)(22)(23).…”

Section: G Mellonella Protein Sequence Of Interest Was Input Into Bla...mentioning

confidence: 99%

Differential gene expression underpinning production of distinct sperm morphs in the wax mothGalleria mellonella

Moth,

Messer,

Chaudhary

et al. 2023

Preprint

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Male Lepidoptera makes two distinct sperm types; each ejaculate contains both eupyrene sperm, which can fertilise the egg, and apyrene sperm, which are not fertilisation competent. These sperm have distinct morphologies, unique functions, and different proteomes. Their production is highly regulated, however very few genes with specific roles in production of one or other morph have been described. We present the first comparative transcriptomics study of precursors of eupyrene and apyrene sperm to identify genes potentially implicated in regulating or enacting the distinct differentiation programmes. Differentially expressed genes included genes with potential roles in transcriptional regulation, cell cycle and sperm morphology. We identified gene duplications generating paralogues with functions restricted to one or other morph. However phylogenetic analysis also revealed evolutionary flexibility in expression patterns of duplicated genes between different Lepidopteran species. Improved understanding of Lepidopteran reproduction will be vital in targeting prevalent pests in agriculture, and on the flip side, ensuring the fertility and thus survival of pollinator populations in response to environmental stress.

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“…The following antibodies and dilutions were used for IF: rabbit anti-Dsn1 1/1000, rabbit anti-CENPT 1/1000, and rabbit anti-Spc24/25 1/1000 (gift from Ines Drinnenberg [47]), rat anti-SMC1 1/250 (gift from Scott Hawley [93]), anti-tubulin cocktail (Synaptic Systems 302 209 1/500 + sigma T6074-200 1/500). The following secondary antibodies were all from Invitrogen and used at 1/500: donkey anti-mouse 488 (A21202), donkey anti-mouse 555 (A31570), donkey anti-mouse 647 (A31571), donkey anti-rabbit 488 (A21206), donkey anti-rabbit 555 (A31572), donkey anti-rabbit 647 (A31573), donkey anti-chicken 488 (A78948), and donkey anti-rat 647 plus (A48272).…”

Section: Meiotic Squashes Meiotic Staging If and Dna Fish On Meiotic ...mentioning

confidence: 99%

Chromosome segregation during spermatogenesis occurs through a unique center-kinetic mechanism in holocentric moth species

Hockens,

Lorenzi,

Wang

et al. 2024

PLoS Genet

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Precise regulation of chromosome dynamics in the germline is essential for reproductive success across species. Yet, the mechanisms underlying meiotic chromosomal events such as homolog pairing and chromosome segregation are not fully understood in many species. Here, we employ Oligopaint DNA FISH to investigate mechanisms of meiotic homolog pairing and chromosome segregation in the holocentric pantry moth, Plodia interpunctella, and compare our findings to new and previous studies in the silkworm moth, Bombyx mori, which diverged from P. interpunctella over 100 million years ago. We find that pairing in both Bombyx and Plodia spermatogenesis is initiated at gene-rich chromosome ends. Additionally, both species form rod shaped cruciform-like bivalents at metaphase I. However, unlike the telomere-oriented chromosome segregation mechanism observed in Bombyx, Plodia can orient bivalents in multiple different ways at metaphase I. Surprisingly, in both species we find that kinetochores consistently assemble at non-telomeric loci toward the center of chromosomes regardless of where chromosome centers are located in the bivalent. Additionally, sister kinetochores do not seem to be paired in these species. Instead, four distinct kinetochores are easily observed at metaphase I. Despite this, we find clear end-on microtubule attachments and not lateral microtubule attachments co-orienting these separated kinetochores. These findings challenge the classical view of segregation where paired, poleward-facing kinetochores are required for accurate homolog separation in meiosis I. Our studies here highlight the importance of exploring fundamental processes in non-model systems, as employing novel organisms can lead to the discovery of novel biology.

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A molecular cell biology toolkit for the study of meiosis in the silkworm Bombyx mori

Cited by 4 publications

References 65 publications

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

Differential gene expression underpinning production of distinct sperm morphs in the wax mothGalleria mellonella

Chromosome segregation during spermatogenesis occurs through a unique center-kinetic mechanism in holocentric moth species

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