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

PLoS Genet. 2024 Jun 24;20(6):e1011329. doi: 10.1371/journal.pgen.1011329. eCollection 2024 Jun.

Abstract

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.

MeSH terms

  • Animals
  • Bombyx* / genetics
  • Bombyx* / physiology
  • Chromosome Pairing / genetics
  • Chromosome Segregation* / genetics
  • Chromosomes, Insect / genetics
  • In Situ Hybridization, Fluorescence
  • Kinetics
  • Kinetochores / metabolism
  • Male
  • Meiosis* / genetics
  • Metaphase
  • Microtubules / genetics
  • Microtubules / metabolism
  • Moths* / genetics
  • Moths* / physiology
  • Spermatogenesis* / genetics
  • Telomere / genetics
  • Telomere / metabolism

Grants and funding

“This work was funded by the Intramural Program of the Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health (including salaries for C.H., T.T.W., and L.F.R.; HD009019-01 to L.F.R.; https://www.nichd.nih.gov/about/org/dir), and the Intramural Program of the National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health (including salaries for H.L. and E.P.L.; DK015602 to E.P.L.; https://www.niddk.nih.gov/about-niddk/offices-divisions/division-intramural-research). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.