Skip to main content
SpringerLink
Log in

Distance segregation of sex chromosomes in crane-fly spermatocytes studied using laser microbeam irradiations

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Univalent sex chromosomes in crane-fly spermatocytes have kinetochore spindle fibres to each spindle pole (amphitelic orientation) from metaphase throughout anaphase. The univalents segregate in anaphase only after the autosomes approach the poles. As each univalent moves in anaphase, one spindle fibre shortens and the other spindle fibre elongates. To test whether the directionality of force production is fixed at anaphase, that is, whether one spindle fibre can only elongate and the other only shorten, we cut univalents in half with a laser microbeam, to create two chromatids. In both sex-chromosome metaphase and sex-chromosome anaphase, the two chromatids that were formed moved to opposite poles (to the poles to which their fibre was attached) at speeds about the same as autosomes, much faster than the usual speeds of univalent movements. Since the chromatids moved to the pole to which they were attached, independent of the direction to which the univalent as a whole was moving, the spindle fibre that normally elongates in anaphase still is able to shorten and produce force towards the pole when allowed (or caused) to do so.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Bauer H, Dietz R, Röbbelen C (1961) Die Spermatocytenteilungen der Tipuliden. III Mitteilung. Das Bewegungshalten der chromosomen in translokationsheterozygoten von Tipula oleracea. Chromosoma 12:116–189

    Article  PubMed  CAS  Google Scholar 

  • Camenzind R, Nicklas RB (1968) The non-random segregation in spermatocytes of Gryllotalpa hexadactyla. A micromanipulation analysis. Chromosoma 24:324–335

    Article  PubMed  CAS  Google Scholar 

  • Dietz R (1969) Bau und funktion des spindelapparats. Naturwissensch 56:237–248

    Article  CAS  Google Scholar 

  • Fabian L, Xia X, Venkitaramani DV, Johansen KM, Johansen J, Andrew DJ, Forer A (2007) Titin in insect spermatocyte spindle fibers associates with microtubules, actin, myosin and the matrix proteins skeletor, megator and chromator. J Cell Sci 120:2190–2204

    Article  PubMed  CAS  Google Scholar 

  • Forer A, Koch C (1973) Influence of autosome movements and of sex-chromosome movements on sex-chromosome segregation in crane fly spermatocytes. Chromosoma 40:417–442

    Article  PubMed  CAS  Google Scholar 

  • Forer A, Pickett-Heaps J (2005) Fibrin clots keep non-adhering living cells in place on glass for perfusion or fixation. Cell Biol Int 29:721–730

    Article  PubMed  CAS  Google Scholar 

  • Forer A, Swedak J (1991) Practical experiences using biological systems to monitor indoor air pollutants. In: Baird JC, Berglund B, Jackson WT (eds) Indoor air quality for people and plants. Swedish Council for Building Research, Stockholm, pp 129–158

    Google Scholar 

  • Fuge H (1972) Morphological studies on the structure of univalent sex chromosomes during anaphase movement in spermatocytes of the crane fly Pales ferruginea. Chromosoma 39:403–417

    Article  PubMed  CAS  Google Scholar 

  • Fuge H (1985) The three-dimensional architecture of chromosome fibres in the crane fly. II. Amphitelic sex univalents in meiotic anaphase I. Chromosoma 91:322–328

    Article  PubMed  CAS  Google Scholar 

  • Göltenboth F, Heitkamp U (1977) Mesostoma ehrenbergi (Fowke 1836). Plattwűrmer (Strudelwűrmer). Biologie, mikroskopische Anatomie und Cytogenetik. Grosses Zoologisches Praktikum vol 6a (1977), pp. 1–60, Gustav Fischer Stuttgart, New York.

  • Harsono MS, Zhu Q, Shi LZ, Duquette M, Berns MW (2012) Development of a dual joystick-controlled laser trapping and cutting system for optical micromanipulation of chromosomes inside living cells. J Biophotonics. doi:10.1002/jbio.201200019

  • Hughes-Schrader S (1969) Distance segregation and compound sex chromosomes in Mantispids (Neuroptera: Mantispidae). Chromosoma 27:109–129

    Article  PubMed  CAS  Google Scholar 

  • Hughes-Schrader S (1975) Male meiosis in camel-flies (Raphidioptera; Neuropteroidea). Chromosoma 51:99–110

    Article  PubMed  CAS  Google Scholar 

  • Hughes-Schrader S (1979) Diversity of chromosomal segregation mechanisms in Mantispids (Neuroptera: Mantispidae). Chromosoma 75:1–17

    Article  Google Scholar 

  • Ingber DE (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104:613–627

    PubMed  Google Scholar 

  • Johansen KM, Forer A, Yao C, Girton J, Johansen J (2011) Do nuclear envelope and intranunclear proteins reorganize during mitosis to form an elastic hydrogel-like spindle matrix? Chromosome Res 19:345–365

    Article  PubMed  CAS  Google Scholar 

  • LaFountain JR Jr, Cole RW, Rieder CL (2002) Partner telomeres during anaphase in crane-fly spermatocytes are connected by an elastic tether that exerts a backward force and resists poleward motion. J Cell Sci 115:1541–1549

    PubMed  CAS  Google Scholar 

  • La Fountain JR Jr, Cohan CS, Oldenbourg R (2011) Functional states of kinetochores revealed by laser microscurgery and fluorescent speckle microscopy. Mol Biol Cell 22:4801–4808

    Article  Google Scholar 

  • La Fountain JR Jr, Cohan CS, Oldenbourg R (2012) Pac-man motility of kinetochores unleashed by laser microsurgery. Mol Biol Cell 23:3133–3142

    Article  Google Scholar 

  • Oakley HA (1983) Male meiosis in Mesostoma ehrenbergii ehrenbergii. In: Brandham E, Bennett MD (eds) Kew chromosome conference II. George Allen and Unwin, London, pp 195–199

    Google Scholar 

  • Oakley HA (1985) Meiosis in Mesostoma ehrenbergii ehrenbergii (Turbellaria, Rhabdocoela). III. Univalent chromosome segregation during the first meiotic division in spermatocytes. Chromosoma 91:91–95

    Article  Google Scholar 

  • Payne F (1912) The chromosomes of Gryllotalpa borealis Burm. Arch Zellforsch 9:141–148

    Google Scholar 

  • Payne F (1916) A study of the germ cells of Gryllotalpa borealis and Gryllotalpa vulgaris. J Morphol 28:287–327

    Article  Google Scholar 

  • Pickett-Heaps JD, Forer A, Spurck T (1997) Traction fibre: toward a “Tensegral” model of the spindle. Cell Motil Cytoskeleton 37:1–6

    Article  PubMed  CAS  Google Scholar 

  • Schaap CJ, Forer A (1979) Temperature effects in anaphase chromosome movement in the spermatocytes of two species of crane flies (Nephrotoma suturalis Loew and Nephrotoma ferruginea Fabricius). J Cell Sci 3(9):29–52

    Google Scholar 

  • Shi LZ, Zhu Q, Wu T, Duquette M, Gomez V, Chandsawangbhuwana C, Harsono MS, Hyun N, Baker N, Nascimento J, You Z, Botvinick EB, Berns MW (2012) Integrated optical systems for laser nanosurgery and optical trapping to study cell structure and function. In: Mendez-Vilas A (ed) Current microscopy contributions to advances in science and technology. Formatex, Badajoz, Spain. Microscopy Book Series – Number 5, 2012

  • Sillers PJ, Forer A (1981) Autosomal spindle fibres influence subsequent sex-chromosome movements in crane-fly spermatocytes. J Cell Sci 49:51–67

    PubMed  CAS  Google Scholar 

  • Spurck T, Forer A, Pickett-Heaps J (1997) Ultraviolet microbeam irradiations of epithelial and spermatocyte spindles suggests that forces act on the kinetochore fibre and are not generated by its disassembly. Cell Motil Cytoskeleton 36:136–148

    Article  PubMed  CAS  Google Scholar 

  • Steffen W, Fuge H (1985) Three-dimensional architecture of chromosome fibres in the crane fly: amphitelic autosomal univalents in late prometaphase. Cytobios 43:199–212

    Google Scholar 

  • White MJD (1951) Cytogenetics of orthopteroid insects. Adv Genet 4:267–330

    Article  Google Scholar 

  • Wilson PJ, Forer A (1989) Acetylated α-tubulin in spermatogenic cells of the crane fly Nephrotoma suturalis: kinetochore microtubules are selectively acetylated. Cell Motil Cytoskeleton 14:237–250

    Article  CAS  Google Scholar 

  • Wise D, Sillers PJ, Forer A (1984) Non-random chromosome segregation in Neocurtilla hexadactyla is controlled by chromosomal spindle fibres: an ultraviolet microbeam analysis. J Cell Sci 69:1–17

    PubMed  CAS  Google Scholar 

  • Wong R, Forer A (2003) ‘Signalling’ between chromosomes in crane-fly spermatocytes studied using ultraviolet microbeam irradiation. Chromosome Res 11:771–786

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from York University (Fieldwork and Research Cost Funds) to JF, the Natural Sciences and Engineering Research Council of Canada to AF and the Beckman Laser Institute Foundation and the Air Force Office of Scientific Research (FA9550-10-0538) to MB. We are grateful to Dr. Linda Shi and Dr. Qingyuan Zhu for their help.

Author information

Authors and Affiliations

  1. Biology Department, York University, Toronto, ON, Canada, M3J 1P3

    Arthur Forer & Jessica Ferraro-Gideon

  2. Department of Bioengineering, University of California, San Diego, CA, 92093, USA

    Michael Berns

  3. Beckman Laser Institute and Department of Biomedical Engineering, University of California, Irvine, CA, 92697, USA

    Michael Berns

Authors
  1. Arthur Forer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessica Ferraro-Gideon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Berns
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arthur Forer.

Additional information

Handling Editor: Peter Nick

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(MOV 2597 kb)

ESM 2

(AVI 1926 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forer, A., Ferraro-Gideon, J. & Berns, M. Distance segregation of sex chromosomes in crane-fly spermatocytes studied using laser microbeam irradiations. Protoplasma 250, 1045–1055 (2013). https://doi.org/10.1007/s00709-013-0480-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-013-0480-4

Keywords

Search

Navigation