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. 1997 Jun;190(Pt 4):563–576. doi: 10.1046/j.1469-7580.1997.19040563.x

Nuclear morphogenesis and the role of the manchette during spermiogenesis in the ostrich (Struthio camelus)

J T SOLEY 1
PMCID: PMC1467641  PMID: 9183679

Abstract

Nuclear condensation during spermiogenesis in the ostrich follows the basic pattern established in other vertebrates. The fine granular nuclear substance of early spermatids is gradually replaced by numbers of coarse dense granules which appear to arise by aggregation of smaller dispersed elements of the chromatin. The granules increase in size and eventually coalesce to form the compact homogenous mass of chromatin typical of the mature sperm. In ostrich spermatids, however, the aggregation of the nuclear material produces large numbers of longitudinally oriented rod-shaped structures in addition to some granular material. Although fibrillar chromatin has been observed during spermiogenesis in a number of vertebrate species, the hollow nature of the rod-shaped chromatin granules in ostrich spermatids is a unique phenomenon. The spiralisation of the chromatin material observed in ostrich spermatids and in some other nonpasserine birds is possibly related to the reduction in nuclear length demonstrated during spermiogenesis in these species. In common with other nonpasserine birds, spermiogenesis in the ostrich is characterised by the appearance both of a circular and a longitudinal manchette. The circular manchette consists of a single row of microtubules reinforced by additional peripherally arranged microtubules. Links between adjacent microtubules, and between the nucleolemma and some of the microtubules, are evident. The longitudinal manchette consists of arrays of interconnected microtubules arranged in approximately 4–6 staggered, ill defined rows. This structure seems to originate as a result of the rearrangement of the microtubules of the circular manchette and is only formed once the process of chromatin condensation is well advanced. Based on the sequence of morphological events observed during spermiogenesis in the ostrich, it is concluded that the circular manchette is responsible for the initial transformation in shape of the spermatid nucleus. Thereafter, the chromatin condenses independently within the confines of the nucleolemma with the circular manchette merely acting to maintain the shape of the nucleus while this process is underway, to compress the nuclear membrane, and possibly to orientate the subunits of the condensing chromatin. The longitudinal manchette appears to assist in the translocation of material during spermatid elongation. There are indications that the developing acrosome is instrumental in effecting nuclear shaping of the apical (subacrosomal) head region of the ostrich spermatid.

Keywords: Nuclear shaping, spermatids

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Selected References

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  1. Aire T. A., Olowo-okorun M. O., Ayeni J. S. The seminiferous epithelium in the guinea fowl (Numida meleagris). Cell Tissue Res. 1980;205(2):319–325. doi: 10.1007/BF00234690. [DOI] [PubMed] [Google Scholar]
  2. Asa C. S., Phillips D. M. Nuclear shaping in spermatids of the Thai leaf frog Megophrys montana. Anat Rec. 1988 Mar;220(3):287–290. doi: 10.1002/ar.1092200309. [DOI] [PubMed] [Google Scholar]
  3. BURGOS M. H., FAWCETT D. W. An electron microscope study of spermatid differentiation in the toad, Bufo arenarum Hensel. J Biophys Biochem Cytol. 1956 May 25;2(3):223–240. doi: 10.1083/jcb.2.3.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BURGOS M. H., FAWCETT D. W. Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J Biophys Biochem Cytol. 1955 Jul 25;1(4):287–300. doi: 10.1083/jcb.1.4.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carrick F. N., Hughes R. L. Aspects of the structure and development of monotreme spermatozoa and their relevance to the evolution of mammalian sperm morphology. Cell Tissue Res. 1982;222(1):127–141. doi: 10.1007/BF00218293. [DOI] [PubMed] [Google Scholar]
  6. Clark A. W. Some aspects of spermiogenesis in a lizard. Am J Anat. 1967 Sep;121(2):369–399. doi: 10.1002/aja.1001210212. [DOI] [PubMed] [Google Scholar]
  7. Cole A., Meistrich M. L., Cherry L. M., Trostle-Weige P. K. Nuclear and manchette development in spermatids of normal and azh/azh mutant mice. Biol Reprod. 1988 Mar;38(2):385–401. doi: 10.1095/biolreprod38.2.385. [DOI] [PubMed] [Google Scholar]
  8. Del Conte E. The subacrosomal granule and its evolution during spermiogenesis in a lizard. Observations about the acrosomal fringe and the spermatid-sertoli cell relationship. Cell Tissue Res. 1976 Sep 1;171(4):483–498. doi: 10.1007/BF00220240. [DOI] [PubMed] [Google Scholar]
  9. Dooher G. B., Bennett D. Abnormal microtubular systems in mouse spermatids associated with a mutant gene at the T-locus. J Embryol Exp Morphol. 1974 Dec;32(3):749–761. [PubMed] [Google Scholar]
  10. FAWCETT W., WITEBSKY F. OBSERVATIONS ON THE ULTRASTRUCTURE OF NUCLEATED ERYTHROCYTES AND THROMBOCYTES, WITH PARTICULAR REFERENCE TO THE STRUCTURAL BASIS OF THEIR DISCOIDAL SHAPE. Z Zellforsch Mikrosk Anat. 1964 May 29;62:785–806. doi: 10.1007/BF00342184. [DOI] [PubMed] [Google Scholar]
  11. Fawcett D. W., Anderson W. A., Phillips D. M. Morphogenetic factors influencing the shape of the sperm head. Dev Biol. 1971 Oct;26(2):220–251. doi: 10.1016/0012-1606(71)90124-2. [DOI] [PubMed] [Google Scholar]
  12. Goodrowe K. L., Heath E. Disposition of the manchette in the normal equine spermatid. Anat Rec. 1984 Jun;209(2):177–183. doi: 10.1002/ar.1092090205. [DOI] [PubMed] [Google Scholar]
  13. Gunawardana V. K., Scott M. G. Ultrastructural studies on the differentiation of spermatids in the domestic fowl. J Anat. 1977 Dec;124(Pt 3):741–755. [PMC free article] [PubMed] [Google Scholar]
  14. Handel M. A. Effects of colchicine on spermiogenesis in the mouse. J Embryol Exp Morphol. 1979 Jun;51:73–83. [PubMed] [Google Scholar]
  15. Humphreys P. N. The differentiation of the acrosome in the spermatid of the budgerigar (Melopsittacus undulatus). Cell Tissue Res. 1975;156(3):411–416. doi: 10.1007/BF00225369. [DOI] [PubMed] [Google Scholar]
  16. Lin M., Jones R. C. Spermiogenesis and spermiation in the Japanese quail (Coturnix coturnix japonica). J Anat. 1993 Dec;183(Pt 3):525–535. [PMC free article] [PubMed] [Google Scholar]
  17. Lin M., Thorne M. H., Martin I. C., Sheldon B. L., Jones R. C. Electron microscopy of the seminiferous epithelium in the triploid (ZZZ and ZZW) fowl, Gallus domesticus. J Anat. 1995 Jun;186(Pt 3):563–576. [PMC free article] [PubMed] [Google Scholar]
  18. Lyke E. B., Robson E. A. Spermatogenesis in Anthozoa: differentiation of the spermatid. Cell Tissue Res. 1975;157(2):185–205. doi: 10.1007/BF00222065. [DOI] [PubMed] [Google Scholar]
  19. McIntosh J. R., Porter K. R. Microtubules in the spermatids of the domestic fowl. J Cell Biol. 1967 Oct;35(1):153–173. doi: 10.1083/jcb.35.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Meistrich M. L., Trostle-Weige P. K., Russell L. D. Abnormal manchette development in spermatids of azh/azh mutant mice. Am J Anat. 1990 May;188(1):74–86. doi: 10.1002/aja.1001880109. [DOI] [PubMed] [Google Scholar]
  21. Myles D. G., Hepler P. K. Shaping of the sperm nucleus in Marsilea: a distinction between factors responsible for shape generation and shape determination. Dev Biol. 1982 Apr;90(2):238–252. doi: 10.1016/0012-1606(82)90373-6. [DOI] [PubMed] [Google Scholar]
  22. NAGANO T. Observations on the fine structure of the developing spermatid in the domestic chicken. J Cell Biol. 1962 Aug;14:193–205. doi: 10.1083/jcb.14.2.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Okamura F., Nishiyama H. The early development of the tail and the transformation of the shape of the nucleus of the spermatid of the domestic fowl, Gallus gallus. Cell Tissue Res. 1976 Jun 28;169(3):345–359. doi: 10.1007/BF00219607. [DOI] [PubMed] [Google Scholar]
  24. Phillips D. M., Asa C. S. Development of spermatozoa in the rhea. Anat Rec. 1989 Mar;223(3):276–282. doi: 10.1002/ar.1092230306. [DOI] [PubMed] [Google Scholar]
  25. Phillips D. M. Nuclear shaping during spermiogenesis in the whip scorpion. J Ultrastruct Res. 1976 Mar;54(3):397–405. doi: 10.1016/s0022-5320(76)80025-1. [DOI] [PubMed] [Google Scholar]
  26. Phillips D. M. Nuclear shaping in the absence of microtubules in scorpion spermatids. J Cell Biol. 1974 Sep;62(3):911–917. doi: 10.1083/jcb.62.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rattner J. B., Brinkley B. R. Ultrastructure of mammalian spermiogenesis. 3. The organization and morphogenesis of the manchette during rodent spermiogenesis. J Ultrastruct Res. 1972 Nov;41(3):209–218. doi: 10.1016/s0022-5320(72)90065-2. [DOI] [PubMed] [Google Scholar]
  29. Rattner J. B. Nuclear shaping in marsupial spermatids. J Ultrastruct Res. 1972 Sep;40(5):498–512. doi: 10.1016/s0022-5320(72)80038-8. [DOI] [PubMed] [Google Scholar]
  30. Rattner J. B., Olson G. Observations on the fine structure of the nuclear ring of the mammalian spermatid. J Ultrastruct Res. 1973 Jun;43(5):438–444. doi: 10.1016/s0022-5320(73)90020-8. [DOI] [PubMed] [Google Scholar]
  31. Russell L. D., Russell J. A., MacGregor G. R., Meistrich M. L. Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am J Anat. 1991 Oct;192(2):97–120. doi: 10.1002/aja.1001920202. [DOI] [PubMed] [Google Scholar]
  32. Russell L. D., Ying L., Overbeek P. A. Insertional mutation that causes acrosomal hypo-development: its relationship to sperm head shaping. Anat Rec. 1994 Apr;238(4):437–453. doi: 10.1002/ar.1092380403. [DOI] [PubMed] [Google Scholar]
  33. Soley J. T. Centriole development and formation of the flagellum during spermiogenesis in the ostrich (Struthio camelus). J Anat. 1994 Oct;185(Pt 2):301–313. [PMC free article] [PubMed] [Google Scholar]
  34. Soley J. T. Ultrastructure of ostrich (Struthio camelus) spermatozoa: I. Transmission electron microscopy. Onderstepoort J Vet Res. 1993 Jun;60(2):119–130. [PubMed] [Google Scholar]
  35. Tingari M. D. Observations on the fine structure of spermatozoa in the testis and excurrent ducts of the male fowl, Gallus domesticus. J Reprod Fertil. 1973 Aug;34(2):255–265. doi: 10.1530/jrf.0.0340255. [DOI] [PubMed] [Google Scholar]
  36. Turner F. R. The effects of colchicine on spermatogenesis in Nitella. J Cell Biol. 1970 Aug;46(2):220–234. doi: 10.1083/jcb.46.2.220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Xia L., Clermont Y., Lalli M., Buckland R. B. Evolution of the endoplasmic reticulum during spermiogenesis of the rooster: an electron microscopic study. Am J Anat. 1986 Nov;177(3):301–312. doi: 10.1002/aja.1001770303. [DOI] [PubMed] [Google Scholar]
  39. Yasuzumi G. Electron microscope studies on spermiogenesis in various animal species. Int Rev Cytol. 1974;37(0):53–119. doi: 10.1016/s0074-7696(08)61357-1. [DOI] [PubMed] [Google Scholar]
  40. Yasuzumi G., Sugioka T. Two types of microtubules appearing in the testicular cells of the lovebird. Arch Histol Jpn. 1966 Nov;27(1):259–265. doi: 10.1679/aohc1950.27.259. [DOI] [PubMed] [Google Scholar]
  41. Yasuzumi G., Yasuda M. Spermatogenesis in animals as revealed by electron microscopy. 18. Fine structure of developing spermatids of the Japanese freshwater turle fixed with potassium permanganate. Z Zellforsch Mikrosk Anat. 1968;85(1):18–33. [PubMed] [Google Scholar]

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