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© The Rockefeller University Press, 0021-9525/1997//5 $5.00
The Journal of Cell Biology, Volume 137, Number 1, , 1997 5-18

Article

Telomeres Cluster De Novo before the Initiation of Synapsis: A Three-dimensional Spatial Analysis of Telomere Positions before and during Meiotic Prophase



Hank W. Bass*, Wallace F. Marshall{ddagger}, John W. Sedat{ddagger}, David A. Agard{ddagger},§, and W. Zacheus Cande*

* Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California 94720; and {ddagger} Department of Biochemistry and Biophysics, § Howard Hughes Medical Institute, University of California at San Francisco, San Francisco, California 94143

We have analyzed the progressive changes in the spatial distribution of telomeres during meiosis using three-dimensional, high resolution fluorescence microscopy. Fixed meiotic cells of maize (Zea mays L.) were subjected to in situ hybridization under conditions that preserved chromosome structure, allowing identification of stage-dependent changes in telomere arrangements. We found that nuclei at the last somatic prophase before meiosis exhibit a nonrandom, polarized chromosome organization resulting in a loose grouping of telomeres. Quantitative measurements on the spatial arrangements of telomeres revealed that, as cells passed through premeiotic interphase and into leptotene, there was an increase in the frequency of large telomere-to-telomere distances and a decrease in the bias toward peripheral localization of telomeres. By leptotene, there was no obvious evidence of telomere grouping, and the large, singular nucleolus was internally located, nearly concentric with the nucleus. At the end of leptotene, telomeres clustered de novo at the nuclear periphery, coincident with a displacement of the nucleolus to one side. The telomere cluster persisted throughout zygotene and into early pachytene. The nucleolus was adjacent to the cluster at zygotene. At the pachytene stage, telomeres rearranged again by dispersing throughout the nuclear periphery. The stagedependent changes in telomere arrangements are suggestive of specific, active telomere-associated motility processes with meiotic functions. Thus, the formation of the cluster itself is an early event in the nuclear reorganizations associated with meiosis and may reflect a control point in the initiation of synapsis or crossing over.

H.W. Bass was supported in the early years of this work by a National Institutes of Health (NIH) grant to J.W. Sedat (R01-GM-25101-16). H.W. Bass is currently supported as a D.O.E. postdoctoral fellow of the Life Sciences Research Foundation. This work was supported by the (NIH) grants to W.Z. Cande (R01-GM-48547) to J.W. Sedat (R01-GM-2510116), and to D.A. Agard (R01-GM-31627). D.A. Agard is an investigator of the Howard Hughes Medical Institute.

1. Abbreviations used in this paper: DAPI 4',6-diamidino-2-phenylindole, dihydrochloride; FISH, fluorescence in situ hybridization; FITC, fluorescein isothiocyanate.

Please address all correspondence to W.Z. Cande, 341 LSA, Department of Molecular and Cell Biology, University of California, Berkeley, CA. Tel.: (510) 642-1669. Fax: (510) 643-6791.


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