There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology

R. Scott Hawley, Holly Irick, Deana A. Haddox, Michelle D. Whitley, Tamar Arbel, Janet Jang, Kim McKim, Anne E. Zitron, Christine New, Geoffrey J. Childs, Allan Lohe

Research output: Contribution to journalArticle

118 Citations (Scopus)

Abstract

There are numerous examples of the regular segregation of achiasmate chromosomes at meiosis I in Drosophila melanogaster females. Classically, the choice of achiasmate segregational partners has been thought to be independent of homology, but rather made on the basis of availability or similarities in size and shape. To the contrary, we show here that heterochromatic homology plays a primary role in ensuring the proper segregation of achiasmate homologs. We observe that the heterochromatin of chromosome 4 functions as, or contains, a meiotic pairing site. We show that free duplications carrying the 4th chromosome pericentric heterochromatin induce high frequencies of 4th chromosome nondisjunction regardless of their size. Moreover, a duplication from which some of the 4th chromosome heterochromatin has been removed is unable to induce 4th chromosome nondisjunction. Similarly, in the absence of either euchromatic homology or a size similarity, duplications bearing the X chromosome heterochromatin also disrupt the segregation of two achiasmate X chromosome centromeres. Although heterochromatic regions are sufficient to conjoin nonexchange homologues, we confirm that the segregation of heterologous chromosomes is determined by size, shape, and availability. The meiotic mutation Axs differentiates between these two processes of achiasmate centromere coorientation by disrupting only the homology‐dependent mechanism. Thus there are two different mechanisms by which achiasmate segregational partners are chosen. We propose that the absence of diplotene‐diakinesis during female meiosis allows heterochromatic pairings to persist until prometaphase and thus to co‐orient homologous centromeres. We also propose that heterologous disjunctions result from a separate and homology‐independent process that likely occurs during prometaphase. The latter process, which may not require the physical association of segregational partners, is similar to those observed in many insects, in Saccharomyces cerevisiae and in C. elegans males. We also suggest that the physical basis of this process may reflect known properties of the Drosophila meiotic spindle. © 1993 Wiley‐Liss, Inc.

Original languageEnglish (US)
Pages (from-to)440-467
Number of pages28
JournalDevelopmental Genetics
Volume13
Issue number6
DOIs
StatePublished - 1992

Fingerprint

Heterochromatin
Drosophila
Centromere
Chromosomes
Prometaphase
Chromosome Segregation
Meiosis
X Chromosome
Physical Phenomena
Chromosomes, Human, Pair 4
Spindle Apparatus
Drosophila melanogaster
Saccharomyces cerevisiae
Insects
Mutation

Keywords

  • Drosophila
  • heterochromatin
  • homology
  • Meiosis
  • pairing
  • segregation

ASJC Scopus subject areas

  • Genetics
  • Developmental Biology
  • Cell Biology

Cite this

There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. / Hawley, R. Scott; Irick, Holly; Haddox, Deana A.; Whitley, Michelle D.; Arbel, Tamar; Jang, Janet; McKim, Kim; Zitron, Anne E.; New, Christine; Childs, Geoffrey J.; Lohe, Allan.

In: Developmental Genetics, Vol. 13, No. 6, 1992, p. 440-467.

Research output: Contribution to journalArticle

Hawley, RS, Irick, H, Haddox, DA, Whitley, MD, Arbel, T, Jang, J, McKim, K, Zitron, AE, New, C, Childs, GJ & Lohe, A 1992, 'There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology', Developmental Genetics, vol. 13, no. 6, pp. 440-467. https://doi.org/10.1002/dvg.1020130608
Hawley, R. Scott ; Irick, Holly ; Haddox, Deana A. ; Whitley, Michelle D. ; Arbel, Tamar ; Jang, Janet ; McKim, Kim ; Zitron, Anne E. ; New, Christine ; Childs, Geoffrey J. ; Lohe, Allan. / There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. In: Developmental Genetics. 1992 ; Vol. 13, No. 6. pp. 440-467.
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abstract = "There are numerous examples of the regular segregation of achiasmate chromosomes at meiosis I in Drosophila melanogaster females. Classically, the choice of achiasmate segregational partners has been thought to be independent of homology, but rather made on the basis of availability or similarities in size and shape. To the contrary, we show here that heterochromatic homology plays a primary role in ensuring the proper segregation of achiasmate homologs. We observe that the heterochromatin of chromosome 4 functions as, or contains, a meiotic pairing site. We show that free duplications carrying the 4th chromosome pericentric heterochromatin induce high frequencies of 4th chromosome nondisjunction regardless of their size. Moreover, a duplication from which some of the 4th chromosome heterochromatin has been removed is unable to induce 4th chromosome nondisjunction. Similarly, in the absence of either euchromatic homology or a size similarity, duplications bearing the X chromosome heterochromatin also disrupt the segregation of two achiasmate X chromosome centromeres. Although heterochromatic regions are sufficient to conjoin nonexchange homologues, we confirm that the segregation of heterologous chromosomes is determined by size, shape, and availability. The meiotic mutation Axs differentiates between these two processes of achiasmate centromere coorientation by disrupting only the homology‐dependent mechanism. Thus there are two different mechanisms by which achiasmate segregational partners are chosen. We propose that the absence of diplotene‐diakinesis during female meiosis allows heterochromatic pairings to persist until prometaphase and thus to co‐orient homologous centromeres. We also propose that heterologous disjunctions result from a separate and homology‐independent process that likely occurs during prometaphase. The latter process, which may not require the physical association of segregational partners, is similar to those observed in many insects, in Saccharomyces cerevisiae and in C. elegans males. We also suggest that the physical basis of this process may reflect known properties of the Drosophila meiotic spindle. {\circledC} 1993 Wiley‐Liss, Inc.",
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AU - Whitley, Michelle D.

AU - Arbel, Tamar

AU - Jang, Janet

AU - McKim, Kim

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AU - Childs, Geoffrey J.

AU - Lohe, Allan

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