DOI: 10.1093/genetics/161.4.1551. Does <i>Stellate</i> Cause Meiotic Drive in <i>Drosophila melanogaster</i>?

Does Stellate Cause Meiotic Drive in Drosophila melanogaster?

10.1093/genetics/161.4.1551

Crossref journal-article

Oxford University Press (OUP)

Genetics (286)

Abstract

Abstract Drosophila melanogaster males deficient for the crystal (cry) locus of the Y chromosome that carry between 15 and 60 copies of the X-linked Stellate (Ste) gene are semisterile, have elevated levels of nondisjunction, produce distorted sperm genotype ratios (meiotic drive), and evince hyperactive transcription of Ste in the testes. Ste seems to be the active element in this system, and it has been proposed that the ancestral Ste gene was “selfish” and increased in frequency because it caused meiotic drive. This hypothetical evolutionary history is based on the idea that Ste overexpression, and not the lack of cry, causes the meiotic drive of cry– males. To test whether this is true, we have constructed a Ste-deleted X chromosome and examined the phenotype of Ste–/cry– males. If hyperactivity of Ste were necessary for the transmission defects seen in cry– males, cry– males completely deficient for Ste would be normal. Although it is impossible to construct a completely Ste– genotype, we find that Ste–/cry– males have exactly the same phenotype as Ste+/cry– males. The deletion of all X chromosome Ste copies not only does not eliminate meiotic drive and nondisjunction, but it also does not even reduce them below the levels produced when the X carries 15 copies of Ste.

Bibliography

Belloni, M., Tritto, P., Bozzetti, M. P., Palumbo, G., & Robbins, L. G. (2002). Does Stellate Cause Meiotic Drive in Drosophila melanogaster? Genetics, 161(4), 1551â1559.

Authors 5

Massimo Belloni (first)
Patrizia Tritto (additional)
Maria Pia Bozzetti (additional)
Gioacchino Palumbo (additional)
Leonard G Robbins (additional)

References 38 Referenced 17

10.1016/S0960-9822(01)00299-8 / Curr. Biol. / Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline by Aravin (2001)
10.1093/nar/20.14.3731 / Nucleic Acids Res. / Structural organization and diversification of Y-linked sequences comprising Su(Ste) genes in Drosophila melanogaster by Balakireva (1992)
10.1016/S0959-437X(00)00065-4 / Curr. Opin. Genet. Dev. / Making noise about silence: repression of repeated genes in animals by Birchler (2000)
10.1073/pnas.92.13.6067 / Proc. Natl. Acad. Sci. USA / The Ste locus, a component of the parasitic cry-Ste system of Drosophila melanogaster, encodes a protein that forms crystals in primary spermatocytes and mimics properties of the beta subunit of casein kinase 2 by Bozzetti (1995)
10.1038/sj.hdy.6886100 / Heredity / Are Drosophila SR drive chromosomes always balanced? by Carvalho (1999)
Crawley P G , 1996 The development of a Rex-induced spiral exchange technique for mapping the ribosomal DNA of D. melanogaster and further investigations of the genetic properties of Rex. Ph.D. Dissertation, Michigan State University, East Lansing, MI.
10.1016/S0960-9822(07)00537-4 / Curr. Biol. / Imprinted control of gene activity in Drosophila by Golic (1998)
10.1093/genetics/107.4.591 / Genetics / Cytogenetic analysis of a segment of the Y chromosome of Drosophila melanogaster by Hardy (1984)
10.1093/genetics/130.1.229 / Genetics / Is Stellate a relict meiotic driver? by Hurst (1992)
10.1093/genetics/142.2.641 / Genetics / Further evidence consistent with Stellate’s involvement in meiotic drive by Hurst (1996)
10.1093/genetics/128.4.841 / Genetics / Causes of sex-ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane’s rule and related phenomena by Hurst (1991)
10.1093/oxfordjournals.molbev.a026348 / Mol. Biol. Evol. / Molecular evolution of two paralogous tandemly repeated heterochromatic gene clusters linked to the X and Y chromosomes of Drosophila melanogaster by Kogan (2000)
10.1093/genetics/147.3.937 / Genetics / The weaker sex is heterogametic: 75 years of Haldane’s rule by Laurie (1997)
10.1073/pnas.69.1.182 / Proc. Natl. Acad. Sci. USA / The role of X-chromosome inactivation during spermatogenesis by Lifschytz (1972)
{'key': '2022010517422731700_R15', 'volume-title': 'The Genome of Drosophila melanogaster', 'author': 'Lindsley', 'year': '1992'} / The Genome of Drosophila melanogaster by Lindsley (1992)
10.1093/genetics/107.4.611 / Genetics / Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis by Livak (1984)
10.1093/genetics/124.2.303 / Genetics / Detailed structure of the Drosophila melanogaster Stellate genes and their transcripts by Livak (1990)
10.1093/genetics/151.4.1503 / Genetics / Genomic imprinting and position-effect variegation in Drosophila melanogaster by Lloyd (1999)
10.1146/annurev.ge.25.120191.002455 / Annu. Rev. Genet. / Segregation distorters by Lyttle (1991)
10.1016/0168-9525(93)90120-7 / Trends Genet. / Cheaters sometimes prosper: distortion of Mendelian segregation by meiotic drive by Lyttle (1993)
10.1093/genetics/106.3.403 / Genetics / Sex chromosome meiotic drive in Drosophila melanogaster males by McKee (1984)
10.1093/genetics/116.3.409 / Genetics / X-4 translocations and meiotic drive in Drosophila melanogaster males: role of sex chromosome pairing by McKee (1987)
10.1093/genetics/116.3.399 / Genetics / Inseparability of X-heterochromatic functions responsible for X:Y pairing, meiotic drive and male fertility in Drosophila melanogaster by McKee (1987)
10.1093/genetics/142.1.149 / Genetics / Structure of the Y chromosomal Su(Ste) locus in Drosophila melanogaster and evidence for localized recombination among repeats by McKee (1996)
10.1093/genetics/149.1.143 / Genetics / Male sterility and meiotic drive associated with sex chromosome rearrangements in Drosophila: role of X-Y pairing by McKee (1998)
10.1023/A:1026536200594 / Genetica / On the roles of heterochromatin and euchromatin in meiosis in Drosophila: mapping chromosomal pairing sites and testing candidate mutations for effects on X-Y nondisjunction and meiotic drive in male meiosis by McKee (2000)
10.1093/genetics/138.4.1181 / Genetics / Genetic analysis of Stellate elements of Drosophila melanogaster by Palumbo (1994)
10.1016/0168-9525(86)90163-0 / Trends Genet. / The peculiar genetic organization of Drosophila heterochromatin by Pimpinelli (1986)
10.1093/genetics/154.1.13 / Genetics / Do-it-yourself statistics: a computer-assisted likelihood approach to analysis of data from genetic crosses by Robbins (2000)
10.1093/genetics/120.4.1053 / Genetics / Rex-induced recombination implies bi-polar organization of the ribosomal RNA genes of Drosophila melanogaster by Robbins (1988)
10.1093/genetics/142.2.645 / Genetics / Measuring meiotic drive by Robbins (1996)
10.1086/281969 / Am. Nat. / Meiotic drive as an evolutionary force by Sandler (1957)
10.1093/genetics/151.2.749 / Genetics / Genetic and molecular characterization of sting, a gene involved in crystal formation and meiotic drive in the male germ line of Drosophila melanogaster by Schmidt (1999)
10.1093/genetics/132.4.1033 / Genetics / Copies of a Stellate gene variant are located in the X heterochromatin of Drosophila melanogaster and are probably expressed by Shevelyov (1992)
{'key': '2022010517422731700_R35', 'first-page': '955', 'article-title': 'Position effect variegation in Drosophila', 'volume-title': 'The Genetics and Biology of Drosophila', 'author': 'Spofford', 'year': '1976'} / The Genetics and Biology of Drosophila / Position effect variegation in Drosophila by Spofford (1976)
10.1007/s004120100136 / Chromosoma / A role of the Drosophila homeless gene in repression of Stellate in male meiosis by Stapleton (2001)
Tritto P , 2000 Charatterizzazione genetica e molecolare di mutazioni autosomiche che interferiscono con l’espressione delle sequenze Stellate in Drosophila melanogaster. Ph.D. Dissertation, University of Bari, Italy (available from http://www.biologia. uniba.it/dottorato/Tesi.html).
10.1093/genetics/146.1.253 / Genetics / Heterochromatic Stellate gene cluster in Drosophila melanogaster: structure and molecular evolution by Tulin (1997)

Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 12:49 a.m.)
Deposited	3 years, 7 months ago (Jan. 5, 2022, 12:43 p.m.)
Indexed	1 year, 10 months ago (Oct. 11, 2023, 1:59 p.m.)
Issued	23 years ago (Aug. 1, 2002)
Published	23 years ago (Aug. 1, 2002)
Published Online	23 years ago (Aug. 1, 2002)
Published Print	23 years ago (Aug. 1, 2002)

Funders 0

None

BibTeX

@article{Belloni_2002, title={Does Stellate Cause Meiotic Drive in Drosophila melanogaster?}, volume={161}, ISSN={1943-2631}, url={http://dx.doi.org/10.1093/genetics/161.4.1551}, DOI={10.1093/genetics/161.4.1551}, number={4}, journal={Genetics}, publisher={Oxford University Press (OUP)}, author={Belloni, Massimo and Tritto, Patrizia and Bozzetti, Maria Pia and Palumbo, Gioacchino and Robbins, Leonard G}, year={2002}, month=aug, pages={1551–1559} }

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  "abstract": "<jats:title>Abstract</jats:title>\n               <jats:p>Drosophila melanogaster males deficient for the crystal (cry) locus of the Y chromosome that carry between 15 and 60 copies of the X-linked Stellate (Ste) gene are semisterile, have elevated levels of nondisjunction, produce distorted sperm genotype ratios (meiotic drive), and evince hyperactive transcription of Ste in the testes. Ste seems to be the active element in this system, and it has been proposed that the ancestral Ste gene was \u201cselfish\u201d and increased in frequency because it caused meiotic drive. This hypothetical evolutionary history is based on the idea that Ste overexpression, and not the lack of cry, causes the meiotic drive of cry\u2013 males. To test whether this is true, we have constructed a Ste-deleted X chromosome and examined the phenotype of Ste\u2013/cry\u2013 males. If hyperactivity of Ste were necessary for the transmission defects seen in cry\u2013 males, cry\u2013 males completely deficient for Ste would be normal. Although it is impossible to construct a completely Ste\u2013 genotype, we find that Ste\u2013/cry\u2013 males have exactly the same phenotype as Ste+/cry\u2013 males. The deletion of all X chromosome Ste copies not only does not eliminate meiotic drive and nondisjunction, but it also does not even reduce them below the levels produced when the X carries 15 copies of Ste.</jats:p>",
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      "volume": "10",
      "author": "Birchler",
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      "volume": "138",
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      "volume": "2",
      "author": "Pimpinelli",
      "year": "1986",
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      "DOI": "10.1093/genetics/142.2.645",
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      "article-title": "Meiotic drive as an evolutionary force",
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      "author": "Sandler",
      "year": "1957",
      "journal-title": "Am. Nat."
    },
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      "DOI": "10.1093/genetics/151.2.749",
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      "volume": "151",
      "author": "Schmidt",
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      "volume": "132",
      "author": "Shevelyov",
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    {
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      "article-title": "Position effect variegation in Drosophila",
      "volume-title": "The Genetics and Biology of Drosophila",
      "author": "Spofford",
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      "volume": "110",
      "author": "Stapleton",
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    },
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      "key": "2022010517422731700_R37",
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      "article-title": "Heterochromatic Stellate gene cluster in Drosophila melanogaster: structure and molecular evolution",
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