A Link between Meiotic Prophase Progression and Crossover Control

Carlton, Peter M.; Farruggio, Alfonso P.; Dernburg, Abby F.

doi:10.1371/journal.pgen.0020012

A Link between Meiotic Prophase Progression and Crossover Control

Journal Article · Fri Feb 03 00:00:00 EST 2006 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.0020012· OSTI ID:1627265

Carlton, Peter M. ^[1]; Farruggio, Alfonso P. ^[2]; Dernburg, Abby F. ^[3]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; DOE/OSTI
Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology

During meiosis, most organisms ensure that homologous chromosomes undergo at least one exchange of DNA, or crossover, to link chromosomes together and accomplish proper segregation. How each chromosome receives a minimum of one crossover is unknown. During early meiosis in Caenorhabditis elegans and many other species, chromosomes adopt a polarized organization within the nucleus, which normally disappears upon completion of homolog synapsis. Mutations that impair synapsis even between a single pair of chromosomes in C. elegans delay this nuclear reorganization. We quantified this delay by developing a classification scheme for discrete stages of meiosis. Immunofluorescence localization of RAD-51 protein revealed that delayed meiotic cells also contained persistent recombination intermediates. Through genetic analysis, we found that this cytological delay in meiotic progression requires double-strand breaks and the function of the crossover-promoting heteroduplex HIM-14 (Msh4) and MSH-5. Failure of X chromosome synapsis also resulted in impaired crossover control on autosomes, which may result from greater numbers and persistence of recombination intermediates in the delayed nuclei. We conclude that maturation of recombination events on chromosomes promotes meiotic progression, and is coupled to the regulation of crossover number and placement. Our results have broad implications for the interpretation of meiotic mutants, as we have shown that asynapsis of a single chromosome pair can exert global effects on meiotic progression and recombination frequency.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Wellcome Trust

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627265

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 2 Vol. 2; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (45)

IVE (Image Visualization Environment): A Software Platform for All Three-Dimensional Microscopy Applications Chen, Hans; Hughes, Diana D.; Chan, Tan-An Journal of Structural Biology, Vol. 116, Issue 1 https://doi.org/10.1006/jsbi.1996.0010	journal	January 1996
Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans Alpi, Arno; Pasierbek, Pawel; Gartner, Anton Chromosoma, Vol. 112, Issue 1 https://doi.org/10.1007/s00412-003-0237-5	journal	July 2003
The relation of recombination to mutational advance Muller, H. J. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 1, Issue 1 https://doi.org/10.1016/0027-5107(64)90047-8	journal	May 1964
Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans MacQueen, Amy J.; Phillips, Carolyn M.; Bhalla, Needhi Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.034	journal	December 2005
When Size Does Not Matter: Pairing Sites during Meiosis McKim, Kim S. Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.11.031	journal	December 2005
Chromosome-Wide Control of Meiotic Crossing over in C. elegans Hillers, Kenneth J.; Villeneuve, Anne M. Current Biology, Vol. 13, Issue 18 https://doi.org/10.1016/j.cub.2003.08.026	journal	September 2003
Imposition of Crossover Interference through the Nonrandom Distribution of Synapsis Initiation Complexes Fung, Jennifer C.; Rockmill, Beth; Odell, Michael Cell, Vol. 116, Issue 6 https://doi.org/10.1016/s0092-8674(04)00249-1	journal	March 2004
Crossover/Noncrossover Differentiation, Synaptonemal Complex Formation, and Regulatory Surveillance at the Leptotene/Zygotene Transition of Meiosis Börner, G. Valentin; Kleckner, Nancy; Hunter, Neil Cell, Vol. 117, Issue 1 https://doi.org/10.1016/s0092-8674(04)00292-2	journal	April 2004
The genetics of meiosis in Caenorhabditis elegans Zetka, Monique; Rose, Ann Trends in Genetics, Vol. 11, Issue 1 https://doi.org/10.1016/s0168-9525(00)88983-0	journal	January 1995
C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein Ahmed, Shawn; Alpi, Arno; Hengartner, Michael O. Current Biology, Vol. 11, Issue 24 https://doi.org/10.1016/s0960-9822(01)00604-2	journal	December 2001
Caenorhabditis elegans HUS-1 Is a DNA Damage Checkpoint Protein Required for Genome Stability and EGL-1-Mediated Apoptosis Hofmann, E. Randal; Milstein, Stuart; Boulton, Simon J. Current Biology, Vol. 12, Issue 22 https://doi.org/10.1016/s0960-9822(02)01262-9	journal	November 2002
Synaptonemal Complex Assembly in C. elegans Is Dispensable for Loading Strand-Exchange Proteins but Critical for Proper Completion of Recombination Colaiácovo, Mónica P.; MacQueen, Amy J.; Martinez-Perez, Enrique Developmental Cell, Vol. 5, Issue 3 https://doi.org/10.1016/s1534-5807(03)00232-6	journal	September 2003
To err (meiotically) is human: the genesis of human aneuploidy Hassold, Terry; Hunt, Patricia Nature Reviews Genetics, Vol. 2, Issue 4 https://doi.org/10.1038/35066065	journal	April 2001
Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map Wicks, Stephen R.; Yeh, Raymond T.; Gish, Warren R. Nature Genetics, Vol. 28, Issue 2 https://doi.org/10.1038/88878	journal	June 2001
The effects of translocations on recombination frequency in Caenorhabditis elegans. McKim, K. S.; Howell, A. M.; Rose, A. M. Genetics, Vol. 120, Issue 4 https://doi.org/10.1093/genetics/120.4.987	journal	December 1988
Recombination between small X chromosome duplications and the X chromosome in Caenorhabditis elegans. Herman, R. K.; Kari, C. K. Genetics, Vol. 121, Issue 4 https://doi.org/10.1093/genetics/121.4.723	journal	April 1989
Chiasma Interference as a Function of Genetic Distance Foss, E.; Lande, R.; Stahl, F. W. Genetics, Vol. 134, Issue 3 https://doi.org/10.1093/genetics/134.3.997	journal	July 1993
Meiotic mutants that cause a polar decrease in recombination on the X chromosome in Caenorhabditis elegans. Broverman, S. A.; Meneely, P. M. Genetics, Vol. 136, Issue 1 https://doi.org/10.1093/genetics/136.1.119	journal	January 1994
A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Villeneuve, A. M. Genetics, Vol. 136, Issue 3 https://doi.org/10.1093/genetics/136.3.887	journal	March 1994
The Budding Yeast Msh4 Protein Functions in Chromosome Synapsis and the Regulation of Crossover Distribution Novak, Janet E.; Ross-Macdonald, Petra B.; Roeder, G. Shirleen Genetics, Vol. 158, Issue 3 https://doi.org/10.1093/genetics/158.3.1013	journal	July 2001
Roles for Caenorhabditis elegans rad-51 in Meiosis and in Resistance to Ionizing Radiation During Development Rinaldo, Cinzia; Bazzicalupo, Paolo; Ederle, Sara Genetics, Vol. 160, Issue 2 https://doi.org/10.1093/genetics/160.2.471	journal	February 2002
Crossover Distribution and High Interference for Both the X Chromosome and an Autosome During Oogenesis and Spermatogenesis in Caenorhabditis elegans Meneely, Philip M.; Farago, Anna F.; Kauffman, Tate M. Genetics, Vol. 162, Issue 3 https://doi.org/10.1093/genetics/162.3.1169	journal	November 2002
Interchromosomal Effects and the Relation Between Crossing-Over and Nondisjunction Roberts, Paul Genetics, Vol. 47, Issue 12 https://doi.org/10.1093/genetics/47.12.1691	journal	December 1962
Interchromosomal Effects on Crossing over in Drosophila Melanogaster. ii. a Reexamination of x Chromosome Inversion Effects Suzuki, David T. Genetics, Vol. 48, Issue 12 https://doi.org/10.1093/genetics/48.12.1605	journal	December 1963
THE GENETICS OF CAENORHABDITIS ELEGANS Brenner, S. Genetics, Vol. 77, Issue 1 https://doi.org/10.1093/genetics/77.1.71	journal	May 1974
CHROMOSOMAL SITES NECESSARY FOR NORMAL LEVELS OF MEIOTIC RECOMBINATION IN DROSOPHILA MELANOGASTER . I. EVIDENCE FOR AND MAPPING OF THE SITES Hawley, R. Scott Genetics, Vol. 94, Issue 3 https://doi.org/10.1093/genetics/94.3.625	journal	March 1980
Chromosome size-dependent control of meiotic recombination Kaback, D.; Guacci, V.; Barber, D. Science, Vol. 256, Issue 5054 https://doi.org/10.1126/science.1566070	journal	April 1992
The Interchromosomal Control of Recombination Lucchesi, J. C.; Suzuki, D. T. Annual Review of Genetics, Vol. 2, Issue 1 https://doi.org/10.1146/annurev.ge.02.120168.000413	journal	December 1968
Imposition of Crossover Interference through the Nonrandom Distribution of Synapsis Initiation Complexes Fung, Jennifer C.; Rockmill, Beth; Odell, Michael Cell, Vol. 116, Issue 6 https://doi.org/10.1016/S0092-8674(04)00249-1	journal	March 2004
Crossover/Noncrossover Differentiation, Synaptonemal Complex Formation, and Regulatory Surveillance at the Leptotene/Zygotene Transition of Meiosis Börner, G. Valentin; Kleckner, Nancy; Hunter, Neil Cell, Vol. 117, Issue 1 https://doi.org/10.1016/S0092-8674(04)00292-2	journal	April 2004
The genetics of meiosis in Caenorhabditis elegans Zetka, Monique; Rose, Ann Trends in Genetics, Vol. 11, Issue 1 https://doi.org/10.1016/S0168-9525(00)88983-0	journal	January 1995
C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein Ahmed, Shawn; Alpi, Arno; Hengartner, Michael O. Current Biology, Vol. 11, Issue 24 https://doi.org/10.1016/S0960-9822(01)00604-2	journal	December 2001
Caenorhabditis elegans HUS-1 Is a DNA Damage Checkpoint Protein Required for Genome Stability and EGL-1-Mediated Apoptosis Hofmann, E. Randal; Milstein, Stuart; Boulton, Simon J. Current Biology, Vol. 12, Issue 22 https://doi.org/10.1016/S0960-9822(02)01262-9	journal	November 2002
Synaptonemal Complex Assembly in C. elegans Is Dispensable for Loading Strand-Exchange Proteins but Critical for Proper Completion of Recombination Colaiácovo, Mónica P.; MacQueen, Amy J.; Martinez-Perez, Enrique Developmental Cell, Vol. 5, Issue 3 https://doi.org/10.1016/S1534-5807(03)00232-6	journal	September 2003
C. elegans HIM-17 Links Chromatin Modification and Competence for Initiation of Meiotic Recombination Reddy, Kirthi C.; Villeneuve, Anne M. Cell, Vol. 118, Issue 4 https://doi.org/10.1016/j.cell.2004.07.026	journal	August 2004
HIM-8 Binds to the X Chromosome Pairing Center and Mediates Chromosome-Specific Meiotic Synapsis Phillips, Carolyn M.; Wong, Chihunt; Bhalla, Needhi Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.035	journal	December 2005
MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans Ahmed, Shawn; Hodgkin, Jonathan Nature, Vol. 403, Issue 6766 https://doi.org/10.1038/35003120	journal	January 2000
Systematic functional analysis of the Caenorhabditis elegans genome using RNAi Kamath, Ravi S.; Fraser, Andrew G.; Dong, Yan Nature, Vol. 421, Issue 6920 https://doi.org/10.1038/nature01278	journal	January 2003
Sex increases the efficacy of natural selection in experimental yeast populations Goddard, Matthew R.; Godfray, H. Charles J.; Burt, Austin Nature, Vol. 434, Issue 7033 https://doi.org/10.1038/nature03405	journal	March 2005
A mechanical basis for chromosome function Kleckner, N.; Zickler, D.; Jones, G. H. Proceedings of the National Academy of Sciences, Vol. 101, Issue 34 https://doi.org/10.1073/pnas.0402724101	journal	August 2004
Chiasma interference as a function of genetic distance. Foss, E.; Lande, R.; Stahl, F. W. Genetics, Vol. 133, Issue 3 https://doi.org/10.1093/genetics/133.3.681	journal	March 1993
Mutant rec-1 eliminates the meiotic pattern of crossing over in Caenorhabditis elegans. Zetka, M. C.; Rose, A. M. Genetics, Vol. 141, Issue 4 https://doi.org/10.1093/genetics/141.4.1339	journal	December 1995
Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2 MacQueen, A. J. Genes & Development, Vol. 15, Issue 13 https://doi.org/10.1101/gad.902601	journal	July 2001
Chromosome-Wide Regulation of Meiotic Crossover Formation in Caenorhabditis elegans Requires Properly Assembled Chromosome Axes Nabeshima, Kentaro; Villeneuve, Anne M.; Hillers, Kenneth J. Genetics, Vol. 168, Issue 3 https://doi.org/10.1534/genetics.104.030700	journal	November 2004
Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans Meneely, Philip M.; Farago, Anna F.; Kauffman, Tate M. Genetics, Vol. 162, Issue 3, 1169-1177 https://doi.org/10.3410/f.1007838.177310	journal	November 2002

Cited By (22)

akirinis required for diakinesis bivalent structure and synaptonemal complex disassembly at meiotic prophase I Clemons, Amy M.; Brockway, Heather M.; Yin, Yizhi Molecular Biology of the Cell, Vol. 24, Issue 7 https://doi.org/10.1091/mbc.e12-11-0841	journal	April 2013
Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation Sato-Carlton, Aya; Nakamura-Tabuchi, Chihiro; Chartrand, Stephane Kazuki The Journal of Cell Biology https://doi.org/10.1101/211672	posted_content	October 2017
Crossovers Get a Boost inBrassicaAllotriploid and Allotetraploid Hybrids Leflon, Martine; Grandont, Laurie; Eber, Frédérique The Plant Cell, Vol. 22, Issue 7 https://doi.org/10.1105/tpc.110.075986	journal	July 2010
Polyploidization increases meiotic recombination frequency in Arabidopsis Pecinka, Ales; Fang, Wei; Rehmsmeier, Marc BMC Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1741-7007-9-24	journal	April 2011
ZHP-3 Acts at Crossovers to Couple Meiotic Recombination with Synaptonemal Complex Disassembly and Bivalent Formation in C. elegans Bhalla, Needhi; Wynne, David J.; Jantsch, Verena PLoS Genetics, Vol. 4, Issue 10 https://doi.org/10.1371/journal.pgen.1000235	journal	October 2008
Leptotene/Zygotene Chromosome Movement Via the SUN/KASH Protein Bridge in Caenorhabditis elegans Baudrimont, Antoine; Penkner, Alexandra; Woglar, Alexander PLoS Genetics, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pgen.1001219	journal	November 2010
Identification of DSB-1, a Protein Required for Initiation of Meiotic Recombination in Caenorhabditis elegans, Illuminates a Crossover Assurance Checkpoint Stamper, Ericca L.; Rodenbusch, Stacia E.; Rosu, Simona PLoS Genetics, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pgen.1003679	journal	August 2013
Evidence That Masking of Synapsis Imperfections Counterbalances Quality Control to Promote Efficient Meiosis Mlynarczyk-Evans, Susanna; Roelens, Baptiste; Villeneuve, Anne M. PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1003963	journal	December 2013
A compartmentalized signaling network mediates crossover control in meiosis Zhang, Liangyu; Köhler, Simone; Rillo-Bohn, Regina eLife, Vol. 7 https://doi.org/10.7554/elife.30789	journal	March 2018
BRDT is an essential epigenetic regulator for proper chromatin organization, silencing of sex chromosomes and crossover formation in male meiosis Manterola, Marcia; Brown, Taylor; Oh, Min Young Columbia University https://doi.org/10.7916/d8795mq2	text	January 2018
Defects in meiotic recombination delay progression through pachytene in Tex19.1−/− mouse spermatocytes Crichton, James H.; Read, David; Adams, Ian R. Chromosoma, Vol. 127, Issue 4 https://doi.org/10.1007/s00412-018-0674-9	journal	June 2018
Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation Sato-Carlton, Aya; Nakamura-Tabuchi, Chihiro; Chartrand, Stephane Kazuki Journal of Cell Biology, Vol. 217, Issue 2 https://doi.org/10.1083/jcb.201707161	journal	December 2017
The tumor suppressor BRCA1/BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans Li, Qianyan; Saito, Takamune T.; Deshong, Alison J. PLOS Genetics https://doi.org/10.1101/280909	posted_content	March 2018
Regulation of Crossover Frequency and Distribution during Meiotic Recombination Saito, Takamune T.; Colaiácovo, Monica P. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 82 https://doi.org/10.1101/sqb.2017.82.034132	journal	January 2017
Recombination suppression in heterozygotes for a pericentric inversion induces the interchromosomal effect on crossovers in Arabidopsis Termolino, Pasquale; Falque, Matthieu; Aiese Cigliano, Riccardo The Plant Journal, Vol. 100, Issue 6 https://doi.org/10.1111/tpj.14505	journal	October 2019
Erratum to: Polyploidization increases meiotic recombination frequency in Arabidopsis Pecinka, Ales; Fang, Wei; Rehmsmeier, Marc BMC Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1741-7007-10-33	journal	April 2012
Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females Mehrotra, S.; McKim, K. S. PLoS Genetics, Vol. 2, Issue 11 https://doi.org/10.1371/journal.pgen.0020200	journal	January 2006
BRDT is an essential epigenetic regulator for proper chromatin organization, silencing of sex chromosomes and crossover formation in male meiosis Manterola, Marcia; Brown, Taylor M.; Oh, Min Young PLOS Genetics, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pgen.1007209	journal	March 2018
The tumor suppressor BRCA1-BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans Li, Qianyan; Saito, Takamune T.; Martinez-Garcia, Marina PLOS Genetics, Vol. 14, Issue 11 https://doi.org/10.1371/journal.pgen.1007701	journal	November 2018
Synapsis-Defective Mutants Reveal a Correlation Between Chromosome Conformation and the Mode of Double-Strand Break Repair During Caenorhabditis elegans Meiosis Smolikov, Sarit; Eizinger, Andreas; Hurlburt, Allison Genetics, Vol. 176, Issue 4 https://doi.org/10.1534/genetics.107.076968	journal	August 2007
The Synaptonemal Complex Shapes the Crossover Landscape Through Cooperative Assembly, Crossover Promotion and Crossover Inhibition During Caenorhabditis elegans Meiosis Hayashi, Michiko; Mlynarczyk-Evans, Susanna; Villeneuve, Anne M. Genetics, Vol. 186, Issue 1 https://doi.org/10.1534/genetics.110.115501	journal	June 2010
Progression of Meiosis Is Coordinated by the Level and Location of MAPK Activation Via OGR-2 in Caenorhabditis elegans Achache, Hanna; Laurent, Lévana; Hecker-Mimoun, Yaël Genetics, Vol. 212, Issue 1 https://doi.org/10.1534/genetics.119.302080	journal	March 2019

Similar Records

A Link between Meiotic Prophase Progression and CrossoverControl

Journal Article · Wed Jul 06 00:00:00 EDT 2005 · Public Library of Science (PLoS) Genetics · OSTI ID:890634

The conserved AAA ATPase PCH-2 distributes its regulation of meiotic prophase events through multiple meiotic HORMADs in C. elegans

Journal Article · Thu Apr 13 20:00:00 EDT 2023 · PLoS Genetics · OSTI ID:2469722

ATM signaling modulates cohesin behavior in meiotic prophase and proliferating cells

Journal Article · Sun Mar 05 19:00:00 EST 2023 · Nature Structural & Molecular Biology · OSTI ID:2470954

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Genetics & Heredity

A Link between Meiotic Prophase Progression and Crossover Control

Citation Formats

References (45)

Cited By (22)

Similar Records

Related Subjects