Two Types of Meiotic Crossovers Coexist in Maize[W]

We apply modeling approaches to investigate the distribution of late recombination nodules in maize (Zea mays). Such nodules indicate crossover positions along the synaptonemal complex. High-quality nodule data were analyzed using two different interference models: the “statistical” gamma model and the “mechanical” beam film model. For each chromosome, we exclude at a 98% significance level the hypothesis that a single pathway underlies the formation of all crossovers, pointing to the coexistence of two types of crossing-over in maize, as was previously demonstrated in other organisms. We estimate the proportion of crossovers coming from the noninterfering pathway to range from 6 to 23% depending on the chromosome, with a cell average of ∼15%. The mean number of noninterfering crossovers per chromosome is significantly correlated with the length of the synaptonemal complex. We also quantify the intensity of interference. Finally, we develop inference tools that allow one to tackle, without much loss of power, complex crossover interference models such as the beam film. The lack of a likelihood function in such models had prevented their use for parameter estimation. This advance will allow more realistic mechanisms of crossover formation to be modeled in the future.

[1]  J. Higgins,et al.  AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. , 2008, The Plant journal : for cell and molecular biology.

[2]  G. Copenhaver,et al.  Crossover interference in Arabidopsis. , 2002, Genetics.

[3]  S. Keeney,et al.  ATM Promotes the Obligate XY Crossover and both Crossover Control and Chromosome Axis Integrity on Autosomes , 2008, PLoS genetics.

[4]  L. Anderson,et al.  Two-dimensional spreads of synaptonemal complexes from solanaceous plants , 1986, Chromosoma.

[5]  L. Huang,et al.  A demonstration of a 1:1 correspondence between chiasma frequency and recombination using a Lolium perenne/Festuca pratensis substitution. , 2002, Genetics.

[6]  C. Grey,et al.  Crossover and noncrossover pathways in mouse meiosis. , 2005, Molecular cell.

[7]  J. Weber,et al.  Characterization of human crossover interference. , 2000, American journal of human genetics.

[8]  S. Keeney,et al.  Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein Family , 1997, Cell.

[9]  K.,et al.  A Polymerization Model of Chiasma Interference and Corresponding Computer Simulation , 2022 .

[10]  T P Speed,et al.  Modeling interference in genetic recombination. , 1995, Genetics.

[11]  M. Novatchkova,et al.  SHOC1, an XPF Endonuclease-Related Protein, Is Essential for the Formation of Class I Meiotic Crossovers , 2008, Current Biology.

[12]  J. Higgins,et al.  Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. , 2008, The Plant journal : for cell and molecular biology.

[13]  J. Wienberg,et al.  Male mouse recombination maps for each autosome identified by chromosome painting. , 2002, American journal of human genetics.

[14]  R. Hawley,et al.  Chromosome Choreography: The Meiotic Ballet , 2003, Science.

[15]  Karl W Broman,et al.  Crossover interference in the mouse. , 2002, Genetics.

[16]  F. C. H. Franklin,et al.  Meiotic Crossing-over: Obligation and Interference , 2006, Cell.

[17]  M. Hultén,et al.  Chiasma frequency, distribution and interference maps of mouse autosomes , 1995, Chromosoma.

[18]  E. Foss,et al.  Chiasma interference as a function of genetic distance. , 1993, Genetics.

[19]  C. Heyting,et al.  The Mismatch Repair Protein MLH1 Marks a Subset of Strongly Interfering Crossovers in Tomato[W][OA] , 2007, The Plant Cell Online.

[20]  S. Stack,et al.  Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). , 1995, Genetics.

[21]  K. V. SRINATH,et al.  Mechanism of Crossing-over , 1946, Nature.

[22]  L. Anderson,et al.  High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. , 2003, Genetics.

[23]  S. Keeney,et al.  Crossover Homeostasis in Yeast Meiosis , 2006, Cell.

[24]  T. Hassold,et al.  Variation in human meiotic recombination. , 2004, Annual review of genomics and human genetics.

[25]  T. Speed,et al.  On genetic map functions. , 1996, Genetics.

[26]  A. Sturtevant,et al.  The behavior of the chromosomes as studied through linkage , 1915, Zeitschrift für induktive Abstammungs- und Vererbungslehre.

[27]  N. Kleckner,et al.  Meiotic chromosomes: integrating structure and function. , 1999, Annual review of genetics.

[28]  N. M. Hollingsworth,et al.  The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. , 2004, Genes & development.

[29]  O. Martin,et al.  chromosomes: modeling effects of interference and obligate chiasma , 2007 .

[30]  J. K. Holloway,et al.  MUS81 Generates a Subset of MLH1-MLH3–Independent Crossovers in Mammalian Meiosis , 2008, PLoS genetics.

[31]  L. Anderson,et al.  The relationship between genome size and synaptonemal complex length in higher plants. , 1985, Experimental cell research.

[32]  J. Drouaud,et al.  The road to crossovers: plants have their say. , 2007, Trends in genetics : TIG.

[33]  Hadi Quesneville,et al.  Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination "hot spots". , 2005, Genome research.

[34]  C. Heyting,et al.  Meiotic interference among MLH1 foci requires neither an intact axial element structure nor full synapsis , 2007, Journal of Cell Science.

[35]  G. Copenhaver,et al.  Does Crossover Interference Count in Saccharomyces cerevisiae? , 2004, Genetics.

[36]  F W Stahl,et al.  Is There Variation in Crossover Interference Levels Among Chromosomes From Human Males? , 2009, Genetics.

[37]  M. Doutriaux,et al.  Two Meiotic Crossover Classes Cohabit in Arabidopsis One Is Dependent on MER3,whereas the Other One Is Not , 2005, Current Biology.

[38]  Luke E. Berchowitz,et al.  The Role of AtMUS81 in Interference-Insensitive Crossovers in A. thaliana , 2007, PLoS genetics.

[39]  C. Heyting,et al.  Two levels of interference in mouse meiotic recombination. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Lalitha Viswanath,et al.  InterferenceAnalyzer: Tools for the analysis and simulation of multi-locus genetic data , 2005, BMC Bioinformatics.

[41]  N. Kleckner,et al.  Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. , 2003, Trends in genetics : TIG.

[42]  K. McKim,et al.  Temporal Analysis of Meiotic DNA Double-Strand Break Formation and Repair in Drosophila Females , 2006, PLoS genetics.

[43]  C. Bidau,et al.  General pattern of meiotic recombination in male dogs estimated by MLH1 and RAD51 immunolocalization , 2008, Chromosome Research.

[44]  L. K. Anderson and S. M. Stack,et al.  Meiotic Recombination in Plants , 2002 .

[45]  T. Karamysheva,et al.  Immunofluorescent analysis of meiotic recombination in the domestic cat , 2007, Cell and Tissue Biology.

[46]  M. Doutriaux,et al.  Zip4/Spo22 Is Required for Class I CO Formation but Not for Synapsis Completion in Arabidopsis thaliana , 2007, PLoS genetics.

[47]  Anna Malkova,et al.  Gene Conversion and Crossing Over Along the 405-kb Left Arm of Saccharomyces cerevisiae Chromosome VII , 2004, Genetics.

[48]  Jones Gh The control of chiasma distribution. , 1984 .

[49]  J. Higgins,et al.  The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. , 2004, Genes & development.

[50]  J. Searle,et al.  Recombination Map of the Common Shrew, Sorex araneus (Eulipotyphla, Mammalia) , 2008, Genetics.

[51]  G. Copenhaver,et al.  Crossover Interference on Nucleolus Organizing Region-Bearing Chromosomes in Arabidopsis , 2005, Genetics.

[52]  D. Zickler,et al.  Early Decision Meiotic Crossover Interference prior to Stable Strand Exchange and Synapsis , 2004, Cell.

[53]  N. M. Hollingsworth,et al.  The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. , 2003, Genetics.

[54]  F. Stahl,et al.  Crossover interference in humans. , 2003, American journal of human genetics.

[55]  M. Spence,et al.  Analysis of human genetic linkage , 1986 .

[56]  G. Davis,et al.  A maize map standard with sequenced core markers, grass genome reference points and 932 expressed sequence tagged sites (ESTs) in a 1736-locus map. , 1999, Genetics.

[57]  Nancy Kleckner,et al.  A mechanical basis for chromosome function. , 2004, Proceedings of the National Academy of Sciences of the United States of America.