Home LiteratureArticle Details
PMID: 19629172 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis.

PLoS genetics ·Vol. 5 ·No. 7 ·2009-07-00 ·Pages e1000557

Joshi N, Barot A, Jamison C, Börner GV

Abstract

Segregation of homologous chromosomes during meiosis I depends on appropriately positioned crossovers/chiasmata. Crossover assurance ensures at least one crossover per homolog pair, while interference reduces double crossovers. Here, we have investigated the interplay between chromosome axis morphogenesis and non-random crossover placement. We demonstrate that chromosome axes are structurally modified at future crossover sites as indicated by correspondence between crossover designation marker Zip3 and domains enriched for axis ensemble Hop1/Red1. This association is first detected at the zygotene stage, persists until double Holliday junction resolution, and is controlled by the conserved AAA+ ATPase Pch2. Pch2 further mediates crossover interference, although it is dispensable for crossover formation at normal levels. Thus, interference appears to be superimposed on underlying mechanisms of crossover formation. When recombination-initiating DSBs are reduced, Pch2 is also required for viable spore formation, consistent with further functions in chiasma formation. pch2Delta mutant defects in crossover interference and spore viability at reduced DSB levels are oppositely modulated by temperature, suggesting contributions of two separable pathways to crossover control. Roles of Pch2 in controlling both chromosome axis morphogenesis and crossover placement suggest linkage between these processes. Pch2 is proposed to reorganize chromosome axes into a tiling array of long-range crossover control modules, resulting in chiasma formation at minimum levels and with maximum spacing.

MeSH Terms
Cell Cycle Proteins/metabolism Chromosomes, Fungal/metabolism Crossing Over, Genetic DNA-Binding Proteins/metabolism Gene Conversion Meiosis Nuclear Proteins/metabolism Saccharomyces cerevisiae/cytology,genetics,metabolism Saccharomyces cerevisiae Proteins/metabolism Ubiquitin-Protein Ligases/metabolism
Chemicals
Cell Cycle Proteins DMC1 protein, S cerevisiae DNA-Binding Proteins HOP1 protein, S cerevisiae Nuclear Proteins Pch2 protein, S cerevisiae RED1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Ubiquitin-Protein Ligases Zip3 protein, S cerevisiae
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Joshi Neeraj
Department of Biological, Geological, and Environmental Sciences, Center for Gene Regulation in Health and Disease, Cleveland State University, Cleveland, Ohio, United States of America.
Barot Aekam
Jamison Christine
Börner G Valentin
Conflict of Interest

The authors have declared that no competing interests exist.

References (57)
57 references, click to expand
  1. Meiotic chromosomes: integrating structure and function.
    Annu Rev Genet. 1999;33:603-754 PMID: 10690419
  2. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast.
    Genetics. 2003 May;164(1):81-94 PMID: 12750322
  3. ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes.
    PLoS Genet. 2008 May 23;4(5):e1000076 PMID: 18497861
  4. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion.
    Genes Dev. 2008 Oct 15;22(20):2886-901 PMID: 18923085
  5. Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit.
    Genes Dev. 2008 Jan 15;22(2):194-211 PMID: 18198337
  6. Characterization of human crossover interference.
    Am J Hum Genet. 2000 Jun;66(6):1911-26 PMID: 10801387
  7. ZMM proteins during meiosis: crossover artists at work.
    Chromosome Res. 2007;15(5):591-605 PMID: 17674148
  8. Crossover homeostasis in yeast meiosis.
    Cell. 2006 Jul 28;126(2):285-95 PMID: 16873061
  9. Initiation of meiotic chromosome synapsis at centromeres in budding yeast.
    Genes Dev. 2008 Nov 15;22(22):3217-26 PMID: 19056898
  10. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae.
    PLoS Biol. 2007 Dec;5(12):e324 PMID: 18076285
  11. Global analysis of the meiotic crossover landscape.
    Dev Cell. 2008 Sep;15(3):401-415 PMID: 18691940
  12. The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination.
    Cell. 2001 Jul 13;106(1):59-70 PMID: 11461702
  13. Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis.
    Nat Genet. 2008 Mar;40(3):299-309 PMID: 18297071
  14. Pch2 links chromatin silencing to meiotic checkpoint control.
    Cell. 1999 Apr 30;97(3):313-24 PMID: 10319812
  15. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes.
    Cell. 2004 Mar 19;116(6):795-802 PMID: 15035982
  16. Physical association between nonhomologous chromosomes precedes distributive disjunction in yeast.
    Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):331-4 PMID: 8278388
  17. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway.
    Cell. 1997 Sep 19;90(6):1123-35 PMID: 9323140
  18. Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis.
    PLoS Genet. 2007 Aug;3(8):e130 PMID: 17696610
  19. A mechanical basis for chromosome function.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12592-7 PMID: 15299144
  20. Sex-related differences in crossing over in Caenorhabditis elegans.
    Genetics. 1990 Oct;126(2):355-63 PMID: 2245915
  21. Differential timing and control of noncrossover and crossover recombination during meiosis.
    Cell. 2001 Jul 13;106(1):47-57 PMID: 11461701
  22. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation.
    Cell. 2002 Dec 13;111(6):791-802 PMID: 12526806
  23. Meiosis I is established through division-specific translational control of a cyclin.
    Cell. 2008 Apr 18;133(2):280-91 PMID: 18423199
  24. Synthesis-dependent strand annealing in meiosis.
    PLoS Biol. 2007 Nov 6;5(11):e299 PMID: 17988174
  25. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis.
    Cell. 1993 Feb 12;72(3):365-78 PMID: 7916652
  26. Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast.
    Curr Biol. 2006 Dec 19;16(24):2473-9 PMID: 17174924
  27. Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis.
    Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3327-32 PMID: 18305165
  28. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
    Cell. 1999 Jul 9;98(1):91-103 PMID: 10412984
  29. Mapping of meiotic single-stranded DNA reveals double-stranded-break hotspots near centromeres and telomeres.
    Curr Biol. 2007 Dec 4;17(23):2003-12 PMID: 18060788
  30. Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1.
    Mol Biol Cell. 2005 Dec;16(12):5804-18 PMID: 16221890
  31. Does crossover interference count in Saccharomyces cerevisiae?
    Genetics. 2004 Sep;168(1):35-48 PMID: 15454525
  32. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes.
    Genes Dev. 1998 Jul 15;12(14):2208-21 PMID: 9679065
  33. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family.
    Cell. 1997 Feb 7;88(3):375-84 PMID: 9039264
  34. The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control in meiosis.
    EMBO J. 1999 Oct 15;18(20):5714-23 PMID: 10523314
  35. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis.
    Cell. 2004 Apr 2;117(1):29-45 PMID: 15066280
  36. Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex.
    Chromosoma. 2006 Jun;115(3):175-94 PMID: 16555016
  37. ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans.
    PLoS Genet. 2008 Oct;4(10):e1000235 PMID: 18949042
  38. Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation.
    Genetics. 2009 Jan;181(1):39-51 PMID: 18957704
  39. Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII.
    Genetics. 2004 Sep;168(1):49-63 PMID: 15454526
  40. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis.
    Cell. 2004 Apr 2;117(1):9-15 PMID: 15066278
  41. Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks.
    Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4519-24 PMID: 15070750
  42. Meiotic segregation, synapsis, and recombination checkpoint functions require physical interaction between the chromosomal proteins Red1p and Hop1p.
    Mol Cell Biol. 2000 Sep;20(18):6646-58 PMID: 10958662
  43. Coupling meiotic chromosome axis integrity to recombination.
    Genes Dev. 2008 Mar 15;22(6):796-809 PMID: 18347098
  44. The yeast Red1 protein localizes to the cores of meiotic chromosomes.
    J Cell Biol. 1997 Mar 10;136(5):957-67 PMID: 9060462
  45. Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference.
    Genes Dev. 1997 Jul 15;11(14):1786-800 PMID: 9242487
  46. Covariation of synaptonemal complex length and mammalian meiotic exchange rates.
    Science. 2002 Jun 21;296(5576):2222-5 PMID: 12052900
  47. On the "NPD ratio" as a test for crossover interference.
    Genetics. 2008 May;179(1):701-4 PMID: 18493082
  48. Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length.
    Trends Genet. 2003 Nov;19(11):623-8 PMID: 14585614
  49. Adaptive advantage for chiasma interference: a novel suggestion.
    Heredity (Edinb). 1980 Aug;45(1):127-31 PMID: 6777340
  50. The origin of human aneuploidy: where we have been, where we are going.
    Hum Mol Genet. 2007 Oct 15;16 Spec No. 2:R203-8 PMID: 17911163
  51. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination.
    Cell. 2008 Mar 7;132(5):758-70 PMID: 18329363
  52. Biochemical Mutants in the Smut Fungus Ustilago Maydis.
    Genetics. 1949 Sep;34(5):607-26 PMID: 17247336
  53. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins.
    Cell. 2000 Jul 21;102(2):245-55 PMID: 10943844
  54. A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans.
    Science. 2005 Dec 9;310(5754):1683-6 PMID: 16339446
  55. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules.
    Cell. 2007 Jul 27;130(2):259-72 PMID: 17662941
  56. Crossover interference is abolished in the absence of a synaptonemal complex protein.
    Cell. 1994 Oct 21;79(2):283-92 PMID: 7954796
  57. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression.
    Cell. 1992 May 1;69(3):439-56 PMID: 1581960
Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7404
Published
2009-07-00
Epub
2009-00-24
Pages
e1000557
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC2708914
Subset
IM
Grants
NIGMS NIH HHS · R15 GM080715 · United States
NIGMS NIH HHS · R15GM080715 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]