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Review
. 2015 May 18;7(6):a016626.
doi: 10.1101/cshperspect.a016626.

Recombination, Pairing, and Synapsis of Homologs during Meiosis

Denise Zickler  1 , Nancy Kleckner  2
Affiliations
Review

Recombination, Pairing, and Synapsis of Homologs during Meiosis

Denise Zickler et al. Cold Spring Harb Perspect Biol. .

Abstract

Recombination is a prominent feature of meiosis in which it plays an important role in increasing genetic diversity during inheritance. Additionally, in most organisms, recombination also plays mechanical roles in chromosomal processes, most notably to mediate pairing of homologous chromosomes during prophase and, ultimately, to ensure regular segregation of homologous chromosomes when they separate at the first meiotic division. Recombinational interactions are also subject to important spatial patterning at both early and late stages. Recombination-mediated processes occur in physical and functional linkage with meiotic axial chromosome structure, with interplay in both directions, before, during, and after formation and dissolution of the synaptonemal complex (SC), a highly conserved meiosis-specific structure that links homolog axes along their lengths. These diverse processes also are integrated with recombination-independent interactions between homologous chromosomes, nonhomology-based chromosome couplings/clusterings, and diverse types of chromosome movement. This review provides an overview of these diverse processes and their interrelationships.

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Figures

Figure 1.
Figure 1.
General features of meiosis. (A) At meiosis I, homologs segregate; at meiosis II, sisters segregate. At metaphase I (left), maternal (red) and paternal (black) chromosomes are held together by a chiasma comprising a reciprocal crossover (CO) plus connections along sister arms, which are released during segregation. (B) Monochiasmate bivalent of Locusta after bromodeoxyuridine (BrdU) incorporation. Differential staining of the sister chromatids confirms that exchange has occurred, for example, between red and purple chromatids in corresponding drawings. (From Jones 1987; reprinted, with permission, from Academic Press © 1987.) (C) Diplotene bivalent of grasshopper with three chiasmata (arrows) and corresponding drawing. (From Jones and Franklin 2006; reprinted, with permission, from Elsevier © 2006.) (D) Top: Meiotic prophase in rye microsporocytes; chromosomes are stained by hematoxylin (pictures by D.Z.). Bottom: corresponding timing of the recombination steps from double-strand breaks (DSBs) to COs; timing of intermediates as in budding yeast (Hunter 2007). SEI, Single-end invasion; dHJ, double Holliday junction; SDSA, synthesis-dependent strand annealing; NCO, noncrossover.
Figure 2.
Figure 2.
Chromosome axes and synaptonemal complex. (A) Electronic microscope (EM) longitudinal section of Blaps cribrosa synaptonemal complex (SC) with distinct central region transverse filaments. (From Schmekel et al. 1993; reprinted, with permission, from Springer © 1993.) (B) Co-oriented sister linear loop arrays cojoined by meshwork of structural proteins (green; see text). (C) SC with recombination nodule; reconstruction from serial section through Drosophila female SC. (From Carpenter 1975; with permission from the National Academy of Sciences © 1975.) (D) Sordaria bivalent at pachytene by immunofluorescence microscopy (top) and by EM (bottom). Top: Crossover (CO) sites marked by the E3 ligase Hei10-mCherry and chromosome axes visualized by cohesin-associated Spo76-GFP (arrows point to Hei10 foci). Bottom: Sordaria SC with late recombination nodule (RN) (both from D.Z.). Scale bars, 2 μm (top); 100 nm (bottom). (E) Sordaria bouquet stage stained by axis component Spo76/Pds5-GFP (left) and by DAPI (right). Note that axis width comprises a significant fraction of the total DAPI width, suggesting that, albeit with limitations of imaging resolution, the axis meshwork may include a significant fraction of the DNA. DAPI staining indicates that chromatin bridges join the two homologs (magnification right) (from D.Z.). (F) COSA-1 foci mark sites of COs in C. elegans. SC marked by ZHP3 staining. (From Yokoo et al. 2012; reprinted, courtesy of a PMC Open Access license.) (G) Recombination complexes are indirectly tethered to underlying chromosome axes (see discussion in Blat et al. 2002). (H) Coordinate variation in axis/SC length and CO frequency can be explained by development of axis-associated pre-double-strand break (DSB) recombination complexes at constant spacing along axes followed by identical probabilities of DSB formation per complex and identical CO-designation/interference (Adapted from Kleckner et al. 2003). ch, Chromatin; le, lateral element; ce, central element.
Figure 3.
Figure 3.
Interhomolog recombination-dependent interactions. (A–C) Sordaria leptotene. (A) In wild type (WT), homologs align at a 300- to 400-nm distance all along their lengths. (B,C) In the absence of Spo11, axes do not align (asynapsis; B) except C in a few meiocytes when one chromosome pair (light and dark green; indicated by white arrows) is seen aligned. Chromosomes are stained by Spo76-GFP in A and B. (A from Storlazzi et al. 2010; reprinted, with permission, from the authors; B and C from Storlazzi et al. 2003; reprinted, with permission, from the authors.) C is a reconstruction from serial sections of a spo11 mutant. (D) Axis association of early recombination nodules and interhomolog bridges from early leptotene (left) through pachytene (right). (From Albini and Jones 1987; reprinted, with permission, from Springer © 1987, except for the image on the left, which is from Stack and Anderson 1986; reprinted, with permission, from JSTOR, Early Journal Content © 1986.) (E) Presumptive recombination intermediate at the interaxis coalignment bridge stage. Double-strand break (DSB) engages a homolog partner chromatid and directs juxtaposition of associated donor and partner chromosome axes to a distance of ∼400 nm (as in panels D and F–H). (F) Replication protein A (RPA) staining in human cells at leptotene/zygotene identifies interaxis bridges and configurations showing approaching and completed synapsis (insets, compare with panel D). (From Oliver-Bonet et al. 2007; reprinted, with permission, from Oxford University Press © 2007.) (G) RecA homologs Rad51 and Dmc1 decorate interaxis bridges in mouse. (From Tarsounas et al. 1999; reprinted, with permission, from Rockefeller University Press under a Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported license.) (H) Mer3 foci face each other on coaligned late leptotene homologs. Scale bar, 2 μm. (From Storlazzi et al. 2010; reprinted, with permission, from the authors.) SC, Synaptonemal complex.
Figure 4.
Figure 4.
Rabl/Bouquet and Interlockings. (A) Left: Cartoon of anaphase of mitotic division; chromosomes segregate with their centromeres facing the spindle pole (and corresponding microtubule organizing center [MTOC], in blue) plus telomeres at arm-size latitude and remain in this “Rabl” disposition. Right: During meiotic prophase, telomeres turn position and now cluster facing the MTOC with centromeres more or less dispersed in the nucleus (Sordaria image from D.Z.). (B) Interlockings. Left: Interlocking of one bivalent (green) in a half-synapsed second bivalent (red) from spread zygotene chromosomes of the silkworm. (From Rasmussen 1986; reprinted, with permission, from Elsevier © 1982.) Right: Interlocking of Sordaria in which the lower bivalent shows one open end (no synaptonemal complex [SC], in gray), thus allowing easy resolution by sliding of the entrapped bivalent (from D.Z.). (C) Interlocking (arrow) during the bouquet stage (left) and corresponding drawing; right entanglements (arrow) start at late leptotene during coalignment. Scale bar, 2 μm. (From Storlazzi et al. 2010; reprinted, with permission, from the authors.) (D) An example of interwoven chromosomes in Sordaria mer3 null mutant with corresponding drawing. (From Storlazzi et al. 2010; with permission, from the authors.) RN, Recombination nodule; nu, nucleus.
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