The challenge of evolving stable polyploidy: could an increase in "crossover interference distance" play a central role?

Abstract

Whole genome duplication is a prominent feature of many highly evolved organisms, especially plants. When duplications occur within species, they yield genomes comprising multiple identical or very similar copies of each chromosome ("autopolyploids"). Such genomes face special challenges during meiosis, the specialized cellular program that underlies gamete formation for sexual reproduction. Comparisons between newly formed (neo)-autotetraploids and fully evolved autotetraploids suggest that these challenges are solved by specific restrictions on the positions of crossover recombination events and, thus, the positions of chiasmata, which govern the segregation of homologs at the first meiotic division. We propose that a critical feature in the evolution of these more effective chiasma patterns is an increase in the effective distance of meiotic crossover interference, which plays a central role in crossover positioning. We discuss the findings in several organisms, including the recent identification of relevant genes in Arabidopsis arenosa, that support this hypothesis.

Keywords: Chiasmata; Crossover interference; Homologous chromosomes; Meiosis; Polyploidy; Recombination.

Fig. 1

Metaphase I (MI) configurations in diploids and newly arisen autotetraploids of Arabidopsis. Chromosomes are being pulled towards opposite spindle poles (above and below, respectively) via attachments of microtubules to the respective centromere/kinetochore regions. a (Left) Arabidopsis thaliana diploid showing five bivalents (from López et al. 2012). The chromosome number of each bivalent is indicated. 45S and 5S rDNA loci are indicated. a (Right) Arabidopsis arenosa diploid showing eight bivalents (C.F. and C. Morgan, unpublished). b Cartoons showing chromosome associations that give rise to three of the metaphase I configurations seen in a (left). The arrows indicate the orientation of centromeres (filled circles) towards opposite spindle poles. II denotes the bivalent; superscript denotes the chromosome number. c (Left) An experimentally created autotetraploid of A. thaliana showing a mixture of bivalents (II) and quadrivalents (IV) (from Santos et al. 2003). c (Right) An experimentally created autotetraploid of A. arenosa showing some identifiable bivalents, many complex configurations in which multiple chromosomes are entangled (E) and one apparent univalent (U) (Chris Morgan and C. F., unpublished)

Fig. 2

Chiasma configurations for an autotetraploid that are either effective for ensuring two-by-two segregation (a) or not (b). Effective segregation requires that each chromosome be linked to either one or two other chromosomes. Only three configurations satisfy this requirement. By contrast, if any chromosome (or more than one chromosome) is unlinked to a partner or is linked to all three other homologs, segregation will be aberrant, as illustrated for representative single chromosome cases

Fig. 3

Two metaphase I complements for a fully evolved autotetraploid of Arabidopsis arenosa (C. F. and C. Morgan, unpublished). a A majority of bivalents plus a minority chain and ring quadrivalents (10 bivalents corresponding to 5 pairs plus 3 quadrivalents). Accompanying color-inverted images show chromosome constitution and multivalent configurations. b Full complement of 16 bivalents corresponding to 8 pairs

Fig. 4

Prophase chromosomal events in diploid meiosis. a “Fill-in-the-holes” model for CO position selection (see also Wang et al. 2015). The array of early total DSB-mediated recombinational interactions (e.g., bridges; b–d (below)) is acted upon by a CO designation process. Each CO designation (red star) sets up an inhibitory zone of “CO interference” (blue arrows) via a signal that spreads outwards in both directions, dissipating with distance. This signal prevents bridge interactions in the affected region from undergoing CO designation (indicated by bridges changed to yellow). Subsequent CO designations occur in regions away from previously established interference zones, ultimately filling in the holes between previous CO sites. CO designation is very efficient, thus ensuring that all homolog pairs acquire at least one (first, obligatory) CO. b–f Homolog coalignment (“pairing”) is mediated by inter-axis bridges that comprise DSB-mediated recombinational interactions and followed by SC formation (“synapsis”). b, e Human male meiotic prophase chromosomes visualized by immunofluorescence illumination. c, d, f Allium cepa axes and associated “zygotene” recombination nodules (ZNs) or bridges (corresponding approximately to many/all DSB-mediated interactions) visualized by electron microscopy of PTA-stained spread preparations (from Albini and Jones 1987). b Leptotene/zygotene nucleus illustrates bridges containing single-strand binding protein RPA (white arrows), a direct player in Rad51/Dmc1-mediated strand exchange for recombination, with accompanying onset of synapsis. Green indicates SMC3 cohesin axis, blue centromeres (blue), and red RPA protein (from Oliver-Bonet et al. 2007). c, d Bridge configurations and incipient synapsis corresponding to the stage in b. e Pachytene synaptic configurations with SYCP3 axes of the SC (red), centromeres (blue), and Mlh1 foci marking sites of COs (green) (from Gruhn et al. 2013). f Two bivalents showing, respectively, extensive synapsis in progress and coalignment. In c, d, f, black arrows indicate examples of “nodules” or bridges of five types: (a) associated with SCs, (b) with association sites, (c) midway between axial cores in close alignment, (d) paired structures at matching sites on axial cores, and (e) apparently bridging the space between two converging axial cores. Blue arrows and text indicate positions of forming/formed SC

Fig. 5

Prophase relationships among homologous chromosomes in autotetraploids. a Coalignment of four homologous chromosome axes at mid-prophase in tetraploid onion (Allium porrum) (from Stack and Roelofs 1996). The arrows indicate early recombination nodules which mark the sites of early recombination interactions. b Immunostaining of the spread Arabidopsis arenosa tetraploid for axis component ASY1 and SC component ZYP1, showing both coalignment of all four homolog axes (left arrow) and pairwise synapsis (right arrow) (c) (C. Morgan and C.F., unpublished). c–g Quadrivalents in tetraploid Bombyx spermatocytes (from Rasmussen 1987). c–e Three examples of configurations exhibiting partial synapsis plus pre-synaptic associations (e.g., arrow in d). f, g Two configurations exhibiting nearly complete synapsis. The four chromosomes are drawn with different colors. Note that chromosomes twist during SC formation. Quadrivalent frequencies diminish as the extent of synapsis increases such that, by the end of pachytene, the frequency of quadrivalents closely matches the frequency of chiasmata seen at metaphase I. By implication, the associations seen at the end of pachytene are stabilized by the occurrence of crossing over (or, at least, “crossover designation”), with one CO on each of the four arms. Once the SC disappears, these pachytene quadrivalents lead to ring quadrivalents at metaphase I

Fig. 6

Predicted chiasma/CO patterns for an evolved autotetraploid. a CO sites are proposed to be selected with efficient CO designation and accompanying CO interference which extends over an effective distance comparable to the length(s) of the chromosome(s) (text; representations as in Fig. 4a). If the interference distance is longer than the chromosome length, the predicted outcome is a full complement of bivalents, each with a single chiasma (not shown). b, c Predicted outcomes if the interference distance is somewhat less than the total chromosome length comprise a mixture of bivalents and quadrivalents, where the quadrivalents are chains or rings in which all chromosomes are linked by (sub-)terminal chiasmata. b Bivalents of different types can arise if the first chiasma is interstitial (i) or sub-terminal (ii) and according to the starting array of early recombinational interactions (not shown). c Quadrivalents can only arise if the first chiasma is sub-terminal and will comprise rings (i) or chains (ii) according to the particular starting array of early recombinational interactions. In the example shown, the right-most interaction between top and bottom chromosomes is present in i but absent in ii, thereby limiting the number of CO designations to 3. Importantly, the occurrence of univalents, e.g., in trivalent-plus-univalent configurations, is precluded with efficient CO designation which ensures that every chromosome will experience at least one such event (text; not shown)