Meiotic chromosome pairing between homoeologous chromosomes was reported in many nascent allopolyploids. Homoeologous pairing is gradually eliminated and replaced by exclusive homologous pairing in well‐established allopolyploids, an evolutionary process referred to as the diploidization of allopolyploids. A fundamental question of the diploidization of allopolyploids is whether and to what extent the DNA sequence variation among homoeologous chromosomes contribute to the establishment of exclusive homologous chromosome pairing. We developed aneuploid tetraploid maize lines that contain three copies of chromosome 10 derived from inbred lines B73 and H99. We were able to identify the parental origin of each copy of chromosome 10 in the materials using oligonucleotide‐based haplotype‐specific chromosome painting. We demonstrate that the two identical copies of chromosome 10 from H99 pair preferentially over chromosome 10 from B73 in different stages of prophase I and metaphase I during meiosis. Thus, homologous chromosome pairing is favored to partners with the most similar DNA sequences and can be discriminated based on cryptic sequence variation. We propose that innate preference of homologous chromosome pairing exists in nascent allopolyploids and serves as the first layer that would eventually block all homoeologous chromosome pairing in allopolyploids.
Meiotic homolog pairing involves associations between homologous DNA regions scattered along the length of a chromosome. When homologs associate, they tend to do so by a processive zippering process, which apparently results from avidity effects. Using a computational model, we show that this avidity-driven processive zippering reduces the selectivity of pairing. When active random forces are applied to telomeres, this drop in selectivity is eliminated in a force-dependent manner. Further simulations suggest that active telomere forces are engaged in a tug-of-war against zippering, which can be interpreted as a Brownian ratchet with a stall force that depends on the dissociation constant of pairing. When perfectly homologous regions of high affinity compete with homeologous regions of lower affinity, the affinity difference can be amplified through this tug of war effect provided the telomere force acts in a range that is strong enough to oppose zippering of homeologs while still permitting zippering of correct homologs. The degree of unzippering depends on the radius of the nucleus, such that complete unzippering of homeologous regions can only take place if the nucleus is large enough to pull the two chromosomes completely apart. A picture of meiotic pairing thus emerges that is fundamentally mechanical in nature, possibly explaining the purpose of active telomere forces, increased nuclear diameter, and the presence of ‘Maverick’ chromosomes in meiosis.
more » « less- NSF-PAR ID:
- 10302441
- Publisher / Repository:
- IOP Publishing
- Date Published:
- Journal Name:
- Physical Biology
- Volume:
- 16
- Issue:
- 4
- ISSN:
- 1478-3967
- Page Range / eLocation ID:
- Article No. 046005
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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