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In vascular plants, heterosporous lineages typically have fewer chromosomes than homosporous lineages. The underlying mechanism causing this disparity has been debated for over half a century. Although reproductive mode has been identified as critical to these patterns, the symmetry of meiosis during sporogenesis has been overlooked as a potential cause of the difference in chromosome numbers. In most heterosporous plants, meiosis during megasporogenesis is asymmetric, meaning one of the four meiotic products survives to become the egg. Comparatively, meiosis is symmetric in homosporous megasporogenesis and all meiotic products survive. The symmetry of meiosis is important because asymmetric meiosis enables meiotic drive and associated genomic changes, while symmetric meiosis cannot lead to meiotic drive. Meiotic drive is a deviation from Mendelian inheritance where genetic elements are preferentially inherited by the surviving egg cell, and can profoundly impact chromosome (and genome) size, structure, and number. Here we review how meiotic drive impacts chromosome number evolution in heterosporous plants, how the lack of meiotic drive in homosporous plants impacts their genomes, and explore future approaches to understand the role of meiotic drive on chromosome number across land plants.
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Conflicting Kinesin-14s in a single chromosomal drive haplotype
Abstract In maize, there are 2 meiotic drive systems that target large heterochromatic knobs composed of tandem repeats known as knob180 and TR-1. The first meiotic drive haplotype, abnormal chromosome 10 (Ab10) confers strong meiotic drive (∼75% transmission as a heterozygote) and encodes 2 kinesins: KINDR, which associates with knob180 repeats, and TRKIN, which associates with TR-1 repeats. Prior data show that meiotic drive is conferred primarily by the KINDR/knob180 system while the TRKIN/TR-1 system seems to have little or no role, making it unclear why Trkin has been maintained in Ab10 haplotypes. The second meiotic drive haplotype, K10L2, confers a low level of meiotic drive (∼51–52%) and only encodes the TRKIN/TR-1 system. Here, we used long-read sequencing to assemble the K10L2 haplotype and showed that it has strong homology to an internal portion of the Ab10 haplotype. We also carried out CRISPR mutagenesis to test the role of Trkin on Ab10 and K10L2. The data indicate that the Trkin gene on Ab10 does not improve drive or fitness but instead has a weak deleterious effect when paired with a normal chromosome 10. The deleterious effect is more severe when Ab10 is paired with K10L2: in this context, functional Trkin on either chromosome nearly abolishes Ab10 drive. Mathematical modeling based on the empirical data suggests that Trkin is unlikely to persist on Ab10. We conclude that Trkin either confers an advantage to Ab10 in untested circumstances or that it is in the process of being purged from the Ab10 population.
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- PAR ID:
- 10661353
- Editor(s):
- Barbash, D
- Publisher / Repository:
- Genetics
- Date Published:
- Journal Name:
- GENETICS
- Volume:
- 230
- Issue:
- 3
- ISSN:
- 1943-2631
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Meiotic drive elements are regions of the genome that are transmitted to progeny at frequencies that exceed Mendelian expectations, often to the detriment of the organism. In maize there are three prevalent chromosomal drive elements known as Abnormal chromosome 10 (Ab10), K10L2, and the B chromosome. There has been much speculation about how these drivers might interact with each other and the environment in traditional maize landraces and their teosinte ancestors. Here we used genotype-by-sequencing data to score more than 10,000 maize and teosinte lines for the presence or absence of each driver. Fewer than ~0.5% of modern inbred lines carry chromosomal drivers. In contrast, among individuals from 5331 open-pollinated landraces, 6.32% carried Ab10, 5.16% carried K10L2, and 12.28% carried at least one B chromosome. These frequencies are consistent with those reported in previous studies. Using a GWAS approach we identified unlinked loci that associate with the presence or absence of the selfish genetic elements. Many significant SNPs are positively associated with the drivers, suggesting that there may have been selection for alleles that ameliorate their negative fitness consequences. We then assessed the contributions of population structure, associated loci, and the environment on the distribution of each chromosomal driver. There was no significant relationship between any chromosomal driver and altitude, contrary to conclusions based on smaller studies. Our data suggest that the distribution of the major chromosomal drivers is primarily influenced by neutral processes and the deleterious fitness consequences of the drivers themselves. While each driver has a unique relationship to genetic background and the environment, they are largely unconstrained by either.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/genetics/iyaf091
