The meiotic drive mechanism of a selfish chromosome in Zea mays
Lowry, Elizabeth Grace
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Abnormal chromosome 10 (Ab10) is a selfish chromosome in maize. By exploiting the asymmetric nature of female meiosis, Ab10 eschews Mendel’s law of equal segregation and passes into 80% of offspring in a single generation. This meiotic drive is caused by “neocentromere” movement in which knobs, or dense heterochromatic repeats, race along the meiotic spindle into the predestined seed. Knobs are composed of two distinct sequence repeats controlled by separate loci: Knob 180 and TR-1. Knob 180 neocentromeres correlate with meiotic drive and are activated by trans-acting loci located on the “distal tip” of Ab10, a euchromatic region that does not pair with any other region of the maize genome. Ab10 was first discovered in 1942, but for 70 years the molecular mechanism of drive remained elusive. Here we present a comparative meiotic transcriptome analysis that identifies 9 genes unique to the distal tip of Ab10. Probing a BAC library homozygous for Ab10 allowed sequencing and assembly of corresponding genomic regions, resulting in construction of the first genetic map of the Ab10-specific genome. Two of five suppressor of meiotic drive (smd) Ab10 mutants, smd3 and smd8, are characterized as large terminal deletions. One of the nine distal genes is a C-terminal kinesin we call Kin618. Kin618 is a member of a multicopy gene family completely unique to the abnormal haplotype with closest homology to native maize Kinesin 11. Identification of Ab10 mutant smd12 as an epimutation, in which all copies of Kin618 have been silenced by DNA methylation, presents compelling evidence that Kin618 causes the drive phenotype by specifically moving Knob 180 neocentromeres. A second transcriptome analysis across haplotypes that vary in TR-1 neocentromeres did not identify any TR-1 specific factors. Contrary to hypothesis, TR-1 knobs are not targeted by a second highly evolved kinesin. In sum, the research presented here offers an illuminating look at the molecular mechanism of meiotic drive. By co-opting a native meiotic kinesin, the selfish chromosome evolved into a highly effective driver whose story plays out across the entire maize genome.