Marcus Rhoades on Preferential Segregation in Maize.

On Christmas Day 1941,GENETICS received a gift: amanuscript from Marcus Rhoades describing an unexpected violation ofMendelian inheritance inmaize. This was the first report of preferential segregation; a phenomenon later known as meiotic drive. Rhoades was studying a variant form of chromosome 10 with a conspicuous abnormality; it carried extensive heterochromatin at the tip of the long arm. This variant had been found by Albert Longley in indigenous maize varieties from the southwestern United States and provided to Rhoades for the pedestrian task of determining the recombination frequency between the anthocyanin pigment gene, R, and the end of the chromosome. The abnormal chromosome 10 originally carried the recessive, r, allele (colorless kernels) and was crossed to other lines carrying the dominant R (red kernels). Much to the surprise of Rhoades, when these heterozygotes were testcrossed with the recessive, there was a strong skew from a 1:1 ratio. Rather than the roughly even mix of colorless and red kernels that he expected, around two-thirds were colorless. This excess of r alleles was caused by linkage to the variant chromosome; in the few progeny that transferred the dominant R allele to the abnormal chromosome 10, subsequent testcrosses demonstrated that it was now the dominant allele that was preferentially inherited. What was the basis of this behavior? Rhoades systematically ruled out hypotheses until the only option leftwas biased segregation during meiosis. In plants, female meiosis produces fourmegaspores, but threeof thesedegenerateandonly the megaspore in the basal position develops into the female gametophyte that harbors the egg. Rhoades postulated that recombination between the centromere and the terminal heterochromatin produced a heteromorphic dyad, such that at anaphase II the abnormal chromosome had a greater tendency to enter the basal megaspore. Amusingly, Rhoades tested whether this tendency was due to the extra weight of the abnormal chromosome by turning some plants upside down during meiosis; there was no effect. Rhoades continued to study this phenomenon for his entire career. Subsequent work revealed that the extra heterochromatin on chromosome 10 induced neocentromere formation at heterochromatic knob sites across the genome, including a large one on the abnormal chromosome. These neocentromeres proceed to the poles in meiosis much faster than the canonical centromeres, causing preferential segregation of linked genes and providing a striking visual confirmation of Rhoades’ hypothesis. But what about the other mystery posed by this article? How could a manuscript be received on Christmas Day at a time when submissions were delivered by the postal service? Marcus Rhoades was the Editor-in-Chief of GENETICS at the time, and he submitted it to himself!