Barbara McClintock and the Discovery of Jumping Genes (Transposons)

Figure 2: Variation in kernel phenotypes is used to study transposon behavior.

Kernels on a maize ear show unstable phenotypes due to the interplay between a transposable element (TE) and a pigment gene.

© 2002 Nature Publishing Group Feschotte, C. et al. Plant transposable elements: where genetics meets genomics. Nature Reviews Genetics 3, 330. All rights reserved.

McClintock worked with what is known as the Ac/Ds system in maize, which she discovered by conducting standard genetic breeding experiments with an unusual phenotype. Through these experiments, McClintock recognized that breakage occurred at specific sites on maize chromosomes. Indeed, the first transposable element she discovered was a site of chromosome breakage, aptly named "dissociation" (Ds). Although McClintock eventually found that some TEs can "jump" autonomously, she initially noted that the movements of Ds are regulated by an autonomous element called "activator" (Ac), which can also promote its own transposition.

Of course, these discoveries were preceded by extensive breeding experimentation. It was known at the time from previous work by Rollins A. Emerson, another American maize geneticist and the "rediscoverer" of Mendel's laws of inheritance, that maize had genes encoding variegated, or multicolored, kernels; these kernels were described as colorless (although they were actually white or yellow), except for spots or streaks of purple or brown (Figure 2). Emerson had proposed that the variegated streaking was due to an "unstable mutation," or a mutation for the colorless phenotype that would sometimes revert back to its wild-type variant and result in an area of color. However, he couldn't explain why or how this occurred. As McClintock discovered, the unstable mutation Emerson puzzled over was actually a four-gene system, as outlined in Table 1.

Table 1: Maize Genes Studied by Barbara McClintock

Adapted from McClean, 1997

In her experiments, McClintock bred females that were homozygous for C and bz and that lacked Ds (denoted CCbzbz--, where the dashes indicate the absence of Ds alleles) with males that were homozygous for C', Bz, and Ds (denoted C'C'BzBzDsDs) to yield heterozygotes with an aleurone layer that had the genotype C'CCBzbzbz--Ds. (Remember, in double fertilization, the sperm provides one set of alleles, and the egg provides two.) Because of the presence of the dominant inhibitor allele C', the offspring kernels were expected to be colorless, no matter what their genetic makeup at the Bz/bz locus. In fact, upon crossbreeding, many of these kernels were indeed colorless. However, McClintock also observed many kernels with colorless backgrounds and varying amounts of dark brown spots or streaks, and she concluded that individual cells in those kernels had lost their C' and Bz alleles because of a chromosomal break at the Ds locus. Without either the C' allele (to prevent color expression) or the Bz (purple) allele, the cells that had experienced a breakage at the Ds locus ended up with some brown coloring.

Within the affected seeds, the amount of colored streaking or spotting depended upon when during seed development the somatic cell mutation at Ds occurred. If this mutation occurred early in development, then, as the one mutant cell continued to divide, more cells in the mature kernel would have the brownish phenotype, and the spot or streak of color on the kernel would be larger. On the other hand, if the mutation occurred later in development, the spotting would be smaller, because the kernel would undergo less cell division prior to maturity.

McClintock also performed additional experiments to demonstrate that the phenotypic effect of Ds depended upon the presence of another element, which she called Ac. McClintock had trouble mapping both the Ac and Ds elements, however, noting that they changed their positions on the chromosome in different maize plants. In fact, further experiments showed that Ds didn't just break chromosomes, but it could actually move from one chromosomal location to another. When Ds inserts itself into the Bz allele, for example, it causes a mutation in the Bz gene (but only when Ac is present), thereby destroying the ability of the Bz gene to produce any pigment at all. Ds can also excise from the Bz allele (again, only in the presence of Ac), causing Bz to revert back to its purple or brown phenotype. Again, the amount of purple or brown depends upon when during development Ds is inserted or excised. If excision happens prior to fertilization, then the affected kernel will be entirely purple or brown, depending upon the Bz/bz genotype.

Years after McClintock discovered the Ac/Ds system, scientists were finally able to study both TEs in much more molecular detail. Today, we know that Ac elements are about 4,500 base pairs long and are similar in structure to other DNA transposons.