If not for a single-nucleotide mutation, each kernel on a juicy corn cob would be trapped inside an inedible casing as tough as a walnut shell. In the July issue of GENETICS, Wang et al. identify an amino acid substitution that was key to the development of the so-called “naked” kernels that characterize modern corn (maize).

The domestication of maize has long fascinated biologists studying evolution. It can provide clues to how organisms change under selection — whether it’s natural selection or selection by humans choosing the most delicious and productive plants to grow in next year’s crop. Maize is a particularly powerful system because many methods and resources are available for its study and because it can be crossed with its wild progenitors for genetic analysis.

Maize was domesticated in Mexico around 9,000 years ago from the grass teosinte. Teosinte seeds are protected by a hard casing that makes them impractical to eat, but ancient plant breeders developed varieties with naked kernels. In these plants, the structures that form the seed case (technically a “fruitcase”) instead become the cob at the center of the ear, leaving the seed exposed for us to eat. Humans effectively turned the teosinte ear inside out, says study leader John Doebley (University of Wisconsin-Madison).

Left: Teosinte ear; right: maize ear; center: ear from the first generation hybrid of a cross between teosinte and maize. Photo credit: John Doebley.

Left: Teosinte ear; right: maize ear; center: ear from the first generation hybrid of a cross between teosinte and maize. Photo credit: John Doebley.

Besides having lost the inconvenient fruitcase, corn kernels today remain firmly attached to the cob, rather than scattering easily as they do in teosinte. The cobs are also much larger, and maize has fewer leaf branches than its ancestor. All these changes evolved relatively quickly, within a few thousand years at most.

Over the last few decades, Doebley and his colleagues have mapped the genes responsible for these differences. They found that genes controlling many of these traits mapped to as few as six genomic locations. Fine-mapping revealed the major gene controlling naked kernel formation is tga1, a transcription factor from a family that regulates floral development.

The teosinte version of tga1 allows formation of an enclosed fruitcase. But maize tga1 disrupts this process, resulting in cases that are smaller and don’t fully enclose the kernel. But what exactly is different about the two versions of the tga1 gene?

To find out, the team compared the tga1 DNA sequence in 16 different maize varieties and 20 varieties of teosinte. They discovered only one variant fixed in all the maize samples but present in none of the teosinte: a single nucleotide change in the coding sequence of tga1 that changes one amino acid in the encoded protein from lysine to asparagine.

When the researchers tested the effect of this substitution on the TGA1 protein, they found that the maize version of the protein had a greater tendency to form dimers. The maize allele also seemed to turn TGA1 into a transcriptional repressor of its target genes, while the teosinte TGA1 did not act as a repressor in reporter assays.

This evidence suggests that repressing TGA target genes alters fruitcase development, contributing to the naked kernel trait.

Consistent with this idea, the researchers found that using RNAi to dampen expression of the maize tga1 gene itself—which should relieve repression of the target genes—enlarged the fruitcase remnant structures in maize. In other words, levels of the maize version of tga1 control the size of the maize structures that would normally form the seed case in teosinte.

These results provide an example of how selection by ancient plant breeders triggered profound structural change in an organism through relatively minor genetic alterations, allowing new traits to evolve rapidly.

“Twenty years ago, it was much harder to study evolution in such detail. It’s exciting that we can now understand complex examples like maize domestication at their most fundamental level,” says Doebley. He also acknowledged the major contributions of lead author Huai Wang for his “series of brilliant experiments that solved a big problem in maize evolution.”

 

CITATION

Evidence that the origin of naked kernels during maize domestication was caused by a single amino acid substitution in tga1 (2015). Huai Wang, Anthony J. Studer, Qiong Zhao, Robert Meeley, and John F. Doebley. Genetics 200(3): 965-974 doi: 10.1534/genetics.115.175752

http://genetics.org/content/200/3/965

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Cristy Gelling is a science writer, lapsed yeast geneticist, and former Communications Director at the GSA.

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