Borrowed genes help maize adapt to high-altitude, cold temperatures

An important gene in maize called HPC1, which regulates certain chemical processes that affect flowering time, originated in the Mexican bighorn sheep (teosinte mexicana), the precursor to modern Mexican highland wild maize. These findings provide insights into plant evolution and trait selection, and may have implications for adaptation to low temperature in maize and other crops.

North Carolina State University researchers have discovered that an important gene in corn called HPC1, which regulates certain chemical processes that affect flowering time, originated in the teosinte mexicana, a modern Predecessor of wild corn in the Mexican highlands. These findings provide insights into plant evolution and trait selection, and may have implications for adaptation to low temperature in maize and other crops.

"We're interested in understanding how natural changes in lipids are involved in plant growth and development, and how these compounds help plants adapt to their immediate environment," said Rubén Rellán-álvarez, a professor of structural and molecular biochemistry at North Carolina State University. "Specifically, we wanted to learn more about changes in phospholipids (composed of phosphorus and fatty acids) and their role in adaptation to cold, low phosphorus, and important processes such as flowering time that regulate plant fitness and yield."

Maize grown at high altitudes, such as the Mexican highlands, requires special environments to grow successfully. Compared to maize grown at low altitudes and high temperatures, lower temperatures in these mountainous areas place maize at a slightly disadvantageous position.

Rellán-álvarez said: "At high altitude and low temperature, corn takes longer to grow, and corn needs to accumulate heat or growth units due to lower accumulation of heat units." "At 10,000 feet (2600 meters) above sea level, it takes three times as long to cultivate a corn plant as at lower altitudes. In order to adapt to these particular conditions, small farmers must grow early in the season and penetrate deep into the soil; growth is very slow but steady in the first few months before the rainy season comes. For thousands of years, farmers have chosen corn varieties that can thrive under these special conditions, grow at low temperatures and bloom as early as possible before the colder months of winter."

That's where the HPC1 gene comes into play, the researchers say. In corn varieties grown at lower elevations, including most grown in the United States, the gene breaks down phospholipids, which in other varieties have been shown to bind to proteins important for accelerating flowering time.

"Phospholipids are also important components of cell membranes. All lipids have different shapes, and balancing these shapes keeps the membrane intact and helps plants survive under stress," Alison Barnes, a postdoctoral researcher at the Rellán-álvarez laboratory and one of the first authors of the paper, said.

Although in the mountains, the gene did not succeed, it was beneficial for highland maize.

"A defective version of the gene was selected in highland maize, which resulted in high levels of phospholipids," said Rellán-álvarez. "We developed a CRISPR-Cas9 mutant and confirmed the gene's metabolic function. We also demonstrate similar phospholipid-protein interactions that have been described in other species to regulate flowering time."

Barnes added: "Phospholipids that are not broken down on high altitude may be more conducive to keeping cell membranes together and allowing plants to survive in adverse environments."

In this paper, the researchers show the results of a large number of experiments performed in lowlands and highlands across Mexico, where highland versions of genes exist. They found that corn carrying highland genes flowered one day earlier than corn without highland genes. At the same time, corn planted in the lowland with highland genes blooms one day later than corn without such genes.

"This helps plants adapt better to the local environment," says Fausto Rodríguez-Zapata, PhD student at the laboratory of Rellán-álvarez, who is also one of the first authors of the paper. "If flowering is unsuccessful, there will be no seeds, so it is not surprising that things related to flowering time are also related to local adaptation."

This study also investigated the evolutionary process of maize during thousands of years of farmer selection in the Western Hemisphere. Thousands of years ago, in southwestern Mexico, Indians domesticated corn from a wild plant called teosinte parviglumis and very cleverly brought it to various parts of the Americas, from the desert and Perú of Arizona, to the humid forests of Yucatán and Colombia, including the Mexican highlands, where corn was crossed with another wild rat plant, teosinte mexicana.

Rellán-álvarez said: "Our results show that a mixture of corn and leafy red Mexican corn helps corn adapt to upland conditions, and this mixture is associated with modern corn."

In this study, the researchers showed that gene fragments from Mexican ruminants (i.e., highland versions of HPC1) were retained in modern maize.

"This retention, scientists call gene introgression, is similar to modern humans retaining some Neanderthal genes in their genetic code. These works were retained because they were selected over time and brought some advantages." Rodríguez-Zapata says.

The study also showed upland variation of HPC1 in maize grown in Canada, northern USA, and northern Europe, which makes sense because the climate is colder in these areas.

Researchers at North Carolina State University are now studying the role of this and other genes involved in phosphorus metabolism to understand more sustainable ways to grow corn and may introduce more ruminants into modern corn.

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