Study shows how crops have evolved by exchanging genetic modules between cells

Comparing individual cells across maize, sorghum and millet reveals evolutionary differences between these important grain crops, according to a new study led by researchers from New York University.

Results published in naturebrings researchers closer to identifying genes that control important agricultural traits such as drought tolerance, which in the face of climate change will help scientists adapt crops to drier environments.

Maize, sorghum, and millet provide food for humans and animals around the world. Corn and sorghum are ancient relatives that evolved into two distinct species roughly 12 million years ago, and millet is a distant relative.

Despite their common ancestry, the crops have fundamental differences in key traits – for example, sorghum is more drought tolerant than maize, and the plants release unique sticky substances from their roots to shape how they interact with the soil around them. These differences can be traced back to maize that underwent whole genome duplication after splitting from sorghum.

“The importance of these crops, their evolutionary proximity, and their functional differences present an exciting opportunity to compare patterns of gene expression at the cell level,” he said.

Bruno Guillotin, a postdoctoral fellow in the NYU Department of Biology and first author of the study. “While these three crops are similar, how they differ from each other is important because they have traits that we might want to carry over from one to the other, such as drought tolerance.”

The researchers performed single-cell RNA profiling of the roots of maize, sorghum and millet, dissecting the roots to look at the cells individually and observe exactly where genes were expressed in a given cell. Then they compared the same specialized cells across the three crops.

“Roots are the first line of defense against drought and heat. You can think of a root as a machine with many working parts — in this case, types of cells — so knowing how the machine works to collect water and deal with drought and heat,” said Kenneth Birnbaum, a professor in the University’s Department of Biology. New York Center for Genomics and Systems Biology and first author of the study, “is really important.” Comparing different species helps us rule out genes that lead to key agricultural traits.

In studying how cells develop and diverge in different species, researchers have identified several trends that indicate “grafting” — or rearranging of existing elements — of cells over time. First, they note that cells often exchange gene expression modules, or groups of 10 or 50 genes with coordinated functions, between cell types over the course of development.

“Genetic unit swapping has been shown in animal systems, but the data we have generated is the first time that this has been demonstrated at such a large level in plants,” Birnbaum added.

This exchange of units is illustrated in a discovery about root clay — the sticky, nutrient-packed substance that roots release into the soil. The slime is useful for lubricating the soil so roots can pass through and can attract beneficial bacteria that protect the plant or provide hard-to-get nutrients.

The researchers found that the genes that aid in root slime production were present in different parts of maize, sorghum, and millet rootstock. In sorghum, the slime genes were found in the outer tissues of the root, while in maize they were switched to a new cell type in the root cap, an evolutionary change that may enable the corn to attract bacteria that help the plant gain nitrogen.

They also identified other gene regulators that are switched in different cell types depending on the crop, providing researchers with prime candidates for testing genes that convey specific traits.

In addition, the researchers found that complete genome replication in maize after it split from sorghum 12 million years ago affected specific cell types, allowing maize cells to rapidly specialize. They also noticed that certain types of cells acted as donors of the new genes while others seemed to collect new gene duplicates, which may indicate that gene duplication speeds up the development of certain cells.

Recent advances in single-cell sequencing technologies have made this research possible and opened up new avenues to explore the relationship between genes and cellular traits in crops.

“A decade ago, we were only able to analyze a dozen or a few dozen cells using primary single-cell sequencing techniques. Now we can sample tens of thousands of cells in a pretty routine experiment,” Birnbaum said.

Future studies will compare how single cells from these three crops respond to stress, such as drought.

“That response may be the key to finding that set of genes that are really important for drought tolerance,” Birnbaum said.