Cell-to-Cell Genetic Module Exchange for Crop Evolution

According to a recent study conducted by researchers at New York University, comparing individual cells from corn, sorghum, and millet indicates discrepancies in these significant cereal crops’ evolutionary history.

Cell-to-Cell Genetic Module Exchange for Crop Evolution
The researchers used a technology called Molecular Cartography, a spatial transcriptomics method, in collaboration with Resolve Biosciences to map the cellular location of about a hundred genes at once. This allowed them to validate the cell-by-cell cross-species map of gene expression. Image Credit: Bruno Guillotin/Ramin Rahni)

The results, which were published in Nature, help scientists better understand which genes regulate crucial agricultural properties like drought tolerance, which will help them adapt crops to drier conditions as a result of climate change.

All around the world, both humans and animals consume food made of corn, sorghum, and millet. Around 12 million years ago, the ancestral cousins of corn and sorghum, as well as millet, split into two distinct species.

Despite having the same ancestor, the crops differ significantly in several important characteristics. For example, sorghum is far more tolerant of drought than corn, and the plants emit special sticky substances from their roots to affect how they interact with the soil around them.

These variations can be attributed to the whole genome duplication that corn underwent after separating from sorghum.

The importance of these crops, their evolutionary proximity, and their functional differences present an exciting opportunity for comparing patterns of gene expression at the cell level. While these three crops are similar, how they differ from each other is important because they have traits that we may want to transfer from one to the other, such as drought tolerance.

Bruno Guillotin, Study First Author and Postdoctoral Associate, Department of Biology, New York University

When dissecting the roots of corn, sorghum, and millet to examine the individual cells, the researchers performed single-cell mRNA profiling. They were able to pinpoint exactly where genes are expressed in a particular cell. The same specialized cells from all three crops were then compared.

Roots are the first line of defense against drought and heat. You can think of the root as a machine with many working parts—in this case, cell types—so knowing how the machine works to collect water and to deal with drought and heat is really important. Comparing the different species helps us tease apart which genes lead to key agricultural traits.

Kenneth Birnbaum, Study Senior Author and Professor, Department of Biology and Center for Genomics and Systems Biology, New York University

The researchers examined how cells have changed and diverged in various species and found multiple patterns that suggest that cells have been “tinkered” with over time, or have had their components rearranged. First, they noticed that throughout evolution, cells often exchange gene expression modules or collections of 10 or 50 genes with coordinated activities.

Birnbaum added, “This gene module swapping has been shown in animal systems, but the data we generated is the first time it’s been illustrated on a large level in plants.

The discovery of root slime—the slimy, nutrient-rich liquid that roots exude into the soil—served as an example of this module swapping. Slime helps lubricate the soil to allow for root passage and can draw in beneficial bacteria that defend the plant or provide nutrients that are difficult to obtain.

The scientists discovered that distinct regions of the corn, sorghum, and millet roots contained the genes that contribute to the production of root slime. The slime genes were discovered in the root’s outer tissue of sorghum; however, they were switched into a new cell type in the root cap in corn. This evolutionary modification may allow corn to draw bacteria that aid the plant’s uptake of nitrogen.

Additionally, they discovered other gene regulators that were shifted between different cell types based on the crop, giving researchers excellent possibilities for examining genes that are linked to particular features.

The total genome duplication that occurred in corn when it separated from sorghum 12 million years ago also affected particular types of cells, the researchers discovered, allowing corn cells to quickly specialize.

They also noticed that some cell types contributed new genes, while others appeared to accumulate new gene duplicates, which may indicate that gene duplication accelerated the development of certain cell types.

This research was made feasible by recent developments in single-cell sequencing techniques, which also provide new avenues for investigating 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 with the early single-cell sequencing techniques. Now we can profile tens of thousands of cells in a pretty routine experiment,” Birnbaum stated.

Future research will analyze how single cells from these three crops react to stresses like drought.

Birnbaum concluded, “It is that response that may be the key to finding that set of genes that are really important for drought tolerance.

Source:
Journal reference:

Guillotin, B., et al. (2023). A pan-grass transcriptome reveals patterns of cellular divergence in crops. Nature. doi.org/10.1038/s41586-023-06053-0

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