Mutations drive evolution, but they can also be risky. New research led by plant biologists at the University of California, Davis, published Nov. 10 in Proceedings of the National Academy of Sciences, reveals how plants control mutation rates in different stem cells to balance adaptability with safety and stability. The findings have implications for breeding some of the world's most important fruit and vegetable crops, such as potatoes and bananas.
The researchers showed that DNA mutations accumulated up to 4.5 times more frequently in the stem cells that produce a plant's skin compared to stem cells that produce eggs and sperm. These results show how plants prioritize maintaining a stable genome for their offspring while allowing greater flexibility and adaptability in other cell types and, by extension, in adult plants.
"Mutations fuel variation, and variation fuels both evolution and our ability as plant breeders to make better crops," said Luca Comai, a distinguished professor of plant biology and senior author on the study. "Having a layered stem cell architecture allows plants to exquisitely regulate the mutation rate in different cells to optimize their success and the success of their offspring."
Layers of complexity
Whereas humans store their stem cells in bone marrow, plants carry a cluster of stem cells at the tips of their shoots called the "apical meristem." This dome-shaped structure consists of around 10 stem cells arranged in three layers (L1, L2 and L3) that are responsible for producing all of a plant's new tissues: from stems, leaves and roots to the plant's skin, vasculature and gametes (sperm and eggs).
"Why flowering plants have different layers in their apical meristem is not really known, but one possibility is that these layers provide flexibility to control different processes in different ways, such as the accumulation of mutations in different parts of the plant," said Comai.
Only stem cells in the L2 layer produce gametes, which means that when plants reproduce sexually, their offspring inherit only L2 mutations. In contrast, plants that reproduce clonally or "vegetatively" - for example through bulbs, runners or suckers - can accumulate and pass on mutations from all three layers.
"Many of the world's most important crops - potato, banana, grape, strawberry and cassava - can reproduce through seeds, but are vegetatively grown from stems, roots or tubers, which allows mutations to build up over time," said first author Kirk Amundson, who worked on the study as a graduate student and then postdoctoral scholar in Comai's lab and is now a postdoctoral associate at the University of Massachusetts Amherst.
"We asked how quickly and what kinds of mutations accumulated. A better understanding of mutational buildup could pave the way to harnessing or minimizing mutations to improve vegetatively propagated crops."
Separating the layers
To understand how mutations accumulate within vegetatively propagated crops, the researchers examined two potato varieties, Desiree and Red Polenta, that have each been clonally propagated for more than 50 years, accumulating mutations in the process. To compare mutation rates in the different layers of the apical meristem, they isolated individual stem cells from each layer and grew them to produce plants that were derived solely from L1, L2 or L3 cells.
Surprisingly, they found that the L3 layer was almost completely absent in apical meristems within the plants' leaves, because it had been invaded and replaced by L2 cells. When they compared L1 and L2 cells, they found that the layers had accumulated different sets of mutations. For both potato varieties, L1 cells had accumulated many more mutations compared to L2 cells (4.5 times more in Desiree potatoes and 1.6 times more in Red Polenta).
Since L2 cells are responsible for producing the plant's gametes, this difference suggests that plants prioritize maintaining genomic stability in their gametes and offspring, which is a safer bet since most mutations are not beneficial. However, there could also be a benefit of having a higher mutation rate in the L1 layer, Comai says, because L1 cells give rise to the plant's "skin."
"Plants interact with the environment through their skin, so having higher adaptability in those cells might allow them to adapt more rapidly to changing aspects of their environment, such as pathogens and herbivores," said Comai.
A cautionary tale for biotechnology
The difference in mutations in L1 and L2 cells is important for plant biotechnology, because genetically modified plants are usually produced by editing or inserting DNA into a single plant cell, which is then grown into a new plant. Since these genetically modified plants arise from a single cell from a single layer of the apical meristem, they could lack beneficial mutations present in the other layers.
"From a biotechnology point of view, researchers should be aware that if you transform a clonal plant, there's a possibility that you will lose important traits because your variety is chimeric," said Comai. "In the future, we'd like to find out how we can control this process."
Additional authors on the study are: Mohan Prem Anand Marimuthu, Oanh Nguyen, Konsam Sarika, Isabelle DeMarco, Angelina Phan and Isabelle Henry.
The work was supported by the National Science Foundation. This research utilized the DNA Technologies and Expression Analysis Core and the Flow Cytometry Shared Resource.
