A protein complex that normally puts the brakes on genes may also be crucial for reproduction in plants, according to new research published in Science Advances. In thale cress, DREAM appears to switch on genes during meiosis that are important for the exchange of genetic material. But when the complex is missing, reproductive development becomes defective and fertility is severely reduced.
During meiosis, chromosomes must be distributed with great precision. This requires genes to be active and proteins to be present at the correct location, time, and concentration. Consequently, the entire process needs to be tightly regulated.
As part of her PhD project at the University of Hamburg, molecular biologist and postdoctoral researcher at the Institute of Science and Technology Austria (ISTA) Hasibe Tunçay investigated which molecular regulators control this process in thale cress (Arabidopsis thaliana, A. thaliana).
Her research has shed new light on the importance of the DREAM complex. Since related DREAM complexes also affect reproduction in animals, the findings may point to an evolutionarily conserved mechanism underlying fertility across many organisms.
The research was carried out in collaboration with the Université Paris-Saclay, Fudan University, and South China Agricultural University.
Not all cell divisions are the same
In sexually reproducing organisms, there are two fundamental types of cell division: mitosis and meiosis.
During mitosis, one cell produces two largely identical daughter cells. This process is important for an organism's development and growth, as well as for tissue renewal and maintenance.
Meiosis, by contrast, produces reproductive cells with half the usual number of chromosomes. The full chromosome set is restored only upon fertilization.
For meiosis to work, genes need to be switched on at the right time so that they can be transcribed into RNA. This RNA can then serve as the blueprint for proteins needed to carry out the process.
Meiosis may be a textbook classic, but how it is transcriptionally regulated in plants is still not fully understood. The molecular switches behind the process—known as transcription factors—first need to be identified.
That was precisely the task Tunçay set out to tackle, using thale cress as her model organism.
The DREAM complex
Studying gene regulation during meiosis was technically challenging. Meiotic cells are located deep inside the plant's reproductive tissues and can only be isolated in small quantities.
Despite these limitations, Tunçay and her colleagues were able to identify an important molecular regulator: the DREAM complex.
The DREAM complex is a transcription-factor complex that also exists in humans. In somatic cells—non-reproductive cells that proliferate through mitosis—DREAM usually represses gene expression. For example, it can help stop the cell cycle when errors occur and damage needs to be repaired.
Now, Tunçay's research shows that DREAM seems to play another role as well.
DREAM wakes up genes
"We studied mutants—plants in which parts of the DREAM complex are missing—and found that pollen and seed production did not function properly," says Tunçay. "That made it clear to me that DREAM is also important for plant reproduction, apparently by regulating gene expression during meiosis."
Tunçay identified the gene MER3, which is activated by the DREAM complex. The resulting MER3 protein plays an important role in crossover formation, a process essential for meiosis.
During a crossover, homologous chromosomes—one inherited from the maternal and one from the paternal side—exchange genetic material.
"This mechanism does not just generate genetic diversity," Tunçay explains. "It also keeps chromosomes physically connected, allowing them to be distributed correctly to daughter cells during the first meiotic division."
In mutants in which the DREAM complex does not function properly, MER3 is not transcribed sufficiently. As a result, crossover formation is impaired: chromosomes do not remain connected for long enough and instead occur as individual chromosomes.
"These are called univalent chromosomes," says Tunçay. These can then be distributed incorrectly or randomly among daughter cells, she adds, producing reproductive cells with an unbalanced number of chromosomes—and ultimately leading to fertility problems.
"In some of our mutants where only a single DREAM complex-component was disrupted, seed production was severely reduced, but the plants remained fertile," Tunçay explains. "In comparison, mutants carrying disruptions in multiple components produced no seed, indicating that they were sterile."
But what does that mean for the plant?
Plant sex
A. thaliana is a self-fertilising hermaphroditic plant. Both male stamens and the female pistil are found within the same flower. After fertilisation, the ovary develops into a long, slender fruit called a silique, in which the seeds grow.
Whether mutations affect reproduction can be assessed by examining pollen and seeds.
"For example, you can dip the flower into a solution. This releases the pollen grains, which can then be stained and examined under a microscope to determine whether they are viable," Tunçay says. "You can also open the silique and assess the seeds inside. Undeveloped or aborted seeds indicate sterility and problems with reproduction."
The findings show that a known regulatory complex can take on an unexpected activating role during plant meiosis. Because related DREAM complexes also influence reproduction in animals, the results suggest that fertility may be regulated by an evolutionarily conserved mechanism across a wide range of organisms.
