A new pace for molecular clocks

Climate change and other human impacts are altering natural species communities and so may disrupt species distributions. For example, invasive species are being introduced into new habitats. Plants and animals are shifting their ranges in response to global warming. Biodiversity is continually transformed as result of changing environmental conditions at an increasing rate. Evidently, reconstructing the timing of such recent events that predate speciation would be a major breakthrough.

So-called molecular clocks have widely been used in recent decades as they enable researchers to estimate speciation events in absolute time. The method is based on undirected, random mutations in the genetic material, which occur over time as regularly as clocks tick. Based on the differences in the sequence of bases in the genetic information (deoxyribonucleic acid, DNA) of two species, it is possible to reconstruct when they must have arisen from a common ancestor. However, because these clocks tick comparatively slowly, they cannot keep up with the speed at which biodiversity changes over short time-scales.

In the latest issue of the Science journal, a team of scientists from Germany, Great Britain and the United States of America presents a faster ticking clock which achieves a resolution in the order of years to decades. Their clock is set by cytosine methylation, a chemical modification of DNA that is often linked with adaptive responses of organisms to their environments. In plants, however, there are also undirected methylation changes in certain gene segments, known as epimutations, with no discernible consequences for the fitness of an organism. This phenomenon was exploited by the team led by Profesor Dr. Thorsten Reusch from GEOMAR Helmholtz Centre for Ocean Research Kiel, Profesor Dr. Frank Johannes from the Technical University of Munich and Profesor Dr. Robert Schmitz from the University of Georgia.

Using Arabidopsis thaliana as a model plant, the teams led by Robert Schmitz and Frank Johannes previously showed that epimutations accumulate in plant genomes at a rate that exceeds the rate of DNA mutations by several orders of magnitude. Later work also revealed that these molecular events can serve as an aging clock in long-lived trees. The breakthrough of the current work lies in the realization that this timer in plants, termed “epimutation clock”, can also be applied to shorter evolutionary time periods, down to a few generations. “This is only possible because epimutations in plants can be stably inherited and therefore permit a detailed reconstruction of the tree of life,” explains Frank Johannes.

Researchers at GEOMAR contributed to the development of this new epimutation clock by analysing clones of the seagrass Zostera marina. Seagrass is one of the plants that reproduces and spreads clonally via runners and can also form new genetic variants in the process. If its clones could be dated to time scales of a few years, it would also be easier to assess how well seagrass can withstand a changing marine environment.

To test the epimutation clock on short time scales, two genetically different seagrass clones cultivated in California since 2004 were analysed in the GEOMAR laboratory. Differences in cytosine methylation pointed back relatively accurately to the year in which the two clones began to develop independently of each other – whereas analyses with a classical DNA mutation-based molecular clock revealed an uncertainty of about a decade.

“The step that is now coming is, of course, to date the very large seagrass clones that are found at many sites around the world in order to finally solve the mystery of their true age,” Thorsten Reusch announces.

“In this context, we also plan to investigate whether the epimutation clock can be combined with classical DNA-based clocks. This would make it possible to measure seamlessly over short and long time scales,” adds Frank Johannes.

Further research could also clarify how epimutation clocks work at the molecular level. “Although it is not essential to understand how the ‘inside’ of a clock works to get accurate time information, the molecular mechanisms that cause epimutations are very interesting to us”, says Robert Schmitz.

The existence of a fast-ticking molecular clock in plants could provide high-resolution insights into a wider range of time scales of evolution. For example, it could be used explored when invasive species were introduced into certain regions or how human activity have affected the divergence of species, lineages or populations.

Original publication:

Yao, N, Zhang Z, Yu, L. Hazarika R. Yu, C, Jang H, Smith, LM, Ton, J, Liu, L, Stachowicz, JJ, Reusch, TBH, Schmitz RJ, Johannes F (2023): An evolutionary epigenetic clock in plants. Science, doi: 10.1126/science.adh9443.