Tübingen, Baden-Württemberg, Germany. Mutations are the basic raw material of evolution. Charles Darwin recognized this, discovering that evolution depends on heritable differences between individuals. Those individuals who are better adapted to the environment will have better chances to pass on their genes to the next generation.

A species can only evolve if the genome changes through new mutations, with the best new variants surviving the sieve of selection. Scientists have now measured the speed with which new mutations occur in plants. They scrutinized the signature of evolution before selection occured.

Research teams from the Max Planck Institute for Developmental Biology, and Indiana University (Bloomington) followed all genetic changes in five lines of the mustard relative Arabidopsis thaliana that occurred during 30 generations. In the genome of the final generation they then searched for differences to the genome of the original ancestor. Their findings appear in the journal Science.

The new work sheds new light on a fundamental evolutionary process, explaining, for example, why resistance to herbicides can appear within just a few years.

Arabidopsis
thaliana

... a favorite of many plant biologists and commonly used to test genetic questions.

Plants, animals and other organisms share a number of the same or similar genes — particularly those that arose early in evolution and were retained as organisms differentiated over time.

A. thaliana is widely used by scientists as an easily manipulated model organism because it is simple to grow in the laboratory, has a short life cycle, and a comparatively small genome.

Compared to corn, which might have as many as 2.5 billion base pairs of DNA and the human genome with roughly 3 billion pairs, Arabidopsis only has about 120 million base pairs of DNA.

Faster growth, darker leaves, and a different way of branching — wild varieties of this small mustard plant, Arabidopsis thaliana, are often substantially different from the laboratory strain.

Moreover, plants from different geographical origins differ in many traits.

Research teams have investigated which detailed differences distinguish the genomes of strains from a wide variety of locations (the polar circle or the subtropics, from America, Africa or Asia).

The plant is self-pollinating and can produce many genetically identical offspring. Current reports date the start of this reproduction mode ("selfing") to at least a million years ago.

Investigators have been surprised by the results: the extent of the genetic differences far exceeds expectations for such a streamlined genome.

These identical plants still have subtle individual differences (just like human twins).

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Image courtesy of Max Planck Institute for Developmental Biology.

It is routine today to compare the genomes of related animal or plant species. Such comparisons, however, ignore mutations that have been lost in the millions of years since two species separated.

The painstakingly detailed comparison of the entire genome revealed that in over the course of only a few years some 20 DNA building blocks, the base pairs, had mutated in each of the five lines.

"The probability that any letter of the genome changes in a single generation is thus about one in 140 million," explains Michael Lynch.

To put it differently, each seedling has on average one new mutation in each of the two copies of its genome that it inherits from mum and dad. To find these tiny alterations in the 120 million base pair genome of Arabidopsis was akin to finding the proverbial needle in a haystack.

The number of new mutations in each individual plant might appear very small. But considering that they occur in the genomes of every member of a species, it becomes clear how fluid the genome really is. Each letter in the genome changes, on average, once in a collection of 60 million Arabidopsis plants, e. For an organism that produces thousands of seeds in each generation, 60 million is not such a big number.

Apart from the speed of new mutations, the study revealed that not every part of the genome is equally affected. With four different DNA letters, there are six possible changes—but only one of these is responsible for half of all the mutations found. In addition, scientists can now calculate more precisely when species split up. Arabidopsis thaliana and its closest relative, Arabidopsis lyrata, differ in a large number of traits including size and smell of flowers or longevity: Arabidopsis lyrata plants often live for years, while Arabidopsis thaliana plants normally survive only for a few months.

Colleagues had previously assumed that only five million years had passed by since the two species went their separate ways. The new data suggest instead that the split occurred already 20 million years ago. Similar arguments might affect estimates of when in prehistory animals and plants were first domesticated.

On a positive note, the team results show that in sufficiently large populations, every possible mutation in the genome should be present. Thus, breeders should be able to find any simple mutation that has the potential to increase yield or make plants tolerate drought in a better manner. Finding these among all the unchanged siblings remains nevertheless a challenging task.

On the other hand, the new findings easily explain why weeds become quickly resistant to herbicides. In a large weed population, a few individuals might have a mutation in just the right place in their genome to help them withstand the herbicide. "This is in particular a problem because herbicides often affect only the function of individual genes or gene products," says Weigel. A solution would be provided by herbicides that simultaneously interfere with the activity of several genes.

Turning to the larger picture, Weigel suggests that changes in the human genome are at least as rapid as in Arabidopsis: "If you apply our findings to humans, then each of us will have on the order of 60 new mutations that were not present in our parents." With more than six billion people on our planet, this implies that on average each letter of the human genome is altered in dozens of fellow citizens.

"Everything that is genetically possible is being tested in a very short period," adds Lynch, emphasizing a very different view than perhaps the one we are all most familiar with: that evolution reveals itself only after thousands, if not millions of years.

CitationThe rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Stephan Ossowski, Korbinian Schneeberger, José Ingnacio Lucas-Lledó, Norman Warthmann, Richard M. Clark, Ruth G. Shaw, Detlef Weigel and Michael Lynch. Science 2010; 327(5961): 92-94. doi: 10.1126/science.1180677

Abstract

To take complete advantage of information on within-species polymorphism and divergence from close relatives, one needs to know the rate and the molecular spectrum of spontaneous mutations. To this end, we have searched for de novo spontaneous mutations in the complete nuclear genomes of five Arabidopsis thaliana mutation accumulation lines that had been maintained by single-seed descent for 30 generations. We identified and validated 99 base substitutions and 17 small and large insertions and deletions. Our results imply a spontaneous mutation rate of 7 x 10–9 base substitutions per site per generation, the majority of which are G:C->A:T transitions. We explain this very biased spectrum of base substitution mutations as a result of two main processes: deamination of methylated cytosines and ultraviolet light–induced mutagenesis.

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