Inversion gives plant dual lifestyle

DUKE (US) — The yellow monkeyflower that lives as both a perennial on the  Pacific Northwest coast and a dry-land annual hundreds of miles inland harbors a significant clue about evolution.

Interested in how a single species can live such different lifestyles, Duke University graduate student David Lowry set out to find a gene or genes that would account for the monkeyflower (Mimulus guttatus) being a lush, moisture-loving, salt-tolerant perennial on the coast, but a shorter, faster-flowering, drought-tolerant annual inland.

What he found instead was that a large chunk of the plant’s genome—2.2 million letters of DNA and 350 genes—are working differently in each ecotype of the plant.

The difference is called a genetic inversion, a long piece of DNA that has been clipped out of a chromosome at both ends and then reinserted essentially upside down.

“When you look at one plant species across a broad landscape with lots of different habitat conditions, you find differences in the genes from one place to the next,” says Lowry, now at the University of Texas at Austin.

“The cause of these differences has been a source of contention among evolutionary biologists for decades as they’ve tried to figure out what mechanisms drive the origin of species.”

A single species with a broad range of habitats like the monkeyflower can be expected to have a suite of genes available to help it adapt to the various conditions it would encounter within its range. But depending on where an individual plant finds itself, some of those genes aren’t being used.

In the case of the monkeyflower, each ecotype has a large suite of adaptive genes carried within the inversion.

The inland plants set about producing flowers and getting their reproduction done in the spring, before hot, dry weather arrives.

The coastal plants grow a lot more foliage and flower much later without the threat of drought, leaving them better suited to overwinter and to compete for space in a riotous plant environment.

Those adaptations lie within the inverted section: transplanted to the other environment, neither variety does well.

The study appears in the Sept. 28 issue of PLoS Biology.

The inversion can be a driver of speciation. In the process of gene-shuffling during the formation of sex cells (known as recombination), an inverted region can’t successfully swap genes with its counterpart chromosome precisely because it’s backwards.

The first clue was that crosses between the two ecotypes didn’t produce any recombinations in the part of the chromosome where the inversion was eventually found.

Because they aren’t reshuffled by recombination, the genes within the inverted stretch end up traveling through time as one large block of genes, rather than an assortment. “So the inversion sort of works like a super gene,” Lowry explains.

Inversions are particularly interesting to biologists who are trying to figure out how one species becomes two. Notably, many significant inversions have been identified between humans and chimpanzees.

One of Lowry’s Duke advisors, biologist Mohamed Noor, has found inversions help separate new species of fruitflies.

“Inversions are going to be seen as an important part of local adaptation as more people look for them,” says John Willis, professor of biology at Duke, who was Lowry’s thesis advisor and co-author.

“This is an extremely important argument and could explain a lot of the inversions that people are finding.”

To prove the adaptations were in the inversions, Lowry put the annual spelling of the inversion into perennial plants and the perennial spelling into the annuals through a long series of crosses.

Then he took 1,600 of the edited plants out to test plots across several habitats in the Pacific Northwest to see how they would do in the 2009 growing season.

Not only will these hardiness differences help drive the two ecotypes apart, their different flowering times will help prevent pollen-swapping that would mingle their genes.

With time, they should become separate species, “depending on which definition of species you want to use,” Lowry says. “They’re not full species, but they’re going in that direction.”

This is the first time in a natural setting that anyone has shown inversions directly affecting adaptation to local conditions and a shift between annual and perennial life history in plants.

“We actually showed through experimentation that the inversion contributes to adaptation and reproductive isolation,” Lowry says.

The research was supported by the National Institutes of Health, the National Science Foundation and Duke.

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