ANN ARBOR—The pigments that give beets their red color may have helped a major group of flowering plants repeatedly adapt to dry environments, setting the stage for the evolution of traits that allowed plants to adapt to some of the harshest environments on Earth, according to a University of Michigan study.
The pigment, called betalain, is only produced by species in the flowering plant group Caryophyllales, which also has many drought-tolerant species. Previously, researchers have noted a link between plants that produce betalain and their ability to tolerate drought. Prior work has also shown conditions that stress the plant, such as exposure to salt, drought and intense ultraviolet light, cause plants to produce more of the pigment.
A study led by recent U-M postdoctoral researcher Tom Carruthers shows that betalain likely underpinned drought tolerance in Caryophyllales, allowing plants to evolve drought specializations such as succulence—thick, fleshy leaves and stems in which a plant stores water.
"Succulence is a really costly adaptation in most cases: You have these really thick leaves that you're filling with water, and there are a lot of costs associated with that," said Carruthers, who is now at University College Dublin. "It's likely that betalains are enabling plants to start to inhabit these dry conditions, and that's subsequently leading to succulents to evolve."
The group also found that the pigment evolved independently in several different species early in the plant group's evolution—something that was of particular interest to the researchers, according to study co-author and U-M scientist Stephen Smith .
"One thing that has always struck me about Caryophyllales is how many different lineages have independently evolved to live in extremely dry environments. We wanted to understand whether traits made those repeated transitions possible," said Smith, professor of ecology and evolutionary biology. "Betalains stood out because they are unusual, they occur only in this group of flowering plants, and they repeatedly appear in lineages that have made that transition into arid environments. That made us wonder whether betalains were not simply associated with drought tolerance, but actually helped create the conditions that allowed other drought adaptations to evolve."
Their results, supported by the U.S. National Science Foundation, are published in the journal New Phytologist.
To examine the role of betalain in drought-resistant plants, the researchers first created an evolutionary tree for Caryophyllales, including about 4,500 of the group's species. The researchers ensured the evolutionary tree included species from across the breadth of Caryophyllales, and fossil species that existed in the past.
They then grouped the species depending on whether they: do or do not produce betalains; are or are not succulent; and are or are not drought tolerant. The researchers then reconstructed the evolution of betalains, succulence and drought tolerance.
"When we did that, we showed that the evolution of betalains across Caryophyllales is really closely associated with drought tolerance, and betalain pigmentation seems to be gained at a much higher rate on lineages that go on to be drought tolerant," Carruthers said.
Carruthers says betalain pigments may work by soaking up harmful metabolic byproducts that plants produce when stressed—for example, when plants lack water or if photosynthesis doesn't happen properly. Researchers have also demonstrated in the lab that an accumulation of betalain in a plant cell might help the cell draw water from its surroundings.
Their study may also provide information about another Caryophyllales mystery: Many plant species in the group have what's called medullary bundles, a unique kind of vascular tissue that spreads all the way across a plant's stem.
"No one quite understands what this tissue does, but it's reasonable to hypothesize that it's associated with water transport or storage," Carruthers said. "One thing we show is that most of the species with this weird vasculature are also betalain pigmented. Again, you're getting another link between betalains being this precursor for all of these other oddities like medullary bundles and succulence to evolve."
The researchers say the study demonstrates how the complex interactions between different traits can contribute to the evolution of plants overall.
"We often look at a cactus or another succulent and focus on the obvious adaptations like the thick, water-storing stem or leaf. But those traits may only have been possible because of less visible innovations that evolved earlier," Smith said. "Our study gives us a much richer picture of how plants came to occupy some of the harshest environments on Earth."
