GAINESVILLE, Florida – Plants are DNA hoarders. True to the maxim never to throw away anything that could be useful later, they often duplicate their entire genome and get stuck on the added genetic baggage. All of these extra genes can then freely mutate and produce new physical traits, thereby accelerating the pace of evolution.

A new study shows that such duplication events were critical throughout the evolutionary history of gymnosperms, a diverse group of seed plants that include pines, cypresses, sequoias, ginkgos, and cycads. Published today in Nature plants, research suggests that genome duplication in the ancestors of modern gymnosperms may have contributed directly to the formation of the group over 350 million years ago. Subsequent replicas provided raw materials for the development of innovative traits that enabled these plants to survive in dramatically changing ecosystems, laying the foundation for a recent resurgence over the past 20 million years.

“This early evolutionary event gave genes the opportunity to evolve and create entirely new functions that may aid gymnosperms’ transition to new habitats and ecological advancement,” said Gregory Stull, a recent PhD graduate from the Florida Museum of natural history and lead author of the study.

Take a closer look at gymnosperms

While having more than two sets of chromosomes – a phenomenon called polyploidy – is rare in animals, it is commonplace in plants. For example, most of the fruits and vegetables we eat are polyploid and often involve hybridizations between two closely related species. Many plants, including wheat, peanuts, coffee, oats, and strawberries, benefit from multiple divergent copies of DNA, which can lead to faster growth rates and increases in size and weight.

However, until now it was unclear how polyploidy could have influenced the evolution of gymnosperms. Although they have some of the largest genomes in the plant kingdom, they are low in chromosome numbers, leading scientists for decades to believe that polyploidy was not as common or important in these plants.

Gymnosperm genetics are also complex. Their large genomes make them difficult to study, and much of their DNA is made up of repetitive sequences that code for nothing.

“What makes gymnosperm genomes complex is that they appear to have a tendency to accumulate many repeating elements,” said study co-author Douglas Soltis, curator of the Florida Museum and distinguished professor at the University of Florida. “Things like ginkgos, cycads, pine trees and other conifers are full of all these repetitive things that have nothing to do with genome duplication.”

However, a recent collaborative effort by plant biologists, including Soltis, to extract huge numbers of genetic sequences from more than 1,000 plants has opened new doors for scientists trying to summarize the long history of terrestrial plant evolution. Stull, now a postdoc at the Kunming Institute of Botany of the Chinese Academy of Sciences, and his colleagues used a combination of this data and newly generated sequences to give gymnosperms a different look.

Genome duplication resulted in gymnosperms

By comparing the DNA of living gymnosperms, the researchers were able to look back in time and uncover evidence of several ancient genome duplication events that coincided with the origins of important groups.

Gymnosperms have experienced significant extinctions over their long history, making it difficult to decipher the exact nature of their relationships. But the genomes of all living gymnosperms share the signature of an ancient replica in the distant past, more than 350 million years ago. More than 100 million years later, another replication resulted in the pine family, while a third gave rise to the origin of the podocarps, a group that contains mostly trees and shrubs that are now mostly restricted to the southern hemisphere.

In each case, analyzes revealed a strong link between duplicated DNA and the development of unique traits. While future studies are needed to determine exactly which traits resulted from polyploidy, possible candidates are the strange egg-shaped roots of cycads, which harbor nitrogen-fixing bacteria, and the diverse cone structures found in modern conifers. Podocarp cones, for example, are heavily modified and look deceptively like fruit, says Stull: “Their cones are very fleshy, have different colors and are distributed by different animals.”

Competition and climate change led to extinction and diversification

Stull and his colleagues also wanted to know whether genome duplication influenced the speed at which new gymnosperm species evolved over time. But instead of a clear pattern, they found a complex interplay of extinction and diversification against the background of a significantly changing global climate.

Today there are around 1,000 species of gymnosperms, which do not appear like many compared to the roughly 300,000 species of flowering plants. But in their prime, gymnosperms were much more diverse.

Gymnosperms flourished even before the asteroid extinction 66 million years ago, which was best known for the demise of the dinosaurs. But the dramatic ecological changes caused by the impact tipped the scales: after the dinosaurs disappeared, flowering plants quickly began to displace gymnosperm lines, which, as a result, were critically endangered. Some groups have been completely wiped out, while others have barely managed to survive to this day. The once thriving ginkgo family, for example, is now represented by a single living species.

However, the results of this study show that at least some gymnosperm groups made a comeback about 20 million years ago, which coincided with the Earth’s transition to a cooler, drier climate.

“We see points in history where gymnosperms not only continued to decline, but diversified in species numbers, leading to a more dynamic picture of their evolutionary history,” said co-author Pamela Soltis, curator of the Florida Museum and UF distinguished professor.

While some gymnosperms were not up to the dual aspects of climate change and competition, others had an advantage in certain habitats because of the traits they lost in their old rivalry with flowering plants. Groups like pines, spruces, firs and junipers got a fresh start.

“In some ways gymnosperms may not be that flexible,” says Pamela Soltis. “They somehow have to ‘wait’ until the climate is more favorable so that they can diversify.”

In some settings, gymnosperms have adapted to life at extremes. In pine forests in southeast North America, long-leaf pines are adapted to frequent fires that burn their competition, and conifers dominate the boreal forests of the far north. But take away the fire or the cold, and flowering plants will quickly begin to advance.

While gymnosperms are still in the process of diversification, they have been disrupted by human-made changes in the environment. Currently, more than 40% of gymnosperms are critically endangered due to the cumulative pressures of climate change and habitat loss. Future studies that clarify how their underlying genetics enabled them to persist into the present could give scientists a better framework to ensure they survive well into the future.

“Although some groups of conifers and cycads have diversified over the last 20 million years, many species have a very limited distribution and are threatened with extinction,” said Stull. “Efforts to reduce habitat loss are likely to be essential to the conservation of the many species that are currently threatened with extinction.”

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Other co-authors on the study are Xiao-Jian Qu from Shandong Normal University; Caroline Parins-Fukuchi from the University of Chicago; Ying-Ying Yang, Jun-Bo Yang, Zhi-Yun Yang, De-Zhu Li, and Ting-Shuang Yi from the Chinese Academy of Sciences; Yi Hu and Hong Ma from Pennsylvania State University; and Stephen Smith from the University of Michigan.

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