DNA of Storied Plant Provides Insight into the Evolution of Flowering Plants, Study Finds

Amborella female flower. Photograph by Sangtae Kim.

The newly sequenced genome of the Amborella plant addresses Darwin's "abominable mystery" -- the question of why flowers suddenly proliferated on Earth millions of years ago. The genome sequence sheds new light on a major event in the history of life on Earth: the origin of flowering plants, including all major food crop species. On 20 December 2013, a paper by the Amborella Genome Sequencing Project that includes a full description of the analyses performed by the project, as well as implications for flowering plant research, will be published in the journal Science. The paper is among three on different research areas related to the Amborella genome that will be published in the same issue of the journal and posted online at www.sciencemag.org.

Amborella female flowers. Photograph by Sangtae Kim

Amborella (Amborella trichopoda) is unique as the sole survivor of an ancient evolutionary lineage that traces back to the last common ancestor of all flowering plants. The plant is a small understory tree found only on the main island of New Caledonia in the South Pacific. An effort to decipher the Amborella genome -- led by scientists at Penn State University, the University at Buffalo, the University of Florida, the University of Georgia, and the University of California-Riverside -- is uncovering evidence for the evolutionary processes that paved the way for the amazing diversity of the more than 300,000 flowering plant species we enjoy today.

This unique heritage gives Amborella a special role in the study of flowering plants. "In the same way that the genome sequence of the platypus -- a survivor of an ancient lineage -- can help us study the evolution of all mammals, the genome sequence of Amborella can help us learn about the evolution of all flowers," said Victor Albert of the University at Buffalo.

Scientists who sequenced the Amborella genome say that it provides conclusive evidence that the ancestor of all flowering plants, including Amborella, evolved following a "genome doubling event" that occurred about 200 million years ago. Some duplicated genes were lost over time but others took on new functions, including contributions to the development of floral organs.

"Genome doubling may, therefore, offer an explanation to Darwin's "abominable mystery" -- the apparently abrupt proliferation of new species of flowering plants in fossil records dating to the Cretaceous period," said Claude dePamphilis of Penn State University. "Generations of scientists have worked to solve this puzzle," he added.

Amborella flower underside. Photograph by Joel McNeal.

Comparative analyses of the Amborella genome are already providing scientists with a new perspective on the genetic origins of important traits in all flowering plants -- including all major food crop species. "Because of Amborella's pivotal phylogenetic position, it is an evolutionary reference genome that allows us to better understand genome changes in those flowering plants that evolved later, including genome evolution of our many crop plants -- hence, it will be essential for crop improvement," stressed Doug Soltis of the University of Florida. As another example of the value of the Amborella genome, Joshua Der at Penn State noted "We estimate that at least 14,000 protein-coding genes existed in the last common ancestor of all flowering plants. Many of these genes are unique to flowering plants, and many are known to be important for producing the flower as well as other structures and other processes specific to flowering plants."

"This work provides the first global insight as to how flowering plants are genetically different from all other plants on Earth," Brad Barbazuk of the University of Florida said, "and it provides new clues as to how seed plants are genetically different from non-seed plants."

Amborella female flowers and fruits. Photograph by Joel McNeal.

Jim Leebens-Mack from UGA noted that "The Amborella genome sequence facilitated reconstruction of the ancestral gene order in the 'core eudicots,' a huge group that comprises about 75 percent of all angiosperms. This group includes tomato, apple and legumes, as well as timber trees such as oak and poplar." As an evolutionary outsider to this diverse group, the Amborella genome allowed the researchers to estimate the linear order of genes in an ancestral eudicot genome and to infer lineage-specific changes that occurred over 120 million years of evolution in the core eudicot.

At the same time, Amborella seems to have acquired some unusual genomic characteristics since it split from the rest of the flowering plant tree of life. For example, DNA sequences that can change locations or multiply within the genome (transposable elements) seem to have stabilized in the Amborella genome. Most plants show evidence of recent bursts of this mobile DNA activity, "But Amborella is unique in that it does not seem to have acquired many new mobile sequences in the past several million years," stated Sue Wessler of the University of California-Riverside. "Insertion of some transposable elements can affect the expression and function of protein-coding genes, so the cessation of mobile DNA activity may have slowed the rate of evolution of both genome structure and gene function."

Amborella male flowers. Photograph by Joel McNeal.

In addition to its utility in retrospective studies of the evolution of flowering plants, the Amborella genome sequence offers insights into the history and conservation of Amborella populations. There are only 18 known populations of this very special angiosperm in mountainous regions New Caledonia.

"Resequencing of individual Amborella plants across the species' range reveals geographic structure with conservation implications plus evidence of a recent, major genetic bottleneck," noted Pam Soltis of the University of Florida. A similar narrowing of genetic variation occurred when humans migrated from Africa to found modern-day Eurasian populations.

The complete genome sequence of Amborella has been deposited in Genbank -- the U.S. National Institutes of Health database of publicly available gene sequences -- and also is available in the Amborella Genome Database (www.Amborella.org).

Amborella female flower. Photograph by Sangtae Kim

In addition to the paper about the nuclear genome sequence, two other papers appear in this same issue: one that reports the complete mitochondrial genome sequence of Amborella, which contains large amounts of foreign DNA resulting from horizontal transfer (Rice et al. 2013); and another that describes the novel assembly and validation of the nuclear genome using a combination of approaches that can be applied to other complex genomes of non-model species (Chamala et al. 2013).

In addition to researchers at Penn State University, the University at Buffalo, the University of Florida, the University of Georgia, and the University of California-Riverside, the paper's authors include scientists from other universities in the United States, Canada, Mexico, China, Korea, Taiwan, Singapore, Germany, Italy, Denmark, France, and New Caledonia.

The work was funded by the National Science Foundation's Plant Genome Research Program.

CONTACTS

Claude dePamphilis at Penn State: 814-321-2256, cwd3@psu.edu

Victor Albert at the University of Buffalo: 716-341-5582, vaalbert@buffalo.edu

Pamela Soltis at the University of Florida: 352-273-1964, psoltis@flmnh.ufl.edu

Jim Leebens-Mack at the University of Georgia: 706-583-5573, jleebensmack@plantbio.uga.edu

Barbara Kennedy (PIO): 814-863-4682, science@psu.edu

GRANT NUMBER:

NSF Plant Genome Research Program (0922742)