The Amborella genome: A window into the origins of plant sex and reproduction

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Plant reproduction is a cornerstone of our food system and ecological balance; however, it is a complex process. Plants have fascinating reproductive strategies, some being either male or female, some being hermaphroditic, and still some changing sex over their lifetime. Understanding the mechanisms that determine plant sex is crucial for modern agriculture.

A study published in Nature Plants has shed new light on the complicated reproductive strategies of flowering plants. The study, led by researchers at the HudsonAlpha Institute for Biotechnology and the University of Georgia, delved into the genetics of Amborella trichopoda, a species of flowering plants that offers a unique window into the early evolution of flowering plants.

With their much-improved assembly of the Amborella genome and sex chromosomes, the researchers have gained valuable insights into the evolution of flowering plants and their reproductive strategies.

The evolution of the Amborella genome

Amborella trichopoda is the sole surviving species of a lineage that diverged from all other flowering plants early in their evolutionary history. Its genome provides invaluable insights into the genetic underpinnings of plant diversity.

Eleven years ago, an international team of researchers co-led by Jim Leebens-Mack, Ph.D., professor of plant biology at the University of Georgia, completed the first Amborella genome, the results of which were published in Science in 2013.

"The evolutionary lineage leading to Amborella diverged from all other flowering plant lineages approximately 150 million years ago, so our draft genome published in 2013 has been a foundation for comparative analyses of genes tracing back to the origin of flowering plants and earlier," says Leebens-Mack.

The new insights gained from the improved genome assembly are especially exciting for HudsonAlpha Faculty Investigator Alex Harkess, Ph.D., who was a Ph.D. student in Leebens-Mack's lab working on the Amborella genome. Now the leader of his own lab at HudsonAlpha, Harkess and one of his mentees, HudsonAlpha Senior Scientist Sarah Carey, Ph.D., worked on the new Amborella genome analyses with Leebens-Mack and HudsonAlpha Faculty Investigators Jeremy Schmutz and Jane Grimwood, Ph.D.

"Working on the original Amborella genome in Jim's [Leeben-Mack] lab was transformative because it allowed me as a first-year Ph.D. student to be on the very edge of newly developing technologies and software that was coming out to help handle all of this massive genomic data we were creating," reflects Harkess.

"This genome reveals so much about the evolution of flowers, but also about the evolution of my own research career and the way I, and now my entire laboratory, view reproduction through the lens of diversity."

Carey was a postdoctoral fellow in the Harkess lab when the new Amborella genome assembly was completed. She led much of the genome analysis, including the analysis of the Amborella sex chromosomes.

Advancing technology enables a more complete Amborella genome

Thanks to advanced sequencing and assembly technology and emerging computational tools, Carey, along with members of the HudsonAlpha Genome Sequencing Center, were able to assemble a much-improved Amborella genome. The new, highly-contiguous genome reference made it easier for Carey to search for the Amborella sex chromosomes, which are Z and W instead of the familiar human X and Y.

"The first Amborella genome was a mixture of short segments of DNA from different sequencing types and technologies," says Carey when asked how the improved genome came to be.

"Advancements in long-read sequencing and access to other pieces of information, like Hi-C data, allowed us to assemble larger pieces that made it easier to search for the ZW chromosomes than if it were in lots of smaller pieces."

In addition to the improved sequencing and assembly tools, Carey also credits staying at the forefront of new and emerging computational tools. The lab developed a pipeline, called cytogenetics-by-sequencing, to help more easily and inexpensively identify and characterize sex chromosomes in plants, successfully using it on nearly 30 dioecious plant and animal species so far.

Through their analysis of the Amborella sex chromosomes, the team discovered some interesting things about Amborella's sex-determination system. For starters, the Z and W chromosomes are young, having arisen more than 100 million years after Amborella diverged from all other flowering plant lineages.

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In many sex-determination systems (think the tiny human Y chromosome), the sex chromosomes stop swapping genetic material with their chromosome pair partner, a phenomenon known as recombination. The halting of recombination allows for the divergence of the two sex chromosomes through the accumulation of different rearrangements, deletions, and insertions.

Although the team found evidence of suppressed recombination in Amborella, the Z and W chromosomes look very similar, making the assembly of each sex chromosome more difficult.

"The Cytogenetics-by-Sequencing pipeline helped us to identify a difficult border on the Amborella sex chromosomes: where they no longer recombine," explains Carey. "This is an important task because within this region of non-recombination are expected to be the carpel and stamen sterility genes associated with the evolution of separate female and male plants."

Through the careful analysis of the sex chromosomes, Carey and the team identified two genes hypothesized to be responsible for sex determination in Amborella.

"The big picture takeaway from this study is that we're learning another exception for how you can maintain separate sexes in plants," says Harkess.

"That gives us another tool in our toolkit for engineering new ways to do plant breeding, creating separate sexes, preventing plants from self-pollinating, and enforcing outcrossing in a way that is controllable and predictable."

The new Amborella genome project was part of the Open Green Genomes Initiative, a Department of Energy Joint Genome Institute Community Science Program.

"The Open Green Genomes initiative is filling phylogenetic gaps in the availability of reference-quality genomes for land plants," says Leebens-Mack, lead PI for the OGG initiative.

"Our haplotype-resolved chromosomal assembly of the Amborella genome has enabled us to better understand aspects of the ancestral angiosperm genome and the derived characteristics of Amborella's sex chromosomes."

Other collaborators on this project include Auburn University, Arizona Genomics Institute, University of Lyon, Missouri Botanical Garden, The Institut de Systématique, Evolution, Biodiversité, University Montpellier, Indiana University, and Florida Museum of Natural History.

More information: Sarah B. Carey et al, ZW sex chromosome structure in Amborella trichopoda, Nature Plants (2024). DOI: 10.1038/s41477-024-01858-x

Journal information: Nature Plants , Science

Provided by HudsonAlpha Institute for Biotechnology