Researchers use living fossils to uncover a wealth of genes for seed improvement

Seed plants are essential as a source of food, fuel, medicine, and more. Now, a multidisciplinary team of researchers has combined deep botanical knowledge with powerful genomic technology to decode and mine the DNA of non-flowering seed plants and uncover genes that evolved to help plants build seeds. These findings, published in Nature Communications, may aid scientists in improving seed crop production in agriculture and in the conservation of these ancient endangered seed plants.

In this study by members of the New York Plant Genomics Consortium—a multi-institutional collaboration of botanists, evolutionary and genomics scientists, and bioinformaticians—the researchers isolated and studied seed genes encoded in the genomes of the oldest living seed plants: gymnosperms. Gymnosperms, which include conifers and Ginkgo, bear “naked” seeds unprotected by a fruit and are one of the most threatened plant groups. Many gymnosperms are also “living fossils,” a term coined by Darwin, for their persistence on Earth since the age of the dinosaurs.

“Now that scientists can sequence any genome, the question becomes which species to sequence and why?” said Gloria Coruzzi, the Carroll & Milton Petrie Professor in NYU’s Department of Biology and Center for Genomics and Systems Biology. “By studying gymnosperms—the species in which seeds first evolved, and which make up 30 percent of the world’s forests—we identified the genes supporting the evolution of seeds.” 

“Based upon our studies of reconstructing the evolutionary tree of life for gymnosperms, we know which species to investigate, where to collect them and how to grow them in elucidating the origin and development of their unique structural components such as the seed,” said Dennis Stevenson, senior curator emeritus at the New York Botanical Garden (NYBG).

NYBG researchers collected developing seeds, called ovules, and leaves from 14 different gymnosperms and four flowering plants, as well as spores from two fern species, which do not produce seeds, for comparison. In collaboration with the Cold Spring Harbor Laboratory (CSHL), they extracted transcripts from these samples and utilized powerful DNA-sequencing technology. The team at NYU’s Center for Genomics & Systems Biology then assembled over 586,000 genes for these species, creating the largest collection of gymnosperm ovule transcriptomes to date.

“This study highlights the power of biodiversity to answer fundamental questions,” said Barbara Ambrose, curator in plant genomics and director of laboratory research at NYBG. “The breadth of our living collections along with a modern laboratory in proximity to our collections to process the samples is vital for molecular biodiversity research.”  

To identify how these genes play a role in seed development, NYU researchers employed a novel two-pronged analysis combining evolutionary history with gene expression data using NYU’s High Performance Computing Cluster. To do this, they identified shared genes across species, called orthologs, and integrated information on how genes are turned on or expressed in different tissues with their influence on the evolutionary history of these plants.

By creating a genome-scale evolutionary tree of these 20 species, the researchers identified over 22,000 genes containing information on the history of these seed plants. Moreover, they observed for the first time that major evolutionary changes in seed plant history are driven by selection of genes whose expression changes during development of leaves and ovules in seed plants. The research team ultimately uncovered 4,076 candidate genes that likely played specific roles in seed evolution, including genes in model species whose function was previously unknown. 

“Model plants are species whose genomes have been heavily studied to answer basic science questions,” said Veronica Sondervan, who led the phylogenomic analysis at NYU and conducted in-plant studies at NYBG. “That we can still uncover new roles for these genes in model species using genome information from these early seed plants is very exciting.”  

“This is an interdisciplinary team that has worked together for a long time, and this study shows the very impactful advances that approach can make,” said team member W. Richard McCombie, the Davis Family Professor of Human Genetics at CSHL.

To confirm whether the newly identified genes play functional roles in seed development, the team at NYBG conducted experiments in several gymnosperms. In one example, they tested how two candidate genes were expressed in the ovules of a gymnosperm, the yew plant Taxus baccata first described in 1753 by Carl Linnaeus in his Species Plantarum. Yew plants are notable for the unique red cup-like “fruits” that surround their seeds, called arils—the only non-toxic organ in the plant—which are eaten by birds to enable seed dispersal. 

The results confirmed the evolutionary significance of these genes in seed dispersal by showing that the genes were expressed throughout the ovules. They also demonstrated different expression patterns than those observed in other gymnosperm species, including expression in the unique arils. This suggests that sequence changes in developmentally regulated genes may play an important part in how seed structures are created to enhance dispersal and aid in persistence in plant evolution. 

“This genetic resource for understanding seed development across plant species may not only help scientists enhance seed traits in a variety of crops, but could also provide tools to protect and propagate plants at risk of extinction, including these valuable living fossils,” noted Sondervan.

Botanical collaborators include Barbara Ambrose, Damon Little, Dennis Stevenson, Cecilia Zumajo-Cardona, and members of their research teams at NYBG, as well as Sebastiano Nigris of the Orto Botanico di Padua, Italy. The deep transcriptome sequencing effort was led by W. Richard McCombie and his team at CSHL DNA Sequencing Center. The transcriptome assemblies into genes and ensuing phylogenomic analysis were performed at NYU in the Plant Systems Biology lab of Gloria Coruzzi, led by Veronica Sondervan and Gil Eshel with input from Manpreet Katari as well as collaborator Kranthi Varala of Purdue University.

The research was supported by the US National Science Foundation's Plant Genome Research Program (NSF-PGRP:IOS-0922738 and NSF-PGRP:IOS-1758800), the European Union’s Horizon 2020 RISE program (Marie Skłodowska-Curie grant 101007738), the STARS@UNIPD ‘SeedDive’ program, and the US National Institutes of Health’s Quantitative Biological Systems Training Program (T32 GM132037) at NYU.