OPUS: Genome doubling in an evolutionary model: Synthesis across biological and temporal scales

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Genome doubling, which doubles all genetic information in a cell, is a major evolutionary force that has produced much of the species diversity on Earth. Even the human genome has duplicated segments that result from ancient genome doubling in early vertebrates hundreds of millions of years ago. Although it occurs in animals and fungi, genome doubling is particularly common in plants. Organisms that have undergone genome doubling are often more successful than their non-duplicated parents and have new traits; for example, plants with doubled genomes are often larger than their parents and produce more fruits and seeds. In fact, most agricultural crops and the world’s worst weeds have all originated through this process. As a result, genome doubling is very important both ecologically and economically, yet scientists do not yet understand how the presence of duplicated genes produces new traits. Although the earliest stages of this process are the most critical for understanding the connection between genes and traits, it is precisely these early stages that are the most difficult to study, mainly because nearly all genome doubling events occurred in the very distant past, millions of years ago. In this project, the researchers will investigate these early stages by focusing on two species of plants in the sunflower family that formed in nature via genome doubling in the past 90 years. These species are unique in that their time of origin is so recent; as a result, they are perfect models for learning about how genome doubling generates new traits and how this process can be used to address societal problems related to food security, human health, and climate change. Whole-genome duplication (WGD, or polyploidy) is a major evolutionary force, yet the critical early stages of polyploid evolution remain poorly understood. This project will promote novel understanding of WGD by providing new insights into recurring polyploid formation and the consequences of genomic merger through analysis of data compiled over the past 30 years for Tragopogon, a genus of plants from the sunflower family that includes two recently (~90 years old) and repeatedly formed natural allotetraploids (T. mirus, T. miscellus) and their diploid parents (T. dubius, T. pratensis, T. porrifolius). New tools, including genetic manipulation via CRISPR-Cas9, will be applied, and new long-read sequence data for both genomes and transcriptomes will be acquired to maximize the value of available data. New analyses to address fundamental questions regarding WGD will focus on: 1) Distribution of natural populations of the polyploids and their diploid parents; 2) Introductions of the diploid parents from Europe to U.S.; 3) Crossability between tetraploids of separate origin; 4) Genetic/genomic consequences of polyploid formation (transcriptomes; reference genomes; proteomes; alternative splicing); 5) Properties of synthetic lines; and 6) Ecological comparisons of polyploids and their diploid parents (greenhouse data; niche modeling). Emphasis will be placed on synthesizing information on the early stages of WGD in Tragopogon and other systems, both natural and synthetic. This broad synthesis will not only provide new insights into WGD, but also set the stage for future investigations by diverse researchers to investigate the patterns, tempo, mechanisms, and forces driving and shaping post-WGD genome evolution.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.