Measuring conflict in polyploid genomes

Arabidopsis thaliana, a small flowering plant in the mustard family, was the first plant to have its genome sequenced.  A. thaliana can be thought of as the “mouse model” of botanical research – just as the lab mouse has formed a cornerstone of research in mammals, A. thaliana is used to demonstrate genomic principles that are far-reaching and pertain to multiple plant species. As part of an investigation of polyploidy, Dr. Gavin Conant has extensively analyzed the genes of A. thaliana. Polyploidy simply means that each cell of an organism has more than two sets of chromosomes. Conant explained that duplication events creating such polyploid organisms have occurred across many species throughout the course of evolution, often several times in the same group. Most often, the genome doublings are coupled to a hybridization between two species and help mitigate some of the problems such crosses might otherwise induce. He relates the idea to a more familiar example in mammals.  “For instance, the modern carnivorous marvel liger, which blended the genes of a lion and a tiger, has valuable traits.  However, it will often be sterile, unable to reproduce and thus, sustain itself without direct human intervention,” said Conant. Polyploidy often results from an event in which  two sets of chromosomes are pulled from each parent, instead of the usual single set. Shortly after this conjoining, many of the acquired “extra” genes from the hybrid parents are discharged from the cells and lost altogether. Common sense might dictate that this would be a balanced process, selecting an equal number of genes from each parent. Instead, many geneticists believe that this process of gene selection carries a measure of preference, a term known as biased fractionation, but the evidence for this claim has been controversial.

Conant’s methodology, an algorithmic computer program he designed as a postdoctoral fellow, allowed him to confirm this bias by testing many genomes simultaneously, as opposed to the previous method, which tested one polyploid genome at a time. Beginning as a class research project (taught by Conant) at the University of Missouri, researchers compared the polyploid genomes of Arabidopsis plants against non-polyploid, closely-related species. The objective of the study was to estimate the strength of the bias observed after the polyploidy event. The research team built two models, one with the selection bias built-in, and one without. Utilizing data extracted from Conant’s program, the research team concluded that the loss pattern in the duplicate genes aligned more closely with the bias model, supporting that the genetic fractionation in polyploidy beings is indeed biased. Suspected reasons for this bias vary, but it likely is the result of the combinatorial manner which genes function. “Genes work together in tandem to perform certain functions. To work effectively, those gene groupings must all be from one parent. Matching individual genes together from both parents would be like taking certain parts from the engine block of a Ford and attempting to combine them with engine parts from a Chevy. Those parts are specifically designed to work together for that exact function. This is probably why the polyploidy genome ejects certain genes from one side, instead of maintaining a perfect balance,” Conant explained.

Conant’s findings have practical uses, as many important crops are polyploid, which may enable plants become larger or take on other beneficial characteristics. He further explained that “It’s important to understand this process. Agriculturally, knowing how to make stronger crops is essential to commercial success.”

Prior to joining the Bioinformatics Research Center (BRC) at North Carolina State University, Dr. Conant served as a postdoctoral researcher at Sandia National Labs. He studied biology and mathematics as an undergraduate, while working as an IT specialist. Following the completion of his PhD, he worked in Dublin, Ireland for nearly four years, where he conducted research involving baker’s yeast and its unique fermentation effects, which are likely due to an ancient polyploidy event. It was this background, combined with the clearinghouse of knowledge at the BRC, that facilitated the continued research of Dr. Conant and his fellow researchers.

What’s Next?

Dr. Conant’s lab is now applying similar methodology to eight fish species. Each of these fish contains a polyploid genome, while the gar fish serves as the non-polyploid counterpart. Fish polyploidy events are estimated to have occurred roughly 300 million years ago. Such an early event will be challenging to study – the Arabidopsis polyploidy event has been estimated as occurring only 25 million years ago.

Emery M, Willis MMS, Hao Y, Barry K, Oakgrove K, Peng Y, et al. (2018) Preferential retention of genes from one parental genome after polyploidy illustrates the nature and scope of the genomic conflicts induced by hybridization. PLoS Genet 14(3): e1007267. https://doi.org/10.1371/journal.pgen.1007267

Researchers and co-authors involved with this study include Gavin Conant, Marianne Emery, M. Madeline S. Willis, Yue Hao, Kerrie Barry, Khouanchy Oakgrove, Yi Peng, Jeremy Schmutz, Eric Lyons, J. Chris Pires, and Patrick P. Edger.

This work was supported by the US National Science Foundation (www.nsf.gov) under grant number NSF-IOS-1339156 (YH, EL, JCP and GCC) and by the US Department of Energy (www.doe.gov) under contract Number DE-AC02-05CH11231 (KB, KO, YP, JS). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under the contract number above. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.