CAREER: Genomic, cellular, and physiological effects of whole genome duplications on organismal energy production

This award is funded in whole or in part under the American Rescue Plan Act of 2021 (Public Law 117-2).

Understanding the genetic underpinnings of how plant cells produce energy represents a central goal in plant biology, especially in the context of crop improvement efforts. However, the connection between genes and the energy-related traits those genes encode is complicated for two primary reasons: (1) energy-related genes are spread across three separate cellular compartments (the nucleus, the chloroplasts, and the mitochondria), and (2) all plants have experienced one or more whole genome duplication events, in which the nuclear genome has been doubled or more, during their evolutionary history.

Indeed, many of our most important crop species have more than two copies of their nuclear genome inside their cells. How this “genomic redundancy” affects energy production is largely unknown; however, the balance between nuclear genome copy number and the mitochondria and chloroplasts appears to be critical to plant energy production. We will employ and train a diverse group of early career scientists at New Mexico Tech (Hispanic Serving Institution), to investigate how plant cells maintain this balance.

Much of the research will take place in the context of Course-based Research Experiences in which undergraduate and early-stage-graduate students will simultaneously learn the necessary biological techniques and contribute to the understanding of plant bioenergetics. We will also engage high school students in the genomics revolution by sequencing the genomes of creosote and snowflower live-and-in person at Socorro High School (Socorro, NM) and North Tahoe High School (Tahoe City, CA) respectively, and one high-school intern will participate in plant genomics research at NMT each summer.

Whole genome duplication events (WGDs), in which the nuclear genome is doubled or more as a result of allopolyploidization or autopolyploidization, are a major force for plant diversification. Because the cytoplasmic genomes are separately replicated (and inherited) from the nuclear genome, the stoichiometric balance between the three genomic compartments (i.e., cytonuclear stoichiometry) is expected to be perturbed following WGD.

Recent work indicates that cytonuclear stoichiometry is maintained following WGD in both monocots and eudicots, suggesting that gene dosage balance between the nuclear and cytoplasmic genomes represents an important component of polyploid lineage formation and evolution. We therefore hypothesize that cytonuclear stoichiometry is critical for establishing the cell’s chloroplast and mitochondrial content, such that variation in cytonuclear stoichiometry leads to variation in photosynthetic and respiratory performance and that the genomic architecture of cytonuclear stoichiometry is responsive to changes in nuclear genome size and content.

We will test these hypotheses first in diploid, polyploid, and aneuploid contexts by quantifying and measuring organelles, evaluating photosynthetic performance, and comparing nuclear vs. cytoplasmic transcript pools of single cells. We will also perform association tests in the Arabidopsis thaliana genome and confirm those associations with molecular knockouts to disentangle the complex genomic architecture underlying cytonuclear stoichiometry.

The diverse coalition of researchers employed as part of this research will be instrumental in setting the stage for future applied efforts aimed at improving metabolic function in polyploid crops, both by addressing knowledge gaps and by adding to the human infrastructure necessary for 21st century agricultural improvement efforts.

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.