Selection for seed size has uneven effects on specialized metabolite abundance in oat (Avena sativa L.)

Authors: BRZOZOWSKI, LAUREN - Cornell University; HU, HAIXIAO - Cornell University; CAMPBELL, MALACHY - Cornell University; BROECKLING, COREY - Colorado State University; CAFFE, MELANIE - South Dakota State University; GUTIERREZ, LUCIA - University Of Wisconsin; SMITH, KEVIN - University Of Minnesota; SORRELLS, MARK - Cornell University; GORE, MICHAEL - Cornell University; Jannink, Jean-Luc

Submitted to: Genes, Genomes, Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/29/2021
Publication Date: 12/10/2021
Citation: Brzozowski, L.J., Hu, H., Campbell, M.T., Broeckling, C.D., Caffe, M., Gutierrez, L., Smith, K.P., Sorrells, M.E., Gore, M.A., Jannink, J. 2021. Selection for seed size has uneven effects on specialized metabolite abundance in oat (Avena sativa L.). Genes, Genomes, Genetics. 12(3): Article ejkab419. https://doi.org/10.1093/g3journal/jkab419.
DOI: https://doi.org/10.1093/g3journal/jkab419

Interpretive Summary: Improving crop healthfulness has been a longstanding goal of plant breeding. Breeding for more healthy crops includes nutrients like unsaturated fats and vitamins, and there has been more recent attention on health-promoting compounds, like antioxidants. In oats, a cereal crop lauded for cardiac health promoting compounds like beta-glucans, we studied antioxidants and other health-promoting compounds in seeds that have not yet been a direct target of plant breeding efforts. We measured these compounds in over 500 oat varieties, and used genome and transcriptome (gene expression) sequences to better understand if these oat varieties can be used in breeding for antioxidants (e.g., sufficient trait variation), and how antioxidant concentrations related to other important traits, like yield. We found that modern oat varieties had reduced variation in antioxidant content compared to less intensively bred oat varieties. This change was indirectly tied to seed size, where seed size led to increased concentrations of some compounds, but decreased concentrations of others. This research increases our understanding of how antioxidant abundance has been historically shaped by plant breeding, and also provide new insights for plant breeders to optimize antioxidant content as to develop healthy new oat varieties.

Technical Abstract: Plant breeding strategies to optimize metabolite profiles are necessary to develop health-promoting food crops. In oats (Avena sativa L.), seed metabolites are of interest for their antioxidant properties, yet have not been a direct target of selection in breeding. In a diverse oat germplasm panel spanning a century of breeding, we investigated the degree of variation of these specialized metabolites and how it has been molded by selection for other traits, like yield components. We also ask if these patterns of variation persist in modern breeding pools. Integrating genomic, transcriptomic, metabolomic, and phenotypic analyses for three types of seed specialized metabolites—avenanthramides, avenacins, and avenacosides—we found reduced heritable genetic variation in modern germplasm compared with diverse germplasm, in part due to increased seed size associated with more intensive breeding. Specifically, we found that abundance of avenanthramides increases with seed size, but additional variation is attributable to expression of biosynthetic enzymes. In contrast, avenacoside abundance decreases with seed size and plant breeding intensity. In addition, these different specialized metabolites do not share large-effect loci. Overall, we show that increased seed size associated with intensive plant breeding has uneven effects on the oat seed metabolome, but variation also exists independently of seed size to use in plant breeding. This work broadly contributes to our understanding of how plant breeding has influenced plant traits and tradeoffs between traits (like growth and defense) and the genetic bases of these shifts.