Heritable temporal gene expression patterns correlate with metabolomic seed content in developing hexaploid oat seed

Authors: HU, HAIXIAO - Cornell University; GUTIERREZ-GONZALEZ, JUAN - University Of Leon; LIU, XINFANG - Liaoning University; YEATS, TREVOR - Cornell University; Garvin, David; HOEKENGA, OWEN - Cayuga Genetics Consulting Group, Llc; SORRELLS, MARK - Cornell University; GORE, MICHAEL - Cornell University; Jannink, Jean-Luc

Submitted to: Plant Biotechnology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/26/2019
Publication Date: 11/1/2019
Citation: Hu, H., Gutierrez-Gonzalez, J.J., Liu, X., Yeats, T.H., Garvin, D.F., Hoekenga, O.A., Sorrells, M.E., Gore, M.A., Jannink, J. 2019. Heritable temporal gene expression patterns correlate with metabolomic seed content in developing hexaploid oat seed. Plant Biotechnology Journal. 18:1211-1222. https://doi.org/10.1111/pbi.13286.
DOI: https://doi.org/10.1111/pbi.13286

Interpretive Summary: Oat ranks sixth in world cereal production and has a higher content of health-promoting compounds compared with other cereals. However, there is neither a robust oat reference DNA sequence nor sequences of its transcribed genes (its transcriptome). Using deeply sequenced libraries of transcribed genes we assembled an oat seed transcriptome. With this reference transcriptome we quantified gene expression during seed development of 22 diverse lines across six time points. Gene expression showed higher correlations between adjacent than distant time points. We identified 22 major temporal expression patterns of gene expression and were able to show that these patterns associated with biological processes. Within each temporal pattern, there were sets of genes with expression patterns affected by oat genotype. Seventeen of the 22 temporal patterns included gene sets with median heritabilities higher than 0.50. Regression between 634 metabolites from mature seeds and the gene sets showed statistically significant linear relationships. Temporal expression patterns of oat avenanthramides and lipid biosynthetic genes were concordant with previous studies of avenanthramide biosynthetic enzyme activity and lipid accumulation. This study expands our understanding of gene activity during oat seed maturation and provides plant breeders the means to change oat seed composition through targeted manipulation of key pathways.

Technical Abstract: Oat ranks sixth in world cereal production and has a higher content of health-promoting compounds compared with other cereals. However, there is neither a robust oat reference genome nor transcriptome. Using deeply sequenced full-length mRNA libraries of oat cultivar Ogle-C, a de novo high-quality and comprehensive oat seed transcriptome was assembled. With this reference transcriptome and QuantSeq 3' mRNA sequencing, gene expression was quantified during seed development from 22 diverse lines across six time points. Transcript expression showed higher correlations between adjacent time points. Based on differentially expressed genes, we identified 22 major temporal co-expression (TCoE) patterns of gene expression and revealed enriched gene ontology biological processes. Within each TCoE set, highly correlated transcripts, putatively commonly affected by genetic background, were clustered and termed genetic co-expression (GCoE) sets. Seventeen of the 22 TCoE sets had GCoE sets with median heritabilities higher than 0.50, and these heritability estimates were much higher than that estimated from permutation analysis, with no divergence observed in cluster sizes between permutation and non-permutation analyses. Linear regression between 634 metabolites from mature seeds and the PC1 score of each of the GCoE sets showed significantly lower p-values than permutation analysis. Temporal expression patterns of oat avenanthramides and lipid biosynthetic genes were concordant with previous studies of avenanthramide biosynthetic enzyme activity and lipid accumulation. This study expands our understanding of physiological processes that occur during oat seed maturation and provides plant breeders the means to change oat seed composition through targeted manipulation of key pathways.