Genetic architecture of inter-specific and -generic grass hybrids by network analysis on multi-omics data

Abstract

Understanding the mechanisms underlining forage production and its biomass nutritive quality at the omics level is crucial for boosting the output of high-quality dry matter per unit of land. Despite the advent of multiple omics integration for the study of biological systems in major crops, investigations on forage species are still scarce. Therefore, this study aimed to combine multi-omics from grass hybrids by prioritizing omic features based on the reconstruction of interacting networks and assessing their relevance in explaining economically important phenotypes. Transcriptomic and NMR-based metabolomic data were used for sparse estimation via the fused graphical lasso, followed by modularity-based gene expression and metabolite-metabolite network reconstruction, node hub identification, omic-phenotype association via pairwise fitting of a multivariate genomic model, and machine learning-based prediction study. Analyses were jointly performed across two data sets composed of family pools of hybrid ryegrass (Lolium perenne x L. multiflorum) and Festulolium loliaceum (L. perenne x Festuca pratensis), whose phenotypes were recorded for eight traits in field trials across two European countries in 2020/21. Our results suggest substantial changes in gene co-expression and metabolite-metabolite network topologies as a result of genetic perturbation by hybridizing L. perenne with another species within the genus relative to across genera. However, conserved hub genes and hub metabolomic features were detected between pedigree classes, some of which were highly heritable and displayed one or more significant edges with agronomic traits in a weighted omics-phenotype network. In spite of tagging relevant biological molecules as, for example, the light-induced rice 1 (LIR1), hub features were not necessarily better explanatory variables for omics-assisted prediction than features stochastically sampled. The use of the graphical lasso method for network reconstruction and identification of biological targets is discussed with an emphasis on forage grass breeding.