Differential Analysis of Proteomes and Metabolomes Reveals Additively Balanced Networking for Metabolism in Maize Heterosis

Abstract

A century ago, dominance and overdominance hypotheses were developed to explain the phenomenon of heterosis, both hypotheses were in a nonadditive pattern. Here, a principal component analysis (PCA) of maize seed proteomes was used for representative inbreds of five heterotic germplasms and three classes of hybrid. Hybrids congregated in the center region of inbreds, forming an additive distribution with hybrids in the middle of their parents. Principal components 1 and 2 indicated biased distributions of proteins with functions of amino acid–protein or carbohydrate–energy metabolisms, respectively, after loading analysis and MS identification of proteins. Then, GC–MS was used to examine free amino acids, carbohydrates, and organic acids. A lower level of these metabolites were found in hybrids than inbreds. Further, we performed similar analyses of germinating seeds of a parent–F1 triad and three F2 segregants and confirmed these results. Therefore, an additive pattern of protein abundances for an unimpeded flow of metabolites was established in heterotic hybrids. That is, an additively balanced networking but not the nonadditive dominance or overdominance regulates heterosis. The less expensive metabolism in hybrids suggested the evolution of sexual reproduction. The Mendelian phenotypic ratio can be better explained based on this additive pattern than dominance