A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding

Contents   Summary 923 I. Introduction 924 II. Early studies of heterosis 924 III. Heterosis in diverse species 926 IV. Gene expression studies 926 V. Protein metabolism 927 VI. Allele-specific gene expression 928 VII. Quality control 929 VIII. A synthesis model 930 IX. Putting the model to work 932   Acknowledgements 933   References 933 Summary Hybrids between genetically diverse varieties display enhanced growth, and increased total biomass, stress resistance and grain yield. Gene expression and metabolic studies in maize, rice and other species suggest that protein metabolism plays a role in the growth differences between hybrids and inbreds. Single trait heterosis can be explained by the existing theories of dominance, overdominance and epistasis. General multigenic heterosis is observed in a wide variety of different species and is likely to share a common underlying biological mechanism. This review presents a model to explain differences in growth and yield caused by general multigenic heterosis. The model describes multigenic heterosis in terms of energy-use efficiency and faster cell cycle progression where hybrids have more efficient growth than inbreds because of differences in protein metabolism. The proposed model is consistent with the observed variation of gene expression in different pairs of inbred lines and hybrid offspring as well as growth differences in polyploids and aneuploids. It also suggests an approach to enhance yield gains in both hybrid and inbred crops via the creation of an appropriate computational analysis pipeline coupled to an efficient molecular breeding program.