How to be dispensable: genomic and transcriptomic determinants in maize genes

Abstract

BackgroundPlant genomes harbour a substantial proportion of dispensable genes - present only in a subset of individuals - that differ from ubiquitously shared core genes in multiple genomic and expression features. While these differences have been repeatedly documented, the factors shaping gene dispensability remain poorly understood. ResultsWe assembled a pan-gene set from eight maize inbred lines from American and European germplasms, together with their transcriptomic profile across 22 tissues/conditions, revealing the genomic and transcriptomic determinants of maize gene dispensability. Multivariate analysis demonstrates that gene expression level and purifying selection - rather than gene size - are the primary factors distinguishing core from dispensable genes. Dispensable genes overlap Helitrons at 4.6 times the rate of core genes, implicating Helitron-mediated gene capture as a major mechanism of dispensable gene formation. Classifying genes into stably expressed, variably expressed, and on-off categories shows that all three classes contain dispensable genes, though in different proportions than for core genes. Contrary to previous assumptions, we show that dispensable genes can participate in basal biological functions just as core genes, and that gene duplication likely provides only a partial mechanism for functional complementation of accessory genes absence. ConclusionsOur results provide novel insights into the molecular and evolutionary factors distinguishing core from dispensable genes and into the biological mechanisms shaping gene dispensability in maize, and demonstrate that classifying genes by transcriptional patterns provides a powerful framework for understanding the biological functions and evolutionary dynamics of both core and dispensable genes.