Sequence of the supernumerary B chromosome of maize provides insight into its drive mechanism and evolution

Abstract

Significance B chromosomes are nonvital chromosomes found in thousands of plants and animals that persist through various drive mechanisms. The drive mechanism of the maize B chromosome consists of mitotic nondisjunction at the second pollen division to produce two unequal sperm and then the sperm with the B chromosomes preferentially fertilizes the egg in double fertilization. A high-quality sequence of the maize B chromosome together with genetic analysis reveals the cis factor for nondisjunction is a B chromosome-specific repeat interspersed in and around the centromere. The gene and transposable element content of the B chromosome and relaxed purifying selection of transposed protein-encoding genes suggest that the chromosome has been present in the evolutionary lineage for millions of years. B chromosomes are enigmatic elements in thousands of plant and animal genomes that persist in populations despite being nonessential. They circumvent the laws of Mendelian inheritance but the molecular mechanisms underlying this behavior remain unknown. Here we present the sequence, annotation, and analysis of the maize B chromosome providing insight into its drive mechanism. The sequence assembly reveals detailed locations of the elements involved with the cis and trans functions of its drive mechanism, consisting of nondisjunction at the second pollen mitosis and preferential fertilization of the egg by the B-containing sperm. We identified 758 protein-coding genes in 125.9 Mb of B chromosome sequence, of which at least 88 are expressed. Our results demonstrate that transposable elements in the B chromosome are shared with the standard A chromosome set but multiple lines of evidence fail to detect a syntenic genic region in the A chromosomes, suggesting a distant origin. The current gene content is a result of continuous transfer from the A chromosomal complement over an extended evolutionary time with subsequent degradation but with selection for maintenance of this nonvital chromosome.