Identification of trans-acting factors that control the non-Mendelian drive of the rye B chromosome

Abstract

The genomes of many plants, animals, and fungi comprise dispensable B chromosomes which rely on various chromosomal drive mechanisms to counteract the tendency of non-essential genetic elements to be purged over time. The B chromosome of rye – a model system for nearly a century – undergoes targeted nondisjunction during first pollen mitosis, favouring segregation of both B chromosome sister chromatids into the generative nucleus, thus increasing their numbers over generations. However, the genetic mechanisms underlying this process are poorly understood. Here, using a newly assembled ~430 Mb-long rye B chromosome pseudomolecule, I identified five candidate genes whose role as trans-acting moderators of the chromosomal drive is supported by karyotyping, chromosome drive analysis and comparative RNA-seq. Among them, I identified DCR28, coding a microtubule-associated protein related to cell division. The DCR28 gene family is a neo-functionalised and serially-duplicated gene with ~15 B chromosome-located copies that are specifically highly expressed in the first pollen mitosis of rye. Using Virus-Induced Genome Editing (VIGE), I demonstrated that the further size reduction of the drive control region of the rye B chromosomes is possible by employing B-repeat-specific gRNAs.