The genetic mechanism of B chromosome drive in rye illuminated by chromosomescale assembly

Abstract

The genomes of many plants, animals, and fungi frequently comprise dispensable
B chromosomes that rely upon 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 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, ~430Mb-long
rye B chromosome pseudomolecule, we identify 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, we identify DCR28, coding a microtubule-associated protein related to
cell division, and detect this gene also in the B chromosome of Aegilops speltoides.
The DCR28 gene family is neo-functionalised and serially-duplicated
with 15 B chromosome-located copies that are uniquely highly expressed in the
first pollen mitosis of rye.