Chromosome-level Atlantic switchgrass assemblies reveal a supernumerary B-Chromosome with transcriptional and evolutionary impacts

Abstract

Supernumerary B-Chromosomes are extra genetic elements that frequently deviate from Mendelian inheritance to ensure their own survival. Their evolutionary origins and biological impacts within natural plant populations remain largely unexplored. Switchgrass (Panicum virgatum) is a model for studies of local adaptation, but reliance on a single reference genome has limited the detection of lineage-specific genomic content. We generated chromosome-level genome assemblies from the diverged Atlantic switchgrass subpopulation and discovered a previously undetected genomic element: a ~34 Mb supernumerary B-Chromosome, validated by Hi-C contact mapping and long-read depth, which indicates two to four B copies per nucleus. The B-Chromosome has a bipartite architecture including a gene-rich, single-copy proximal region (~8 Mb) and a repeat-rich, gene-poor distal region (~27 Mb) dominated by LTR/Ty3 (Gypsy) elements and punctuated by Mutator TIR peaks. High-resolution mapping reveals a highly rearranged chimera of fragments from multiple autosomes, biased toward the N-subgenome. Intact LTR retrotransposons on the B-Chromosome are younger than those on the A-Chromosomes, especially in its distal region, consistent with a B-Chromosome that arose and expanded within the Atlantic lineage. Population screening and phylogenetic analysis indicate that the B-Chromosome is largely restricted to the Atlantic subpopulation and likely has a single origin. In a typical family, 70% of open-pollinated progeny of B-positive maternal plants were B-positive, with substantial variation among families. Finally, B-Chromosome presence is associated with expression differences in A-Chromosome genes that differ between genetic backgrounds. Together, our results show how accessory chromosomes contribute to the evolutionary and genomic diversity of natural plant populations.