Single-cell and spatial transcriptomics uncover the role of B chromosomes in driving plant invasiveness

Abstract

Invasive plants pose a major threat to global biodiversity, yet the molecular and genomic mechanisms underlying their success remain poorly understood. Here, we investigate the common reed (Phragmites australis), a grass species that became invasive in North America after introduction from Europe, to unravel the molecular mechanisms of its invasiveness. By integrating single-cell RNA sequencing, spatial transcriptomics, and comparative genomics, we constructed a single-cell atlas of P. australis and identified 19 transcriptionally distinct cell types, including shoot apical meristem, epidermal, and vascular tissues. Comparative analysis of common garden-grown native (European) and invasive (North American) populations revealed a significant proportion of differentially expressed genes (DEGs) located on B chromosomes, which underwent copy number expansion in invasive genomes. The proportion of B chromosome genes in DEGs varies across cell types, with the highest proportions observed in the epidermis and mesophyll, and lower proportions in the vascular tissues. Gene IMPA-3, a B chromosome gene likely derived from transposable element activity, exhibited an elevated mutation rate compared to its ancestral counterparts, potentially enhancing adaptive evolution in invasive populations. Invasive individuals also displayed molecular regulatory networks related to photosynthetic efficiency, stress tolerance, and growth-defense trade-offs. Together, our findings provide a cell-type-resolved molecular atlas of a non-model invasive plant and offer key insights into the cellular and genomic architecture of plant invasiveness, with implications for ecological management.