Genomic Loss and Silencing on the Y Chromosomes of Rumex.

Abstract

Across many unrelated lineages of plants and animals, Y chromosomes show a recurrent pattern of gene degeneration and loss, but the relative importance of inefficient selection, adaptive gene silencing, and neutral genetic drift in causing degeneration remain poorly understood. Here, we use next-generation genome and transcriptome sequencing to investigate patterns of ongoing Y chromosome degeneration in two annual plant species of Rumex (Polygonaceae) differing in their degree of degeneration and sex chromosome heteromorphism. We find evidence for both gene loss as well as silencing in these young plant sex chromosomes. Our analyses revealed significantly more gene deletion relative to silencing in R. rothschildianus, which has had a larger nonrecombining region for a longer period than R. hastatulus, consistent with this system being at a more advanced stage of degeneration. Intra- and interspecific comparisons of genomic coverage and heterozygosity indicated that loss of expression precedes gene deletion, implying that the final stages of mutation accumulation and gene loss may often occur neutrally. We found no evidence for adaptive silencing of genes that have lost expression. Our results suggest that the initial spread of deleterious regulatory variants and/or epigenetic silencing may be an important driver of early degeneration of Y chromosomes.