Genomic compartmentalization of pervasive sex-biased gene expression in the vine mealybug Planococcus ficus

Abstract

The vine mealybug, Planococcus ficus, is a globally invasive pest of grapevine and a vector of leafroll viruses. Like other mealybugs, it reproduces through paternal genome elimination, a sex-determination system that operates without sex chromosomes and is associated with extreme sexual dimorphism. To characterize genome organization and sex-biased expression in this species, we generated a long-read reference genome spanning 369 Mb with 23,489 annotated genes and macrosynteny conserved with the citrus mealybug, Planococcus citri. Resequencing of four California field individuals yielded a first whole-genome estimate of nucleotide diversity and 132 microsatellite markers for population monitoring. Among 2,129 candidate secreted proteins, a conserved core is shared with P. citri, but each species carries a distinct set of lineage-specific effectors. Comparing adult male and female transcriptomes, we found sex-biased expression to be pervasive and skewed toward females: 41% of tested genes differed between the sexes, with female-biased genes both more numerous and showing larger fold changes. These female-biased genes were not randomly distributed but concentrated in discrete blocks of coordinately expressed, tandemly duplicated gene families, a pattern not previously described in a mealybug. Male- and female-biased secreted proteins also differed in origin, with male-biased proteins drawn from a conserved repertoire shared with P. citri and female-biased proteins spanning a more lineage-specific pool. Together, these results reveal a female-skewed, spatially clustered architecture of sex-biased expression in a mealybug that lacks sex chromosomes, and provide genomic resources for managing an invasive vineyard pest.