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Paternal genome elimination (PGE) is an intriguing but poorly understood reproductive strategy in which females are typically diploid, but males lose paternal genomes. Paternal genome heterochromatin (PGH) occurs in arthropods with germline PGE, such as the mealybug, coffee borer beetles, and booklice. Here, we present evidence that PGH initially occurs during early embryo development at around 15 h post-mating (hpm) in the cotton mealybug, Phenacoccus solenopsis Tinsley. Transcriptome analysis followed by qPCR validation indicated that six histone lysine methyltransferase (KMT) genes are predominantly expressed in adult females. We knocked down these five genes through dsRNA microinjection. We found that downregulation of two KMT genes, PsEZH2-X1 and PsEHMT1, resulted in a decrease of heterochromatin-related methylations, including H3K27me1, H3K27me3, and H3K9me3 in the ovaries, fewer PGH male embryos, and reduced male offspring. For further confirmation, we obtained two strains of transgenic tobacco highly expressing dsRNA targeting PsEZH2-X1 and PsEHMT1, respectively. Similarly, fewer PGH embryos and fewer male offspring were observed when feeding on these transgenic tobacco plants. Overall, we present evidence that PsEZH2-X1 and PsEHMT1 have essential roles in male embryo survival by regulating PGH formation in cotton mealybugs. The roles of histone lysine methyltransferases EZH2 and EHMT1 in male embryo development of cotton mealybug are investigated, with RNAi against both genes leading insects to produce fewer PGH embryos and fewer male offspring [ABSTRACT FROM AUTHOR]

Beneficial fungi are well known for their contribution to insects' adaptation to diverse habitats. However, where insect-associated fungi reside and the underlying mechanisms of insect-fungi interaction are not well understood. Here, we show a pellet-like structure on the legs of mealybugs, a group of economically important insect pests. This at-leg pellet, formed by mealybugs feeding on tomato but not by those on cotton, potato, or eggplant, originates jointly from host secretions and mealybug waxy filaments. A fungal strain, Penicillium citrinum, is present in the pellets and it colonizes honeydew. P. citrinum can inhibit mealybug fungal pathogens and is highly competitive in honeydew. Compounds within the pellets also have inhibitory activity against mealybug pathogens. Further bioassays suggest that at-leg pellets can improve the survival rate of Phenacoccus solenopsis under pathogen pressure, increase their sucking frequency, and decrease the defense response of host plants. Our study presents evidences on how a fungi-associated at-leg pellet provides multiple protections for mealybugs through suppressing pathogens and host defense, providing new insights into complex insect × fungi × plant interactions and their coevolution. A Penicillium citrinum-associated pellet at mealybugs' legs, which forms on mealybugs feeding on tomato and originates jointly from plant secretions and waxy filaments, provides multiple protections for mealybugs through suppressing pathogens and host defense. [ABSTRACT FROM AUTHOR]

Mealybugs are highly aggressive to a diversity of plants. The waxy layer covering the outermost part of the integument is an important protective defense of these pests. However, the molecular mechanisms underlying wax biosynthesis in mealybugs remain largely unknown. Here, we analyzed multi-omics data on wax biosynthesis by the cotton mealybug, Phenacoccus solenopsis Tinsley, and found that a fatty acyl-CoA reductase (PsFAR) gene, which was highly expressed in the fat bodies of female mealybugs, contributed to wax biosynthesis by regulating the production of the dominant chemical components of wax, cuticular hydrocarbons (CHCs). RNA interference (RNAi) against PsFAR by dsRNA microinjection and allowing mealybugs to feed on transgenic tobacco expressing target dsRNA resulted in a reduction of CHC contents in the waxy layer, and an increase in mealybug mortality under desiccation and deltamethrin treatments. In conclusion, PsFAR plays crucial roles in the wax biosynthesis of mealybugs, thereby contributing to their adaptation to water loss and insecticide stress. The role of a fatty acyl-CoA reductase (PsFAR) in wax biosynthesis of cotton mealybug is investigated, RNAi against PsFAR resulted in insects with lower generation of waxy filaments and higher mortality under desiccation and deltamethrin treatments. [ABSTRACT FROM AUTHOR]

Mealybugs (Hemiptera: Pseudococcidae) are economically important agricultural pests with several compelling biological phenomena including paternal genome elimination (PGE). However, limited high‐quality genome assemblies of mealybugs hinder a full understanding of this striking and unusual biological phenomenon. Here, we generated a chromosome‐level genome assembly of cotton mealybug, Phenacoccus solenopsis, by combining Illumina short reads, PacBio long reads and Hi‐C scaffolding. The assembled genome was 292.54 Mb with a contig N50 of 489.8 kb and a scaffold N50 of 49.0 Mb. Hi‐C scaffolding assigned 84.42% of the bases to five chromosomes. A total of 110.75 Mb (37.9%) repeat sequences and 11,880 protein‐coding genes were predicted. The completeness of the genome assembly was estimated to be 95.5% based on BUSCO genes. In addition, 27,086 (95.3%) full‐length PacBio transcripts were uniquely mapped to the assembled scaffolds, suggesting the high quality of the genome assembly. We showed that cotton mealybugs lack differentiated sex chromosomes by analysing genome resequencing data of males and females. DAPI staining confirmed that one chromosome set in males becomes heterochromatin at an early embryo stage. Chromatin immunoprecipitation assays with sequencing analysis demonstrated that the epigenetic modifications H3K9me3 and H3K27me3 are distributed across the whole genome in males, suggesting that these two modifications might be involved in maintaining heterochromatin status. Both markers were more likely to be distributed in repeat regions, while H3K27me3 had higher overall enrichment. Our results provide a valuable genomic resource and shed new light on the genomic and epigenetic basis of PGE in cotton mealybugs. [ABSTRACT FROM AUTHOR]