De Novo Transcription Responses Describe Host-Related Differentiation of Paracoccus marginatus (Hemiptera: Pseudococcidae)

SIMPLE SUMMARY: The papaya mealybug, Paracoccus marginatus, is an invasive pest affecting many crop plants. It reproduces and spreads rapidly. They have historically been a pest of potato, Solanum tuberosum, but they have successfully adapted to infesting papaya, Carica papaya. When they feed on papaya, they survive and reproduce more and live longer than when they feed on potato. We do not yet know what biological adaptations they made in order to use this new host plant. We compared the RNA sequences of papaya mealybugs feeding on potato and papaya. A total of 408 genes are expressed differently depending on the host plant. Most of these genes are expressed less when feeding on potato than on papaya. They encode digestive enzymes, detoxifying enzymes, and ribosomes and some have reproductive functions. We further analyzed their known functions using the Kyoto Encyclopedia of Genes and Genomes. This showed that they include genes regulating digestion, detoxification, and longevity. We suggest that papaya is a more suitable host than potato, and that the decreased expression of particular genes may have important effects on the adaptation of the papaya mealybug to this alternative host plant. ABSTRACT: Paracoccus marginatus (Hemiptera: Pseudococcidae) is an invasive pest with a diverse host range, strong diffusion, and high fecundity. It has been observed that P. marginatus feeding on Carica papaya have a higher survival rate, fecundity, and longer lifespan than P. marginatus feeding on Solanum tuberosum, indicating their successful adaptation to C. papaya; however, the mechanisms underlying host plant adaptation remain unclear. Therefore, RNA-seq was performed to study the transcriptional responses of P. marginatus feeding on C. papaya and S. tuberosum plants. A total of 408 genes with significant differential expression were defined; most of them were downregulated in S. tuberosum, including those of digestive enzymes, detoxifying enzymes, ribosomes, and reproductive-related genes, which may result from the adaptation of the host to nutritional needs and changes in toxic chemical levels. Enrichment analysis of the Kyoto Encyclopedia of Genes and Genomes showed that lysosome and longevity regulating pathways related to digestion, detoxification, and longevity were enriched. We suggest that C. papaya is a more suitable host than S. tuberosum, and downregulated target genes may have important effects on the adaptation of P. marginatus to host transfer.