Comparative Transcriptome Analysis of Two Root-Feeding Grape Phylloxera (D. vitifoliae) Lineages Feeding on a Rootstock and V. vinifera

SIMPLE SUMMARY: Grape phylloxera is an American native insect pest that caused heavy damages to the vineyards worldwide since its spreading to wine regions since the 1850s. This insect, able to feed on leaves and roots, induces plant galls and manipulates the grapevine physiology leading to plant damage and may cause plant death. The most successful treatment was the use of mostly partially resistant rootstocks. The degree of resistance is affected by environment, grapevine management and the insect biotype. In this study, we analyse the interaction of insect biotypes feeding on particular host plants. Therefore we evaluated the gene expression of Phylloxera feeding on a susceptible host versus feeding on a rootstock in two different developmental stages. We discovered (mainly in advanced insect developmental stages) genes expressed in higher proportion in one insect compared to the other. These genes related to chemosensory; in plant physiology manipulation and root deformation and insect digestive traits may play a role in the plant-insect interaction determining plant resistance in response to the pest attack. ABSTRACT: Grape phylloxera is one of the most dangerous insect pests for worldwide viticulture. The leaf- and root-galling phylloxerid has been managed by grafting European grapevines onto American rootstock hybrids. Recent reports pinpoint the appearance of host-adapted biotypes, but information about the biomolecular characteristics underlying grape phylloxera biotypisation and its role in host performance is scarce. Using RNA-sequencing, we sequenced the transcriptome of two larval stages: L1 (probing) and L2-3 (feeding) larvae of two root-feeding grape phylloxera lineages feeding on the rootstock Teleki 5C (biotype C) and V. vinifera Riesling (biotype A). In total, 7501 differentially expressed genes (DEGs) were commonly modulated by the two biotypes. For the probing larvae, we found an increased number of DEGs functionally associated with insect chemoreception traits, such as odorant-binding proteins, chemosensory proteins, ionotropic, odorant, and gustatory receptors. The transcriptomic profile of feeding larvae was enriched with DEGs associated with the primary metabolism. Larvae feeding on the tolerant rootstock Teleki 5C exhibited higher numbers of plant defense suppression-associated DEGs than larvae feeding on the susceptible host. Based on the identified DEGs, we discuss their potential role for the compatible grape phylloxera–Vitis interaction belowground. This study was the first to compare the transcriptomes of two grape phylloxera lineages feeding on a tolerant and susceptible host, respectively, and to identify DEGs involved in the molecular interaction with these hosts. Our data provide a source for future studies on host adaptation mechanisms of grape phylloxera and help to elucidate grape phylloxera resistance further.