Abstract
Simple SummaryGrape 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.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.
Highlights
Agricultural food production has continuously been challenged by the advent of newly host-adapted and more aggressive insect biotypes infesting crop species or specific plant genotypes, frequently promoted by predominant agricultural monocultivation, excessive pesticide use, and ongoing climate change, which favored rapid insect development and its reproduction rates [1,2,3].Grape phylloxera (Daktulosphaira vitifoliae fitch) is an aphid-like insect belonging to the Phylloxeridae family within the Hemiptera order [4,5,6]
We report the identification of differentially expressed genes (DEGs) putatively (1) involved in chemoreception and host infestation processes of L1 larvae and (2) DEGs coding for putative effector candidates secreted by L2-3 larvae, some of which are discussed to play a role for the grape phylloxera–Vitis interaction belowground
We identified 7 chemosensory proteins (DV3001980.2, DV3017123.2, DV3001978.2, DV3016484.2, DV3001983.2, DV3009938, DV3009939.2), 8 odorant-binding proteins (DV3020915.2, DV3023216.2, DV3004694.2, DV3005502.2, DV3008378.2, DV3000727.2, DV3013036.2), 3 ionotropic receptors (DV3001676, DV3001936, DV3006519), 15 odorant receptors (DV3018907.2, DV3017121.2, DV3024799.2, DV3025425.1, DV3025426.1, DV3010064.1, DV3021889.2, DV3024733.2, DV3018024.2, DV3012981.2, DV3001698, DV3022346.2, DV3022485.2, DV3003121.2, DV3001559.2), and 1 gustatory receptor (DV3007685.1) expressed higher by the L1 larvae of both biotypes (Figure 3b) following the gene annotation provided by the grape phylloxera genome [44]
Summary
Agricultural food production has continuously been challenged by the advent of newly host-adapted and more aggressive insect biotypes infesting crop species or specific plant genotypes, frequently promoted by predominant agricultural monocultivation, excessive pesticide use, and ongoing climate change, which favored rapid insect development and its reproduction rates [1,2,3].Grape phylloxera (Daktulosphaira vitifoliae fitch) is an aphid-like insect belonging to the Phylloxeridae family within the Hemiptera order [4,5,6]. The insect feeds monophagously on Vitis spp. host plants by imbibing the cellular content retrieved from the nutritive organoid root or histoid leaf galls [8,9,10]. Motile grape phylloxera L1 larvae move and probe Vitis spp. root tips in order to select suitable host plants and feeding sites for the root gall establishment [22]. This interaction is well studied, many aspects of the molecular background of grape phylloxera–root interaction remain unknown. The larval ability to overcome primary and secondary host defense barriers plays a critical role early in the compatible host–parasite interaction [17,23,24]
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