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

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.

Effect of temperature on host plant‐specific leaf‐ and root‐feeding performances: a comparison of grape phylloxera biotypes C and G

“…This may explain why B6 only performs well on RR ( V. vinifera ) when temperatures are moderate; the acquired ability to infest the leaves of V. vinifera more successfully than other biotypes may have led to an increased metabolic energy demand. In a recent study on the grape phylloxera transcriptome, 44% more differentially expressed genes were upregulated during root‐feeding on RR by a V. vinifera ‐adapted biotype, compared to root‐feeding on 5C by a rootstock‐adapted biotype (Savoi et al., 2020). These differences were especially pronounced among effector candidates, of which twice as many differentially expressed genes were upregulated when infesting RR, compared to 5C.…”

Comparative study of neuropeptide signaling systems in Hemiptera

“…Transcriptome data of D. vitifoliae were obtained from the Sequence Read Archive (SRA) database (https://www.ncbi.nlm.nih.gov/sra/, accession numbers: SRX7222761-SRX7222771). These data include L1 (probing) and L2-3 (feeding) larvae of 2 D. vitifoliae lineages feeding on the V. vinifera Riesling (biotype A) and rootstock Teleki 5C (biotype C) (Savoi et al, 2020). In detail, D. vitifoliae eggs were sampled, and after 3 d, 800 hatched L1 larvae (N = 3 for biotype C; N = 2 for biotype A) were collected per sample.…”

“…Larval stages L2 and L3 correspond to 2-7 and 8-13 d after infestation. In total, 80 L2 and 3 larvae per sample (n = 3) were detached (Savoi et al, 2020).…”

“…, 2019; Savoi et al. , 2020). Here, we identified neuropeptides and their corresponding receptors in D. vitifoliae and analyzed their expression levels during host selection.…”

Grape Phylloxera Genetic Structure Reveals Root–Leaf Migration within Commercial Vineyards

“…We thus see that successful colonization does not appear homogeneously in all four vineyard settings and seem to depend on the presence of phylloxera populations in and around the vineyard and the planted grape varieties. In a recent study on the transcriptome of two phylloxera lines with a host adaption to different Vitis spp., it was seen that each phylloxera line transcribed different olfactory genes in the search for a feeding spot [46]. Whether phylloxera larvae actively use this ability to migrate between the different grapevine species in a vineyard setting or if this occurs through random dispersal is still unknown (cf.…”