A Gene Family Coding for Salivary Proteins (SHOT) of the Polyphagous Spider Mite Tetranychus urticae Exhibits Fast Host-Dependent Transcriptional Plasticity

Abstract

The salivary protein repertoire released by the herbivorous pest Tetranychus urticae is assumed to hold keys to its success on diverse crops. We report on a spider mite-specific protein family that is expanded in T. urticae. The encoding genes have an expression pattern restricted to the anterior podocephalic glands, while peptide fragments were found in the T. urticae secretome, supporting the salivary nature of these proteins. As peptide fragments were identified in a host-dependent manner, we designated this family as the SHOT (secreted host-responsive protein of Tetranychidae) family. The proteins were divided in three groups based on sequence similarity. Unlike TuSHOT3 genes, TuSHOT1 and TuSHOT2 genes were highly expressed when feeding on a subset of family Fabaceae, while expression was depleted on other hosts. TuSHOT1 and TuSHOT2 expression was induced within 24 h after certain host transfers, pointing toward transcriptional plasticity rather than selection as the cause. Transfer from an 'inducer' to a 'noninducer' plant was associated with slow yet strong downregulation of TuSHOT1 and TuSHOT2, occurring over generations rather than hours. This asymmetric on and off regulation points toward host-specific effects of SHOT proteins, which is further supported by the diversity of SHOT genes identified in Tetranychidae with a distinct host repertoire.

The Digestive System of the Two-Spotted Spider Mite, Tetranychus urticae Koch, in the Context of the Mite-Plant Interaction

“…In addition, digestive enzymes (e.g. cathepsins, serine proteases, glycoside hydrolases, beta-galactosidases, and beta-mannosidases) together with proteins of unknown functions were identified in TSSM salivary secretions (Jonckheere et al, 2016 , 2018 ). Thus, TSSM feeding is associated with partial digestion and decomposition of plant structures, and the presence of TSSM-secreted proteins, generating a rich source of potential Damage and Herbivory Associated Molecular Patterns (DAMPs and HAMPs), some of which can act as elicitors of plant defenses.…”

Can Plant Defence Mechanisms Provide New Approaches for the Sustainable Control of the Two-Spotted Spider Mite Tetranychus urticae?

“…Whether successful mite adaptation to the host depends on phytoalexin detoxification or on host manipulation is still a matter of debate [ 77 ]. Although effector proteins from T. urticae are still under study, a very recent discovery demonstrates the enormous plasticity of the mite to modify the protein content of its saliva, which changes the composition depending on the host plant [ 93 ].…”

Why Do Herbivorous Mites Suppress Plant Defenses?

“…Thus, in addition to differences in the amino acid sequences between orthologous effectors of non-adapted T. urticae and specialist T. evansi , there are probably also differences at the effector abundance level. Something similar was observed for the spider mite-specific SHOT gene family, which is thought to encode effector proteins ( Jonckheere et al, 2017 ). The genome of generalist T. urticae contains 12 SHOT paralogs while Solanaceae-specialist T. evansi possess only one ortholog and the Fabaceae-specialist Tetranychus lintearius only two ( Jonckheere et al, 2017 ).…”