Abstract

BackgroundAll eukaryotes share a conserved network of processes regulated by the proteasome and fundamental to growth, development, or perception of the environment, leading to complex but often predictable responses to stress. As a specialized component of the ubiquitin-proteasome system (UPS), the RING finger domain mediates protein-protein interactions and displays considerable versatility in regulating many physiological processes in plants. Many pathogenic organisms co-opt the UPS through RING-type E3 ligases, but little is known about how insects modify these integral networks to generate novel plant phenotypes.ResultsUsing a combination of transcriptome sequencing and genome annotation of a grapevine galling species, Daktulosphaira vitifoliae, we identified 138 putatively secretory protein RING-type (SPRINGs) E3 ligases that showed structure and evolutionary signatures of genes under rapid evolution. Moreover, the majority of the SPRINGs were more expressed in the feeding stage than the non-feeding egg stage, in contrast to the non-secretory RING genes. Phylogenetic analyses indicated that the SPRINGs formed clusters, likely resulting from species-specific gene duplication and conforming to features of arthropod host-manipulating (effector) genes. To test the hypothesis that these SPRINGs evolved to manipulate cellular processes within the plant host, we examined SPRING interactions with grapevine proteins using the yeast two-hybrid assay. An insect SPRING interacted with two plant proteins, a cellulose synthase, CSLD5, and a ribosomal protein, RPS4B suggesting secretion reprograms host immune signaling, cell division, and stress response in favor of the insect. Plant UPS gene expression during gall development linked numerous processes to novel organogenesis.ConclusionsTaken together, D. vitifoliae SPRINGs represent a novel gene expansion that evolved to interact with Vitis hosts. Thus, a pattern is emerging for gall forming insects to manipulate plant development through UPS targeting.

Highlights

  • All eukaryotes share a conserved network of processes regulated by the proteasome and fundamental to growth, development, or perception of the environment, leading to complex but often predictable responses to stress

  • Sequence homology searches (BLASTP) indicated that the secretory Really interesting new gene (RING) proteins mostly showed little to no sequence similarity to the known proteins deposited in the GenBank databases, in contrast to the non-secretory proteins, most of which were highly similar to known proteins

  • Compared to the non-secretory RING proteins that were most similar to their Aphididae homologs (104 top BLAST hit species are aphids), the secretory RING proteins were mostly similar to non-insect species (71 top hits), or specific to D. vitifoliae (40 top hits) based on an e-value = 1e-3 threshold (Fig. 2c)

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Summary

Introduction

All eukaryotes share a conserved network of processes regulated by the proteasome and fundamental to growth, development, or perception of the environment, leading to complex but often predictable responses to stress. As a specialized component of the ubiquitin-proteasome system (UPS), the RING finger domain mediates protein-protein interactions and displays considerable versatility in regulating many physiological processes in plants. The ubiquitin-proteasome system (UPS) is a major protein turnover pathway found across the domains of life, but is especially important in regulating almost all plant development and signaling pathways. Hormone-driven growth, ontogenetic change, and responses to stress represent key cellular processes controlled by ubiquitin mediated degradation [1,2,3]. RING containing genes interact with fungal and bacterial effectors to regulate hormone-mediated defense pathways [18, 19]

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