Salivary Protein Cyclin-Dependent Kinase-like from Grain Aphid Sitobion avenae Suppresses Wheat Defense Response and Enhances Aphid Adaptation

Int J Mol Sci. 2024 Apr 23;25(9):4579. doi: 10.3390/ijms25094579.

Abstract

Aphids are insect pests that suck phloem sap and introduce salivary proteins into plant tissues through saliva secretion. The effector of salivary proteins plays a key role in the modulation of host plant defense responses and enhancing aphid host adaptation. Based on previous transcriptome sequencing results, a candidate effector cyclin-dependent kinase-like (CDK) was identified from the grain aphid Sitobion avenae. In this study, the function of SaCDK in wheat defense response and the adaptation of S. avenae was investigated. Our results showed that the transient overexpression of SaCDK in tobacco Nicotiana benthamiana suppressed cell death triggered by mouse pro-apoptotic protein-BAX or Phytophthora infestans PAMP-INF1. SaCDK, delivered into wheat cells through a Pseudomonas fluorescens-mediated bacterial type III secretion system, suppressed callose deposition in wheat seedlings, and the overexpression of SaCDK in wheat significantly decreased the expression levels of salicylic acid and jasmonic acid signaling pathway-related genes phenylalanine ammonia lyase (PAL), pathogenesis-related 1 protein (PR1), lipoxygenase (LOX) and Ω-3 fatty acid desaturase (FAD). In addition, aphid bioassay results showed that the survival and fecundity of S. avenae were significantly increased while feeding on the wheat plants carrying SaCDK. Taken together, our findings demonstrate that the salivary protein SaCDK is involved in inhibiting host defense response and improving its host adaptation, which lays the foundation to uncover the mechanism of the interaction of cereal aphids and host plants.

Keywords: Sitobion avenae; aphid adaptation; bacterial type III secretion system; defense response; salivary protein.

MeSH terms

  • Adaptation, Physiological
  • Animals
  • Aphids* / physiology
  • Cyclopentanes / metabolism
  • Gene Expression Regulation, Plant
  • Insect Proteins / genetics
  • Insect Proteins / metabolism
  • Nicotiana / genetics
  • Nicotiana / parasitology
  • Oxylipins
  • Plant Diseases / parasitology
  • Salivary Proteins and Peptides / genetics
  • Salivary Proteins and Peptides / metabolism
  • Triticum* / genetics
  • Triticum* / metabolism
  • Triticum* / parasitology

Substances

  • Salivary Proteins and Peptides
  • Insect Proteins
  • Cyclopentanes
  • jasmonic acid
  • Oxylipins