A calcium-dependent BAK1-GLR-TPC1-CBP60g-ICS1 module underlies salicylic acid accumulation during whitefly (Bemisia tabaci) feeding in Arabidopsis.

Abstract

INTRODUCTION: Piercing-sucking insects such as whiteflies trigger salicylic acid (SA)-mediated defenses despite causing minimal tissue damage. Although SA accumulation is a hallmark of plant responses to these herbivores, the upstream signaling mechanisms linking insect perception to SA biosynthesis remain poorly understood, particularly in the context of herbivore-associated molecular patterns (HAMPs) and calcium signaling. OBJECTIVES: This study aims to elucidate the molecular pathway connecting whitefly feeding to SA accumulation, focusing on the roles of calcium signaling components, transcriptional regulators, and SA biosynthetic enzymes. METHODS: Using Arabidopsis thaliana, we combined genetic, molecular, and biochemical approaches. SA levels and gene expression were quantified in wild-type and mutant lines (sid2-2, sid2, cbp60g, sard1, bak1, glr3.3/3.6, tpc1) following whitefly infestation. Calcium dynamics were monitored using aequorin-based reporters. Insect performance assays were conducted to evaluate plant resistance. RESULTS: Whitefly feeding significantly induced SA accumulation and PR1 expression in wild-type plants. This response depended on ISOCHORISMATE SYNTHASE 1 (ICS1), as sid2 mutants failed to accumulate SA. The transcription factor CALMODULIN-BINDING PROTEIN 60 g (CBP60g) positively regulates ICS1 expression and SA production. Furthermore, calcium signaling components, including BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED RECEPTOR KINASE 1 (BAK1), GLUTAMATE RECEPTOR-LIKE 3.3 and 3.6 (GLR3.3/GLR3.6), and TWO-PORE CHANNEL 1 (TPC1), were required for full activation of ICS1 expression and SA accumulation. Mutations in these components impaired defense responses and enhanced whitefly performance. Collectively, these elements form a signaling module linking insect perception to SA biosynthesis. CONCLUSION: We identified a BAK1-GLR-TPC1-CBP60g-ICS1 signaling module governing SA accumulation upon whitefly feeding. This pathway highlights the central role of calcium signaling in transducing insect feeding-associated signals into phytohormone defense responses. Our work provides new insights into plant-insect interactions and identifies conserved signaling nodes that can be exploited as molecular targets for breeding or engineering crops with stronger resistance to piercing-sucking pests.

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