The insect effector CSPs activate an atypical plant TNL immune receptor.

Authors

Weiwei Rao, Tianzhu Li, Jing Yang, Liwen Zhu, Wei Zhao, Tingting Ma

Published in

Plant cell reports. Volume 45. Issue 10. Sep 13, 2026. Epub Sep 13, 2026.

Abstract

CSP-mediated activation of RCSP involves noncanonical structural and catalytic mechanisms-including BB-loop deletion, α5α6-loop insertion, and atypical catalytic residues within the RCSP-TIR domain. Chemosensory proteins (CSPs), a conserved effector family in phloem-feeding insects such as aphids and the brown planthopper (Nilaparvata lugens), induce dwarfism in Nicotiana benthamiana through recognition by the Toll-interleukin-1 receptor (TIR) domain-containing nucleotide-binding leucine-rich repeat receptor (TNL) RCSP. However, CSP-mediated RCSP activation and enzymatic mechanism remain unknown. Here, we show that TIR domain of RCSP (RCSP-TIR) exhibits unique features, including a 9-amino acid deletion in the loop between β-strand B and α-helix B (BB-loop), an 8-amino acid insertion in the loop between α5 and α6 (α5α6-loop), and substitution of the canonical catalytic glutamate with glutamine (E87Q). Structural analysis demonstrates that BB-loop deletion disrupts the canonical NAD⁺-binding pocket and prevents standard TIR tetramerization. Strikingly, AlphaFold3/DMFold modeling reveals that RCSP compensates via α5α6-loop insertion, forming a novel interface that stabilizes an atypical tetrameric architecture. Integrated approaches combining molecular docking and site-directed mutagenesis demonstrate that RCSP may utilize a noncanonical NAD⁺-binding pocket and depend on dual catalytic residues (D86/Q87) to mediate weak cell death. Evolutionary analysis classifies RCSP-TIR homologs into four distinct clades, highlighting Solanaceae-specific adaptations. These findings elucidate a novel plant-insect interaction mechanism in which RCSP's structural diversification enables CSPs recognition and immune signaling reprogramming.

PMID:
42732488
Bibliographic data and abstract were imported from PubMed on 14 Sep 2026.

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