The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae

• Published in: Redox biology 2023-11, Vol.67, p.102902, Article 102902
• Main Authors: Arnaiz, Ana, Romero-Puertas, Maria C., Santamaria, M. Estrella, Rosa-Diaz, Irene, Arbona, Vicent, Muñoz, Alfonso, Grbic, Vojislava, González-Melendi, Pablo, Mar Castellano, M., Sandalio, Luisa Maria, Martinez, Manuel, Diaz, Isabel
• Format: Article
• Language: English
• Subjects: Animals; Arabidopsis - genetics; Homeostasis; Plants; Research Paper; Tetranychidae - genetics; Thioredoxins - genetics
• ISSN: 2213-2317; 2213-2317
• DOI: 10.1016/j.redox.2023.102902

The interaction between plants and phytophagous arthropods encompasses a complex network of molecules, signals, and pathways to overcome defences generated by each interacting organism. Although most of the elements and modulators involved in this interplay are still unidentified, plant redox homeostasis and signalling are essential for the establishment of defence responses. Here, focusing on the response of Arabidopsis thaliana to the spider mite Tetranychus urticae, we demonstrate the involvement in plant defence of the thioredoxin TRXh5, a small redox protein whose expression is induced by mite infestation. TRXh5 is localized in the cell membrane system and cytoplasm and is associated with alterations in the content of reactive oxygen and nitrogen species. Protein S-nitrosylation signal in TRXh5 over-expression lines is decreased and alteration in TRXh5 level produces changes in the JA/SA hormonal crosstalk of infested plants. Moreover, TRXh5 interacts and likely regulates the redox state of an uncharacterized receptor-like kinase, named THIOREDOXIN INTERACTING RECEPTOR KINASE (TIRK), also induced by mite herbivory. Feeding bioassays performed withTRXh5 over-expression plants result in lower leaf damage and reduced egg accumulation after T. urticae infestation than in wild-type (WT) plants. In contrast, mites cause a more severe injury in trxh5 mutant lines where a greater number of eggs accumulates. Likewise, analysis of TIRK-gain and -loss-of-function lines demonstrate the defence role of this receptor in Arabidopsis against T. urticae. Altogether, our findings demonstrate the interaction between TRXh5 and TIRK and highlight the importance of TRXh5 and TIRK in the establishment of effective Arabidopsis defences against spider mite herbivory. [Display omitted] •The thioredoxin TRXh5, besides other functions, is a key modulator of plant defences against the phytophagous spider mite Tetranychus urticae by affecting redox homeostasis and JA levels.•Arabidopsis plants with altered expression of TRXh5 have unbalanced amounts of H2O2 and NO, concomitantly to modifications of denitrosylation patterns of proteins, which correlate with changes in the susceptibility to mite attack and in mite behaviour.•TRXh5 interacts and denitrosylates the TIRK transmembrane receptor suggesting a new layer for redox-dependent regulation of this receptor depending on appropriate local environment.•The altered expression of TIRK also correlates with the plant susceptibility to