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

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 homeos...

Full description

Bibliographic Details
Main Authors: Ana Arnaiz, Maria C. Romero-Puertas, M. Estrella Santamaria, Irene Rosa-Diaz, Vicent Arbona, Alfonso Muñoz, Vojislava Grbic, Pablo González-Melendi, M. Mar Castellano, Luisa Maria Sandalio, Manuel Martinez, Isabel Diaz
Format: Article
Language:English
Published: Elsevier 2023-11-01
Series:Redox Biology
Online Access:http://www.sciencedirect.com/science/article/pii/S2213231723003038
_version_ 1797647889346854912
author Ana Arnaiz
Maria C. Romero-Puertas
M. Estrella Santamaria
Irene Rosa-Diaz
Vicent Arbona
Alfonso Muñoz
Vojislava Grbic
Pablo González-Melendi
M. Mar Castellano
Luisa Maria Sandalio
Manuel Martinez
Isabel Diaz
author_facet Ana Arnaiz
Maria C. Romero-Puertas
M. Estrella Santamaria
Irene Rosa-Diaz
Vicent Arbona
Alfonso Muñoz
Vojislava Grbic
Pablo González-Melendi
M. Mar Castellano
Luisa Maria Sandalio
Manuel Martinez
Isabel Diaz
author_sort Ana Arnaiz
collection DOAJ
description 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.
first_indexed 2024-03-11T15:23:45Z
format Article
id doaj.art-6855586dad204d708b12e7394ef32e1f
institution Directory Open Access Journal
issn 2213-2317
language English
last_indexed 2024-03-11T15:23:45Z
publishDate 2023-11-01
publisher Elsevier
record_format Article
series Redox Biology
spelling doaj.art-6855586dad204d708b12e7394ef32e1f2023-10-28T05:07:14ZengElsevierRedox Biology2213-23172023-11-0167102902The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticaeAna Arnaiz0Maria C. Romero-Puertas1M. Estrella Santamaria2Irene Rosa-Diaz3Vicent Arbona4Alfonso Muñoz5Vojislava Grbic6Pablo González-Melendi7M. Mar Castellano8Luisa Maria Sandalio9Manuel Martinez10Isabel Diaz11Centro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, SpainDepartment of Biochemistry and Molecular and Cellular Biology of Plants, Estación Experimental del Zaidín, CSIC, Granada, Spain; Corresponding author.Centro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, SpainCentro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, SpainDepartament de Biologia, Bioquímica i Ciències Naturals, Universitat Jaume I, E-12071, Castelló de la Plana, SpainDepartamento de Sistemas y Recursos Naturales. Escuela Técnica Superior de Ingeniería de Montes, Forestal y del Medio Natural, UPM, Madrid, SpainDepartment of Biology, University of Western Ontario, N6A 5BT, London, Ontario, CanadaCentro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, Spain; Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, UPM, Madrid, SpainCentro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, SpainDepartment of Biochemistry and Molecular and Cellular Biology of Plants, Estación Experimental del Zaidín, CSIC, Granada, SpainCentro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, Spain; Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, UPM, Madrid, SpainCentro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, Spain; Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, UPM, Madrid, Spain; Corresponding author. Centro de Biotecnología y Genómica de Plantas (CBGP), Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/CSIC, Campus de Montegancedo, 20223, Madrid, Spain.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.http://www.sciencedirect.com/science/article/pii/S2213231723003038
spellingShingle Ana Arnaiz
Maria C. Romero-Puertas
M. Estrella Santamaria
Irene Rosa-Diaz
Vicent Arbona
Alfonso Muñoz
Vojislava Grbic
Pablo González-Melendi
M. Mar Castellano
Luisa Maria Sandalio
Manuel Martinez
Isabel Diaz
The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae
Redox Biology
title The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae
title_full The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae
title_fullStr The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae
title_full_unstemmed The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae
title_short The Arabidopsis thioredoxin TRXh5regulates the S-nitrosylation pattern of the TIRK receptor being both proteins essential in the modulation of defences to Tetranychus urticae
title_sort arabidopsis thioredoxin trxh5regulates the s nitrosylation pattern of the tirk receptor being both proteins essential in the modulation of defences to tetranychus urticae
url http://www.sciencedirect.com/science/article/pii/S2213231723003038
work_keys_str_mv AT anaarnaiz thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT mariacromeropuertas thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT mestrellasantamaria thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT irenerosadiaz thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT vicentarbona thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT alfonsomunoz thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT vojislavagrbic thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT pablogonzalezmelendi thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT mmarcastellano thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT luisamariasandalio thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT manuelmartinez thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT isabeldiaz thearabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT anaarnaiz arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT mariacromeropuertas arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT mestrellasantamaria arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT irenerosadiaz arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT vicentarbona arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT alfonsomunoz arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT vojislavagrbic arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT pablogonzalezmelendi arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT mmarcastellano arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT luisamariasandalio arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT manuelmartinez arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae
AT isabeldiaz arabidopsisthioredoxintrxh5regulatesthesnitrosylationpatternofthetirkreceptorbeingbothproteinsessentialinthemodulationofdefencestotetranychusurticae