Insights into ROS‐dependent signalling underlying transcriptomic plant responses to the herbicide 2,4‐D

• Published in: Plant, cell and environment cell and environment, 2022-02, Vol.45 (2), p.572-590
• Main Authors: Romero‐Puertas, María C., Peláez‐Vico, Maria Ángeles, Pazmiño, Diana M., Rodríguez‐Serrano, María, Terrón‐Camero, Laura, Bautista, Rocío, Gómez‐Cadenas, Aurelio, Claros, M. Gonzalo, León, José, Sandalio, Luisa M.
• Format: Article
• Language: English
• Subjects: 2,4-Dichlorophenoxyacetic Acid - adverse effects; Acetic acid; Acyl‐CoA oxidase; Arabidopsis - drug effects; Arabidopsis - physiology; auxin; Auxins; Biodegradation; Biosynthesis; Chloroplasts; Coenzyme A; Cullin; Degradation; Dichlorophenoxyacetic acid; Epinasty; Herbicides; Herbicides - adverse effects; Indoleacetic acid; Mitochondria; Organelles; Oxidase; peroxisomes; Phenotypes; Plant growth; Proteasome 26S; Reactive oxygen species; Reactive Oxygen Species - metabolism; Signal Transduction - drug effects; Signaling; transcriptome; Transcriptome - drug effects; Transcriptomics; Ubiquitin; Ubiquitin-protein ligase; Weed control
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14229

The synthetic auxin 2,4‐dichlorophenoxyacetic acid (2,4‐D) functions as an agronomic weed control herbicide. High concentrations of 2,4‐D induce plant growth defects, particularly leaf epinasty and stem curvature. Although the 2,4‐D triggered reactive oxygen species (ROS) production, little is known about its signalling. In this study, by using a null mutant in peroxisomal acyl CoA oxidase 1 (acx1‐2), we identified acyl‐coenzyme A oxidase 1 (ACX1) as one of the main sources of ROS production and, in part, also causing the epinastic phenotype following 2,4‐D application. Transcriptomic analyses of wild type (WT) plants after treatment with 2,4‐D revealed a ROS‐related peroxisomal footprint in early plant responses, while other organelles, such as mitochondria and chloroplasts, are involved in later responses. Interestingly, a group of 2,4‐D‐responsive ACX1‐dependent transcripts previously associated with epinasty is related to auxin biosynthesis, metabolism, and signalling. We found that the auxin receptor auxin signalling F‐box 3 (AFB3), a component of Skp, Cullin, F‐box containing complex (SCF) (ASK‐cullin‐F‐box) E3 ubiquitin ligase complexes, which mediates auxin/indole acetic acid (AUX/IAA) degradation by the 26S proteasome, acts downstream of ACX1 and is involved in the epinastic phenotype induced by 2,4‐D. We also found that protein degradation associated with ubiquitin E3‐RING and E3‐SCF‐FBOX in ACX1‐dependent signalling in plant responses to 2,4‐D is significantly regulated over longer treatment periods. Summary Statement 2,4‐D induced a reactive oxygen species (ROS)‐related peroxisomal footprint in early plant responses. ACX1 is one of the main sources of ROS production and associated epinasty phenotype following 2,4‐D application in plants. ACX1‐dependent signalling in plant responses to 2,4‐D point to protein degradation associated with auxin signalling at the early response and with ubiquitin E3‐RING and E3‐SCF‐FBOX/proteasome as key processes in the development of epinasty over longer treatment periods.