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Reactive oxygen species signalling in plant stress responses

Abstract

Reactive oxygen species (ROS) are key signalling molecules that enable cells to rapidly respond to different stimuli. In plants, ROS play a crucial role in abiotic and biotic stress sensing, integration of different environmental signals and activation of stress-response networks, thus contributing to the establishment of defence mechanisms and plant resilience. Recent advances in the study of ROS signalling in plants include the identification of ROS receptors and key regulatory hubs that connect ROS signalling with other important stress-response signal transduction pathways and hormones, as well as new roles for ROS in organelle-to-organelle and cell-to-cell signalling. Our understanding of how ROS are regulated in cells by balancing production, scavenging and transport has also increased. In this Review, we discuss these promising developments and how they might be used to increase plant resilience to environmental stress.

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Fig. 1: Regulation of ROS metabolism and signalling in plants.
Fig. 2: Production and scavenging of ROS in different compartments in plants during stress.
Fig. 3: Mechanisms of ROS and redox sensing in plants.
Fig. 4: Integration of ROS signals in plant cells.
Fig. 5: ROS in early and late responses of plants to stress.
Fig. 6: Integration of ROS signalling with stress-response networks in plants and transcriptional regulation by H2O2 during stress.
Fig. 7: Propagation of ROS signals within and between cells.

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Acknowledgements

The authors apologize to the many authors whose important work could not be referred to. This work was supported by funding from the US National Science Foundation (IOS-2110017, IOS-1353886, MCB-1936590 and IOS-1932639), The US National Institutes of Health (GM111364), the Interdisciplinary Plant Group, University of Missouri, Research Foundation — Flanders (project G0D7914N) and the Excellence of Science Research project 30829584.

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R.M., S.I.Z., Y.F. and F.V.B. wrote the Review, designed the figures and approved the final version of the manuscript.

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Correspondence to Ron Mittler.

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Glossary

Acclimatization

Also referred to as ‘acclimation’, a process by which plants adjust their metabolism, physiology and biochemistry to become accustomed to changes in their growth conditions or environment.

Aquaporins

(AQPs). Transmembrane water channel proteins that allow the diffusion of H2O2 from one side of the membrane to the other in a regulated manner.

Photosystems I and II

Multiprotein complexes that reside on the thylakoid membranes inside chloroplasts and participate in the harvesting of light energy for the purpose of CO2 fixation and sugar biosynthesis.

Photorespiration

A biochemical pathway that results in the accumulation of H2O2 in peroxisomes, triggered when CO2 concentrations are limited in C3 plants.

C3 plants

A large group of plants in which the initial product of the assimilation of CO2 through photosynthesis is 3-phosphoglycerate, which contains three carbon atoms.

Stomata

Specialized pore structures found in the epidermal layer of plants and used for gas exchange with the atmosphere.

Nucleophilic attack

Attack of an electron-rich species (the nucleophile) on an electron-deficient species (the electrophile), forming a new bond between the nucleophile and the electrophile.

Yap1

A redox-regulated transcription factor that is essential for yeast survival under conditions of oxidative stress.

Type 2C serine/threonine protein phosphatase 2A

(PP2A). A family of phosphatases that generally function as negative regulators of different stress responses in plants and are inhibited by reactive oxygen species-induced redox reactions.

Dicer proteins

Endoribonucleases that cleave double-stranded RNA and pre-microRNAs into short double-stranded RNA fragments such as small interfering RNA and microRNA.

Brassinosteroid

Member of a class of polyhydroxysteroids that function as plant hormones involved in many developmental processes and responses to stress.

Leucine-rich repeat receptor kinase

A large protein family in plants composed of a leucine-rich repeat-containing extracellular domain, a transmembrane domain and an intracellular kinase domain, involved in developmental processes and stress responses.

Quinones

A redox-active class of cyclic organic compounds containing two carbonyl groups, involved in many electron transport reactions and signalling processes.

EF-hand domains

Helix–loop–helix structural domains with an E and F structural orientation of the two α-helices, found in many calcium-binding proteins.

Stromules, peroxules and matrixules

Dynamic tubular membrane structures extending from the surface of chloroplasts, peroxisomes and mitochondria, respectively, used for the transport of signals between different organelles and the nucleus.

Salicylic acid

A phytohormone, characterized by an aromatic ring and a hydroxy group, involved in the response of plants to different biotic and abiotic stresses.

Plasmodesmata

Small channels or pores that transverse the plant cell walls connecting the cytoplasm and plasma membrane of neighbouring cells with each other, establishing metabolic and signalling bridges between cells.

Mediator complex

An important component of the eukaryotic transcriptional machinery, linking different transcription factors with RNA polymerase II.

Unfolded protein response

A cellular stress response pathway triggered by the presence of unfolded proteins inside the endoplasmic reticulum.

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Mittler, R., Zandalinas, S.I., Fichman, Y. et al. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol (2022). https://doi.org/10.1038/s41580-022-00499-2

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