The interplay between ROS and tubulin cytoskeleton in plants

Abstract

Plants have to deal with reactive oxygen species (ROS) production, since it could potentially cause severe damages to different cellular components. On the other hand, ROS functioning as important second messengers are implicated in various developmental processes and are transiently produced during biotic or abiotic stresses. Furthermore, the microtubules (MTs) play a primary role in plant development and appear as potent players in sensing stressful situations and in the subsequent cellular responses. Emerging evidence suggests that ROS affect MTs in multiple ways. The cellular redox status seems to be tightly coupled with MTs. ROS signals regulate the organization of tubulin cytoskeleton and induce tubulin modifications. This review aims at summarizing the signaling mechanisms and the key operators orchestrating the crosstalk between ROS and tubulin cytoskeleton in plant cells. The contribution of several molecules, including microtubule associated proteins, oxidases, kinases, phospholipases, and transcription factors, is highlighted.

Keywords: antioxidants; macrotubules; microtubules; oxidative stress; reactive oxygen species; redox sensing; tubulin paracrystals.

Figure 1. The disturbance of reactive oxygen species (ROS) homeostasis affects tubulin cytoskeleton organization in transgenic Arabidopsis plants expressing GFP:TUA6. (A-E): Epidermal cells from 4-d-old hypocotyls of seedlings treated with distilled water (A) or with ROS modulators (B-E). The decrease of ROS levels forced either by the NADPH oxidase inhibitor diphenylene iodonium (DPI) or by the ROS scavenger n-acetyl-cysteine (NAC) results in disruption and reorganization of the tubulin cytoskeleton into random mesh-like arrays (B, C; cf. A). Similarly, oxidative stress induced by the oxidizing agent menadione (MEN) and hydrogen peroxide (Η₂Ο₂) results in MT remodeling (D, Ε; cf. A). CONTR, distilled water; DPI, 50 μΜ; ΝΑC, 500 μΜ; ΜΕΝ, 50 μΜ, Η₂Ο₂, 5 mM. Treatments: 2 h. Scale bar: 10 μm.

Figure 2. Simplified hypothetical model describing the changes mediated by reactive oxygen species (ROS) level alteration with respect to the organization of tubulin cytoskeleton. ROS and antioxidant balance is further influenced by abiotic or biotic stimuli. In any case, the ROS produced in the apoplast (e.g., derived from NADPH oxidase) enter the cytosol and together with intracellularly generated ROS constitute the total amount of cellular ROS. Consequently, the result of the tag war between oxidant generation and antioxidant defenses is perceived and either directly or through feedback connected signaling cascades forces the reorganization of tubulin cytoskeleton. The reorganization among others aids the restoration of ROS homeostasis. The microtubule (MT) arrays disappear and MT remodeling, or the assembly of atypical tubulin polymers like macrotubules and tubulin paracrystals, follows. These processes are mediated by MT-associated proteins (MAPs) assisted by other molecules such as phosphatidic acid produced by phospholipase D (PLD). The modifications of tubulin or MAPs at the post-translational level may crucially contribute to this interplay.