The Passage of H2O2 from Chloroplasts to Their Associated Nucleus during Retrograde Signalling: Reflections on the Role of the Nuclear Envelope

Abstract

The response of chloroplasts to adverse environmental cues, principally increases in light intensity, stimulates chloroplast-to-nucleus retrograde signalling, which leads to the induction of immediate protective responses and longer-term acclimation. Hydrogen peroxide (H2O2), generated during photosynthesis, is proposed to both initiate and transduce a retrograde signal in response to photoinhibitory light intensities. Signalling specificity achieved by chloroplast-sourced H2O2 for signal transduction may be dependent upon the oft-observed close association of a proportion of these organelles with the nucleus. In this review, we consider more precisely the nature of the close association between a chloroplast appressed to the nucleus and the requirement for H2O2 to cross both the double membranes of the chloroplast and nuclear envelopes. Of particular relevance is that the endoplasmic reticulum (ER) has close physical contact with chloroplasts and is contiguous with the nuclear envelope. Therefore, the perinuclear space, which transducing H2O2 molecules would have to cross, may have an oxidising environment the same as the ER lumen. Based on studies in animal cells, the ER lumen may be a significant source of H2O2 in plant cells arising from the oxidative folding of proteins. If this is the case, then there is potential for the ER lumen/perinuclear space to be an important location to modify chloroplast-to-nucleus H2O2 signal transduction and thereby introduce modulation of it by additional different environmental cues. These would include for example, heat stress and pathogen infection, which induce the unfolded protein response characterised by an increased H2O2 level in the ER lumen.

A novel glutathione peroxidase-based biosensor disentangles differential subcellular accumulation of H2O2 and lipid hydroperoxides

“…5C) suggests again a capacity for nuclei under stress to make H 2 O 2 or for it to be transferred from chloroplasts or elsewhere. The transfer of H 2 O 2 from photosynthetically active chloroplasts in close physical association with the nuclei in HL conditions was an important conclusion from a more comprehensive analysis conducted using the H 2 O 2 biosensor HyPer (Exposito-Rodriguez et al 2017; Mullineaux et al 2020; Breeze and Mullineaux 2022). However as stated above, the 3h DCMU treatment in in this study (Fig.…”

Redox Signaling in Plant Heat Stress Response

“…Stromules may also promote chloroplasts-to-nucleus contacts, transferring H 2 O 2 to the nucleus [ 138 ]. The close association between the endoplasmic reticulum (ER) with chloroplasts and nucleus has led to suppose that the ER may play a key role in mediating H 2 O 2 retrograde signaling in a double manner: amplifying the signal, generating more H 2 O 2 by a luminal ER oxidase, or attenuating it by activating antioxidant responses such as the ER glutathione peroxidase [ 139 ] ( Figure 1 ).…”

Coordination of Chloroplast Activity with Plant Growth: Clues Point to TOR

“…At the same time, ROS also play a signaling role and communicate the photosynthetic state to the plant cell by taking part in the operational retrograde signaling [ 18 , 19 ]. Hydrogen peroxide (H 2 O 2 ) has been reported to move directly from the chloroplasts to the nucleus and chloroplasts are often associated with the nucleus under stress conditions [ 18 , 20 ]. Singlet Oxygen can directly oxidize the proteins Executer 1 (EX1) and Executer 2 (EX2) and the equilibrium between the two oxidation modulates retrograde signaling [ 21 , 22 ].…”