Cytoplasmic regulation of chloroplast ROS accumulation during effector-triggered immunity

Abstract

Accumulating evidence suggests that chloroplasts are an important battleground during various microbe-host interactions. Plants have evolved layered strategies to reprogram chloroplasts to promote de novo biosynthesis of defense-related phytohormones and the accumulation of reactive oxygen species (ROS). In this minireview, we will discuss how the host controls chloroplast ROS accumulation during effector-triggered immunity (ETI) at the level of selective mRNA decay, translational regulation, and autophagy-dependent formation of Rubisco-containing bodies (RCBs). We hypothesize that regulation at the level of cytoplasmic mRNA decay impairs the repair cycle of photosystem II (PSII) and thus facilitates ROS generation at PSII. Meanwhile, removing Rubisco from chloroplasts potentially reduces both O₂ and NADPH consumption. As a consequence, an over-reduced stroma would further exacerbate PSII excitation pressure and enhance ROS production at photosystem I.

Keywords: Rubisco-containing body (RCB); cotranslational mRNA decay; effector-triggered immunity (ETI); mRNA decay; reactive oxygen species (ROS).

Figure 1

Schematic representations of possible cytoplasmic regulatory mechanisms of cROS accumulation during ETI. ETI activation might trigger both translation-dependent and -independent mRNA decay to actively degrade photosynthetic transcripts. 1) Translation-independent mRNA decay is initiated with CCR4-NOT complex-mediated deadenylation. After 5’ decapping, further degradation is carried out by either 5’-3’ or 3’-5’ decay mediated by XRN or exosome, respectively. 2) Translation-dependent mRNA decay can only occur through XRN-mediated 5’-3’ decay. Bulk mRNA decay of photosynthetic transcripts impairs the repair or turnover cycle of photosynthetic complexes, mainly PSII, resulting in ¹O₂ and OH^• production from damaged PSII, indicated by a red x. 3) NLR activation triggers autophagy-dependent formation of Rubisco-containing body (RCB) through which Rubisco as well as other stroma proteins are delivered into the vacuole for degradation. Removal of Rubisco may cause stroma overreduction and/or reduce O₂ consumption, which facilitates electron leakage from PSI as well as cytochrome b₆f complex (Cyt b₆f) to O₂, resulting in O₂ ^•- formation at both stroma side and inside thylakoid lumen. Other cytoplasmic mechanisms might also contribute to cROS accumulation during ETI.