ROS signaling in the hypersensitive response: when, where and what for?

Abstract

Plants generally react to the attack of non-host and incompatible host microorganisms by inducing pathogenesis-related (PR) genes and localised cell death (LCD) at the site of infection, a process collectively known as the hypersensitive response (HR). Reactive oxygen species (ROS) are generated in various sub-cellular compartments shortly after pathogen recognition, and proposed to cue subsequent orchestration of the HR. Although apoplast-associated ROS production by plasma membrane NADPH oxidases have been most thoroughly studied, recent observations suggest that ROS are generated in chloroplasts earlier in the response and play a key role in execution of LCD. A model is presented in which the initial outcome of successful pathogen detection is ROS accumulation in plastids, likely mediated by mitogen-activated protein kinases and caused by dysfunction of the photosynthetic electron transport chain. ROS signaling is proposed to spread from plastids to the apoplast, through the activation of NADPH oxidases, and from there to adjacent cells, leading to suicidal death in the region of attempted infection.

Figure 1

Schematic diagram of ROS signaling for the LCD associated to the HR in a plant-pathogen interaction. (A) Recognition of an invading pathogen triggers light-dependent ROS production in chloroplasts. Chloroplast-generated ROS then signal for further ROS production in the apoplast by directly or indirectly activating RboH-type NADPH oxidases, which are involved in propagation of the signal to adjacent cells. There is also a relay of information to the nucleus and mitochondria. Altogether, the different signaling factors lead to the establishment of LCD. (B) Flavodoxin (Fld) expression in chloroplasts specifically blocks ROS generation in this organelle, delaying the appearance of LCD symptoms. This experimental evidence supports the central role played by chloroplasts in the signaling pathways for HR-associated LCD.