Iron homeostasis and plant immune responses: Recent insights and translational implications

Abstract

Iron metabolism and the plant immune system are both critical for plant vigor in natural ecosystems and for reliable agricultural productivity. Mechanistic studies of plant iron home-ostasis and plant immunity have traditionally been carried out in isolation from each other; however, our growing understanding of both processes has uncovered significant connections. For example, iron plays a critical role in the generation of reactive oxygen intermediates during immunity and has been recently implicated as a critical factor for immune-initiated cell death via ferroptosis. Moreover, plant iron stress triggers immune activation, suggesting that sensing of iron depletion is a mechanism by which plants recognize a pathogen threat. The iron deficiency response engages hormone signaling sectors that are also utilized for plant immune signaling, providing a probable explanation for iron-immunity cross-talk. Finally, interference with iron acquisition by pathogens might be a critical component of the immune response. Efforts to address the global burden of iron deficiency-related anemia have focused on classical breeding and transgenic approaches to develop crops biofortified for iron content. However, our improved mechanistic understanding of plant iron metabolism suggests that such alterations could promote or impede plant immunity, depending on the nature of the alteration and the virulence strategy of the pathogen. Effects of iron biofortification on disease resistance should be evaluated while developing plants for iron biofortification.

Keywords: Arabidopsis thaliana; host-pathogen interaction; iron metabolism; metal homeostasis; oxygen radicals; plant defense; plant hormone.

Figure 1.

Iron's influence on immunity. A, iron uptake, transport, and storage in plants. Bottom, Fe is absorbed from the rhizosphere, loaded into the xylem, and transported via the vasculature from the root to the shoot (Strategy I is shown). Middle, in the shoot Fe is unloaded from the xylem to the mesophyll cell or the phloem for transport to other sinks. Top, inside cells Fe is transported into organelles for assimilation or to the cell wall or stored in vacuoles and ferritin complexes. B, tug of war between plants and pathogens for iron. Pathogens use varied mechanisms to scavenge plant iron during infection, whereas plants deploy mechanisms, such as iron-sequestering ferritin and defensins and disruption of Fe signaling, to interfere with pathogen iron scavenging. C, activation of immune responses by pathogens and by iron deficiency. PAMPs are recognized by plants to initiate PTI. PTI and iron deficiency initiate similar hormonal responses, and both activate resistance to pathogens. NO and ET buffer SA, modulating the response, and JA/ET act antagonistically to SA. D, perception of pathogen effectors triggers ferroptosis as a mechanism of HR cell death. ETI is initiated through R-protein–mediated recognition of effectors secreted by the pathogen. In the rice interaction with M. oryzae, the plant recruits iron-dependent cell death (ferroptosis) to trigger the HR and halt pathogen growth. Iron-derived ROS lead to runaway lipid peroxidization, as in mammalian ferroptosis.

Figure 2.

Biofortification of iron will influence plant immunity. In the Poaceae, iron is delivered to infection sites to facilitate the ROS burst. In rice, iron accumulates following ETI, leading to ferroptosis. In all plants, low iron availability, from microbial siderophores or iron-sequestering proteins, triggers immunity and the iron deficiency response. In biofortified plants, especially those with up-regulation of genes related to iron uptake and mobility, these responses may be altered. Additional iron at infection sites, could produce more ROS and a stronger ferroptotic HR. This might slow pathogen growth. However, additional iron may limit the plant's capacity to use low-iron status to trigger immunity and promote pathogen growth.