Complexity of responses to ionizing radiation in plants, and the impact on interacting biotic factors

In nature, plants are simultaneously exposed to different abiotic (e.g., heat, drought, and salinity) and biotic (e.g., bacteria, fungi, and insects) stresses. Climate change and anthropogenic pressure are expected to intensify the frequency of stress factors. Although plants are well equipped with unique and common defense systems protecting against stressors, they may compromise their growth and development for survival in such challenging environments. Ionizing radiation is a peculiar stress factor capable of causing clustered damage. Radionuclides are both naturally present on the planet and produced by human activities. Natural and artificial radioactivity affects plants on molecular, biochemical, cellular, physiological, populational, and transgenerational levels. Moreover, the fitness of pests, pathogens, and symbionts is concomitantly challenged in radiologically contaminated areas. Plant responses to artificial acute ionizing radiation exposure and laboratory-simulated or field chronic exposure are often discordant. Acute or chronic ionizing radiation exposure may occasionally prime the defense system of plants to better tolerate the biotic stress or could often exhaust their metabolic reserves, making plants more susceptible to pests and pathogens. Currently, these alternatives are only marginally explored. Our review summarizes the available literature on the responses of host plants, biotic factors, and their interaction to ionizing radiation exposure. Such systematic analysis contributes to improved risk assessment in radiologically contaminated areas.