Repression of pattern-triggered immune responses by hypoxia

Abstract

AbstractCombined abiotic/biotic stresses frequently occur in nature. Yet, relatively little is known about how plants regulate the crosstalk between stress response pathways to trigger a coordinated response to combined stresses. Protein degradation by the ubiquitin/proteasome system (UPS) is central to the regulation of plant responses to multiple stresses, including the crosstalk between pathways. The Arg/N-degron pathway, a subset of the UPS, targets proteins based on their N-termini. In plants, it has been implicated in the responses to both biotic and abiotic stresses, while being a key regulator of hypoxia response through the degradation of ERF-VII transcription factors, which orchestrate the onset of the hypoxia response program. Because of its central position in regulating multiple (a)biotic stresses, we hypothesized that the Arg/N-degron pathway could act in the crosstalk between abiotic/biotic stresses. In exploring this possibility using the model pathogen-associated molecular pattern flg22 to elicit pattern-triggered immunity (PTI), we uncovered a link between the transcriptional response programs to hypoxia and to flg22. Combined hypoxia/flg22 treatments further showed that hypoxia represses the flg22 transcriptional program, as well as the expression of pattern recognition receptors, MAPK signalling and callose deposition during PTI, through mechanisms that are at least partly dependent on the ERF-VIIs. These findings are of relevance to understanding the trade-offs between plant responses to combined abiotic/biotic stresses in the context of our efforts to increase crop resilience to global climate change. Our results also show that the well-known repressive effect of hypoxia on innate immunity in animals also applies to plants.Significance statementUnderstanding how plants regulate the crosstalk between stress response pathways is key to our efforts to increase crop resilience and mitigate yield losses caused by global climate change. Despite the urgency to do so, relatively little remains known about how plants respond to combined stresses, which frequently occur in nature. Here, we show that the hypoxia response program and the basal layer of plant immunity (pattern-triggered immunity or PTI) share components. Our data also show that hypoxia represses several key aspects of the plant’s innate immune response, a situation akin to that discovered in animals decades ago. These findings have implications for our ability to develop resilient crops by limiting the negative trade-offs that exist between hypoxia response and immunity.