Repression of pattern-triggered immune responses by hypoxia

Abstract

Biotic and abiotic stresses frequently co-occur in nature, yet, relatively little is known about how plants co-ordinate the response to combined stresses. Previous research has shown that protein degradation by the ubiquitin/proteasome system is central to the regulation of multiple independent stress response pathways in plants. The Arg/N-degron pathway is a subset of the ubiquitin/proteasome system that targets proteins based on their N-termini and has been specifically implicated in the responses to biotic and abiotic stresses, including hypoxia via accumulation of ERF-VII transcription factors, which orchestrate the onset of the hypoxia response program. Here, we investigated the role of the Arg/N-degron pathway in mediating the crosstalk between coinciding abiotic and biotic stresses using hypoxia treatments and the flg22 elicitor of pattern-triggered immunity (PTI), respectively. We uncovered a link between the transcriptional responses of plants to hypoxia and flg22. Combined hypoxia/flg22 treatments 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 mostly independent from the ERF-VIIs. These findings aid understanding of 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 is 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 PTI, 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.