Immunity and bacterial recruitment in plant leaves are parallel processes whose link shapes sensitivity to temperature stress

Abstract

AbstractRising global temperatures necessitate developing climate-resilient crops with better adaptability to changing climates. Under elevated temperatures, plant immunity is downregulated, putting them at risk of foliar pathogen attack. Manipulating plant defense hormones is one way to mitigate this detrimental effect. However, it is unclear how plant immunity interacts with plant microbiome assembly and how temperature will thus affect overall plant health and stability. We used chemical mutagenesis to identify a phenotypically healthy genotype ofA. thaliana, “CLLF”,that compared to the wild type naturally recruits an altered leaf bacteriome, including unusually high bacteria loads. Simultaneously, CLLF hyperaccumulates salicylic acid (SA) and jasmonates, has constitutively upregulated systemic and innate defenses, and has increased resistance to necrotrophic fungal and hemi-biotrophic bacterial pathogens, indicating that pathogen immunity and non-pathogen recruitment function in parallel. Growth of specific non-pathogenic leaf bacteria on SA as a carbon source suggests the same hormones may even link the two processes. CLLF also showed high tolerance to heat stress in comparison to the wild type, but SA-associated defense processes are not downregulated under heat. Synthetic community (SynCom) experiments showed that when the taxonomic diversity of bacteria available to CLLF is artificially reduced, resilience to heat stress is compromised, leading to dysbiosis, but this does not occur with the full SynCom or in the wild type with any SynCom. Thus, the downregulation of defenses in response to heat may contribute to avoidance of dysbiosis caused by some leaf bacteria, but full bacteriome taxonomic diversity can restore balance.Significance StatementPlants are living ecosystems colonized by diverse microorganisms who strongly shape host health. Understanding how balance arises in host-associated microbiomes is a key step to understanding how to preserve, manage and possibly optimize these complex ecosystems, especially in a changing climate. Using a random mutagenesis approach in a naturalA. thalianaecotype, we find that constitutively upregulated defenses are associated with both tolerance to (a)biotic threats and healthy recruitment of leaf bacteria, very likely in a direct manner. Thus, immunity and bacterial recruitment in leaves operate in parallel. Synthetic community experiments show further that this link plays important roles in shaping plant resilience to heat stress, an important consideration in developing plants more stable to climate change.