Plant growth‐promoting archaea trigger induced systemic resistance in Arabidopsis thaliana against Pectobacterium carotovorum and Pseudomonas syringae

Abstract

Summary Archaea have inhabited the earth for a long period of time and are ubiquitously distributed in diverse environments. However, few studies have focused on the interactions of archaea with other organisms, including eukaryotes such as plants, since it is difficult to cultivate sufficient numbers of archaeal cells for analysis. In this study, we investigated the interaction between soil archaea and Arabidopsis thaliana. We demonstrate for the first time that soil archaea promote plant growth and trigger induced systemic resistance (ISR) against the necrotrophic bacterium Pectobacterium carotovorum subsp. carotovorum SCC1 and biotrophic bacterium Pseudomonas syringae pv. tomato DC3000. Ammonia‐oxidizing archaeon Nitrosocosmicus oleophilus MY3 cells clearly colonized the root surface of Arabidopsis plants, and increased resistance against both pathogenic species via the salicylic acid‐independent signalling pathway. This mechanism of bacterial resistance resembles that underlying soil bacteria‐ and fungi‐mediated ISR signalling. Additionally, volatile emissions from N. oleophilus MY3 were identified as major archaeal determinants that elicit ISR. Our results lay a foundation for archaea–plant interactions as a new field of research.

Archaea, tiny helpers of land plants

“…How do we know that archaea directly interact with plants and are not simply present in the rhizosphere? Previous study found archaeal cells exclusively colonizing and multiplying in plant roots without any soil components [18] , [21] . In the absence of plants, no growth of these cells was detected.…”

“…This suggests that archaea might help plants adapt to abiotic stresses such as heavy metal contamination, high salinity, and high temperature [16] , [17] . There is evidence that archaea are also involved in enhancing plant immune responses, such as triggering induced systemic resistance to pathogenic bacteria in Arabidopsis [18] .…”

“…There are some studies that archaea are also considered as plant growth-promoting archaea (PGPA). For example, Nitrosocosmicus oleophilus MY3 cells promote Arabidopsis growth by oxidizing N into plant-bioavailable forms [18] ( Table 1 ). Some halophilic archaea isolated from marine salterns around the Bhavnagar coast showed functional signatures of P siderophore production [9] ( Table 1 ).…”

Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application

“…Although most microbiome studies take into account bacteria and fungi, other microorganisms are also present in soil and could interact, symbiotically or antagonistically, with plants. For example, a recently isolated ammonia-oxidizing archaeon can promote the growth of Arabidopsis and induce systemic resistance against necrotrophic and biotrophic bacteria ( Jung et al, 2016 ; Song et al, 2019 ). Indeed, archaea are important players in plants (e.g.…”

Genomic insights into the Archaea inhabiting an Australian radioactive legacy site

“…[10] and can even induce systemic resistance to pathogens in plants [11]; Euryarchaeota capable of 62 anaerobic oxidation of methane (AOM) may consume up to 80-90% of the methane produced in 63 6 v1.2 [23] and tree build with IQ-TREE v1.5.5 under the recommended model (LG+R10) and 10,000 110 ultrafast bootstrap replicates [26]. 111 Functional annotation 112 In addition to arCOGs, predicted proteomes were profiled with InterProScan v5.25-64.0 [29].…”