Endophytic yeast protect plants against metal toxicity by inhibiting plant metal uptake through an ethylene‐dependent mechanism

• Published in: Plant, cell and environment cell and environment, 2023-01, Vol.46 (1), p.268-287
• Main Authors: Domka, Agnieszka, Jędrzejczyk, Roman, Ważny, Rafał, Gustab, Maciej, Kowalski, Michał, Nosek, Michał, Bizan, Jakub, Puschenreiter, Markus, Vaculίk, Marek, Kováč, Ján, Rozpądek, Piotr
• Format: Article
• Language: English
• Subjects: Aquatic plants; Cadmium; Defective mutant; Endophytes; Ethylene; Gene expression; Genes; growth; heavy metals; Homeostasis; hormones; Iron; metal toxicity; Metals; Microorganisms; Mutation; Nickel; Original; Phenotypes; Plant metabolism; Protected plants; Saccharomyces cerevisiae; Signaling; symbiosis; Toxicity; Yeasts
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14473

Toxic metal pollution requires significant adjustments in plant metabolism. Here, we show that the plant microbiota plays an important role in this process. The endophytic Sporobolomyces ruberrimus isolated from a serpentine population of Arabidopsis arenosa protected plants against excess metals. Coculture with its native host and Arabidopsis thaliana inhibited Fe and Ni uptake. It had no effect on host Zn and Cd uptake. Fe uptake inhibition was confirmed in wheat and rape. Our investigations show that, for the metal inhibitory effect, the interference of microorganisms in plant ethylene homeostasis is necessary. Application of an ethylene synthesis inhibitor, as well as loss‐of‐function mutations in canonical ethylene signalling genes, prevented metal uptake inhibition by the fungus. Coculture with S. ruberrimus significantly changed the expression of Fe homeostasis genes: IRT1, OPT3, OPT6, bHLH38 and bHLH39 in wild‐type (WT) A. thaliana. The expression pattern of these genes in WT plants and in the ethylene signalling defective mutants significantly differed and coincided with the plant accumulation phenotype. Most notably, down‐regulation of the expression of IRT1 solely in WT was necessary for the inhibition of metal uptake in plants. This study shows that microorganisms optimize plant Fe and Ni uptake by fine‐tuning plant metal homeostasis. Summary statement The symbiotic basidiomycete yeast Sporobolomyces ruberrimus protected plants against excess metals through specific inhibition of Fe and Ni uptake. Downregulation of the expression of Iron Regulated Transporter 1 was necessary for metal uptake inhibition in plants inoculated with S. ruberrimus.