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

Abstract

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.

Mycobiota of Mexican Maize Landraces with Auxin-Producing Yeasts That Improve Plant Growth and Root Development

“…Siderophores can also bind other divalent or trivalent cations, such as Co, Cu, Zn, As, Cr, Pb, and Cd [ 42 ]. Siderophore-producing yeasts allow plant growth under metal stress [ 43 ]. These yeasts have been successfully applied as bioinoculants to assist phytoremediation processes in metal-contaminated soils [ 44 ].…”

Internal Transcribed Spacer and 16S Amplicon Sequencing Identifies Microbial Species Associated with Asbestos in New Zealand

“…Serpentinite and asbestos deposits are harsh environments for plants and microbial species, in part because they are nutrient-poor, have major cation imbalances, high pH (10–12), and high concentrations of phytotoxic trace elements, notably nickel [ 44 ]. Several of the fungi detected in the biofilms from the asbestos mine in Kahurangi National Park have previously been recorded from serpentinite, including Cladosporium cladosporioides , F. oxysporum [ 26 ], and S. ruberrimus [ 45 ]. The presence of two basidiomycete polypore species ( F. hemitephra and G. australe ) may suggest that spores or other material from those species in the surrounding forest are being deposited in the biofilms.…”

How does metal soil pollution change the plant mycobiome?

“…Plants were divided into two groups TM‐treated and non‐TM‐treated (control). The ratio of metal concentrations in TM‐supplemented medium mimicking metal ratio found in the mine dump was: 115 μM of Zn, 112 μM of Fe and 0.55 μM of Cd (Domka et al, 2023).…”

“…Very little is known about the structure of the community of plant‐associated microorganisms, including endophytic fungi, even though the role of these microorganisms in plant adaptation to metal toxicity has been described on several occasions (Foulon et al, 2016; Yung et al, 2021). Endophytic fungi have been shown to fine tune plant metal homeostasis by activating metal detoxification in planta and optimizing plant metal uptake (Domka et al, 2023; Rozpądek et al, 2018). This group of fungi has been extensively studied in recent years due to its potential impact on plant productivity and stress protection, which could be utilized in the phytoremediation of marginal lands (Rozpądek et al, 2019; Ważny, Rozpądek, Domka, et al, 2021; Ważny, Rozpądek, Jędrzejczyk, et al, 2021; Wężowicz et al, 2017).…”