Dark septate endophytes isolated from non-hyperaccumulator plants can increase phytoextraction of Cd and Zn by the hyperaccumulator Noccaea caerulescens

Abstract

Dark septate endophytes (DSEs) can improve plant stress tolerance by promoting growth and affecting element accumulation. Due to its ability to accumulate high Cd, Zn and Ni concentrations in its shoots, Noccaea caerulescens is considered a promising candidate for phytoextraction in the field. However, the ability of DSEs to improve trace element (TE) phytoextraction with N. caerulescens has not yet been studied. The aim of this study was therefore to determine the ability of five DSE strains, previously isolated from poplar roots collected at different TE-contaminated sites, to improve plant development, mineral nutrient status and metal accumulation by N. caerulescens during a pot experiment using two soils differing in their level of TE contamination. Microscopic observations revealed that the tested DSE strains effectively colonized the roots of N. caerulescens. In the highly contaminated (HC) soil, a threefold increase in root biomass was found in plants inoculated with the Leptodontidium sp. Pr30 strain compared to that in the non-inoculated condition; however, the plant nutrient status was not affected. In contrast, the two strains Phialophora mustea Pr27 and Leptodontidium sp. Me07 had positive effects on the mineral nutrient status of plants without significantly modifying their biomass. Compared to non-inoculated plants cultivated on HC soil, Pr27-and Pr30-inoculated plants extracted more Zn (+30%) and Cd (+90%), respectively. In conclusion, we demonstrated that the responses of N. caerulescens to DSE inoculation ranged from neutral to beneficial and we identified two strains (i.e., Leptodontidium sp. (Pr30) and Phialophora mustea (Pr27)) isolated from poplar that appeared promising as they increased the amounts of Zn and Cd extracted by improving plant growth and/or TE accumulation by N. caerulescens. These results generate interest in further characterizing the DSEs that naturally colonize N. caerulescens and testing their ability to improve phytoextraction.

Natural Fungal Endophytes From Noccaea caerulescens Mediate Neutral to Positive Effects on Plant Biomass, Mineral Nutrition and Zn Phytoextraction

“…Noccaea caerulescens has been recently shown to be a potential candidate for fungal-assisted phytoextraction, as plant responses are beneficial when associated with certain host (isolated from the same species) ( Ważny et al, 2021 ) and non-host ( Yung et al, 2021b ) endophytic strains under TE exposure. In the present study, we tested seven fungal endophytes isolated from non-metallicolous and calamine populations of N. caerulescens based on their taxonomy.…”

“…They were selected based on their potential as PGP fungi, according to their description in the literature. The production of inoculum and the soil inoculation procedure are fully described in Yung et al (2021b) . As a control treatment (CTRL), we mixed one aliquot of soil with perlite containing fungus-free agar plugs.…”

“…Chlorophyl, flavonoid and anthocyanin contents in leaves of N. caerulescens and the nitrogen balance index (NBI) were measured using a dual-excitation fluorimeter DUALEX ® SCIENTIFIC+ (Force-A, Orsay, France). Full details about the analytical method are available in Yung et al (2021b) . These measurements were carried out on five mature leaves per plant at the end of the experiment.…”

“…Soil was removed from the roots first by washing them with tap water and then by immersing them in 37.6 mM tetrasodium diphosphate for 16 h. The plant samples were then dried at 70°C for 48 h and weighed. Dried samples (0.5 g) were ground and digested according to the protocol detailed in Yung et al (2021b) . Trace and major elements were analyzed by ICP-OES.…”

“…Various levers have been investigated to increase biomass production, such as the selection of high-growth rate cultivars ( Sterckeman et al, 2017 , 2019 ) and the development of adequate cultural practices ( Maxted et al, 2007 ; Jacobs et al, 2018a , b ; Rees et al, 2020 ), including the addition of biological amendments. Indeed, we previously demonstrated that several DSE strains isolated from poplar roots collected from TE-contaminated sites were able to colonize the roots of N. caerulescens , with plant responses ranging from neutral to beneficial ( Yung et al, 2021b ). We also identified two promising fungal strains for the fungal-assisted phytoextraction of Cd and Zn with N. caerulescens .…”