Mixed planting with a leguminous plant outperforms bacteria in promoting growth of a metal remediating plant through histidine synthesis

Abstract

The effectiveness of plant growth promoting bacteria (PGPB) in improving metal phytoremediation is still limited by stunted plant growth under high soil metal concentrations. Meanwhile, mixed planting with leguminous plants is known to improve yield in nutrient deficient soils but the use of a metal tolerant legume to enhance metal tolerance of a phytoremediator has not been explored. We compared the use of Pseudomonas brassicacearum, Rhizobium leguminosarum, and the metal tolerant leguminous plant Vicia sativa to promote the growth of Brassica juncea in soil contaminated with 400 mg Zn kg(-1), and used synchrotron based microfocus X-ray absorption spectroscopy to probe Zn speciation in plant roots. B. juncea grew better when planted with V. sativa than when inoculated with PGPB. By combining PGPB with mixed planting, B. juncea recovered full growth while also achieving soil remediation efficiency of >75%, the maximum ever demonstrated for B. juncea. μXANES analysis of V. sativa suggested possible root exudation of the Zn chelates histidine and cysteine were responsible for reducing Zn toxicity. We propose the exploration of a legume-assisted-phytoremediation system as a more effective alternative to PGPB for Zn bioremediation.

Role of plant growth promoting bacteria in driving speciation gradients across soil-rhizosphere-plant interfaces in zinc-contaminated soils

“…Histidine is an essential amino acid with a positively charged imidazole functional group (Chakrabarti, 1990;Gluster, 1991;Gramlich et al, 2013). The occurrence of Zn histidine in the roots in the ZnSO4 treatments in the present study agrees with previous studies of Zn hyperaccumulator species (Adediran et al, 2016b;Lasat et al, 1998;Salt et al, 1999). Metal tolerance and hyperaccumulation via histidine complexation has been demonstrated in studies involving Ni (Salt et al 1999) and histidine has been implicated in Cu and Zn toxicity responses (Sharma and Dietz, 2006).…”

“…We found higher proportions of Zn histidine complexes in roots than in the bulk and rhizospheric soils, where the proportions were approximately equal. Therefore, like phytate, we interpret the observed gradient as reflecting histidine production in the form of root exudates (see also Adediran et al, 2016b) but with long range transport into the rhizospheric and bulk soil.…”

“…2a), possibly due to bacterially enhanced solubilisation of Zn through production of siderophores and other metal-chelating substances (Verma et al, 2010). We have previously attributed this apparent paradox of healthy plant growth and increased Zn accumulation to bacterially-mediated changes in Zn speciation, including through complexation with histidine (Adediran et al, 2016b;Medas et al, 2019;Yadav, 2010), organic acids and thiols (Adediran et al, 2015(Adediran et al, , 2016aAdele et al, 2018;Grill et al, 1985).…”

Soil Bacteria Override Speciation Effects on Zinc Phytotoxicity in Zinc-Contaminated Soils

“…Zn−histidine has been reported in previous studies and is thought to help reduce the toxicity of Zn to the plant, 8,41,65 being a ligand for binding metals in hyperaccumulator species, 69 including Zn. 70 Adediran et al 71 also reported Zn−histidine complexation in roots of Vicia sativa, and this was thought to be controlled by nitrogen metabolism potentially driven by legume-associated symbiotic bacteria. This may explain why we also see it only in plant roots inoculated with R. leguminosarum.…”