Fungicide-Tolerant Plant Growth-Promoting Rhizobacteria Mitigate Physiological Disruption of White Radish Caused by Fungicides Used in the Field Cultivation

Abstract

Excessive use of fungicides in agriculture may result in substantial accumulation of active residues in soil, which affect crop health and yield. We investigated the response of Raphanus sativus (white radish) to fungicides in soil and potential beneficial interactions of radish plants with fungicide-tolerant plant growth-promoting rhizobacteria (PGPR). The PGPR were isolated from cabbage and mustard rhizospheres. Morphological and biochemical characteristics measured using standard methods, together with analysis of partial 16S rRNA gene sequences, revealed that fungicide-tolerant PGPR, isolates PS3 and AZ2, were closely related to Pseudomonas spp. These PGPR survived in the presence of high fungicide concentrations i.e., up to 2400 μg mL−1 carbendazim (CBZM) and 3200 μg mL−1 hexaconazole (HEXA). Bacterial isolates produced plant growth stimulants even under fungicide stress, though fungicides induced surface morphological distortion and alteration in membrane permeability of these bacteria, which was proved by a set of microscopic observations. Fungicides considerably affected the germination efficiency, growth, and physiological development of R. sativus, but these effects were relieved when inoculated with PGPR isolates. For instance, CBZM at 1500 mg kg−1 decreased whole dry biomass by 71%, whole plant length by 54%, total chlorophyll by 50%, protein content by 61%, and carotenoid production by 29%. After applying isolate AZ2 for white radish grown in CBZM (10 mg kg−1)-amended soil, it could improve plant growth and development with increased whole plant dry weight (10%), entire plant length (13%) and total chlorophyll content (18%). Similarly, isolate PS3 enhanced plant survival by relieving plant stress with declined biomarkers, i.e., proline (12%), malondialdehyde (3%), ascorbate peroxidase (6.5%), catalase (18%), and glutathione reductase (4%). Application of isolates AZ2 and PS3 could be effective for remediation of fungicide-contaminated soil and for improving the cultivation of radish plants while minimizing inputs of fungicides.