Rhizospheric Bacillus spp. Rescues Plant Growth Under Salinity Stress via Regulating Gene Expression, Endogenous Hormones, and Antioxidant System of Oryza sativa L.

Muhammad Aaqil Khan,Muhammad Hamayun,In-Jung Lee,Sang-Mo Kang,Sajjad Asaf,Byung-Wook Yun,Murtaza Khan

doi:10.3389/fpls.2021.665590

Abstract

Salinity has drastically reduced crop yields and harmed the global agricultural industry. We isolated 55 bacterial strains from plants inhabiting the coastal sand dunes of Pohang, Korea. A screening bioassay showed that 14 of the bacterial isolates secreted indole-3-acetic acid (IAA), 12 isolates were capable of exopolysaccharide (EPS) production and phosphate solubilization, and 10 isolates secreted siderophores. Based on our preliminary screening, 11 bacterial isolates were tested for salinity tolerance on Luria–Bertani (LB) media supplemented with 0, 50, 100, and 150 mM of NaCl. Three bacterial isolates, ALT11, ALT12, and ALT30, had the best tolerance against elevated NaCl levels and were selected for further study. Inoculation of the selected bacterial isolates significantly enhanced rice growth attributes, viz., shoot length (22.8–42.2%), root length (28.18–59%), fresh biomass (44.7–66.41%), dry biomass (85–90%), chlorophyll content (18.30–36.15%), Chl a (29.02–60.87%), Chl b (30.86–64.51%), and carotenoid content (26.86–70%), under elevated salt stress of 70 and 140 mM. Furthermore, a decrease in the endogenous abscisic acid (ABA) content (27.9–23%) and endogenous salicylic acid (SA) levels (11.70–69.19%) was observed in inoculated plants. Antioxidant analysis revealed an increase in total protein (TP) levels (42.57–68.26%), whereas it revealed a decrease in polyphenol peroxidase (PPO) (24.63–34.57%), glutathione (GSH) (25.53–24.91%), SOA (13.88–18.67%), and LPO levels (15.96–26.06%) of bacterial-inoculated plants. Moreover, an increase in catalase (CAT) (26–33.04%), peroxidase (POD) (59.55–78%), superoxide dismutase (SOD) (13.58–27.77%), and ascorbic peroxidase (APX) (5.76–22.74%) activity was observed. Additionally, inductively coupled plasma mass spectrometry (ICP-MS) analysis showed a decline in Na+ content (24.11 and 30.60%) and an increase in K+ (23.14 and 15.45%) and Mg+ (2.82 and 18.74%) under elevated salt stress. OsNHX1 gene expression was downregulated (0.3 and 4.1-folds), whereas the gene expression of OsPIN1A, OsCATA, and OsAPX1 was upregulated by a 7–17-fold in bacterial-inoculated rice plants. It was concluded that the selected bacterial isolates, ALT11, ALT12, and ALT30, mitigated the adverse effects of salt stress on rice growth and can be used as climate smart agricultural tools in ecofriendly agricultural practices.

Highlights

Soil salinity is abiotic stress that significantly limits agricultural productivity and food security (Shrivastava and Kumar, 2015; Kumar et al, 2020)
superoxide dismutase (SOD) is a metalloenzyme that protects cells from oxidative damage, and it catalyzes the conversion of superoxide radicals to H2O2, whereas ascorbic peroxidase (APX) and CAT break down H2O2 to H2O and O2 produced by SOD (Santos et al, 2000; Jaleel et al, 2009; Habib et al, 2016)
The results revealed that isolates ALT11, ALT12, and ALT30 exhibited a high level of 16S rRNA sequence identity with Bacillus

Summary

Introduction

Soil salinity is abiotic stress that significantly limits agricultural productivity and food security (Shrivastava and Kumar, 2015; Kumar et al, 2020). The salinization of agricultural lands occurs because of the accumulation of salts in the soil, sodium and chloride ions, which leads to hypertonic stress (Kumar et al, 2020). To reduce the toxic effect of salinity, the plant antioxidant system, including enzymatic [superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT)] and non-enzymatic [glutathione (GSH), total protein (TP)] antioxidants, has to be activated to control the biosynthesis of ROS and maintain them at a low level (Jha and Subramanian, 2013; Habib et al, 2016; Santos et al, 2018; Khan et al, 2020b). SOD is a metalloenzyme that protects cells from oxidative damage, and it catalyzes the conversion of superoxide radicals to H2O2, whereas ascorbic peroxidase (APX) and CAT break down H2O2 to H2O and O2 produced by SOD (Santos et al, 2000; Jaleel et al, 2009; Habib et al, 2016)

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