Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones

Abstract

Plant growth promoting rhizobacteria (PGPR) are diverse, naturally occurring bacteria that establish a close association with plant roots and promote the growth and immunity of plants. Established mechanisms involved in PGPR-mediated plant growth promotion include regulation of phytohormones, improved nutrient availability, and antagonistic effects on plant pathogens. In this study, we isolated a bacterium from the rhizospheric soil of a soybean field in Chungcheong buk-do, South Korea. Using 16S rRNA sequencing, the bacterium was identified as Bacillus aryabhattai strain SRB02. Here we show that this strain significantly promotes the growth of soybean. Gas chromatography—mass spectrometry analysis showed that SRB02 produced significant amounts of abscisic acid, indole acetic acid, cytokinin and different gibberellic acids in culture. SRB02-treated soybean plants showed significantly better heat stress tolerance than did untreated plants. These plants also produced consistent levels of ABA under heat stress and exhibited ABA-mediated stomatal closure. High levels of IAA, JA, GA12, GA4, and GA7, were recorded in SRB02-treated plants. These plants produced longer roots and shoots than those of control plants. B. aryabhattai SRB02 was found to be highly tolerant to oxidative stress induced by H2O2 and MV potentiated by high catalase (CAT) and superoxide dismutase (SOD) activities. SRB02 also tolerated high nitrosative stress induced by the nitric oxide donors GSNO and CysNO. Because of these attributes, B. aryabhattai SRB02 may prove to be a valuable resource for incorporation in biofertilizers and other soil amendments that seek to improve crop productivity.

Improved germination efficiency of Salicornia ramosissima seeds inoculated with Bacillus aryabhattai SP1016‐20

“…To the best of our knowledge this is the first time this species has been identified in the rhizosphere of S. ramosissima. Previous studies report the ability of B. aryabhattai isolated from rhizospheres of halophytes to promote the growth of Xanthium italicum (Lee, Ka, & Song, ), soybean (Park et al, ) and canola under salt stress (Siddikee, Chauhan, Anandham, Han, & Sa, ).…”

“…This growth promotion potential could be linked to production of 1 aminocyclopropane‐1‐carboxylate (ACC) deaminase and phytohormones (Lee et al, ; Park et al, ) as well as the ability of B. aryabhattai to form biofilms, solubilise phosphates, produce proteases and efficiently utilise the root exudates as an energy source (Bhattacharyya et al, ). B. aryabhattai also displays the capacity of inhibiting mycelial growth of the pathogen Fusarium oxysporum (Castellano‐Hinojosa, Correa‐Galeote, Palau, & Bedmar, ).…”

Chloroplast clustering around the nucleus is a general response to pathogen perception in Nicotiana benthamiana

“…Consistent with a relevant role of chloroplast function in defence, effector proteins from different pathogens, including bacteria, viruses, fungi and oomycetes, have been shown to target this organelle (e.g. Fondong et al , ; Jelenska et al , , ; Li et al , ; Liu et al , ; Park et al , ; Petre et al , ; Rodriguez‐Herva et al , ; Rosas‐Diaz et al , ; de Torres Zabala et al , ). Intriguingly, chloroplasts can establish contact with the nucleus, through clustering around it and extending tubular stroma‐filled protrusions called stromules (Natesan et al , ), under different circumstances, including the activation of ETI triggered by the p50 protein from Tobacco mosaic virus (TMV) (Caplan et al , , ; Kumar et al , ; Kwok and Hanson, ).…”

“…In addition to their function as energy providers, an increasing body of evidence points at chloroplasts as playing an essential role in plant stress responses, serving as hubs in the integration of stimuli and source of downstream signalling molecules (Chan et al , ; de Souza et al , ; Zhu, ). Upon activation of immune responses, chloroplasts produce an array of pro‐defence signals, including cytoplasmic calcium bursts, reactive oxygen species (ROS), and the phytohormones salicylic acid (SA) and jasmonic acid (JA) (Park et al , ; Sowden et al , ; de Torres Zabala et al , ). Consistent with a relevant role of chloroplast function in defence, effector proteins from different pathogens, including bacteria, viruses, fungi and oomycetes, have been shown to target this organelle (e.g.…”

“…These organelles communicate with the nucleus through the so‐called retrograde signalling pathway, which transmits developmental and environmental information to regulate the expression of thousands of nuclear genes (Chan et al , ). During plant–pathogen interactions, chloroplasts act as a source of signalling and/or defensive compounds, including ROS, SA, JA and cytoplasmic calcium bursts, and are required for transcriptional reprogramming and for the plant to mount a full defence response (Nomura et al , ; Park et al , ; Pogorelko et al , ; Sowden et al , ; de Torres Zabala et al , ). It has been previously shown that, upon activation of ETI through expression of the p50 protein from TMV, chloroplasts tend to cluster around the nucleus and emit stromules (Caplan et al , ; Kumar et al , ); interestingly, infection by the geminivirus AbMV also results in the induction of stromules (Krenz et al , , ).…”