Promotion of plant growth by Pseudomonas fluorescens strain SS101 via novel volatile organic compounds

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Highlights

  • Pf.SS101 facilitates plant growth promotion.

  • VOCs derived from Pf.SS101 are key components in plant growth promotion.

  • Eleven different VOCs are identified from Pf.SS101.

  • 13-Tetradecadien-1-ol, 2-Methyl-n-1-tridecene and 2-Butanone significantly enhance plant growth promotion.

Abstract

Volatile organic compounds (VOCs) from plant growth-promoting rhizobacteria (PGPR) play key roles in modulating plant growth and induced systemic resistance (ISR) to pathogens. Despite their significance, the physiological functions of the specific VOCs produced by Pseudomonas fluorescens SS101 (Pf.SS101) have not been precisely elucidated. The effects of Pf.SS101 and its VOCs on augmentation of plant growth promotion were investigated in vitro and in planta. A significant growth promotion was observed in plants exposed Pf.SS101 under both conditions, suggesting that its VOCs play a key role in promoting plant growth. Solid-phase micro-extraction (SPME) and a gas chromatography-mass spectrophotometer (GC–MS) system were used to characterize the VOCs emitted by Pf.SS101 and 11 different compounds were detected in samples inoculated this bacterium, including 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene. Application of these compounds resulted in enhanced plant growth. This study suggests that Pf.SS101 promotes the growth of plants via the release of VOCs including 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene, thus increasing understanding of the role of VOCs in plant-bacterial inter-communication.

Introduction

Volatile organic compounds (VOCs) produced by plant growth-promoting rhizobacteria (PGPR) play key roles in plant growth promotion and induced systemic resistance (ISR) to pathogens [1], [2], [3]. A number of bacterial species, from diverse genera including Bacillus, Pseudomonas, Serratia, Arthrobacter and Stenotrophomonas, produce VOCs influencing plant growth [4], [5], [6]. Acetoin and 2,3-butanediol from Bacillus are the best known of these compounds and are implicated in significant improvements to plant growth [1]. In addition to promoting growth, VOCs produced by bacilli may elicit ISR [2], indicating several potential roles for VOCs within a plant.

The Pseudomonas fluorescens strain SS101 (Pf.SS101), a nonpathogenic rhizobacterium, was isolated from the rhizosphere of wheat (Triticum aestivum) [7]. This strain can produce a cyclic lipopeptide surfactant, massetolide A, which is an important molecule in a variety of traits, including swarming motility, biofilm formation, manipulation of zoospores, defense against protozoan predators and ISR [7], [8], [9], [10], [11]. It has been shown more recently that induced resistance to Pseudomonas syringae pv tomato (Pst) mediated by Pf.SS101 depends upon salicylic acid (SA) signaling and NONEXPRESSOR OF PR1 (NPR1) but not on the jasmonic acid/ethylene (JA/ET) signaling pathway in Arabidopsis [12]. Although previous researchers have focused on such important issues, the roles of VOCs derived from Pf.SS101 facilitating plant growth promotion remain poorly understood.

To fill this gap in our current knowledge of the functions of VOCs produced by Pf.SS101, we investigated whether this bacterium affected plant growth promotion and also how its VOCs modulated plant growth and development. We performed an I-plate assay in which Pf.SS101 and plants were placed on each half of an I-plate, thus avoiding physical contact between them. Increased plant biomass, compared to the control, was observed when Pf.SS101 was inoculated onto one half of the I-plate. In agreement with this finding, tobacco plants exposed to Pf.SS101 were significantly taller and bigger than control plants under soil conditions. These results suggest that VOCs derived from Pf.SS101 are key components in plant growth promotion. Therefore, we analyzed the biochemical profiles of VOCs produced by growing samples of Pf.SS101 using solid-phase micro-extraction (SPME) and a gas chromatography-mass spectrophotometer (GC–MS) system. This clearly identified 11 different chemical compounds presenting in samples inoculated with Pf.SS101. Moreover, tobacco plants exposed to various concentrations of 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene showed clear improvements in plant growth promotion. Collectively, our results suggest that Pf.SS101 enhances plant growth by producing VOCs, including 13-Tetradecadien-1-ol, 2-butanone and 2-Methyl-n-1-tridecene.

Section snippets

Bacterial strain and culture media

The bacterial strain P. fluorescens SS101 (Pf.SS101) was used in all experiments. King's B broth (KB) plus agar was used as the substrate in experiments to determine interactions between Pf.SS101 and plants. Stock cultures of Pf.SS101 were maintained at −80 °C in tryptic soy broth (TSB, Difco, MI, USA) containing 20% glycerol.

Growth promotion by Pf.SS101 in vitro and in planta

For in vitro assays, surface-sterilized tobacco (Nicotiana tabacum cv. Xanthi-nc) seeds were placed in one half of an I-plate containing 0.5 × Murashige and Skoog (MS)

Plant growth promotion by Pf.SS101

To examine whether Pf.SS101 affected plant growth, surface-sterilized tobacco seeds were sown on 0.5 × MS medium plus agar in a square plate and incubated for 1 week. At this point, small plates inoculated with Pf.SS101 were placed within the same square plate and the plants were grown for an additional 3 weeks at 25 °C. Plants exposed to Pf.SS101 showed an increase in shoot and root biomass relative to the controls (Supplementary Fig. S1). This suggests that Pf.SS101 positively modulates plant

Discussion

Previous studies of Pf.SS101 reveal that it is required for ISR and other aspects [7], [8], [9], [10], [11], [12]. However, despite these studies, the full roles of Pf.SS101 and/or VOCs derived from Pf.SS101 in promoting plant growth and development have been rarely reported. Our study produced several novel results: (1) Pf.SS101 stimulated plant growth promotion in vitro and in planta; (2) VOCs derived from Pf.SS101 were key regulators of plant growth promotion; and (3) exposure to three

Conflict of interests

We declare that we have no conflict of interests.

Acknowledgments

This study was supported by the International Cooperation Projects, RDA (PJ010807) and Research Program for Agricultural Science & Technology Development and NAAS, RDA, South Korea (PJ009991).

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These authors contributed equally to this study.

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