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Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis

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Abstract

Certain plant growth-promoting rhizobacteria (PGPR), in the absence of physical contact with a plant stimulate growth via volatile organic compound (VOC) emissions, through largely unknown mechanisms. To probe how PGPR VOCs trigger growth in plants, RNA transcript levels of Arabidopsis seedlings exposed to Bacillus subtilus (strain GB03) were examined using oligonucleotide microarrays. In screening over 26,000 protein-coded transcripts, a group of approximately 600 differentially expressed genes related to cell wall modifications, primary and secondary metabolism, stress responses, hormone regulation and other expressed proteins were identified. Transcriptional and histochemical data indicate that VOCs from the PGPR strain GB03 trigger growth promotion in Arabidopsis by regulating auxin homeostasis. Specifically, gene expression for auxin synthesis was up regulated in aerial regions of GB03-exposed plants; auxin accumulation decreased in leaves and increased in roots with GB03 exposure as revealed in a transgenic DR5::GUS Arabidopsis line, suggesting activation of basipetal auxin transport. Application of the auxin transport inhibitor 1-naphthylphthalamic acid (NPA) restricted auxin accumulation to sites of synthesis thereby preventing GB03-mediated decreases in shoot auxin levels as well as thwarting GB03-mediated growth promotion. In addition, microarray data revealed coordinated regulation of cell wall loosening enzymes that implicated cell expansion with GB03 exposure, which was confirmed by comparative cytological measurements. The discovery that bacterial VOCs, devoid of auxin or other known plant hormones regulate auxin homeostasis and cell expansion provides a new paradigm as to how rhizobacteria promote plant growth.

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Abbreviations

IAA:

Indole acetic acid

NPA:

1-Naphthylphthalamic acid

PGPR:

Plant growth promotion rhizobacteria

rt-PCR:

Real time PCR

RT-PCR:

Reverse transcriptase PCR

VOCs:

Volatile organic compounds

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Acknowledgments

We especially want to thank Drs. Rangasamy Elumalai for technical expertise with microarray analyses; Mary Catherine Hastert for technical expertise with microscopic analyses; and Tom Guilfoyle for the DR5::GUS line. This research was funded in part by the Welch Foundation (Grant D1478), The Frasch Foundation for Chemical Research, Biogreen 21 and Technology Development Programs for Agriculture and Forestry, Ministry of Agriculture and Forestry, Republic of Korea.

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Authors and Affiliations

  1. Departments of Chemistry/Biochemistry and Biology, Texas Tech University, Lubbock, TX, 79409, USA

    Huiming Zhang, Mi-Seong Kim, Venkat Krishnamachari, Yan Sun, Mark Grimson, Mohamed A. Farag, Randy Allen & Paul W. Paré

  2. USDA-ARS Cropping Systems Lab, Lubbock, TX, 79409, USA

    Paxton Payton

  3. Microbial Genomics Lab, Korean Research Institute of Biosci/Biotech, Yusong, Taejon, 305-600, South Korea

    Choong-Min Ryu

  4. EMBRAPA Meio Ambiente, CP 69, 13820, Jaguariúna, SP, Brazil

    Itamar S. Melo

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  1. Huiming Zhang
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  2. Mi-Seong Kim
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  3. Venkat Krishnamachari
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  5. Yan Sun
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Correspondence to Paul W. Paré.

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Zhang, H., Kim, MS., Krishnamachari, V. et al. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis . Planta 226, 839–851 (2007). https://doi.org/10.1007/s00425-007-0530-2

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