Skip to main content
Log in

Volatile organic compounds emitted by Bacillus sp. JC03 promote plant growth through the action of auxin and strigolactone

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The volatile organic compounds (VOCs) emitted by plant rhizobacteria play a significant role in the promotion of plant growth. However, it is unclear how VOCs play a role in plant growth and which component participates in this process. In this study, we assessed the effect of the VOCs emitted by Bacillus sp. JC03 on the promotion of plant growth and identified the overall functional mechanism. The results indicated that the VOCs produced by JC03 could significantly promote the biomass accumulation of Arabidopsis and tomato. Furthermore, an analysis of Arabidopsis mutants perturbations in hormone production and signaling, in conjunction with analyses of hormone contents and gene expression levels, indicated that auxin and strigolactone played essential roles in the promotion of plant growth induced by the VOCs produced by JC03. The results showed that the ARF1 and CCD7 genes were significantly upregulated in the Arabidopsis seedlings exposed to the VOCs emitted by JC03 and the results of the endogenous hormone levels detection experiment reached the same conclusion. Furthermore, the VOC-induced phenotype was reduced or, even lost in the ARF1, and CCD7 mutant lines, while the phenotype remained in A. thaliana ecotype Col-0 seedlings and in other mutants, such as etr1, OST1 and gai1. Finally, GC-MS analysis results positively identified the compounds released from JC03, including 3-hydroxy-2-butanone, 1, 3-propanediol, 2-methyl-dipropanoate, tetrahydrofuran-3-ol, 2-heptanone, 2-ethyl-1-hexanol. Only tetrahydrofuran-3-ol, 2-heptanone and 2-ethyl-1-hexanol, at different concentrations, significantly promoted the growth of the Arabidopsis seedlings. In this study, we first demonstrated that the VOCs emitted by JC03 promoted plant growth through the action of auxin and strigolactone, and identified several new compounds, tetrahydrofuran-3-ol, 2-heptanone and 2-ethyl-1-hexanol, that could promote plant growth. The important achievement of our study is the further elucidation of the interacting mechanisms related to plant responses to the VOCs emitted by microbes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

VOCs:

Volatile organic compounds

PGPR:

Plant-growth-promoting rhizobacteria

IAA:

Indole acetic acid

ABA:

Abscisic acid

GA:

Gibberellins

ETH:

Ethylene

SLs:

Strigolactone

MRM:

Multiple reaction monitoring mode

SPME:

Solid phase microextraction

LSD:

Least significant difference

References

  • Ann M, Cho Y, Ryu H, Kim H, Park K (2013) Growth promotion of tobacco plant by 3-hydroxy-2-butanone from Bacillus vallismortis EXTN-1. Korean J Pestic Sci 17:388–393

    Article  Google Scholar 

  • Asari S, Matzén S, Petersen MA, Bejai S, Meijer J (2016) Multiple effects of Bacillus amyloliquefaciens volatile compounds: plant growth promotion and growth inhibition of phytopathogens. FEMS Microbiol Ecol 92(6):fiw070

    Article  CAS  PubMed  Google Scholar 

  • Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35(4):1044–1051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bensmihen S (2015) Hormonal control of lateral root and nodule development in legumes. Plants 4(3):523–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cook A, Stall R (1969) Necrosis in leaves induced by volatile materials produced in vitro by bacteria. Phytopathology 59:259–260

    Google Scholar 

  • Curran AM, Rabin SI, Prada PA, Furton KG (2005) Comparison of the volatile organic compounds present in human odor using SPME-GC/MS. J Chem Ecol 31(7):1607–1619

    Article  CAS  PubMed  Google Scholar 

  • Farag MA, Ryu CM, Sumner LW, Paré PW (2006) Gc-ms spme profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67(20):2262–2268

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, Cruz HRDL, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51(1):75–83

    Article  CAS  Google Scholar 

  • Hao HT, Zhao X, Shang QH, Wang Y, Guo ZH, Zhang YB, Zhong KX, Wang RY (2016) Comparative digital gene expression analysis of the Arabidopsis response to volatiles emitted by Bacillus amyloliquefaciens. PLoS One 11:e0158621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hung R, Lee S, Bennett JW (2013) Arabidopsis thaliana as a model system for testing the effect of Trichoderma volatile organic compounds. Fungal Ecol 6:19–26

    Article  Google Scholar 

  • Iqbal N, Khan NA, Nazar R, Teixeira da Silva JA (2012) Ethylene-stimulated photosynthesis results from increased nitrogen and sulfur. Environ Exp Bot 78:84–90

    Article  CAS  Google Scholar 

  • Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Mir K (2017) Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci 8(9):1–19

    Google Scholar 

  • Jiang CH, Fan ZH, Ping X, Guo JH (2016) Bacillus cereus AR156 extracellular polysaccharides served as a novel micro-associated molecular pattern to induced systemic immunity to Pst DC3000 in Arabidopsis. Frontiers in Microbiology 7(9):1–16

    Google Scholar 

  • Kanchiswamy C, Malnoy M, Maffei M (2015) Bioprospecting bacterial and fungal volatiles for sustainable agriculture. Trends Plant Sci 20:206–211

    Article  CAS  PubMed  Google Scholar 

  • Kim JS, Lee J, Seo SG, Lee C, Woo SY, Kim SH (2015) Gene expression profile affected by volatiles of new plant growth promoting rhizobacteria, Bacillus subtilis strain JS, in tobacco. Genes Genom 37:387–397

    Article  CAS  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94(11):1259–1266

    Article  CAS  PubMed  Google Scholar 

  • Kopsell DA, Kopsell DE (2008) Genetic and environmental factors affecting plant lutein/zeaxanthin. Agro Food Industry Hi Tech 19(2):44–46

    CAS  Google Scholar 

  • Korpi A, Järnberg J, Pasanen AL (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–193

    Article  CAS  Google Scholar 

  • Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu CM (2012) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS ONE 7:e48744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li ZG, Liu AQ, Wu HS, Tan L, Long YZ, Gou YF (2010) Influence of temperature, light and plant growth regulators on germination of black pepper (Piper nigrum l.) seeds. Afr J Biotech 9(9):1354–1358

    Article  CAS  Google Scholar 

  • López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TD, Thompson AJ, Ruyter-Spira C, Bouwmeester H (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187(2):343–354

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 2009(1):541–556

    Article  CAS  Google Scholar 

  • Minerdi D, Bossi S, Maffei M, Gullino M, Garibaldi A (2011) Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compounds (MVOC) emission. FEMS Microbiol Ecol 76:342–351

    Article  CAS  PubMed  Google Scholar 

  • Mostofa MG, Li W, Nguyen KH, Fujita M, Lam-Son PT (2018) Strigolactones in plant adaptation to abiotic stresses: an emerging avenue of plant research. Plant Cell Environ 41:2227–2243

    Article  CAS  PubMed  Google Scholar 

  • Orozco-Mosqueda M, Velázquez-Becerra C, Macías-Rodríguez LI, Santoyo G, Flores-Cortez I, Alfaro-Cuevas R, Valencia-Cantero E (2013) Arthrobacter agilis UMCV2 induces iron acquisition in Medicago truncatula (strategy I plant) in vitro via dimethylhexadecylamine emission. Plant Soil 362(1–2):51–66

    Article  CAS  Google Scholar 

  • Park YS, Dutta S, Ann M, Raaijmakers JM, Park K (2015) Promotion of plant growth by Pseudomonas fluorescens strain SS101 via novel volatile organic compounds. Biochem Biophys Res Commun 461(2):361–365

    Article  CAS  PubMed  Google Scholar 

  • Per TS, Khan MIR, Anjum NA, Masood A, Hussain SJ, Khan NA (2018) Jasmonates in plants under abiotic stresses: crosstalk with other phytohormones matters. Environ Exp Bot 145:104–120

    Article  CAS  Google Scholar 

  • Rath M, Mitchell TR, Gold SE (2018) Volatiles produced by Bacillus mojavensis RRC101 act as plant growth modulators and are strongly culture dependent. Microbiol Res 208:76–84

    Article  CAS  PubMed  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. P Natl Acad Sci USA 100:4927–4932

    Article  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268(1):285–292

    Article  CAS  Google Scholar 

  • Sánchez-López AM, Baslam M, De Diego N, Muñoz FJ, Bahaji A, Almagro G, Ricarte-Bermejo A, García-Gómez P, Li J, Humplík JF, Novák O, Spíchal L, Doležal K, Baroja-Fernández E, Pozueta-Romero J (2016) Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. Plant Cell Environ 39(12):2592–2608

    Article  CAS  PubMed  Google Scholar 

  • Tahir HA, Gu Q, Wu H, Raza W, Hanif A, Wu L, Colman MV, Gao XW (2017) Plant growth promotion by volatile organic compounds produced by Bacillus subtilis syst2. Front Microbiol 8(e48744):171

    PubMed  PubMed Central  Google Scholar 

  • Valverdebarrantes OJ, Freschet GT, Roumet C, Blackwood CB (2017) A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants. New Phytol 215(4):1562–1573

    Article  Google Scholar 

  • Vassilev N, Vassileva M, Nicolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhou C, Xiao X, Xie Y, Zhu L, Ma Z (2017) Enhanced iron and selenium uptake in plants by volatile emissions of Bacillus amyloliquefaciens (bf06). Appl Sci 7(1):85

    Article  CAS  Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273

    Article  CAS  PubMed  Google Scholar 

  • Zou C, Li Z, Yu D (2010) Bacillus megaterium strain XTBG34 promotes plant growth by producing 2-pentylfuran. J Microbiol 48(4):460–466

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Young Scholars Program) (31701829), National Natural Science Foundation of China (31471812, 31672075), Natural Science Foundation of Jiangsu Province (Young Scholars Program) (BK20170709), National Postdoctoral Program for Innovative Talents (BX201600074), China Postdoctoral Science Foundation (2017M611839).

Author information

Authors and Affiliations

Authors

Contributions

CJ and JG designed research. CJ, YX, KZ, ZL and NW performed experimental work. CJ wrote the paper and GY, JG revised the paper.

Corresponding author

Correspondence to Jian-Hua Guo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 265 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, CH., Xie, YS., Zhu, K. et al. Volatile organic compounds emitted by Bacillus sp. JC03 promote plant growth through the action of auxin and strigolactone. Plant Growth Regul 87, 317–328 (2019). https://doi.org/10.1007/s10725-018-00473-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-018-00473-z

Keywords

Navigation