Skip to main content
SpringerLink
Log in

CO2 is a key constituent of the plant growth-promoting volatiles generated by bacteria in a sealed system

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Plant growth is greatly inhibited in tightly sealed Petri dishes for lack of CO 2 . Bacteria which co-cultured with plant can produce CO 2 to promote plant growth in sealed systems.

Abstract

Bacteria produce a wide variety of volatiles, some of which can support and others can damage plant growth. It is a controversial issue whether CO2 or other bacterial volatile compounds promote plant growth in sealed systems. CO2 is critical for photosynthesis. Here, we show that CO2 is a key constituent of the plant growth-promoting volatiles generated by bacteria in a sealed system. We revealed that the growth of Arabidopsis seedlings in an airtight container was retarded due to insufficient supply of the CO2. When either CO2 was introduced into the container, or the seedlings were co-cultured along with certain bacterial species, the plants’ growth was restored. Conclusion: The benefit of co-culturing was largely due to the CO2 generated by respiration of the bacteria.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta-vulgaris. Plant Physiol 24(1):1–15

    Article  CAS  Google Scholar 

  • Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L, Weisskopf L (2014) The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. Plant J 80(5):758–771

    Article  CAS  Google Scholar 

  • Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011a) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13(11):3047–3058

    Article  CAS  Google Scholar 

  • Blom D, Fabbri C, Eberl L, Weisskopf L (2011b) Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl Environ Microbiol 77(3):1000–1008

    Article  CAS  Google Scholar 

  • Bulgarelli D, Rott M, Schlaeppi K, Loren V, van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488(7409):91–95

    Article  CAS  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  CAS  Google Scholar 

  • Castulo-Rubio DY, Alejandre-Ramirez NA, Orozco-Mosqueda MD, Santoyo G, Macias-Rodriguez LI, Valencia-Cantero E (2015) Volatile organic compounds produced by the rhizobacterium Arthrobacter agilis UMCV2 modulate Sorghum bicolor (strategy II plant) morphogenesis and SbFRO1 transcription in vitro. J Plant Growth Regul 34(3):611–623

    Article  CAS  Google Scholar 

  • Chung JH, Song GC, Ryu CM (2016) Sweet scents from good bacteria: case studies on bacterial volatile compounds for plant growth and immunity. Plant Mol Biol 90(6):677–687

    Article  CAS  Google Scholar 

  • Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149(3):1579–1592

    Article  CAS  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245(1):35–47

    Article  CAS  Google Scholar 

  • Duran P, Thiergart T, Garrido-Oter R, Agler M, Kemen E, Schulze-Lefert P, Hacquard S (2018) Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175(4):973–983.e914

    Article  CAS  Google Scholar 

  • Farre-Armengol G, Filella I, Llusia J, Penuelas J (2016) Bidirectional interaction between phyllospheric microbiotas and plant volatile emissions. Trends Plant Sci 21(10):854–860

    Article  CAS  Google Scholar 

  • Kai M, Piechulla B (2009) Plant growth promotion due to rhizobacterial volatiles—an effect of CO2? FEBS Lett 583(21):3473–3477

    Article  CAS  Google Scholar 

  • Kai M, Piechulla B (2010) Impact of volatiles of the rhizobacteria Serratia odorifera on the moss Physcomitrella patens. Plant Signal Behav 5(4):444–446

    Article  Google Scholar 

  • Kai M, Effmert U, Piechulla B (2016) Bacterial-plant-interactions: approaches to unravel the biological function of bacterial volatiles in the rhizosphere. Front Microbiol 7:108

    Article  Google Scholar 

  • Kanchiswamy CN, Mainoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6:151

    Article  Google Scholar 

  • Lemfack MC, Gohlke BO, Toguem SMT, Preissner S, Piechulla B, Preissner R (2018) mVOC 2.0: a database of microbial volatiles. Nucleic Acids Res 46(D1):D1261–D1265

    Article  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  Google Scholar 

  • Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90

    Article  CAS  Google Scholar 

  • Piechulla B (2017) Considering microbial CO2 during microbe-plant cocultivation. Plant Physiol 173(3):1529

    Article  CAS  Google Scholar 

  • Piechulla B, Schnitzler JP (2016) Circumvent CO2 effects in volatile-based microbe-plant interactions. Trends Plant Sci 21(7):541–543

    Article  CAS  Google Scholar 

  • Piechulla B, Lemfack MC, Kai M (2017) Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ 40(10):2042–2067

    Article  CAS  Google Scholar 

  • Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    Article  CAS  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100(8):4927–4932

    Article  CAS  Google Scholar 

  • Sharifi R, Ryu CM (2018) Sniffing bacterial volatile compounds for healthier plants. Curr Opin Plant Biol 44:88–97

    Article  CAS  Google Scholar 

  • Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73(17):5639–5641

    Article  CAS  Google Scholar 

  • Ward JK, Strain BR (1997) Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations. Plant Cell Environ 20(2):254–260

    Article  Google Scholar 

  • Weise T, Kai M, Piechulla B (2013) Bacterial ammonia causes significant plant growth inhibition. PLoS ONE 8(5):e63538

    Article  CAS  Google Scholar 

  • Wenke K, Wanke D, Kilian J, Berendzen K, Harter K, Piechulla B (2012) Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J 70(3):445–459

    Article  CAS  Google Scholar 

  • Wenke K, Kopka J, Schwachtje J, van Dongen JT, Piechulla B (2019) Volatiles of rhizobacteria Serratia and Stenotrophomonas alter growth and metabolite composition of Arabidopsis thaliana. Plant Biol (Stuttg) 21(Suppl 1):109–119

    Article  CAS  Google Scholar 

  • Yu Z, Xu Y, Zhu L, Zhang L, Liu L, Zhang D, Li D, Wu C, Huang J, Yang G, Yan K, Zhang S, Zheng C (2019) The Brassicaceae-specific secreted peptides, STMPs, function in plant growth and pathogen defense. J Integr Plant Biol 62:403–420

    Article  Google Scholar 

  • Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162(1):304–318

    Article  CAS  Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226(4):839–851

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Caiyun Sun and Prof. Mei shi (Shandong University) for their guidance in performing CO2 measurement. We also thank Professor Yang Bai (Chinese Academy of Science) for the selfless help and suggestions in the manuscript editing. This research was financially supported by the Qingdao Leading Technology Innovator Project and by the Shandong University Youth Interdisciplinary Science and Innovative Research Groups (Grant no. 2020QNQT014).

Author information

Author notes

  1. Chunlei Zhang, Mengyue Zhang, and Zhenwei Yan contributed equally to this work.

Authors and Affiliations

  1. The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, College of Life Sciences, Shandong University, Qingdao, 266237, Shandong, China

    Chunlei Zhang, Mengyue Zhang, Zhenwei Yan, Fengxia Wang, Huiyu Tian & Zhaojun Ding

  2. Shandong Key Laboratory of Water Pollution Control and Resource Reuse, School of Environmental Science and Engineering, Shandong University, Qingdao, 266237, Shandong, China

    Xianzheng Yuan & Shan Zhao

  3. State Key Laboratory of Microbial Technology, Shandong University, Qingdao, 266237, Shandong, China

    Zhaojun Ding

  4. Institute for Translational Medicine, Qingdao University, Qingdao, 266021, Shandong, China

    Lei Zhang

Authors
  1. Chunlei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mengyue Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhenwei Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fengxia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xianzheng Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Huiyu Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhaojun Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZD and HT designed the research. CZ, MZ, and FW conducted the experiments. CZ analyzed the data and wrote the manuscript. XY, SZ, ZY, LZ, HT, and ZD reviewed and edited the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Huiyu Tian or Zhaojun Ding.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Neal Stewart.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 kb)

Supplementary file2 (PPTX 2119 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, C., Zhang, M., Yan, Z. et al. CO2 is a key constituent of the plant growth-promoting volatiles generated by bacteria in a sealed system. Plant Cell Rep 40, 59–68 (2021). https://doi.org/10.1007/s00299-020-02610-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-020-02610-3

Keywords

Search

Navigation