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Reactive oxygen species and hormone signaling cascades in endophytic bacterium induced essential oil accumulation in Atractylodes lancea

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Abstract

Main conclusion

Pseudomonas fluorescens induces gibberellin and ethylene signaling via hydrogen peroxide in planta . Ethylene activates abscisic acid signaling. Hormones increase sesquiterpenoid biosynthesis gene expression and enzyme activity, inducing essential oil accumulation.

Atractylodes lancea is a famous Chinese medicinal plant, whose main active components are essential oils. Wild A. lancea has become endangered due to habitat destruction and over-exploitation. Although cultivation can ensure production of the medicinal material, the essential oil content in cultivated A. lancea is significantly lower than that in the wild herb. The application of microbes as elicitors has become an effective strategy to increase essential oil accumulation in cultivated A. lancea. Our previous study identified an endophytic bacterium, Pseudomonas fluorescens ALEB7B, which can increase essential oil accumulation in A. lancea more efficiently than other endophytes; however, the underlying mechanisms remain unknown (Physiol Plantarum 153:30–42, 2015; Appl Environ Microb 82:1577–1585, 2016). This study demonstrates that P. fluorescens ALEB7B firstly induces hydrogen peroxide (H2O2) signaling in A. lancea, which then simultaneously activates gibberellin (GA) and ethylene (ET) signaling. Subsequently, ET activates abscisic acid (ABA) signaling. GA and ABA signaling increase expression of HMGR and DXR, which encode key enzymes involved in sesquiterpenoid biosynthesis, leading to increased levels of the corresponding enzymes and then an accumulation of essential oils. Specific reactive oxygen species and hormone signaling cascades induced by P. fluorescens ALEB7B may contribute to high-efficiency essential oil accumulation in A. lancea. Illustrating the regulation mechanisms underlying P. fluorescens ALEB7B-induced essential oil accumulation not only provides the theoretical basis for the inducible synthesis of terpenoids in many medicinal plants, but also further reveals the complex and diverse interactions among different plants and their endophytes.

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Abbreviations

ABA:

Abscisic acid

ACC:

1-Aminocyclopropanecarboxylic acid

AOA:

Aminooxyacetic acid

BR:

Brassinosteroid

CAT:

Catalase

DXR:

1-Deoxy-d-xylulose 5-phosphate reductoisomerase

ET:

Ethylene

Flu:

Fluridone

GA:

Gibberellin

GC:

Gas chromatography

HMGR:

3-Hydroxy-3-methylglutaryl-CoA reductase

H2O2 :

Hydrogen peroxide

HPLC:

High Performance Liquid Chromatography

JA:

Jasmonic acid

MEP:

2-C-Methyl-d-erythritol phosphate

MVA:

Mevalonate

NAA:

Naphthaleneacetic acid

NO:

Nitric oxide

PAC:

Paclobutrazol

ROS:

Reactive oxygen species

SA:

Salicylic acid

References

  • Chamam A, Wisniewski-Dyé F, Comte G, Bertrand C, Prigent-Combaret C (2015) Differential responses of Oryza sativa secondary metabolism to biotic interactions with cooperative, commensal and phytopathogenic bacteria. Planta 242:1439–1452

    Article  CAS  PubMed  Google Scholar 

  • Dai ZC, Fu W, Qi SS, Zhai DL, Chen SC, Wan LY, Huang P, Du DL (2016) Different responses of an invasive clonal plant Wedelia trilobata and its native congener to gibberellin: implications for biological invasion. J Chem Ecol 42:85–94

    Article  CAS  PubMed  Google Scholar 

  • De Bruyne L, Höfte M, De Vleesschauwer D (2014) Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Mol Plant 7:943–959

    Article  PubMed  Google Scholar 

  • Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124:1437–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasunuma T, Takeno S, Hayashi S, Sendai M, Bamba T, Yoshimura S, Tomizawa KI, Fukusaki E, Miyake C (2008) Overexpression of 1-deoxy-d-xylulose-5-phosphate reductoisomerase gene in chloroplast contributes to increment of isoprenoid production. J Biosci Bioeng 105:518–526

    Article  CAS  PubMed  Google Scholar 

  • Heinrich M, Hettenhausen C, Lange T, Wünsche H, Fang JJ, Baldwin lan T, Wu JQ (2012) High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuate stems. Plant J 73:591–606

    Article  PubMed  Google Scholar 

  • Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian PP, Xin W, Li HY, Burritt DJ, Fujita M, Tran LSP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420

    PubMed  PubMed Central  Google Scholar 

  • Jacobo-Velázquez DA, González-Agüero M, Cisneros-Zevallos L (2015) Cross-talk between signaling pathways: the link between plant secondary metabolite production and wounding stress response. Sci Rep-UK 5:8608

    Article  Google Scholar 

  • Ji L, Ao P, Pan JG, Yang JY, Yang J, Hu SL (2001) GC–MS analysis of essential oils from rhizomes of Atractylodes lancea (Thunb.) DC. and A. chinensis (DC.) Koidz. China Journal of Chinese Materia Medica 26:182–185 in Chinese

    CAS  PubMed  Google Scholar 

  • Li Y, Zhang L, Lu W, Wang X, Wu CA, Guo X (2014) Overexpression of cotton GhMKK4 enhances disease susceptibility and affects abscisic acid, gibberellin and hydrogen peroxide signalling in transgenic Nicotiana benthamiana. Mol Plant Pathol 15:94–108

    Article  PubMed  Google Scholar 

  • Liang ZC, Ma YN, Xu T, Cui BM, Liu Y, Guo ZX, Yang DF (2013) Effects of abscisic acid, gibberellin, ethylene and their interactions on production of phenolic acids in Salvia miltiorrhiza Bunge hairy roots. PLoS One 8:e72806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang J, Wang Y, Ding G, Li W, Yang G, He N (2015) Biotic stress-induced expression of mulberry cystatins and identification of cystatin exhibiting stability to silkworm gut proteinases. Planta 242:1139–1151

    Article  CAS  PubMed  Google Scholar 

  • Linkies A, Leubner-Metzger G (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Rep 31:253–270

    Article  CAS  PubMed  Google Scholar 

  • Liu YG, Ye NH, Liu R, Chen MX, Zhang JH (2010) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. J Exp Bot 61:2979–2990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mansouri H, Asrar Z, Szopa J (2009) Effects of ABA on primary terpenoids and Δ9–tetrahydrocannabinol in Cannabis sativa L. at flowering stage. Plant Growth Regul 58:269–277

    Article  CAS  Google Scholar 

  • Miller B, Heuser T, Zimmer W (2000) Functional involvement of a deoxy-d-xylulose 5-phosphate reductoisomerase gene harboring locus of Synechococcus leopoliensis in isoprenoid biosynthesis. FEBS Lett 481:221–226

    Article  CAS  PubMed  Google Scholar 

  • Murthy HN, Lee EJ, Paek KY (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tiss Org 118:1–16

    Article  CAS  Google Scholar 

  • Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microbiology early interactions. J Integr Plant Biol 52:195–204

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang Z, Zhang L, Zhao M, Wang P, Wei Y, Fang J (2012) Identification and quantification of sesquiterpenes and polyacetylenes in Atractylodes lancea from various geographical origins using GC–MS analysis. Rev Bras Farmacogn 22:957–963

    Article  CAS  Google Scholar 

  • Rahimi S, Kim YJ, Yang DC (2015) Production of ginseng saponins: elicitation strategy and signal transductions. Appl Microbiol Biot 99:6987–6996

    Article  CAS  Google Scholar 

  • Ren CG, Dai CC (2012) Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets. BMC Plant Biol 12:128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren CG, Dai CC (2013) Nitric oxide and brassinosteroids mediated fungal endophyte-induced volatile oil production through protein phosphorylation pathways in Atractylodes lancea plantlets. J Integr Plant Biol 55:1136–1146

    Article  CAS  PubMed  Google Scholar 

  • Ren CG, Chen Y, Dai CC (2014) Cross-talk between calcium–calmodulin and brassinolide for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets. J Plant Growth Regul 33:285–294

    Article  CAS  Google Scholar 

  • Rijnders JGHM, Yang YY, Kamiya Y, Takahashi N, Barendse GWM, Blom CWPM, Voesenek LACJ (1997) Ethylene enhances gibberellin levels and petiole sensitivity in flooding-tolerant Rumex palustris but not in flooding-intolerant R. acetosa. Planta 203:20–25

    Article  CAS  Google Scholar 

  • Ryan RP, Germaine K, Frank A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    Article  CAS  PubMed  Google Scholar 

  • Shan XY, Yan JB, Xie DX (2012) Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol 15:84–91

    Article  CAS  PubMed  Google Scholar 

  • Steffens B, Wang J, Sauter M (2006) Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223:604–612

    Article  CAS  PubMed  Google Scholar 

  • Toroser D, Huber SC (1998) 3-Hydroxy-3-methylglutaryl-coenzyme A reductase kinase and sucrose-phosphate synthase kinase activities in cauliflower florets: Ca2+ dependence and substrate specificities. Arch Biochem Biophys 355:291–300

    Article  CAS  PubMed  Google Scholar 

  • Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, Van Montagu M, Zabeau M, Inzé D, Breusegem V (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. P Natl Acad Sci USA 100:16113–16118

    Article  CAS  Google Scholar 

  • Wang Y, Dai CC, Zhao YW, Peng Y (2011) Fungal endophyte-induced volatile oil accumulation in Atractylodes lancea plantlets is mediated by nitric oxide, salicylic acid and hydrogen peroxide. Process Biochem 46:730–735

    Article  Google Scholar 

  • Wang Y, Dai CC, Cao JL, Xu DS (2012) Comparison of the effects of fungal endophyte Gilmaniella sp. and its elicitor on Atractylodes lancea plantlets. World J Microb Biot 28:575–584

    Article  Google Scholar 

  • Wang L, Fan XW, Pan JL, Huang ZB, Li YZ (2015a) Physiological characterization of maize tolerance to low dose of aluminum, highlighted by promoted leaf growth. Planta 242:1391–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XM, Yang B, Ren CG, Wang HW, Wang JY, Dai CC (2015b) Involvement of abscisic acid and salicylic acid in signal cascade regulating bacterial endophyte-induced volatile oil biosynthesis in plantlets of Atractylodes lancea. Physiol Plantarum 153:30–42

    Article  CAS  Google Scholar 

  • Würschum T, Tucker MR, Maurer HP, Leiser WL (2015) Ethylene inhibitors improve efficiency of microspore embryogenesis in hexaploid triticale. Plant Cell Tiss Org 122:751–757

    Article  Google Scholar 

  • Yuan J, Sun K, Deng-Wang MY, Dai CC (2016) The mechanism of ethylene signaling induced by endophytic fungus Gilmaniella sp. AL12 mediating sesquiterpenoids biosynthesis in Atractylodes lancea. Front. Plant Sci 7:361

    Google Scholar 

  • Zhou JY, Jia Y, Wang HW, Dai CC (2013) Diversity and plant growth-promoting potential of culturable endophytic bacteria isolated from the leaves of Atractylodes lancea. Acta Ecologica Sinica 33:1106–1117 in Chinese

    Article  CAS  Google Scholar 

  • Zhou JY, Zhao XY, Dai CC (2014) Antagonistic mechanisms of endophytic Pseudomonas fluorescens against Athelia rolfii. J Appl Microbiol 117:1144–1158

    Article  CAS  PubMed  Google Scholar 

  • Zhou JY, Yuan J, Li X, Ning YF, Dai CC (2016) Endophytic bacterium-triggered reactive oxygen species directly increase oxygenous sesquiterpenoid content and diversity in Atractylodes lancea. Appl Environ Microb 82:1577–1585

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by National Natural Science Foundation of China (Grant Number 31070443), Promoting Project for Industrialization of Jiangsu Higher Education Institutions (Grant Number JHB2012-16), Integration of Production and Research Projects of Nanjing Science and Technology Commission (Grant Number 201306019), and Graduate Education Innovation Project of Jiangsu Province (Grant Number KYLX15_0734).

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Authors and Affiliations

  1. Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Industrialization of Microbial Resources, College of Life Sciences, Nanjing Normal University, Nanjing, 210023, Jiangsu, China

    Jia-Yu Zhou, Dan Zhao, Meng-Yao Deng-Wang & Chuan-Chao Dai

  2. Jiangsu High Quality Rice Research and Development Center, Nanjing Branch of China National Center Rice Improvement, Institute of Food Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, Jiangsu, China

    Xia Li

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  1. Jia-Yu Zhou
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Correspondence to Chuan-Chao Dai.

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Zhou, JY., Li, X., Zhao, D. et al. Reactive oxygen species and hormone signaling cascades in endophytic bacterium induced essential oil accumulation in Atractylodes lancea . Planta 244, 699–712 (2016). https://doi.org/10.1007/s00425-016-2536-0

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