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The primary mechanism of endophytic fungus Gilmaniella sp. AL12 promotion of plant growth and sesquiterpenoid accumulation in Atractylodes lancea

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Abstract

Atractylodes lancea is a traditional Chinese herb, and its quality depends on the main active compounds sesquiterpenoids. In recent years, guaranteeing the quality and yield of A. lancea has become problematic. Our previous results have shown that the endophytic fungus AL12 (Gilmaniella sp.) promotes plant growth and sesquiterpenoid biosynthesis of A. lancea. However, little has been done to uncover the mechanism of this “double-promotion”. In this study, plant biomass and sesquiterpenoid content were analyzed to verify this “double-promotion” effect of AL12 on A. lancea. Physiological tests (such as root viability, element content, rubisco content, and some phytohormones levels) were performed to try to identify the mechanism of improved plant growth. The results showed that growth promotion effect induced by AL12 on A. lancea may depend on increased nutrient content, improved photosynthesis and enhanced cytokinin signaling. Secondary metabolite biosynthesis consumes substance and energy during plant growth. Transcript analysis indicated that AL12 stimulates sesquiterpenoid biosynthesis through the MVA pathway. Physiological tests (such as sesquiterpenoid biosynthesis precursors and organic acids of tricarboxylic acid cycle) were performed to try to identify the mechanism of improved sesquiterpenoid accumulation. The results showed that AL12 improves the primary metabolism of A. lancea including photosynthesis, glycolysis, and the TCA cycle, thus providing sufficient carbon and energy for sesquiterpenoid biosynthesis. To summarize, this work uncover the primary mechanism of AL12 promotion of plant growth and sesquiterpenoid accumulation in A. lancea. This study provides a theoretical basis for obtaining higher yield and quality medicinal plants and also provides a framework to understand plant–endophyte interactions.

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Abbreviations

AMF:

Arbuscular mycorrhizal fungi

A. lancea :

Atractylodes lancea

AL12:

Endophytic fungus Gilmaniella sp. AL12

NO:

Nitric oxide

H2O2 :

Hydrogen peroxide

SA:

Salicylic acid

JA:

Jasmonic acid

Br:

Brassinosteroid

Ca2+ :

Calcium

MVA:

Mevalonate

MS medium:

Murashige and Skoog medium

NAA:

Naphthaleneacetic acid

6-BA:

6-Benzyladenine

PDA:

Potato dextrose agar

GC:

Gas chromatograph

MS:

Mass spectrometer

TTC:

Triphenyltetrazolium chloride

TFA:

Trichloroacetic acid

PVPP:

Polyvinylpolypyrrolidone

HPLC:

High-performance liquid chromatography

PVP:

Polyvinylpyrrolidone

BHT:

Butylated hydroxytoluene

2-OG:

2-Oxpentanedioic acid

IAA:

Indole-3-acetic acid

GA:

Gibberellin

ABA:

Abscisic acid

CTK:

Cytokinin

RT-qPCR:

Real-time quantitative PCR

EF1α :

Elongation factor 1 alpha

C t :

Cycle threshold

SD:

Standard deviations

MEP:

2-C-methyl-d-erythritol-4-phosphate

HMGR :

3-Hydroxy-3-methylgutaryl coenzyme A reductase

DXR :

1-Deoxy-d-xylulose 5-phosphate reductoisomerase

TCA cycle:

Tricarboxylic acid cycle

ATP:

Triphosadenine

ETH:

Ethylene

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Acknowledgments

Financial support was provided by the National Natural Science Foundation of China (Grant No. 31070443), a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, Promoting Project for Industrialization of Jiangsu Higher Education Institutions (Grant No. JHB2012-16), and Nanjing Produce-Learn-Research Project (Grant No. 201306019).

Authors’ contribution

J.Y. designed and carried out most of the experiments. J.Y.Z. helped for metabolite determination and GC–MS analysis. X.L. helped for net photosynthesis rate measurement. J.Y. analyzed data and wrote the manuscript. C.C.D. supervised the work and interpreted data with J.Y. All authors read and approved the final manuscript.

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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 Province, China

    Jie Yuan, Jia-Yu Zhou & Chuan-Chao Dai

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

    Xia Li

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  1. Jie Yuan
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Correspondence to Chuan-Chao Dai.

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Yuan, J., Zhou, JY., Li, X. et al. The primary mechanism of endophytic fungus Gilmaniella sp. AL12 promotion of plant growth and sesquiterpenoid accumulation in Atractylodes lancea . Plant Cell Tiss Organ Cult 125, 571–584 (2016). https://doi.org/10.1007/s11240-016-0971-z

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