Fungal endophyte-induced volatile oil accumulation in Atractylodes lancea plantlets is mediated by nitric oxide, salicylic acid and hydrogen peroxide

Wang, Yu; Dai, Chuan‐Chao; Zhao, Yawei; Peng, Yao

doi:10.1016/j.procbio.2010.11.020

Cited by 59 publications

(73 citation statements)

References 41 publications

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“…S4F to I). These results indicate that endophytic bacterium-triggered ROS not only can act as signaling molecules (14) but also can directly oxidize oxygen-free sesquiterpenoids, increasing the content and diversity of oxygenous sesquiterpenoids in planta. Moreover, Yan et al (41) recently reported that the fumitremorgin B endoperoxidase from Aspergillus fumigatus can catalyze the formation of the peroxide bridge in verruculogen, providing a basis for the identification of endophyte-derived oxidases that function in plant oxygenous terpenoid formation.…”

Section: Discussionmentioning

confidence: 85%

“…Higher oxygenous sesquiterpenoid diversity and content are characteristics of the geo-authentic A. lancea grown in the Maoshan area (3). Hinesol, ␤-eudesmol, atractylone, and caryophyllene oxide are characteristic sesquiterpenoid components in the geo-authentic A. lancea (14). The isolation rate of endophytes from the geo-authentic A. lancea is also much higher than that found when A. lancea is grown in other areas (8)(9)(10).…”

Section: Discussionmentioning

confidence: 95%

“…Endogenous H 2 O 2 and hydroxyl radical content were measured with H 2 O 2 and hydroxyl radical assay kits (Nanjing Jiancheng Bio-Engineering Institute, China), respectively (14). Singlet oxygen levels were determined using a spectrophotometric method according to Yang et al (27).…”

Section: Methodsmentioning

confidence: 99%

“…strain AL12, can efficiently increase oxygenous sesquiterpenoid accumulation in A. lancea (11)(12)(13). These endophytes can activate signaling molecules, such as hydrogen peroxide (H 2 O 2 ), salicylic acid, and jasmonic acid (14,15), which increase the expression of genes encoding key enzymes involved in sesquiterpenoid biosynthesis pathways (13), promoting the formation of sesquiterpenoid hydrocarbon scaffolds in A. lancea. However, the mechanisms by which endophytes promote the oxidation of sesquiterpenoid hydrocarbon scaffolds and increase oxygenous sesquiterpenoid accumulation are unknown.…”

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confidence: 99%

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Endophytic Bacterium-Triggered Reactive Oxygen Species Directly Increase Oxygenous Sesquiterpenoid Content and Diversity in Atractylodes lancea

Zhou

Yuan

et al. 2016

Appl Environ Microbiol

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bOxygenous terpenoids are active components of many medicinal plants. However, current studies that have focused on enzymatic oxidation reactions cannot comprehensively clarify the mechanisms of oxygenous terpenoid synthesis and diversity. This study shows that an endophytic bacterium can trigger the generation of reactive oxygen species (ROS) that directly increase oxygenous sesquiterpenoid content and diversity in Atractylodes lancea. A. lancea is a famous but endangered Chinese medicinal plant that contains abundant oxygenous sesquiterpenoids. Geo-authentic A. lancea produces a wider range and a greater abundance of oxygenous sesquiterpenoids than the cultivated herb. Our previous studies have shown the mechanisms behind endophytic promotion of the production of sesquiterpenoid hydrocarbon scaffolds; however, how endophytes promote the formation of oxygenous sesquiterpenoids and their diversity is unclear. After colonization by Pseudomonas fluorescens ALEB7B, oxidative burst and oxygenous sesquiterpenoid accumulation in A. lancea occur synchronously. Treatment with exogenous hydrogen peroxide (H 2 O 2 ) or singlet oxygen induces oxidative burst and promotes oxygenous sesquiterpenoid accumulation in planta. Conversely, pretreatment of plantlets with the ROS scavenger ascorbic acid significantly inhibits the oxidative burst and oxygenous sesquiterpenoid accumulation induced by P. fluorescens ALEB7B. Further in vitro oxidation experiments show that several oxygenous sesquiterpenoids can be obtained from direct oxidation caused by H 2 O 2 or singlet oxygen. In summary, this study demonstrates that endophytic bacterium-triggered ROS can directly oxidize oxygen-free sesquiterpenoids and increase the oxygenous sesquiterpenoid content and diversity in A. lancea, providing a novel explanation of the mechanisms of oxygenous terpenoid synthesis in planta and an essential complementarity to enzymatic oxidation reactions.A tractylodes lancea is a traditional Chinese medicinal plant and is the main ingredient of many famous Chinese medicines. Oxygenous sesquiterpenoids, such as hinesol, ␤-eudesmol, atractylone, and caryophyllene oxide, are the main active components in A. lancea and have medicinal efficacy against rheumatic diseases, digestive disorders, night blindness, and influenza (1). The quality of A. lancea strongly depends on the area in which the herb is produced, and A. lancea grown in the Maoshan area of the Jiangsu Province is the geo-authentic herb (2), which is characterized by higher oxygenous sesquiterpenoid content and diversity than herbs grown in other areas (3). In recent years, the geoauthentic A. lancea has become endangered due to habitat destruction and overexploitation. Although cultivation ensures the production of medicinal materials, the oxygenous sesquiterpenoid content and diversity in cultivated A. lancea is considerably decreased compared to that of the wild herb. Currently, knowledge on the biosynthesis and diversity of oxygenous sesquiterpenoids is insufficient. Some studies have explained...

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Section: Discussionmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 95%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Endophytic Bacterium-Triggered Reactive Oxygen Species Directly Increase Oxygenous Sesquiterpenoid Content and Diversity in Atractylodes lancea

Zhou

Yuan

et al. 2016

Appl Environ Microbiol

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“…Gilmaniella sp. AL12 induced essential oil accumulation in A. lancea via hydrogen peroxide (H 2 O 2 ) and hormone signaling (Ren et al 2014;Ren and Dai 2012;Wang et al 2011;Yuan et al 2016), while Acinetobacter sp. ALEB16 induced essential oil accumulation via abscisic acid (ABA) and salicylic acid (SA) signaling (Wang et al 2015b).…”

Section: Introductionmentioning

confidence: 99%

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

Zhou

Zhao

et al. 2016

Planta

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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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Consequences of antagonistic interactions between endophytic fungus and bacterium on plant growth and defense responses in Atractylodes lancea

Wang

Yang

Wang

et al. 2013

J. Basic Microbiol.

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Many studies have examined pair‐wise interactions between plants and endophytes, while overlooking the interplays among multiple endosymbionts and their combined impacts on hosts. In this study, Atractylodes lancea plantlets were inoculated with endophytic fungus Acremonium strictum AL16, or endophytic bacterium Acinetobacter sp., or both, to investigate the impacts of the three‐way symbiosis on the host. Our results showed that defense‐related responses of the co‐inoculated plantlets were delayed and weakened relative to plantlets with single inoculants, but no detrimental effects on phyto‐physiology (growth, photosynthesis) were observed after combined inoculations. Quantitative PCR analysis verified a decrease in AL16 colonization density within plants after co‐inoculation with the endobacteria. An in vitro assay was then performed to elucidate the suppressed plant defense responses and reduced fungal colonization by dual inoculation. The data showed that the presence of Acinetobacter sp. reduced AL16 colony diameter and spore germination rate without negatively affecting fungal morphology. Additionally, direct hyphal attachment of the bacterium to AL16 in vitro was visualized by scanning electronic microscopy. Therefore, we propose that a balanced and compatible symbiosis might require constraints conferred by the antagonistic endophyte Acinetobacter sp. on the fungus AL16 in the tripartite endophytic bacterium–fungus–plant system.

show abstract

Fungal endophyte-induced volatile oil accumulation in Atractylodes lancea plantlets is mediated by nitric oxide, salicylic acid and hydrogen peroxide

Cited by 59 publications

References 41 publications

Endophytic Bacterium-Triggered Reactive Oxygen Species Directly Increase Oxygenous Sesquiterpenoid Content and Diversity in Atractylodes lancea

Endophytic Bacterium-Triggered Reactive Oxygen Species Directly Increase Oxygenous Sesquiterpenoid Content and Diversity in Atractylodes lancea

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

Consequences of antagonistic interactions between endophytic fungus and bacterium on plant growth and defense responses in Atractylodes lancea

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