Functional analysis of Pogostemon cablin farnesyl pyrophosphate synthase gene and its binding transcription factor PcWRKY44 in regulating biosynthesis of patchouli alcohol

Wang, Xiaobing; Tang, Yun; Huang, Huiling; Wu, Daidi; Chen, Xiuzhen; Li, Junren; Zheng, Hai; Zhan, Ruoting; Chen, Likai

doi:10.3389/fpls.2022.946629

Functional analysis of Pogostemon cablin farnesyl pyrophosphate synthase gene and its binding transcription factor PcWRKY44 in regulating biosynthesis of patchouli alcohol

Journal Article · Fri Aug 26 00:00:00 EDT 2022 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2022.946629· OSTI ID:1883653

Wang, Xiaobing; Tang, Yun; Huang, Huiling; Wu, Daidi; Chen, Xiuzhen; Li, Junren; Zheng, Hai; Zhan, Ruoting; Chen, Likai

Farnesyl pyrophosphate synthase (FPPS) plays an important role in the synthesis of plant secondary metabolites, but its function and molecular regulation mechanism remain unclear in Pogostemon cablin . In this study, the full-length cDNA of the FPP synthase gene from P. cablin ( PcFPPS ) was cloned and characterized. The expressions of PcFPPS are different among different tissues (highly in P. cablin flowers). Subcellular localization analysis in protoplasts indicated that PcFPPS was located in the cytoplasm. PcFPPS functionally complemented the lethal FPPS deletion mutation in yeast CC25. Transient overexpression of PcFPPS in P. cablin leaves accelerated terpene biosynthesis, with an ~47% increase in patchouli alcohol. Heterologous overexpression of PcFPPS in tobacco plants was achieved, and it was found that the FPP enzyme activity was significantly up-regulated in transgenic tobacco by ELISA analysis. In addition, more terpenoid metabolites, including stigmasterol, phytol, and neophytadiene were detected compared with control by GC-MS analysis. Furthermore, with dual-LUC assay and yeast one-hybrid screening, we found 220 bp promoter of PcFPPS can be bound by the nuclear-localized transcription factor PcWRKY44. Overexpression of PcWRKY44 in P. cablin upregulated the expression levels of PcFPPS and patchoulol synthase gene ( PcPTS ), and then promote the biosynthesis of patchouli alcohol. Taken together, these results strongly suggest the PcFPPS and its binding transcription factor PcWRKY44 play an essential role in regulating the biosynthesis of patchouli alcohol.

View Journal Article

Sponsoring Organization:: USDOE Office of Electricity (OE), Advanced Grid Research & Development. Power Systems Engineering Research

OSTI ID:: 1883653

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 13; ISSN 1664-462X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

References (42)

An Improved Transient Expression System UsingArabidopsisProtoplasts Cao, Yangrong; Li, Hong; Pham, An Q. Current Protocols in Plant Biology, Vol. 1, Issue 2 https://doi.org/10.1002/cppb.20013	journal	March 2016
Volatile organic compounds of tobacco leaves versus waste (scrap, dust, and midrib): extraction and optimization Banožić, Marija; Aladić, Krunoslav; Jerković, Igor Journal of the Science of Food and Agriculture, Vol. 101, Issue 5 https://doi.org/10.1002/jsfa.10796	journal	September 2020
Differential expression of farnesyl diphosphate synthase gene from Withania somnifera in different chemotypes and in response to elicitors Gupta, Parul; Akhtar, Nehal; Tewari, Shri Krishna Plant Growth Regulation, Vol. 65, Issue 1 https://doi.org/10.1007/s10725-011-9578-x	journal	March 2011
WRKY45-dependent priming of diterpenoid phytoalexin biosynthesis in rice and the role of cytokinin in triggering the reaction Akagi, Aya; Fukushima, Setsuko; Okada, Kazunori Plant Molecular Biology, Vol. 86, Issue 1-2 https://doi.org/10.1007/s11103-014-0221-x	journal	July 2014
Anti-nociceptive effect of patchouli alcohol: Involving attenuation of cyclooxygenase 2 and modulation of mu-opioid receptor Yu, Xuan; Wang, Xin-pei; Yan, Xiao-jin Chinese Journal of Integrative Medicine, Vol. 25, Issue 6 https://doi.org/10.1007/s11655-017-2952-4	journal	August 2017
Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation Chen, Da-Hua; Ye, He-Chun; Li, Guo-Feng Plant Science, Vol. 155, Issue 2 https://doi.org/10.1016/S0168-9452(00)00217-X	journal	June 2000
Patchouli alcohol protects against chronic unpredictable mild stress-induced depressant-like behavior through inhibiting excessive autophagy via activation of mTOR signaling pathway Zhuo, Jianyi; Chen, Baoyi; Sun, Chaoyue Biomedicine & Pharmacotherapy, Vol. 127 https://doi.org/10.1016/j.biopha.2020.110115	journal	July 2020
Phytol: A review of biomedical activities Islam, Muhammad Torequl; Ali, Eunüs S.; Uddin, Shaikh J. Food and Chemical Toxicology, Vol. 121 https://doi.org/10.1016/j.fct.2018.08.032	journal	November 2018
PatSWC4, a methyl jasmonate-responsive MYB (v-myb avian myeloblastosis viral oncogene homolog)-related transcription factor, positively regulates patchoulol biosynthesis in Pogostemon cablin Chen, Xiuzhen; Li, Junren; Liu, Yanting Industrial Crops and Products, Vol. 154 https://doi.org/10.1016/j.indcrop.2020.112672	journal	October 2020
The subcellular localization of periwinkle farnesyl diphosphate synthase provides insight into the role of peroxisome in isoprenoid biosynthesis Thabet, Insaf; Guirimand, Grégory; Courdavault, Vincent Journal of Plant Physiology, Vol. 168, Issue 17 https://doi.org/10.1016/j.jplph.2011.06.017	journal	November 2011
WRKY transcription factors Rushton, Paul J.; Somssich, Imre E.; Ringler, Patricia Trends in Plant Science, Vol. 15, Issue 5 https://doi.org/10.1016/j.tplants.2010.02.006	journal	May 2010
PatDREB Transcription Factor Activates Patchoulol Synthase Gene Promoter and Positively Regulates Jasmonate-Induced Patchoulol Biosynthesis Chen, Xiuzhen; Wang, Xiaobing; Wu, Daidi Journal of Agricultural and Food Chemistry, Vol. 70, Issue 23 https://doi.org/10.1021/acs.jafc.2c01660	journal	June 2022
The transcription factor OpWRKY2 positively regulates the biosynthesis of the anticancer drug camptothecin in Ophiorrhiza pumila Hao, Xiaolong; Xie, Chenhong; Ruan, Qingyan Horticulture Research, Vol. 8, Issue 1 https://doi.org/10.1038/s41438-020-00437-3	journal	January 2021
AaWRKY17, a positive regulator of artemisinin biosynthesis, is involved in resistance to Pseudomonas syringae in Artemisia annua Chen, Tiantian; Li, Yongpeng; Xie, Lihui Horticulture Research, Vol. 8, Issue 1 https://doi.org/10.1038/s41438-021-00652-6	journal	October 2021
Chromosome-level and haplotype-resolved genome provides insight into the tetraploid hybrid origin of patchouli Shen, Yanting; Li, Wanying; Zeng, Ying Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-31121-w	journal	June 2022
Overexpression ofArabidopsis thalianafarnesyl diphosphate synthase (FPS1S) in transgenicArabidopsisinduces a cell death/senescence-like response and reduced cytokinin levels Masferrer, Angela; Arró, Montserrat; Manzano, David The Plant Journal, Vol. 30, Issue 2 https://doi.org/10.1046/j.1365-313X.2002.01273.x	journal	April 2002
SIMULTANEOUS DETERMINATION OF EIGHT FLAVONOIDS AND POGOSTONE IN POGOSTEMON CABLIN BY HIGH PERFORMANCE LIQUID CHROMATOGRAPHY Li, Ping; Yin, Zhi-Qi; Li, Song-Lin Journal of Liquid Chromatography & Related Technologies, Vol. 37, Issue 12 https://doi.org/10.1080/10826076.2013.809545	journal	March 2014
The WRKY transcription factor AaGSW2 promotes glandular trichome initiation in Artemisia annua Xie, Lihui; Yan, Tingxiang; Li, Ling Journal of Experimental Botany, Vol. 72, Issue 5 https://doi.org/10.1093/jxb/eraa523	journal	November 2020
Genome-wide investigation of WRKY transcription factors in sweet osmanthus and their potential regulation of aroma synthesis Ding, Wenjie; Ouyang, Qixia; Li, Yuli Tree Physiology, Vol. 40, Issue 4 https://doi.org/10.1093/treephys/tpz129	journal	December 2019
Regulation of Specialized Metabolism by WRKY Transcription Factors Schluttenhofer, Craig; Yuan, Ling Plant Physiology, Vol. 167, Issue 2 https://doi.org/10.1104/pp.114.251769	journal	December 2014
LEFPS1, a Tomato Farnesyl Pyrophosphate Gene Highly Expressed during Early Fruit Development Gaffe, Joel; Bru, Jean-Philippe; Causse, Mathilde Plant Physiology, Vol. 123, Issue 4 https://doi.org/10.1104/pp.123.4.1351	journal	August 2000
Antifungal Effect ofAllium tuberosum,Cinnamomum cassia,andPogostemon cablinEssential Oils and Their Components Against Population ofAspergillusSpecies Kocevski, Dragana; Du, Muying; Kan, Jianquan Journal of Food Science, Vol. 78, Issue 5 https://doi.org/10.1111/1750-3841.12118	journal	May 2013
A farnesyl pyrophosphate synthase gene expressed in pollen functions in S ‐ RN ase‐independent unilateral incompatibility Qin, Xiaoqiong; Li, Wentao; Liu, Yang The Plant Journal, Vol. 93, Issue 3 https://doi.org/10.1111/tpj.13796	journal	January 2018
In Vitro and In Vivo Antibacterial Activities of Patchouli Alcohol, a Naturally Occurring Tricyclic Sesquiterpene, against Helicobacter pylori Infection Xu, Y. F.; Lian, D. W.; Chen, Y. Q. Antimicrobial Agents and Chemotherapy, Vol. 61, Issue 6 https://doi.org/10.1128/AAC.00122-17	journal	June 2017
Positive selection and functional divergence of farnesyl pyrophosphate synthase genes in plants Qian, Jieying; Liu, Yong; Chao, Naixia BMC Molecular Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12867-017-0081-4	journal	February 2017
Full-length transcriptome sequencing and methyl jasmonate-induced expression profile analysis of genes related to patchoulol biosynthesis and regulation in Pogostemon cablin Chen, Xiuzhen; Li, Junren; Wang, Xiaobing BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1884-x	journal	June 2019
Molecular identification and expression of sesquiterpene pathway genes responsible for patchoulol biosynthesis and regulation in Pogostemon cablin Tang, Yun; Zhong, Liting; Wang, Xiaobing Botanical Studies, Vol. 60, Issue 1 https://doi.org/10.1186/s40529-019-0259-9	journal	July 2019
Characterization of Arabidopsis FPS Isozymes and FPS Gene Expression Analysis Provide Insight into the Biosynthesis of Isoprenoid Precursors in Seeds Keim, Verónica; Manzano, David; Fernández, Francisco J. PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0049109	journal	November 2012
Analysis ofPogostemon cablinfrom pharmaceutical research to market performances Chen, Meiwan; Zhang, Jinming; Lai, Yunfeng Expert Opinion on Investigational Drugs, Vol. 22, Issue 2 https://doi.org/10.1517/13543784.2013.754882	journal	December 2012
Farnesyl diphosphate synthase; regulation of product specificity. Szkopińska, Anna; Płochocka, Danuta Acta Biochimica Polonica, Vol. 52, Issue 1 https://doi.org/10.18388/abp.2005_3485	journal	March 2005
Structural Analysis of Farnesyl Pyrophosphate Synthase from Parasitic Protozoa, a Potential Chemotherapeutic Target Srivastava, Anuradha; Mukherjee, Prasenjit; Desai, Prashant Infectious Disorders - Drug Targets, Vol. 8, Issue 1 https://doi.org/10.2174/187152608784139587	journal	March 2008
Cloning and characterization of Farnesyl pyrophosphate synthase gene from Anoectochilus Yang, Lin; Zhang, Jun Cheng; Li, Wan Chen Pakistan Journal of Botany, Vol. 52, Issue 3 https://doi.org/10.30848/PJB2020-3(14)	journal	December 2019
Genomic Characterization of WRKY Transcription Factors Related to Andrographolide Biosynthesis in Andrographis paniculata Zhang, Rongrong; Chen, Zhenzhen; Zhang, Libing Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.601689	journal	January 2021
Unraveling the Novel Protective Effect of Patchouli Alcohol Against Helicobacter pylori-Induced Gastritis: Insights Into the Molecular Mechanism in vitro and in vivo Lian, Da-wei; Xu, Yi-fei; Ren, Wen-kang Frontiers in Pharmacology, Vol. 9 https://doi.org/10.3389/fphar.2018.01347	journal	November 2018
Why Do Plants Convert Sitosterol to Stigmasterol? Aboobucker, Siddique I.; Suza, Walter P. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00354	journal	March 2019
Transcriptome-Wide Identification of WRKY Transcription Factor and Functional Characterization of RgWRKY37 Involved in Acteoside Biosynthesis in Rehmannia glutinosa Wang, Fengqing; Li, Xinrong; Zuo, Xin Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.739853	journal	September 2021
Genome-Wide Identification of R2R3-MYB Transcription Factors: Discovery of a “Dual-Function” Regulator of Gypenoside and Flavonol Biosynthesis in Gynostemma pentaphyllum Huang, Ding; Ming, Ruhong; Xu, Shiqiang Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.796248	journal	January 2022
Cloning and Characterization of Farnesyl Diphosphate Synthase Gene Involved in Triterpenoids Biosynthesis from Poria cocos Wang, Jianrong; Li, Yangyuan; Liu, Danni International Journal of Molecular Sciences, Vol. 15, Issue 12 https://doi.org/10.3390/ijms151222188	journal	December 2014
A Comprehensive Review on the Phytochemical Constituents and Pharmacological Activities of Pogostemon cablin Benth.: An Aromatic Medicinal Plant of Industrial Importance Swamy, Mallappa; Sinniah, Uma Molecules, Vol. 20, Issue 5 https://doi.org/10.3390/molecules20058521	journal	May 2015
Strengthening Triterpene Saponins Biosynthesis by Over-Expression of Farnesyl Pyrophosphate Synthase Gene and RNA Interference of Cycloartenol Synthase Gene in Panax notoginseng Cells Yang, Yan; Ge, Feng; Sun, Ying Molecules, Vol. 22, Issue 4 https://doi.org/10.3390/molecules22040581	journal	April 2017
Anti-inflammatory effect of patchouli alcohol isolated from Pogostemonis Herba in LPS-stimulated RAW264.7 macrophages Xian, Yan-Fang; Li, Yu-Cui; Ip, Siu-Po Experimental and Therapeutic Medicine, Vol. 2, Issue 3 https://doi.org/10.3892/etm.2011.233	journal	January 2011
Subcellular evidence for the involvement of peroxisomes in plant isoprenoid biosynthesis Clastre, Marc; Papon, Nicolas; Courdavault, Vincent Plant Signaling & Behavior, Vol. 6, Issue 12 https://doi.org/10.4161/psb.6.12.18173	journal	December 2011

Similar Records

Biosynthesis of the sesquiterpene patchoulol from farnesyl pyrophosphate in leaf extracts of Pogostemon cablin (patchouli): mechanistic considerations

Journal Article · Wed Jul 01 00:00:00 EDT 1987 · Arch. Biochem. Biophys.; (United States) · OSTI ID:6132900

Engineering a universal and efficient platform for terpenoid synthesis in yeast

Journal Article · Tue Dec 27 19:00:00 EST 2022 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:2417703

Structural and thermodynamic basis of the inhibition of Leishmania major farnesyl diphosphate synthase by nitrogen-containing bisphosphonates

Journal Article · Fri Feb 28 23:00:00 EST 2014 · Acta Crystallographica. Section D: Biological Crystallography · OSTI ID:22351310

Functional analysis of Pogostemon cablin farnesyl pyrophosphate synthase gene and its binding transcription factor PcWRKY44 in regulating biosynthesis of patchouli alcohol

Citation Formats

References (42)

Similar Records

Related Subjects