Activation of the plant mevalonate pathway by extracellular ATP

Cho, Sung-Hwan; Tóth, Katalin; Kim, Daewon; Vo, Phuc H.; Lin, Chung-Ho; Handakumbura, Pubudu P.; Ubach, Albert Rivas; Evans, Sterling; Paša-Tolić, Ljiljana; Stacey, Gary

doi:10.1038/s41467-022-28150-w

Title: Activation of the plant mevalonate pathway by extracellular ATP

Journal Article · 20 January 2022 · Nature Communications

DOI: https://doi.org/10.1038/s41467-022-28150-w · OSTI ID:1844182

^[1]; Tóth, Katalin ^[1];

^[1]; Vo, Phuc H. ^[1]; Lin, Chung-Ho ^[1];

^[2]; Ubach, Albert Rivas ^[2];

^[1];

^[2];

^[1]

Univ. of Missouri, Columbia, MO (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)

The mevalonate pathway plays a critical role in multiple cellular processes in both animals and plants. In plants, the products of this pathway impact growth and development, as well as the response to environmental stress. A forward genetic screen of Arabidopsis thaliana using Ca²⁺-imaging identified mevalonate kinase (MVK) as a critical component of plant purinergic signaling. MVK interacts directly with the plant extracellular ATP (eATP) receptor P2K1 and is phosphorylated by P2K1 in response to eATP. Mutation of P2K1-mediated phosphorylation sites in MVK eliminates the ATP-induced cytoplasmic calcium response, MVK enzymatic activity, and suppresses pathogen defense. The data demonstrate that the plasma membrane associated P2K1 directly impacts plant cellular metabolism by phosphorylation of MVK, a key enzyme in the mevalonate pathway. The results underline the importance of purinergic signaling in plants and the ability of eATP to influence the activity of a key metabolite pathway with global effects on plant metabolism.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); Rural Development Administration Korea; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1844182

Report Number(s):: PNNL-SA-155234

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 13; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (78)

Using MetaboAnalyst 4.0 for Comprehensive and Integrative Metabolomics Data Analysis Chong, Jasmine; Wishart, David S.; Xia, Jianguo Current Protocols in Bioinformatics, Vol. 68, Issue 1 https://doi.org/10.1002/cpbi.86	journal	September 2019
Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta Simkin, Andrew J.; Guirimand, Grégory; Papon, Nicolas Planta, Vol. 234, Issue 5 https://doi.org/10.1007/s00425-011-1444-6	journal	June 2011
Fluvastatin suppresses native and recombinant human P2X4 receptor function Li, Jing; Fountain, Samuel J. Purinergic Signalling, Vol. 8, Issue 2 https://doi.org/10.1007/s11302-011-9289-9	journal	January 2012
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave Metabolomics, Vol. 3, Issue 3 https://doi.org/10.1007/s11306-007-0082-2	journal	September 2007
Isolation and characterization of a cDNA encoding Arabidopsis thaliana mevalonate kinase by genetic complementation in yeast Riou, Catherine; Tourte, Yves; Lacroute, François Gene, Vol. 148, Issue 2 https://doi.org/10.1016/0378-1119(94)90701-3	journal	October 1994
Molecular cloning of human mevalonate kinase and identification of a missense mutation in the genetic disease mevalonic aciduria. Schafer, B. L.; Bishop, R. W.; Kratunis, V. J. Journal of Biological Chemistry, Vol. 267, Issue 19 https://doi.org/10.1016/S0021-9258(18)42199-0	journal	July 1992
Elicitor signal transduction leading to production of plant secondary metabolites Zhao, Jian; Davis, Lawrence C.; Verpoorte, Robert Biotechnology Advances, Vol. 23, Issue 4 https://doi.org/10.1016/j.biotechadv.2005.01.003	journal	June 2005
The potential of the mevalonate pathway for enhanced isoprenoid production Liao, Pan; Hemmerlin, Andréa; Bach, Thomas J. Biotechnology Advances, Vol. 34, Issue 5 https://doi.org/10.1016/j.biotechadv.2016.03.005	journal	September 2016
MAP Kinase Signaling Pathways: A Hub of Plant-Microbe Interactions Bi, Guozhi; Zhou, Jian-Min Cell Host & Microbe, Vol. 21, Issue 3 https://doi.org/10.1016/j.chom.2017.02.004	journal	March 2017
Mevalonate pathway: A review of clinical and therapeutical implications Buhaescu, Irina; Izzedine, Hassane Clinical Biochemistry, Vol. 40, Issue 9-10 https://doi.org/10.1016/j.clinbiochem.2007.03.016	journal	June 2007
The Cytokinin-Activated Transcription Factor ARR2 Promotes Plant Immunity via TGA3/NPR1-Dependent Salicylic Acid Signaling in Arabidopsis Choi, Jaemyung; Huh, Sung Un; Kojima, Mikiko Developmental Cell, Vol. 19, Issue 2 https://doi.org/10.1016/j.devcel.2010.07.011	journal	August 2010
Protective perfumes: the role of vegetative volatiles in plant defense against herbivores Unsicker, Sybille B.; Kunert, Grit; Gershenzon, Jonathan Current Opinion in Plant Biology, Vol. 12, Issue 4 https://doi.org/10.1016/j.pbi.2009.04.001	journal	August 2009
Sensing of molecular patterns through cell surface immune receptors Ranf, Stefanie Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.011	journal	August 2017
Extracellular ATP: an unexpected role as a signaler in plants Roux, Stanley J.; Steinebrunner, Iris Trends in Plant Science, Vol. 12, Issue 11 https://doi.org/10.1016/j.tplants.2007.09.003	journal	November 2007
Protein isoprenylation: the fat of the matter Crowell, Dring N.; Huizinga, David H. Trends in Plant Science, Vol. 14, Issue 3 https://doi.org/10.1016/j.tplants.2008.12.001	journal	March 2009
Regulation of the mevalonate pathway Goldstein, Joseph L.; Brown, Michael S. Nature, Vol. 343, Issue 6257 https://doi.org/10.1038/343425a0	journal	February 1990
Anticancer effects of phytosterols Woyengo, T. A.; Ramprasath, V. R.; Jones, P. J. H. European Journal of Clinical Nutrition, Vol. 63, Issue 7 https://doi.org/10.1038/ejcn.2009.29	journal	June 2009
DNAJA1 controls the fate of misfolded mutant p53 through the mevalonate pathway Parrales, Alejandro; Ranjan, Atul; Iyer, Swathi V. Nature Cell Biology, Vol. 18, Issue 11 https://doi.org/10.1038/ncb3427	journal	October 2016
Control of the innate immune response by the mevalonate pathway Akula, Murali K.; Shi, Man; Jiang, Zhaozhao Nature Immunology, Vol. 17, Issue 8 https://doi.org/10.1038/ni.3487	journal	June 2016
Are innate immune signaling pathways in plants and animals conserved? Ausubel, Frederick M. Nature Immunology, Vol. 6, Issue 10 https://doi.org/10.1038/ni1253	journal	September 2005
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.199	journal	June 2007
Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture Chen, Dongqin; Cao, Yangrong; Li, Hong Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02340-3	journal	December 2017
Missing Value Imputation Approach for Mass Spectrometry-based Metabolomics Data Wei, Runmin; Wang, Jingye; Su, Mingming Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-19120-0	journal	January 2018
Metabotyping as a Stopover in Genome-to-Phenome Mapping Handakumbura, Pubudu P.; Stanfill, Bryan; Rivas-Ubach, Albert Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-38483-0	journal	February 2019
Extracellular ATP, a danger signal, is recognized by DORN1 in Arabidopsis Choi, Jeongmin; Tanaka, Kiwamu; Liang, Yan Biochemical Journal, Vol. 463, Issue 3 https://doi.org/10.1042/BJ20140666	journal	October 2014
Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition Reiter, Wolf-Dieter; Chapple, Clint; Somerville, Chris R. The Plant Journal, Vol. 12, Issue 2 https://doi.org/10.1046/j.1365-313X.1997.12020335.x	journal	August 1997
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x	journal	December 1998
Mevalonic Aciduria — An Inborn Error of Cholesterol and Nonsterol Isoprene Biosynthesis Hoffmann, Georg; Gibson, Kenneth M.; Brandt, Ira K. New England Journal of Medicine, Vol. 314, Issue 25 https://doi.org/10.1056/NEJM198606193142504	journal	June 1986
A remorin protein interacts with symbiotic receptors and regulates bacterial infection Lefebvre, B.; Timmers, T.; Mbengue, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 5 https://doi.org/10.1073/pnas.0913320107	journal	January 2010
A role for the mevalonate pathway in early plant symbiotic signaling Venkateshwaran, Muthusubramanian; Jayaraman, Dhileepkumar; Chabaud, Mireille Proceedings of the National Academy of Sciences, Vol. 112, Issue 31 https://doi.org/10.1073/pnas.1413762112	journal	July 2015
Molecular cloning of mevalonate kinase and regulation of its mRNA levels in rat liver. Tanaka, R. D.; Lee, L. Y.; Schafer, B. L. Proceedings of the National Academy of Sciences, Vol. 87, Issue 8 https://doi.org/10.1073/pnas.87.8.2872	journal	April 1990
Identification of Catalytic Residues in Human Mevalonate Kinase Potter, David; Miziorko, Henry M. Journal of Biological Chemistry, Vol. 272, Issue 41 https://doi.org/10.1074/jbc.272.41.25449	journal	October 1997
Online Parallel Accumulation–Serial Fragmentation (PASEF) with a Novel Trapped Ion Mobility Mass Spectrometer Meier, Florian; Brunner, Andreas-David; Koch, Scarlet Molecular & Cellular Proteomics, Vol. 17, Issue 12 https://doi.org/10.1074/mcp.TIR118.000900	journal	November 2018
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
LOVASTATIN INSENSITIVE 1, a Novel Pentatricopeptide Repeat Protein, is a Potential Regulatory Factor of Isoprenoid Biosynthesis in Arabidopsis Kobayashi, Keiko; Suzuki, Masashi; Tang, Jianwei Plant and Cell Physiology, Vol. 48, Issue 2 https://doi.org/10.1093/pcp/pcm005	journal	February 2007
Genetic Evidence for the Role of Isopentenyl Diphosphate Isomerases in the Mevalonate Pathway and Plant Development in Arabidopsis Okada, Kazunori; Kasahara, Hiroyuki; Yamaguchi, Shinjiro Plant and Cell Physiology, Vol. 49, Issue 4 https://doi.org/10.1093/pcp/pcn032	journal	April 2008
The Arabidopsis FLAKY POLLEN1 Gene Encodes a 3-Hydroxy-3-Methylglutaryl-Coenzyme A Synthase Required for Development of Tapetum-Specific Organelles and Fertility of Pollen Grains Ishiguro, S.; Nishimori, Y.; Yamada, M. Plant and Cell Physiology, Vol. 51, Issue 6 https://doi.org/10.1093/pcp/pcq068	journal	May 2010
The challenge of autoinflammatory syndromes: with an emphasis on hyper-IgD syndrome van der Meer, Jos W. M.; Simon, Anna Rheumatology, Vol. 55, Issue suppl 2 https://doi.org/10.1093/rheumatology/kew351	journal	November 2016
Sterols Regulate Development and Gene Expression in Arabidopsis He, Jun-Xian; Fujioka, Shozo; Li, Tsai-Chi Plant Physiology, Vol. 131, Issue 3 https://doi.org/10.1104/pp.014605	journal	February 2003
Lectin Receptor Kinases Participate in Protein-Protein Interactions to Mediate Plasma Membrane-Cell Wall Adhesions in Arabidopsis Gouget, Anne; Senchou, Virginie; Govers, Francine Plant Physiology, Vol. 140, Issue 1 https://doi.org/10.1104/pp.105.066464	journal	December 2005
Dual Lipid Modification of Arabidopsis G γ -Subunits Is Required for Efficient Plasma Membrane Targeting Zeng, Qin; Wang, Xuejun; Running, Mark P. Plant Physiology, Vol. 143, Issue 3 https://doi.org/10.1104/pp.106.093583	journal	January 2007
GS52 Ecto-Apyrase Plays a Critical Role during Soybean Nodulation Govindarajulu, Manjula; Kim, Sung-Yong; Libault, Marc Plant Physiology, Vol. 149, Issue 2 https://doi.org/10.1104/pp.108.128728	journal	November 2008
Extracellular Nucleotides Elicit Cytosolic Free Calcium Oscillations in Arabidopsis Tanaka, Kiwamu; Swanson, Sarah J.; Gilroy, Simon Plant Physiology, Vol. 154, Issue 2 https://doi.org/10.1104/pp.110.162503	journal	July 2010
Suppressing Farnesyl Diphosphate Synthase Alters Chloroplast Development and Triggers Sterol-Dependent Induction of Jasmonate- and Fe-Related Responses Manzano, David; Andrade, Paola; Caudepón, Daniel Plant Physiology, Vol. 172, Issue 1 https://doi.org/10.1104/pp.16.00431	journal	July 2016
A Single Arabidopsis Gene Encodes Two Differentially Targeted Geranylgeranyl Diphosphate Synthase Isoforms Ruiz-Sola, M. Águila; Barja, M. Victoria; Manzano, David Plant Physiology, Vol. 172, Issue 3 https://doi.org/10.1104/pp.16.01392	journal	October 2016
Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense Tripathi, Diwaker; Zhang, Tong; Koo, Abraham J. Plant Physiology, Vol. 176, Issue 1 https://doi.org/10.1104/pp.17.01477	journal	November 2017
Extracellular ATP Shapes a Defense-Related Transcriptome Both Independently and along with Other Defense Signaling Pathways Jewell, Jeremy B.; Sowders, Joel M.; He, Ruifeng Plant Physiology, Vol. 179, Issue 3 https://doi.org/10.1104/pp.18.01301	journal	January 2019
Arabidopsis Lectin Receptor Kinase P2K2 Is a Second Plant Receptor for Extracellular ATP and Contributes to Innate Immunity Pham, An Quoc; Cho, Sung-Hwan; Nguyen, Cuong The Plant Physiology, Vol. 183, Issue 3 https://doi.org/10.1104/pp.19.01265	journal	April 2020
3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase1 Interacts with NORK and Is Crucial for Nodulation in Medicago truncatula Kevei, Zoltán; Lougnon, Géraldine; Mergaert, Peter The Plant Cell, Vol. 19, Issue 12 https://doi.org/10.1105/tpc.107.053975	journal	December 2007
Dolichol Biosynthesis and Its Effects on the Unfolded Protein Response and Abiotic Stress Resistance in Arabidopsis Zhang, Hairong; Ohyama, Kiyoshi; Boudet, Julie The Plant Cell, Vol. 20, Issue 7 https://doi.org/10.1105/tpc.108.061150	journal	July 2008
Loss of function of 3-hydroxy-3-methylglutaryl coenzyme A reductase 1 (HMG1) in Arabidopsis leads to dwarfing, early senescence and male sterility, and reduced sterol levels Suzuki, Masashi; Kamide, Yukiko; Nagata, Noriko The Plant Journal, Vol. 37, Issue 5 https://doi.org/10.1111/j.1365-313X.2004.02003.x	journal	March 2004
The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses: AtGenExpress global abiotic stress data set Kilian, Joachim; Whitehead, Dion; Horak, Jakub The Plant Journal, Vol. 50, Issue 2 https://doi.org/10.1111/j.1365-313X.2007.03052.x	journal	March 2007
Extracellular ATP is a regulator of pathogen defence in plants Chivasa, Stephen; Murphy, Alex M.; Hamilton, John M. The Plant Journal, Vol. 60, Issue 3 https://doi.org/10.1111/j.1365-313X.2009.03968.x	journal	November 2009
The Arabidopsis thaliana FPP synthase isozymes have overlapping and specific functions in isoprenoid biosynthesis, and complete loss of FPP synthase activity causes early developmental arrest: Arabidopsis thaliana FPP synthase mutants Closa, Marta; Vranová, Eva; Bortolotti, Cristina The Plant Journal, Vol. 63, Issue 3 https://doi.org/10.1111/j.1365-313X.2010.04253.x	journal	May 2010
Reverse genetic characterization of two paralogous acetoacetyl CoA thiolase genes in Arabidopsis reveals their importance in plant growth and development: Arabidopsis acetoacetyl CoA thiolases Jin, Huanan; Song, Zhihong; Nikolau, Basil J. The Plant Journal, Vol. 70, Issue 6 https://doi.org/10.1111/j.1365-313X.2012.04942.x	journal	March 2012
Inhibition by mevinolin of plant growth, sterol formation and pigment accumulation Bach, Thomas J.; Lichtenthaler, Hartmut K. Physiologia Plantarum, Vol. 59, Issue 1 https://doi.org/10.1111/j.1399-3054.1983.tb06570.x	journal	September 1983
The Arabidopsis thaliana lectin receptor kinase LecRK-I.9 is required for full resistance to Pseudomonas syringae and affects jasmonate signalling: LecRK-I.9: disease resistance and JA signalling Balagué, Claudine; Gouget, Anne; Bouchez, Olivier Molecular Plant Pathology, Vol. 18, Issue 7 https://doi.org/10.1111/mpp.12457	journal	September 2016
The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in Solanaceous plants Bouwmeester, Klaas; Han, Miao; Blanco-Portales, Rosario Plant Biotechnology Journal, Vol. 12, Issue 1 https://doi.org/10.1111/pbi.12111	journal	August 2013
Structural Mechanism for Statin Inhibition of HMG-CoA Reductase Istvan, E. S. Science, Vol. 292, Issue 5519 https://doi.org/10.1126/science.1059344	journal	May 2001
Identification of a Plant Receptor for Extracellular ATP Choi, J.; Tanaka, K.; Cao, Y. Science, Vol. 343, Issue 6168 https://doi.org/10.1126/science.343.6168.290	journal	January 2014
Qinghaosu (Artemisinin): an Antimalarial Drug from China Klayman, Daniel L. Science, Vol. 228, Issue 4703 https://doi.org/10.1126/science.3887571	journal	May 1985
Network Analysis of the MVA and MEP Pathways for Isoprenoid Synthesis Vranová, Eva; Coman, Diana; Gruissem, Wilhelm Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120116	journal	April 2013
Salicylic Acid, a Multifaceted Hormone to Combat Disease Vlot, A. Corina; Dempsey, D'Maris Amick; Klessig, Daniel F. Annual Review of Phytopathology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.phyto.050908.135202	journal	September 2009
MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data Pluskal, Tomáš; Castillo, Sandra; Villar-Briones, Alejandro BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-395	journal	July 2010
Mevalonate kinase deficiencies: from mevalonic aciduria to hyperimmunoglobulinemia D syndrome Haas, Dorothea; Hoffmann, Georg F. Orphanet Journal of Rare Diseases, Vol. 1, Issue 1 https://doi.org/10.1186/1750-1172-1-13	journal	April 2006
DAMPs, MAMPs, and NAMPs in plant innate immunity Choi, Hyong Woo; Klessig, Daniel F. BMC Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12870-016-0921-2	journal	October 2016
Terpene Specialized Metabolism in Arabidopsis thaliana Tholl, Dorothea; Lee, Sungbeom The Arabidopsis Book, Vol. 9 https://doi.org/10.1199/tab.0143	journal	January 2011
Chemical Phenotypes of the hmg1 and hmg2 Mutants of Arabidopsis Demonstrate the In-planta Role of HMG-CoA Reductase in Triterpene Biosynthesis Ohyama, Kiyoshi; Suzuki, Masashi; Masuda, Kazuo Chemical and Pharmaceutical Bulletin, Vol. 55, Issue 10 https://doi.org/10.1248/cpb.55.1518	journal	January 2007
Negative Feedbacks by Isoprenoids on a Mevalonate Kinase Expressed in the Corpora Allata of Mosquitoes Nyati, Pratik; Rivera-Perez, Crisalejandra; Noriega, Fernando G. PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0143107	journal	November 2015
The Lectin Receptor Kinase LecRK-I.9 Is a Novel Phytophthora Resistance Component and a Potential Host Target for a RXLR Effector Bouwmeester, Klaas; de Sain, Mara; Weide, Rob PLoS Pathogens, Vol. 7, Issue 3 https://doi.org/10.1371/journal.ppat.1001327	journal	March 2011
Loss of Arabidopsis thaliana Dynamin-Related Protein 2B Reveals Separation of Innate Immune Signaling Pathways Smith, John M.; Leslie, Michelle E.; Robinson, Samuel J. PLoS Pathogens, Vol. 10, Issue 12 https://doi.org/10.1371/journal.ppat.1004578	journal	December 2014
A novel orange-colored bimolecular fluorescence complementation (BiFC) assay using monomeric Kusabira-Orange protein Fujii, Yuta; Yoshimura, Ayaka; Kodama, Yutaka BioTechniques, Vol. 64, Issue 4 https://doi.org/10.2144/btn-2017-0121	journal	April 2018
Mevalonate kinase deficiency: current perspectives Schulert, Grant; Favier, Leslie The Application of Clinical Genetics, Vol. Volume 9 https://doi.org/10.2147/TACG.S93933	journal	January 2016
The Arabidopsis Mitogen-Activated Protein Kinase Kinase Kinase 20 (MKKK20) Acts Upstream of MKK3 and MPK18 in Two Separate Signaling Pathways Involved in Root Microtubule Functions Benhamman, Rachid; Bai, Fangwen; Drory, Samuel B. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01352	journal	August 2017
Salicylic Acid Biosynthesis in Plants Lefevere, Hannes; Bauters, Lander; Gheysen, Godelieve Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00338	journal	April 2020
Molecular Cloning, Characterization, and Functional Analysis of Acetyl-CoA C-Acetyltransferase and Mevalonate Kinase Genes Involved in Terpene Trilactone Biosynthesis from Ginkgo biloba Chen, Qiangwen; Yan, Jiaping; Meng, Xiangxiang Molecules, Vol. 22, Issue 1 https://doi.org/10.3390/molecules22010074	journal	January 2017

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Title: Activation of the plant mevalonate pathway by extracellular ATP

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