Supplemental Information

Triterpene messages from the EU-FP7 project TriForC

Alain Goossens1,2,*, Anne Osbourn3, Franck Michoux4, Søren Bak5

1Ghent University, Department of Plant Biotechnology and Bioinformatics, Technologiepark 927, B-9052 Ghent, Belgium;

2VIB Center for Plant Systems Biology, Technologiepark 927, B-9052 Ghent, Belgium;

3Department of Metabolic Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom

4Evonik Advanced Botanicals, 220 rue Henri Potez, 37210, Parçay Meslay, France

5Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Copenhagen, Denmark

*Correspondence: (A. Goossens)

Table S1. List of Scientific Publications

Title / DOI / Main author / Title of the periodical or the series / Number, date or frequency / Publisher / Place of publication / Date of publication / Relevant pages / Is open access provided to this publication? / Type
Triterpene Biosynthesis in Plants 10.1146/annurev-arplant-050312-120229 / Ramesha Thimmappa, Katrin Geisler, Thomas Louveau, Paul O'Maille, Anne Osbourn / Annual Review of Plant Biology / Vol. 65/Issue 1 / Annual Reviews Inc. / United States / 29-04-2014 / 225-257 / No / Peer reviewed
A translational synthetic biology platform for rapid access to gram-scale quantities of novel drug-like moleculesdoi.org/10.1016/j.ymben.2017.06.012 / James Reed, Michael J. Stephenson, Karel Miettinen, Bastiaan Brouwer, Aymeric Leveau, Paul Brett,Rebecca J.M. Goss, Alain Goossens, Maria A. O’Connell, Anne Osbourn / Metabolic Engineering / Vol. 42 / Academic Press Inc. / United States / 01-07-2017 / 185-193 / Yes / Peer reviewed
A conserved amino acid residue critical for product and substrate specificity in plant triterpene synthases
10.1073/pnas.1605509113 / Melissa Salmon, Ramesha B. Thimmappa, Robert E. Minto, Rachel E. Melton, RichardK. Hughes, Paul E. O’Maille, Andrew
M. Hemmings, Anne Osbourn / Proceedings of the National Academy of Sciences of the United States / Vol. 113/Issue 30 / National Academy of Sciences / United States / 26-07-2016 / E4407-E4414 / No / Peer reviewed
GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway
10.1038/ncomms10654 / Pablo D. Cárdenas, Prashant D. Sonawane, Jacob Pollier, Robin Vanden Bossche, Veena Dewangan, Efrat Weithorn, Lior Tal, Sagit Meir, Ilana Rogachev, Sergey Malitsky, Ashok P. Giri, Alain Goossens, Saul Burdman, Asaph Aharoni / Nature Communications / Vol. 7 / Nature Publishing Group / United Kingdom / 15-02-2016 / 10654 / Yes / Peer reviewed
The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis
10.1038/ncomms14153 / Karel Miettinen, Jacob Pollier, Dieter Buyst, Philipp Arendt, René Csuk, Sven Sommerwerk, Tessa Moses, Jan Mertens, Prashant D Sonawane, Laurens Pauwels, Asaph Aharoni, José Martins, David R. Nelson, Alain Goossens / Nature Communications / Vol. 8 / Nature Publishing Group / United Kingdom / 06-02-2017 / 14153 / Yes / Peer reviewed
Metabolic and functional diversity of saponins, biosynthetic intermediates and semi-synthetic derivatives
10.3109/10409238.2014.953628 / Tessa Moses, Kalliope K. Papadopoulou, Anne Osbourn / Critical Reviews in Biochemistry and Molecular Biology / Vol. 49/Issue 6 / Informa Healthcare / United Kingdom / 01-11-2014 / 439-462 / Yes / Peer reviewed
The bitter side of the nightshades: Genomics drives discovery in Solanaceae steroidal alkaloid metabolism
10.1016/j.phytochem.2014.12.010 / P.D. Cárdenas, P.D. Sonawane, U. Heinig, S.E. Bocobza, S. Burdman, A. Aharoni / Phytochemistry / Vol. 113 / Elsevier Limited / United Kingdom / 01-05-2015 / 24-32 / Yes / Peer reviewed
OSC2 and CYP716A14v2 Catalyze the Biosynthesis of Triterpenoids for the Cuticle of Aerial Organs of Artemisia annua
10.1105/tpc.114.134486 / Tessa Moses, Jacob Pollier, Qian Shen, Sandra Soetaert, James Reed, Marie-Laure Erffelinck, Filip C.W. Van Nieuwerburgh, Robin Vanden Bossche, Anne Osbourn, Johan M. Thevelein, Dieter Deforce, Kexuan Tang, Alain Goossens / Plant Cell / Vol. 27/Issue 1 / American Society of Plant Biologists / United States / 01-01-2015 / 286-301 / Yes / Peer reviewed
Standards for plant synthetic biology: a common syntax for exchange of DNA parts
10.1111/nph.13532 / Nicola J. Patron, Diego Orzaez, Sylvestre Marillonnet, et. al / New Phytologist / Vol. 208/Issue 1 / Blackwell Publishing / United Kingdom / 01-10-2015 / 13-19 / No / Peer reviewed
Auxin Response Factor SlARF2 Is an Essential Component of the Regulatory Mechanism Controlling Fruit Ripening in Tomato
doi.org/10.1371/journal.pgen.1005649 / Yanwei Hao, Guojian Hu, Dario Breitel, Mingchun Liu, Isabelle Mila, Pierre Frasse, Yongyao Fu, Asaph Aharoni, Mondher Bouzayen, Mohamed Zouine / PLoS Genetics / Vol. 11/Issue 12 / Public Library of Science / United States / 30-12-2015 / e1005649 / Yes / Peer reviewed
Identification and genome organization of saponin pathway genes from a wild crucifer, and their use for transient production of saponins in Nicotiana benthamiana
10.1111/tpj.13012 / Bekzod Khakimov, Vera Kuzina, Pernille Ø. Erthmann, Ery Odette Fukushima, JörgM. Augustin, Carl Erik Olsen, Jelle Scho ltalbers, Hanne Volpin, Sven Bode Andersen, Thure P. Hauser, Toshiya Muranaka, Søren Bak / Plant Journal / Vol. 84/Issue 3 / Blackwell Publishing / United Kingdom / 01-11-2015 / 478-490 / Yes / Peer reviewed
The triterpene echinocystic acid and its 3-O-glucoside derivative are revealed as
potent and selective glucocorticoid receptor agonists
10.1016/j.biocel.2016.08.028 / Demetra Georgatza, Vyron A. Gorgogietas, Paraskevi Kylindri, Maria Ch. Charalambous, Kalliope K. Papadopoulou, Joseph M. Hayes, Anna- Maria G. Psarra / International Journal of Biochemistry and Cell Biology / Vol. 79 / Elsevier Limited / United Kingdom / 01-10-2016 / 277-287 / No / Peer reviewed
An endoplasmic reticulum-engineered yeas t platform for overproduction of triterpenoids
doi.org/10.1016/j.ymben.2017.02.007 / Philipp Arendt, Karel Miettinen, Jacob Pollier, Riet De Rycke, Nico Callewaert, Alain Goossens / Metabolic Engineering / Vol. 40 / Academic Press Inc. / United States / 01-03-2017 / 165-175 / No / Peer reviewed
Plant cholesterol biosynthetic pathway overlaps with phytosterol metabolism 10.1038/nplants.2016.205 / Prashant D. Sonawane, Jacob Pollier, Sayantan Panda, Jedrzej Szymanski, Hassan Massalha, Meital Yona, Tamar Unger, Sergey Malitsky, Philipp Arendt, Laurens Pauwels, Efrat Almekias-Siegl, Ilana Rogachev, Sagit Meir, Pablo D. Cárdenas, Athar Masri, Marina Petrikov, Hubert Schaller, Arthur A. Schaffer,Avinash Kamble, Ashok P. Giri, Alain Goossens, Asaph Aharoni / Nature plants / Vol. 3/Issue 1 / Nature Publishing Group / United States / 22-12-2016 / 16205 / No / Peer reviewed
Screening for Triterpenoid Saponins in Plants Using Hyphenated Analytical Platforms
10.3390/molecules21121614 / Bekzod Khakimov, Li Tseng, Markus Godejohann, Søren Bak, Søren Engelsen / Molecules / Vol. 21/Issue 12 / Molecular Diversity Preservation International / Switzerland / 01-12-2016 / 1614 / Yes / Peer reviewed
Clade IVa Basic Helix–Loop–Helix Transcription Factors Form Part of a Conserved Jasmonate Signaling Circuit for the Regulation of Bioactive Plant Terpenoid Biosynthesis
10.1093/pcp/pcw168 / Jan Mertens, Alex Van Moerkercke, Robin Vanden Bossche, Jacob Pollier, Alain Goossens / Plant and Cell Physiology / Vol. 57/Issue 12 / Oxford University Press / United Kingdom / 01-12-2016 / 2564-2575 / No / Peer reviewed
Electrophilic Triterpenoid Enones: A Comparative Thiol-Trapping and Bioactivity Study 10.1021/acs.jnatprod.7b00271 / Danilo Del Prete, OrazioTaglialatela-Scafati, Alberto Minassi, Carmina Sirignano, Cristina Cruz, MariaL. Bellido, EduardoMuñoz, Giovanni Appendino / Journal of Natural Products / Vol. 80/Issue 8 / American Chemical Society / United States / 25-08-2017 / 2276-2283 / Yes / Peer reviewed
Identification and genome organization of saponin pathway genes from a wild crucifer, and their use for transient production of saponins in Nicotiana benthamiana
10.1111/tpj.13012 / Bekzod Khakimov, Vera Kuzina, Pernille Ø. Erthmann, Ery Odette Fukushima, JörgM. Augustin, Carl Erik Olsen, Jelle Scho ltalbers, Hanne Volpin, Sven Bode Andersen, Thure P. Hauser, Toshiya Muranaka, Søren Bak / Plant Journal / Vol. 84/Issue 3 / Blackwell Publishing / United Kingdom / 01-11-2015 / 478-490 / Peer reviewed
The TriForC database: a comprehensive up-to-date resource of plant triterpene biosynthesis
10.1093/nar/gkx925 / Karel Miettinen, Sabrina Iñigo, Lukasz Kreft, Jacob Pollier, Christof De Bo, Alexander Botzki, Frederik Coppens, Søren Bak, Alain Goossens / Nucleic Acids Research / 45 / Oxford University Press / United Kingdom / 17-10-2017 / 1 / No / Peer reviewed
Occurrence and biogenesis of seco-triterpenoids: A focus on the biosynthetic pathway of #-onocerin in Ononis spinosa. / Aldo Almeida / University of Copenhagen / Denmark / 06-07-2017 / Thesis

Table S2. List of Dissemination Activities

Type of activities / Main Leader / Title / Date / Place / Type of audience / Countries addressed
Press releases / VIVACELL BIOTECHNOLOGY ESPANA SL / VivaCell enhances its R&D drug discovery program with the European Community’s FP7 TRIFORC Project / 02-12-2013 / Córdoba / Scientific community (higher education, Research) - Industry / All
Films / UNIVERSITA DEGLI STUDI DEL PIEMONTE ORIENTALE AMEDEO AVOGADRO / ISOLATION: CHEMICAL DIVERSITY FROM BIODIVERSITY (Fractionation protocol) / 01-09-2017 / / Scientific community (higher education, Research) / Various European countries
Oral presentation to a wider public / JOHN INNES CENTRE / Unlocking plant metabolic diversity / 03-03-2014 / Walnut Creek, CA, USA / Scientific community (higher education, Research) / international
Oral presentation to a wider public / JOHN INNES CENTRE / Plant specialized metabolism Harnessing nature’s chemical toolkit / 02-06-2014 / Banff, Canada / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / Unlocking plant metabolic diversity / 01-09-2014 / Sant Feliu, Spain / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / Unlocking plant metabolic diversity / 01-07-2014 / Xiamen, China / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / UNIVERSITY OF COPENHAGEN / From ecometabolomics to synthetic biology – exploring the plasticity of the triterpenoid biosynthetic pathway / 02-06-2014 / York, UK / Scientific community (higher education, Research) / Scientific community/Industry
Oral presentation toa scientific event / JOHN INNES CENTRE / Making new molecules / 05-05-2014 / MIT, Boston / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / From genomes to synthetic biology / 01-12-2014 / York, UK / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Deciphering Steroidal Alkaloids Metabolism in the Solanacea through the Integration of Data from Genetics, Informatics and Metabolomics / 01-07-2014 / Xiamen, China / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Deciphering Steroidal Alkaloids Metabolism in the Solanacea through the Integration of Data from Genetics, Informatics and Metabolomics / 01-07-2014 / Shanghai, China / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / How jasmonates can feed synthetic biology programs / 02-07-2014 / Xiamen, China / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Gene Discovery in the Glycoalkaloids Pathway / 01-09-2014 / Warsaw, Poland / Scientific community (higher education, Research) / international
Oral presentation to a wider public / WEIZMANN INSTITUTE OF SCIENCE / The Bitter Side of the Nightshades: Steroidal Alkaloids Metabolism in the Solanaceae. / 01-08-2014 / Raleigh, USA / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / The Bitter Side of the Nightshades: Steroidal Alkaloids Metabolism in the Solanaceae. / 01-08-2014 / Queenstown, New Zealand / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Deciphering Steroidal Alkaloids Metabolism in the Solanacea through the Integration of Data from Genetics, Informatics and Metabolomics / 15-08-2014 / Brisbane, Australia. / Scientific community (higher education, Research) / international
Oral presentation to a wider public / JOHN INNES CENTRE / Harnessing plant metabolic diversity. Natural Product Discovery and Development in the Post genomic Era. / 12-01-2015 / San Diego, USA / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Deciphering Steroidal Alkaloids Metabolism in the Solanacea through the Integration of Data from Genetics, Informatics and Metabolomics / 02-03-2015 / Rehovot, Israel / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / Making all kinds of everything: the joy of transient expression / 01-05-2015 / Manchester, UK / Scientific community (higher education, Research) - Industry / national
Oral presentation to a scientific event / JOHN INNES CENTRE / Fine-tuning transient expression levels: when less can be more. / 20-07-2015 / Waterville Valley Resort, Waterville Valley, New Hamp shire, USA / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / Making sense of metabolic diversity / 20-07-2015 / Waterville Valley Resort, Waterville Valley, New Hamp shire, USA / Scientific community (higher education, Research) - Industry / national
Oral presentation to a scientific event / JOHN INNES CENTRE / Plant production platforms. KTN-CO EBP meeting / 15-10-2015 / Manchester UK / Scientific community (higher education, Research) / national
Oral presentation to a scientific event / JOHN INNES CENTRE / Solanum steroidal alkaloids: from a greasy start to the bitter end / 26-10-2015 / Bordeaux, France / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Unravelling plant metabolism: integrating metabolomics, genetics & informatic / 06-07-2015 / Toulouse, France / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Increasing the resolution of plant metabolomics: unambiguous identification & spatial analysis. / 15-06-2015 / MPI-Golm, Germany / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Unravelling plant metabolism through the integration of heterogeneous data from metabolomics, genetics and informatics / 14-10-2015 / INRA, Montpellier, France / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / UNIVERSITY OF COPENHAGEN / Symposium: 14th Symposium on Chemometrics / 15-06-2015 / Sardinia, / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / Engineering plant specialized metabolism. Can we break the multiple feedback loops? / 24-09-2015 / Halle, Germany / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / Meeting: 57th Annual meeting of the Japanese Society of Plant Physiologists / 18-03-2016 / Morioka, Japan / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / Annual Meeting: 'Experimental Plant Sciences', Lunteren / 11-04-2016 / Lunteren, The Netherlands / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / Meeting: Tomatoes, trends towards 2020 / 15-04-2016 / Antwerp, Belgium / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / UNIVERSITY OF COPENHAGEN / Evolution and impact of cyanogenic glucosides in butter flies and moths / 24-09-2015 / Halle, Germany / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / UNIVERSITA DEGLI STUDI DEL PIEMONTE ORIENTALE AMEDEO AVOGADRO / Abstract: Plant Engine: Plant metabolic engineering for high value products / 15-09-2015 / Sorrento, Italy / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / Conference: TERPNET 2015 / 01-06-2015 / Vancouver, Canada / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / Conference: 26th international conference on Arabidopsis research / 06-07-2015 / Paris, France / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / UNIVERSITY OF COPENHAGEN / Metabolomics / 05-09-2016 / University in Tashkent, Uzbekistan / Scientific community (higher education, Research) / national
Oral presentation to a scientific event / UNIVERSITY OF COPENHAGEN / From ecometabolomics to synthetic biology – exploring the plasticity of the triterpenoid biosynthetic pathway / 25-11-2015 / Osaka University, Osaka, Japan / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Deciphering Metabolic Traits in Tomato & other Solanaceous Species: Integration of Heterogeneous Data from Metabolomics, Genetics and Informatics / 10-03-2015 / Noble foundation, Ardmore OK, USA / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Unravelling Plant Metabolism through the Integration of Heterogeneous Data from Metabolomics, Genetics and Informatics / 06-04-2015 / Geneva University, Switzerland / Scientific community (higher education, Research) / national
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / The Bitter Side of the Nightshades: OMICS drives Discovery in Solanaceae Alkaloid Metabolism / 11-03-2015 / University of North Texas, Denton, USA / Scientific community (higher education, Research) / national
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Unravelling Plant Metabolism through the Integration of Heterogeneous Data from Metabolomics, Genetics and Informatics. / 08-04-2015 / ETH, Zurich, Switzerland / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / WEIZMANN INSTITUTE OF SCIENCE / Unravelling plant metabolism through the integration of heterogeneous data from metabolomics, genetics and informatics / 15-04-2015 / Sorrento, Italy / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / JOHN INNES CENTRE / Making new molecules / 15-04-2015 / Sorrento, Italy. / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / UNIVERSITY OF COPENHAGEN / TriForC / 15-04-2015 / Sorrento, Italy / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / SPICER CONSULTING LIMITED / Capitalising microalgae technology: Biorefineries for organic bioactive fertilisers and oils / 20-04-2015 / Kota Kinabalu, Sabah / Scientific community (higher education, Research) / international
Oral presentation to a wider public / UNIVERSITY OF COPENHAGEN / From ecometabolomics to synthetic biology – exploring the plasticity of the triterpenoid biosynthetic pathway / 15-11-2016 / Ghent, Belgium / Scientific community (higher education, Research) / national
Oral presentation to a scientific event / JOHN INNES CENTRE / Harnessing plant metabolic diversity. Natural Product Discovery and Development in the Post genomic Era. / 11-07-2016 / Austin, Texas, US. / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / The CYP716 family has a central role in producing the triterpenoid diversity in eudicots / 14-07-2016 / Vancouver, Canada / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis / 16-07-2016 / Dalian, China / Scientific community (higher education, Research) / international
Oral presentation to a scientific event / VIB / Dissecting tomato metabolic networks to provide novel tools for trait engineering. / 24-12-2015 / Valencia, Spain / Scientific community (higher education, Research) / international
Posters / UNIVERSITY OF COPENHAGEN / Bioprospecting of natural and synthetic cucurbitane related compounds / 11-08-2014 / North Carolina, USA / Scientific community (higher education, Research) / international
Posters / UNIVERSITY OF COPENHAGEN / #- Onocerin is an un usual triterpene in Ononis spinosa / 21-08-2014 / North Carolina, USA / Scientific community (higher education, Research) / international
Posters / ALKION BIO PHARMA SAS / In vitro propagation of Euphorbia resinifera / 24-09-2014 / Guimaraes, Portugal / Scientific community (higher education, Research) / international