dhr. dr. ir. R.C. (Rob) Schuurink
Faculteit der Natuurwetenschappen, Wiskunde en Informatica
Swammerdam Institute for Life Sciences
Science Park A
Science Park 904 Kamernummer: C2.211
1090 GE Amsterdam
The topics in my group concern the biosynthesis, regulation and biological role of volatiles for plants in their environment. In the last decade Petunia hybrida has emerged as the model of choice to study volatile benzenoid and phenylpropanoid synthesis, emission and regulation. These volatiles are synthesized predominantly in the corolla limb and emission is highly regulated, with a circadian rhythm, during corolla development, pollination and senescence. With all the biochemical and molecular tools available much of our understanding of volatile benzenoid/phenylpropanoid has been obtained with Petunia. The knowledge obtained with this system is being applied to tomato fruit and strawberry volatile production and thereby taste. In addition, we use tomato as a model system to study the role of terpenoids in its interaction with insects. We focus on terpene synthases expressed in trichomes and haveidentified several terpenoids that repel or attract whiteflies. Our aim is to engineer the production of these terpenoids for which we have identified trichome specific promoters. We use Arabidopsis for forward genetic screens to identify genes important in the response to the wound-induced C6-volatile E -2-hexenal. We also aim to identify genes that are specifically regulated by E -2-hexenal using a transcriptomics approach. Finally, a relative new topic in my group concerns effectors produced by herbivores that manipulate plant defenses. Together with the IBED at UvA we have discovered the first effectors from spider mites that manipulate the SA defense response. We are now focusing on their interactors in the plant and on effectors from whiteflies and thrips.
Floral scent production by Petunia
We study the biosynthesis of volatile benzenoids in Petunia and the regulation thereof. We have discovered, through a targeted metabolomics and transcriptomics approach, ODORANT1, the first transcription factor that regulates volatile benzenoid synthesis and provided insight in how Petunia flowers developmentally separate color and scent biosynthesis; we have recently discovered that the transcription factor EOBII (Emission of benzenoids II) acts upstream of ODO1. We are currently using Chip-Seq to identify all targets of ODO1 and EOBII. Moreover, we identified a 3-keto-acylthiolase that catalyzes an important step in benzoic acid biosynthesis, a crucial precursor for several benzenoids. We are currently working on an ABC transporter and a recently discovered biosynthetic gene that are regulated by ODO1.
The role of volatile terpenoids in tomato-insect interactions.
We are particularly interested in the role of volatile terpenoids in tomato-insect interactions. We have established a role for jasmonate (JA) in the production of volatile terpenoids in tomato upon herbivory and discovered that JA induces the expression of salicylic acid (SA) methyl transferase that converts SA to the volatile methyl salicylate, an volatile crucial in attracting predatory mites as shown by silencing SAMT in tomato. We have also identified and characterized the first monoterpene synthases from tomato that are specifically expressed and induced by JA in trichomes. This was recently followed up by the identification and characterization of all terpene synthases in tomato. Moreover, we have shown that geranyldiphosphate synthase is essential in tomato and Arabidopsis for the synthesis of gibberellins and that JA and SA are both necessary for the induction of the C16-homoterpene TMTT. Recently we identified the terpenoids that are directly involved in repelling or attracting whiteflies. Through 454 and GS-flex sequencing of trichome cDNAs of wild tomatoes we identified the corresponding terpenoid synthases. We modified cultivated tomato plants to produce the relevant terpenoids using trichome specific promoters that were discovered in my lab and made them more resistant to herbivorous insects. With yeast-1-hybrid we have identified a transcription factor that specifically can upregulate certain terpene synthases in the glandular trichomes of tomato. We have used RNASeq datasets of glandular trichomes of various wild tomato species to identify sesquiterpenoid modifiers.
Identification of effectors of whiteflies and thrips that manipulate plant responses.
Whitefly saliva contains many proteins and since whiteflies suppress certain defenses in plants it is thought that this occurs via effectors, similar to the situation in plant pathogenic bacteria and fungi. Together with the IBED at UvA we have discovered the first effectors from spider mites that manipulate the SA defense response and we have just submitted a manuscript describing these effectors. We are now focusing on their interactors in the plant and on effectors from whiteflies and thrips.
Green leaf volatiles
As a third topic we study the role of C6 volatiles as signaling and priming molecules. These C6 volatiles are produced in most, if not all, plants upon wounding, pathogen infection and insect herbivory and can prime the defense of neighboring plants. We have identified the first Arabidopsis mutants that are resistant to E-2-hexenal (her mutants) and have mapped the her1 mutation to discover a role for GABA in this process as well as in the defense against Pseudomonas. We also mapped and cloned the her2 mutant and determined that several WRKY transcription factors may regulate the E-2-hexenal response in Arabidopsis. Moreover, in the Arabidopsis-Pseudomonas interaction, the microbe seems to hijack the C6 volatiles to enhance jasmonate biosynthesis and susceptibility.
Section of Plant Physiology
I work within the Plant Physiology group headed by Prof. dr. Michel Haring. Dr. Petra Bleeker (natural variation of metabolic defense pathways) is the other staff member.
I coordinate the first year course 'Plant Biology' and the MSc course 'Biotic Interactions'. I also give lectures in various other courses.
Current members of the lab
Silke Allmann Postdoc
Michel de Vries technician
Jiesen Xu PhD student
Aldana Ramirez Postdoc
Paula van Kleeff Postdoc
Ahmed Abd-el-Haliem Postdoc
Suzanne Alves Aflitos-Hoogstrate, technician
Fariza Shaipulah PhD student
Maaike Boersma PhD student
Previous members of the lab
Chun Sui, China
Carlos Alberto Villarroel PhD student
Eleni Spyropoulou Postdoc
Alessandra Scala UvA
Arjen van Doorn (Munich)
Petra Bleeker (ENZA Seeds plus VIDI Plant Physiology, UvA)
Julian Verdonk (WUR)
Merijn Kant (UvA, IBED)
Chris van Schie (ENZA Seeds)
Doerte Klaus (Toulouse)
Chunlin Liu (China)
Kai Ament Bejo Seeds
Alex Van Moerkercke (Gent)
Rossana Mirabella, Lausanne
Current and previous undergraduate students
Rachelle van der Waall
Mallory van Heiningen
Adriana Mejia (Columbia)
Marie Malange (Cameroon)
Tu Phan (Vietnam)
Laura Medina Puche (Spain)
Juan Manuel Alba Cano
Cynthia Mugo (Japan)
Prof. dr. N. Dudareva, Purdue, USA
Prof. dr. E. Pichersky, Michigan, USA
Prof. A. Tissier Halle, Germany
Dr. M. de Both Keygene
Prof. dr. T. Lange TU Braunschweig
Prof. dr. I. Baldwin MPI-Jena
Prof. dr. D. Clark University of Florida
Prof. dr. H. Klee University of Florida
Prof. dr. S. Schütz Göttingen University
Prof. dr. C. Kuhlemeier Bern University
Prof. dr. A. Collmer Cornell Univ, NY
Dr. C. Triantaphylidès DEVM, France
Dr. I.Meskiene Vienna, Austria
Prof. dr. Kenji Matsui Japan
Dr. M. Kant IBED, UVA
Prof. dr. H. Hiemstra HIMS, UvA
Prof. dr. H. Bouwmeester PRI
Prof. dr. R. Koes VU
Dr. H. Rauwerda MAD, UvA
Prof. dr. C. Jakobs VU
Unravelling plant defence signals
Plants are organisms that cannot move so they have evolved several mechanisms to face environmental stress. When a leaf is wounded or is infected by pathogenic bacteria many signals are triggered into the whole plant and the combination of these informations are fundamental for life and death struggle. In our lab we are interested in shedding light in this complex field, plant signal transduction, to reach a basal knowledge on which applied research is established ( develop resistance to stress ). In particular we pointed our attention on E-2-hexenal, a volatile compound, emitted under mechanical or biotic stress, that we have found is related with GABA, another molecule that is induced during several kinds of stress. Our aim is to discover the connection between these two signals and also with the others plant signals that trigger defences, such as jasmonic acid and salicylicacid.
Pseudomonas syringae and Arabidopsis thaliana
are the two components of our biological system. We have several lines of Arabidopsis, for example one which overproduce GABA, another one that has a lower synthesis of E-2-hexenal, and different strains of Pseudomonas that we would like to use to trigger a response in these plants.
To analyse the plant-pathogen system we use a wide range of experimental approaches like molecular biology techniques (DNA/RNA isolation, cDNA synthesis, PCR, quantitative PCR, plant transformation), biochemistry techniques (quantification of plant hormones an signalling molecules with LC/MS and GC/MS), biological assays (Pseudomonas infection of plants and score symptoms on leaves) and microbiology techniques (collect leaves infiltrated with bacteria and check their growth after it).
Controlling insect pest by improving the plants defence
On commercial tomato three arthropod pests constitute enormous problems for agriculture; aphids, whiteflies and spider mites. In our lab we have been working on tomato-whitefly and tomato-spider mite interactions for many years. The long-term aim of this research is to develop resistance to infestation.
Whitefly ( Bemisia tabaci ) is the vector of viruses in tomato and control of virus infection will be based on prevention of infection. It appears that the host plant is an important factor in selection for resistance; some tomato cultivars appear to exhibit resistance to whitefly infestation and repel whitefly through the production of specific compounds (terpenoids). Previously we established which compounds can decrease whitefly visitation. Forthis internship we will try to elucidate partof thepathway ofterpenoid production and its regulation at the level of terpene biosynthesis which finally will result in application in breeding programmes.
We have cloned several key enzymes in the terpenoid biosynthesis pathway and have created transgenic tomato lines. These lines will be characterised at gene-expression level (Q-PCR) and production of volatile terpenes (Gas Chromatography-Mass Spectrometry). The effect of altered terpene biosynthesis on whitefly (or spider mite) visitation can then be assessed in bioassays.
New terpene synthases will be cloned in expression vectors for in-vivo production of terpenes (by expression in E. coli ), in order to find out which products they actually make. This can also be done by transient expression in a tobacco plant via A grobacterium infiltration. We check whether the gene is expressed and if so, which volatiles are produced.
Experimental techniques include molecular, biochemical and ecological assays (cloning, E. coli expression, GG-MS, DNA/RNA isolation, cDNA synthesis, PCR and quantitative PCR, bioassays)
Characterizing a candidate gene required for scent biosynthesis in Petunia flowers
The reproductive success of many plants is dependent on pollination by animals like hummingbirds and bees. Attractive floral traits like color and scent can enhance the reproductive success of a plant. Petunia is a wonderful plant to study the biosynthesis of these scent molecules, so called floral volatiles. A mix of floral volatiles is synthesized and emitted by Petunia flowers in a highly regulated manner. These volatiles are synthesized when the pollinators are active and the flower ready to be pollinated. The biosynthesis pathway of floral volatiles is described, but still some enzymes in this pathway are missing. Moreover, the regulation of this pathway is poorly understood. Four transcription factors are known to regulate this pathway, but how they regulate volatile biosynthesis remains largely unknown. Recently we have done Next Generation Sequencing on RNA of several transgenic petunia’s. From this sequencing data we can pick candidate genes that either regulate biosynthesis (transcription factors) or synthesize specific volatiles (biosynthetic genes).
Hypothesis and objectives
The project aims to characterize a new biosynthetic gene or transcription factor and determine its role in floral volatile biosynthesis. For this purpose three objectives will be addressed:
1. Determine the expression pattern of the candidate gene
Floral volatile genes are expressed mainly in the flower and expression cycles in time. To determine if the candidate displays the same tissue specific and rhythmic expression as other floral volatile genes expression analysis will be performed. For this purpose RNA will be isolated, cDNA synthesized and the expression level will be determined with quantitative RT-PCR.
2. To elucidate the subcellular localization of the candidate
To determine if the candidate localizes to the same subcellular compartments as related floral volatile enzymes Agrobacterium Transient Transformatiom Assays (ATTA) will be performed. The candidate will be labeled with a fluorescent tag to visualize its subcellular localization in Nicotiana benthamiana leaves and Petunia flowers.
3a. To determine the function of the biosynthetic gene
To test if the candidate has the predicted enzymatic activity it will be expressed in vitro in E.coli. The produced protein will be analyzed by Western blotting and enzymatic assays.
3b. To determine the function of the transcription factor
To elucidate the role of the transcription factor in floral volatile biosynthesis the gene will be silenced in petunia plants. For this purpose a RNAi construct will be cloned and Petunia petals will be transient silenced. Volatile emission will be measured by GC-MS.
Cloning, RNA isolation, cDNA synthesis, qPCR, ATTA, microscopy,
In vitro E. coli expression, Western blotting and enzymatic assays or GC-MS
- refereed (59)
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- erkenning (4)
- supervised theses (1)
- Steenbergen, M., Abd-El-Haliem, A., Bleeker, P., Dicke, M., Escobar-Bravo, R., Cheng, G., ... Broekgaarden, C. (2018). Thrips advisor: exploiting thrips-induced defences to combat pests on crops. Journal of Experimental Botany, 69(8), 1837-1848. DOI: 10.1093/jxb/ery060
- Zhang, N. X., Messelink, G. J., Alba, J. M., Schuurink, R. C., Kant, M. R., & Janssen, A. (2018). Phytophagy of omnivorous predator Macrolophus pygmaeus affects performance of herbivores through induced plant defences. Oecologia, 186(1), 101-113. DOI: 10.1007/s00442-017-4000-7 [details]
- Scala, A., Mirabella, R., Goedhart, J., de Vries, M., Haring, M. A., & Schuurink, R. C. (2017). Forward genetic screens identify a role for the mitochondrial HER2 in E-2-hexenal responsiveness. Plant Molecular Biology, 95(4-5), 399-409. DOI: 10.1007/s11103-017-0659-8 [details]
- Hickman, R., Van Verk, M. C., Van Dijken, A. J. H., Mendes, M. P., Vroegop-Vos, I. A., Caarls, L., ... Van Wees, S. C. M. (2017). Architecture and Dynamics of the Jasmonic Acid Gene Regulatory Network. The Plant Cell, 29(9), 2086-2105. DOI: 10.1105/tpc.16.00958
- Spyropoulou, E. A., Dekker, H. L., Steemers, L., van Maarseveen, J. H., de Koster, C. G., Haring, M. A., ... Allmann, S. (2017). Identification and Characterization of (3Z):(2E)-Hexenal Isomerases from Cucumber. Frontiers in Plant Science, 8, . DOI: 10.3389/fpls.2017.01342 [details]
- Adebesin, F., Widhalm, J. R., Boachon, B., Lefèvre, F., Pierman, B., Lynch, J. H., ... Dudareva, N. (2017). Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter. Science, 356(6345), 1386-1388. DOI: 10.1126/science.aan0826
- Ameye, M., Allmann, S., Verwaeren, J., Smagghe, G., Haesaert, G., Schuurink, R. C., & Audenaert, K. (2017). Green leaf volatile production by plants: a meta-analysis. New Phytologist. DOI: 10.1111/nph.14671
- Caarls, L., Elberse, J., Awwanah, M., Ludwig, N. R., de Vries, M., Zeilmaker, T., ... Van den Ackerveken, G. (2017). Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proceedings of the National Academy of Sciences of the United States of America, 114(24), 6388-6393. DOI: 10.1073/pnas.1701101114 [details]
- Schimmel, B. C. J., Ataide, L. M. S., Chafi, R., Villarroel, C. A., Alba, J. M., Schuurink, R. C., & Kant, M. R. (2017). Overcompensation of herbivore reproduction through hyper-suppression of plant defenses in response to competition. New Phytologist, 214(4), 1688-1701. DOI: 10.1111/nph.14543
- Zhou, Y., Vroegop-Vos, I., Schuurink, R. C., Pieterse, C. M. J., & Van Wees, S. C. M. (2017). Atmospheric CO2 Alters Resistance of Arabidopsis to Pseudomonas syringae by Affecting Abscisic Acid Accumulation and Stomatal Responsiveness to Coronatine. Frontiers in Plant Science, 8, . DOI: 10.3389/fpls.2017.00700 [details]
- Amrad, A., Moser, M., Mandel, T., de Vries, M., Schuurink, R. C., Freitas, L., & Kuhlemeier, C. (2016). Gain and Loss of Floral Scent Production through Changes in Structural Genes during Pollinator-Mediated Speciation. Current Biology, 26(24), 3303-3312. DOI: 10.1016/j.cub.2016.10.023 [details]
- Ataide, L. M. S., Pappas, M. L., Schimmel, B. C. J., Lopez-Orenes, A., Alba, J. M., Duarte, M. V. A., ... Kant, M. R. (2016). Induced plant-defenses suppress herbivore reproduction but also constrain predation of their offspring. Plant Science, 252, 300-310. DOI: 10.1016/j.plantsci.2016.08.004 [details]
- van Kleeff, P. J. M., Galland, M., Schuurink, R. C., & Bleeker, P. M. (2016). Small RNAs from Bemisia tabaci Are Transferred to Solanum lycopersicum Phloem during Feeding. Frontiers in Plant Science, 7, . DOI: 10.3389/fpls.2016.01759 [details]
- Kortbeek, R., Xu, J., Ramirez, A., Spyropoulou, E., Diergaarde, P., Otten-Bruggeman, I., ... Bleeker, P. M. (2016). Engineering of Tomato Glandular Trichomes for the Production of Specialized Metabolites. Methods in Enzymology, 576, 305-31. DOI: 10.1016/bs.mie.2016.02.014
- Bombarely, A., Moser, M., Amrad, A., Bao, M., Bapaume, L., Barry, C. S., ... Kuhlemeier, C. (2016). Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nature Plants, 2, . DOI: 10.1038/nplants.2016.74 [details]
- Jonckheere, W., Dermauw, W., Zhurov, V., Wybouw, N., Van den Bulcke, J., Villarroel, C. A., ... Van Leeuwen, T. (2016). The salivary protein repertoire of the polyphagous spider mite Tetranychus urticae: a quest for effectors. Molecular & Cellular Proteomics, 15(12), 3594-3613. DOI: 10.1074/mcp.M116.058081
- Onkokesung, N., Reichelt, M., van Doorn, A., Schuurink, R. C., & Dicke, M. (2016). Differential Costs of Two Distinct Resistance Mechanisms Induced by Different Herbivore Species in Arabidopsis. Plant Physiology, 170(2), 891-906. DOI: 10.1104/pp.15.01780 [details]
- Shaipulah, N. F. M., Muhlemann, J. K., Woodworth, B. D., Van Moerkercke, A., Verdonk, J. C., Ramirez, A. M., ... Schuurink, R. C. (2016). CCoAOMT down-regulation activates anthocyanin biosynthesis in petunia. Plant Physiology, 170(2), 717-731. DOI: 10.1104/pp.15.01646 [details]
- Sun, P., Schuurink, R. C., Caissard, J. C., Hugueney, P., & Baudino, S. (2016). My Way: Noncanonical Biosynthesis Pathways for Plant Volatiles. Trends in Plant Science, 21(10), 884-894. DOI: 10.1016/j.tplants.2016.07.007 [details]
- Villarroel, C. A., Jonckheere, W., Alba Cano, J. M., Glas, J. J., Dermauw, W., Haring, M. A., ... Kant, M. R. (2016). Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction. Plant Journal, 86(2), 119–131. DOI: 10.1111/tpj.13152 [details]
- Mirabella, R., Rauwerda, H., Allmann, S., Scala, A., Spyropoulou, E. A., de Vries, M., ... Schuurink, R. C. (2015). WRKY40 and WRKY6 act downstream of the green leaf volatile E-2-hexenal in Arabidopsis. Plant Journal, 83(6), 1082-1096. DOI: 10.1111/tpj.12953 [details]
- Alba, J. M., Schimmel, B. C. J., Glas, J. J., Ataide, L. M. S., Pappas, M. L., Villarroel, C. A., ... Kant, M. R. (2015). Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytologist, 205(2), 828-840. DOI: 10.1111/nph.13075 [details]
- Hofberger, J. A., Ramirez, A. M., van den Bergh, E., Zhu, X., Bouwmeester, H. J., Schuurink, R. C., & Schranz, M. E. (2015). Large-Scale Evolutionary Analysis of Genes and Supergene Clusters from Terpenoid Modular Pathways Provides Insights into Metabolic Diversification in Flowering Plants. PLoS One, 10(6), e0128808. DOI: 10.1371/journal.pone.0128808 [details]
- Kant, M. R., Jonckheere, W., Knegt, B., Lemos, F., Liu, J., Schimmel, B. C. J., ... Alba, J. M. (2015). Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Annals of Botany, 115(7), 1015-1051. DOI: 10.1093/aob/mcv054 [details]
- VanDoorn, A., de Vries, M., Kant, M. R., & Schuurink, R. C. (2015). Whiteflies glycosylate salicylic acid and secrete the conjugate via their honeydew. Journal of Chemical Ecology, 41(1), 52-58. DOI: 10.1007/s10886-014-0543-9 [details]
- Zeilmaker, T., Ludwig, N. R., Elberse, J., Seidl, M. F., Berke, L., van Doorn, A., ... Van den Ackerveken, G. (2015). DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant Journal, 81(2), 210-222. DOI: 10.1111/tpj.12719 [details]
- Medina-Puche, L., Molina-Hidalgo, F. J., Boersma, M., Schuurink, R. C., López-Vidriero, I., Solano, R., ... Muñoz-Blanco, J. (2015). An R2R3-MYB Transcription Factor Regulates Eugenol Production in Ripe Strawberry Fruit Receptacles. Plant Physiology, 168(2), 598-614. DOI: 10.1104/pp.114.252908 [details]
- Glas, J. J., Alba, J. M., Simoni, S., Villarroel, C. A., Stoops, M., Schimmel, B. C. J., ... Kant, M. R. (2014). Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities. BMC Biology, 12, . DOI: 10.1186/s12915-014-0098-9 [details]
- Spyropoulou, E. A., Haring, M. A., & Schuurink, R. C. (2014). Expression of Terpenoids 1, a glandular trichome-specific transcription factor from tomato that activates the terpene synthase 5 promoter. Plant Molecular Biology, 84(3), 345-357. DOI: 10.1007/s11103-013-0142-0 [details]
- Spyropoulou, E. A., Haring, M. A., & Schuurink, R. C. (2014). RNA sequencing on Solanum lycopersicum trichomes identifies transcription factors that activate terpene synthase promoters. BMC Genomics, 15, 402. DOI: 10.1186/1471-2164-15-402 [details]
- Falara, V., Alba, J. M., Kant, M. R., Schuurink, R. C., & Pichersky, E. (2014). Geranyllinalool synthases in solanaceae and other angiosperms constitute an ancient branch of diterpene synthases involved in the synthesis of defensive compounds. Plant Physiology, 166(1), 428-441. DOI: 10.1104/pp.114.243246 [details]
- Onkokesung, N., Reichelt, M., van Doorn, A., Schuurink, R. C., van Loon, J. J. A., & Dicke, M. (2014). Modulation of flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor: role of kaempferol-3,7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae. Journal of Experimental Botany, 65(8), 2203-2217. DOI: 10.1093/jxb/eru096 [details]
- Scala, A., Allmann, S., Mirabella, R., Haring, M. A., & Schuurink, R. C. (2013). Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens. International Journal of Molecular Sciences, 14(9), 17781-177811. DOI: 10.3390/ijms140917781 [details]
- Scala, A., Mirabella, R., Mugo, C., Matsui, K., Haring, M. A., & Schuurink, R. C. (2013). E-2-hexenal promotes susceptibility to Pseudomonas syringae by activating jasmonic acid pathways in Arabidopsis. Frontiers in Plant Science, 4, 74. DOI: 10.3389/fpls.2013.00074 [details]
- van Schie, C. C. N., Haring, M. A., & Schuurink, R. C. (2013). Prenyldiphosphate synthases and gibberellin biosynthesis. In T. J. Bach, & M. Rohmer (Eds.), Isoprenoid synthesis in plants and microorganisms: new concepts and experimental approaches (pp. 213-232). New York: Springer. DOI: 10.1007/978-1-4614-4063-5_15 [details]
- Vos, I. A., Verhage, A., Schuurink, R. C., Watt, L. G., Pieterse, C. M. J., & van Wees, S. C. M. (2013). Onset of herbivore-induced resistance in systemic tissue primed for jasmonate-dependent defenses is activated by abscisic acid. Frontiers in Plant Science, 4, 539. DOI: 10.3389/fpls.2013.00539 [details]
- Alba, J. M., Bleeker, P. M., Glas, J. J., Schimmel, B. C. J., van Wijk, M., Sabelis, M. W., ... Kant, M. R. (2012). The impact of induced plant volatiles on lant-arthropod interactions. In G. Smagghe, & I. Diaz (Eds.), Arthropod-plant interactions: novel insights and approaches for IPM (pp. 15-73). (Progress in biological control; No. 14). Dordrecht: Springer. DOI: 10.1007/978-94-007-3873-7_2 [details]
- Bleeker, P. M., Mirabella, R., Diergaarde, P. J., Vandoorn, A., Tissier, A., Kant, M. R., ... Schuurink, R. C. (2012). Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proceedings of the National Academy of Sciences of the United States of America, 109(49), 20124-20129. DOI: 10.1073/pnas.1208756109 [details]
- Glas, J. J., Schimmel, B. C. J., Alba, J. M., Escobar-Bravo, R., Schuurink, R. C., & Kant, M. R. (2012). Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. International Journal of Molecular Sciences, 13(12), 17077-17103. DOI: 10.3390/ijms131217077 [details]
- Van Moerkercke, A., Haring, M. A., & Schuurink, R. C. (2012). A model for combinatorial regulation of the petunia R2R3-MYB transcription factor ODORANT1. Plant Signaling & Behavior, 7(4), 518-520. DOI: 10.4161/psb.19311 [details]
- Colquhoun, T. A., Marciniak, D. M., Wedde, A. E., Kim, J. Y., Schwieterman, M. L., Levin, L. A., ... Clark, D. G. (2012). A peroxisomally localized acyl-activating enzyme is required for volatile benzenoid formation in a Petuniaxhybrida cv. 'Mitchell Diploid' flower. Journal of Experimental Botany, 63(13), 4821-4833. DOI: 10.1093/jxb/ers153 [details]
- Ducluzeau, A-L., Wamboldt, Y., Elowsky, C. G., Mackenzie, S. A., Schuurink, R. C., & Basset, G. J. (2012). Gene network reconstruction identifies the authentic trans-prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone-9 in Arabidopsis. Plant Journal, 69(2), 366-375. DOI: 10.1111/j.1365-313X.2011.04796.x [details]
- Van Moerkercke, A., Galván-Ampudia, C. S., Verdonk, J. C., Haring, M. A., & Schuurink, R. C. (2012). Regulators of floral fragrance production and their target genes in petunia are not exclusively active in the epidermal cells of petals. Journal of Experimental Botany, 63(8), 3157-3171. DOI: 10.1093/jxb/ers034 [details]
- Almeida Sarmento, R., Lemos, F., Bleeker, P. M., Schuurink, R. C., Pallini, A., Oliveira, M. G. A., ... Janssen, A. (2011). A herbivore that manipulates plant defence. Ecology Letters, 14(3), 229-236. DOI: 10.1111/j.1461-0248.2010.01575.x [details]
- Bleeker, P. M., Diergaarde, P. J., Ament, K., Schütz, S., Johne, B., Dijkink, J., ... Schuurink, R. C. (2011). Tomato-produced 7-epizingiberene and R-curcumene act as repellents to whiteflies. Phytochemistry, 72(1), 68-73. DOI: 10.1016/j.phytochem.2010.10.014 [details]
- Bleeker, P. M., Spyropoulou, E. A., Diergaarde, P. J., Volpin, P., de Both, M. T. J., Zerbe, P., ... Schuurink, R. C. (2011). RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Molecular Biology, 77(4-5), 323-336. DOI: 10.1007/s11103-011-9813-x [details]
- Colquhoun, T. A., Kim, J. Y., Wedde, A. E., Levin, L. A., Schmitt, K. C., Schuurink, R. C., & Clark, D. G. (2011). PhMYB4 fine-tunes the floral volatile signature of Petunia×hybrida through PhC4H. Journal of Experimental Botany, 62(3), 1133-1143. DOI: 10.1093/jxb/erq342 [details]
- Dal Cin, V., Tieman, D. M., Tohge, T., McQuinn, R., de Vos, R. C. H., Osorio, S., ... Klee, H. J. (2011). Identification of genes in the phenylalanine metabolic pathway by ectopic expression of a MYB transcription factor in tomato fruit. The Plant Cell, 23(7), 2738-2753. DOI: 10.1105/tpc.111.086975 [details]
- Falara, V., Akhtar, T. A., Nguyen, T. T. H., Spyropoulou, E. A., Bleeker, P. M., Schauvinhold, I., ... Pichersky, E. (2011). The tomato terpene synthase gene family. Plant Physiology, 157(2), 770-789. DOI: 10.1104/pp.111.179648 [details]
- Van Moerkercke, A., Haring, M. A., & Schuurink, R. C. (2011). The transcription factor EMISSION OF BENZENOIDS II activates the MYB ODORANT1 promoter at a MYB binding site specific for fragrant petunias. Plant Journal, 67(5), 917-928. DOI: 10.1111/j.1365-313X.2011.04644.x [details]
- Allmann, S., Halitschke, R., Schuurink, R. C., & Baldwin, I. T. (2010). Oxylipin channelling in Nicotiana attenuata: lipoxygenase 2 supplies substrates for green leaf volatile production. Plant, cell and environment, 33(12), 2028-2040. DOI: 10.1111/j.1365-3040.2010.02203.x [details]
- Ament, K., Krasikov, V., Allmann, S., Rep, M., Takken, F. L. W., & Schuurink, R. C. (2010). Methyl salicylate production in tomato affects biotic interactions. Plant Journal, 62(1), 124-134. DOI: 10.1111/j.1365-313X.2010.04132.x [details]
- van den Burg, H. A., Kini, R. K., Schuurink, R. C., & Takken, F. L. W. (2010). Arabidopsis small ubiquitin-like modifier paralogs have distinct functions in development and defense. The Plant Cell, 22(6), 1998-2016. DOI: 10.1105/tpc.109.070961 [details]
- Park, D. H., Mirabella, R., Bronstein, P. A., Preston, G. M., Haring, M. A., Lim, C. K., ... Schuurink, R. C. (2010). Mutations in γ-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant Journal, 64(2), 318-330. DOI: 10.1111/j.1365-313X.2010.04327.x [details]
- Bleeker, P. M., Diergaarde, P. J., Ament, K., Guerra, J., Weidner, M., Schütz, S., ... Schuurink, R. C. (2009). The role of specific tomato volatiles in tomato-whitefly interaction. Plant Physiology, 151(2), 925-935. DOI: 10.1104/pp.109.142661 [details]
- Kant, M. R., Bleeker, P. M., van Wijk, M., Schuurink, R. C., & Haring, M. A. (2009). Plant Volatiles in Defence. In L. C. van Loon (Ed.), Plant innate immunity (pp. 613-666). (ADVANCES IN BOTANICAL RESEARCH; No. 51). Amsterdam: Academic Press. DOI: 10.1016/S0065-2296(09)51014-2 [details]
- Van Moerkercke, A., Schauvinhold, I., Pichersky, E., Haring, M. A., & Schuurink, R. C. (2009). A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production. Plant Journal, 60(2), 292-302. DOI: 10.1111/j.1365-313X.2009.03953.x [details]
- Kant, M. R., Sabelis, M. W., Haring, M. A., & Schuurink, R. C. (2008). Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proceedings of the Royal Society B-Biological Sciences, 275(1633), 443-452. DOI: 10.1098/rspb.2007.1277 [details]
- Mirabella, R., Rauwerda, H., Struys, E. A., Jakobs, C., Triantaphylidès, C., Haring, M. A., & Schuurink, R. C. (2008). The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. Plant Journal, 53(2), 197-213. DOI: 10.1111/j.1365-313X.2007.03323.x [details]
- Clark, D. G., Pichersky, E., Verdonk, J., Dudareva, N., Haring, M., Klahre, U., & Schuurink, R. (2009). Benzenoids dominate the fragrance of Petunia flowers. In T. Gerats, & J. Strommer (Eds.), Petunia: evolutionary, developmental and physiological genetics. - 2nd ed. (pp. 51-69). New York: Springer. DOI: 10.1007/978-0-387-84796-2_3 [details]
- Schuurink, R. C. (2012). Kastomaat kan weer zelf lastige vliegen verjagen. NRC Handelsblad.
- Villarroel Figueroa, C. A., Jonckheere, W., Alba Cano, J. M., Glas, J. J., Dermauw, W., Haring, M., ... Kant, M. (2016). Effector proteins of spider mites improve their performance by plant defense manipulation. Abstract from EURAAC 2016 Valencia, Valencia, Spain.
- Schuurink, R.C. (invited speaker) (8-12-2016): Regulation of terpene biosynthesis in tomato trichomes., John Innes Center, Norwich.
- Schuurink, R.C. (invited speaker) (10-9-2016): Circadian rhythm of volatile production., 15th World Petunia Days, Wittenberg, Germany.
- Schuurink, R.C. (invited speaker) (11-5-2016): Plants and insects, a volatile interaction., International Centre of Insect Physiology and Ecology (icipe).
- Schuurink, R.C. (invited speaker) (4-2-2016): Signal Transduction by Green Leaf Volatiles, Plant Volatiles Gordon Research Conference 2016, Ventura, United States.
- Sun, P. (2017). Molecular and biochemical studies of fragrance biosynthesis in rose [details]
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