Evolution of Plant Secondary Metabolites

Kliebenstein Lab

UC Davis Plant Sciences

Burow, M, Halkier, B.A. and D.J. Kliebenstein (2010) “Regulatory networks of glucosinolates shape Arabidopsis thaliana fitness.” Current Opinion of Plant Biology 13(3)348-53. (Pubmed link)


Rowe, H.C. and Kliebenstein, D.J. (2010) “All mold is not alike: the importance of intraspecific diversity in necrotrophic plant pathogens” PLoS Pathogens 6(3):e1000759. (Pubmed link)


Kliebenstein, D.J. (2010) “Systems biology uncovers the foundation of natural genetic diversity” Plant Physiology 152(2)487-499. (Pubmed link)


Kliebenstein, D.J. (2009) “A quantitative genetics and ecological model system: Understanding the aliphatic glucosinolate biosynthetic network via QTLs” Phytochemistry Reviews 8(1)243-54 . (Direct link) (draft)


Kliebenstein, D.J. and H.C. Rowe. (2008) “Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction.Plant Science 174(6)551-6. (Pubmed Link)(draft)


Hansen, B.G., Halkier, B.A. and D.J. Kliebenstein (2008) “Identifying the molecular basis of QTLs: eQTLs add a new dimension.” Trends in Plant Sciences 13(2):72-77 . (Pubmed link)


Kliebenstein, D.J. (2007) “Metabolomics and plant quantitative trait locus analysis – The optimum genetical genomics platform?” In Concepts in Plant Metabolomics, B.J. Nikolau and E.S. Wurtele, eds (Dordrect, The Netherlands: Springer), pp.29-45. (pdf Preprint)


Kliebenstein, D.J., Kroymann, J., and T. Mitchell-Olds.  (2005) The glucosinolate-myrosinase system in an ecological and evolutionary context. Current Opinion in Plant Biology 8(3):264-271. (Pubmed link)


Kliebenstein, D.J. (2004) Secondary metabolites and plant/environment interactions: a view through Arabidopsis thaliana tinged glasses. Plant Cell and Environment 27(6):675-684. (Journal link)


Wittstock, U., Kliebenstein, D.J., Lambrix, V., Reichelt, M. and J. Gershenzon. (2003) Glucosinolate hydrolysis and its impact on generalist and specialist insect herbivores. Rec Adv Phytochem 37: 101-125 (eds. Romeo JT, Dixon RA, Vol. 37: Integrative Phytochemistry: From Ethnobotany to Molecular Ecology. Pergamon, Amsterdam).

Sønderby, I.E., Burow, M., Rowe, H.C., Kliebenstein, D.J. and B.A. Halkier (2010) “A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiology 153(1)348-63. (Pubmed link)


Hansen, B.G., Kerwin, R.E., Ober, J.A., Lambrix, V.M., Mitchell-Olds, T., Gershenzon, J., Halkier, B.A. and D.J. Kliebenstein. (2008) “A novel 2-oxoacid dependent dioxygenases involved in the formation of the goiterogenic 2-hydroxybut-3-enyl glucosinolate and generalist insect resistance in Arabidopsis thaliana. Plant Physiology 148(4):2096-2108. (Direct link)


Li, J., Hansen, B.H., Ober, J.A., Kliebenstein, D.J. and B.A. Halkier. (2008) A crucifer-specific radiation of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiology 148(3)1721-33. (Direct link)


Vergara, F., Wenzler, M., Hansen, B.G., Kliebenstein, D.J., Halkier, B.A., Gershenzon, J. and B. Schneider. (2008) “Determination of the absolute configuration of the glucosinolate methylsulfoxide group reveals a stereospecific biosynthesis of the side chain.” Phytochemistry 69(15)2737-42. (Direct Link)


Lankau, R.A. and D.J. Kliebenstein. (2009) “Competition and herbivory interact to determine the accumulation and fitness consequences of a secondary compound.” Journal of Ecology 97(1)78-88. (Editors Choice)(Direct Link)


Bidart-Bouzat, M.G. and D.J. Kliebenstein. (2008) “Differential levels of insect herbivory in the field associated with genotypic variation in glucosinolates in Arabidopsis thaliana”. Journal of Chemical Ecology 34(8)1026-37. (Direct link)


Kliebenstein, D.J. (2008) “A quantitative genetics and ecological model system: Understanding the aliphatic glucosinolate biosynthetic network via QTLs” Phytochemistry Reviews v(i)pp. (Direct link) (draft)


Kliebenstein, D.J. (2008) “A role for gene duplication and natural variation of gene expression in the evolution of metabolism”.  PLoS ONE 3(3)e1838. (Free Access)


Sønderby, I.E., Hansen, B.G., Bjarnholt, N., Ticconi, C., Halkier, B.A. and D.J. Kliebenstein. (2007) “A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates in Arabidopsis.” PLoS ONE 2(12):e1257. (Free Access)


Kliebenstein, D.J. , D’Auria, J.C., Behere, A.S., Kim, J.H., Gunderson, K.L., Breen, J.N., Lee, G., Gershenzon, J., Last, R.L., Jander, G. (2007) “Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana.” Plant Journal 51(6):1062-76. (Pubmed link).


Hansen, B.G., Kliebenstein, D.J. and B.A. Halkier (2007) “Identification of an Arabidopsis flavin monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis.” Plant Journal 50(5):902-10. (Pubmed link)


Oscar, O.R., Kliebenstein, D.J., Arbizu, C., Ortega, R. And C.F. Quiros. (2006) Glucosinolate survey in cultivated and feral mashua (Tropaeolum tuberosum Ruiz & Pavon). Journal of Economic Botany 60(3):254-64 .


Windsor, A.J., Reichelt, M., Figuth, A., Svatoš, A., Kroymann, J., Kliebenstein, D.J., Gershenzon, J. and T. Mitchell-Olds. (2005) Geographic and evolutionary diversification of glucosinolates among near relatives of Arabidopsis thaliana (Brassicaceae). Phytochemistry 66(11):1321-1333. (Pubmed link)


Reichelt, M., Brown, P.D., Schneider, B., Oldham, N.J., Stauber, E., Tokuhisa, J., Kliebenstein, D.J., Mitchell-Olds, T., and J. Gershenzon. (2002) Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 59(6):663-671. (Pubmed link)


Kliebenstein, D.J., Lambrix, V.M., Reichelt, M., Gershenzon, J. and T. Mitchell-Olds. (2001) Gene duplication and the diversification of secondary metabolism: glucosinolate biosynthetic enzymes in Arabidopsis thaliana as an example. Plant Cell 13(3):681-693. (Pubmed link)


Kliebenstein, D.J., Kroymann, J., Brown, P., Figuth, A., Pedersen, D., Gershenzon, J. and T. Mitchell-Olds. (2001). Genetic Control of Natural Variation in Arabidopsis thaliana Glucosinolate Accumulation. Plant Physiology 126(2):811-825. (Pubmed link)

Agee, A.E., Surpin, M. Sohn, E.J., Girke, T., Rosado, A., Kram, B.W., Carter, C., Wentzell, A.M., Kliebenstein, D.J., Jin, H.C., Park, O.K., Jin, H., Hicks, G.R., and N. Raikhel. (2010) “MODIFIED VACUOLE PHENOTYPE1 is an Arabidopsis myrosinase-associated protein involved in endomembrane protein trafficking.” Plant Physiology 152(1)120-132. (Pubmed Link)


Burow, M., Losansky, A., Muller, R., Plock, A., Kliebenstein, D.J. And U. Wittstock. (2009) The genetic basis of constitutive and herbivore-induced ESP-independent nitrile formation in Arabidopsis thaliana. Plant Physiology 149(1):561-574 . (Open Access)


Wentzell, A.M., Boeye, I., Zhang, Z.-Y. and D.J. Kliebenstein. (2008) “Genetic networks controlling structural outcome of glucosinolate activation across development.” PLoS Genetics 4(10)e1000234 (Open Access)


Wentzell, A.M. and D.J. Kliebenstein. (2008) Genotype, age, tissue and environment regulate the structural outcome of glucosinolate activation. Plant Physiology 147(5)415-28. (Open Access)(Pubmed link)(Editors‘ Choice mention in Science)


Burow, M., Zhang, Z., Ober, J.A., Lambrix, V.M., Wittstock, U., Gershenzon, J. And D.J. Kliebenstein. (2008) ESP and ESM1 mediate Indol-3-acetonitrile production from Indol-3-ylmethyl glucosinolate in Arabidopsis. Phytochemistry 69(3)663-71. (Pubmed Link).


Zhang, Z., Ober, J.A. and D.J. Kliebenstein. (2006) The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis. Plant Cell 18(6):1524-36. (Pubmed link).


Ratzka, A., Vogel, H., Kliebenstein, D.J., Mitchell-Olds, T. and J. Kroymann. (2002). Disarming the mustard oil bomb. Proceedings of the National Academy of  Sciences (USA)  99(17):11223-11228. (Pubmed link)


Kliebenstein, D.J., Pedersen, D. and T. Mitchell-Olds. (2002) Comparative analysis of insect resistance QTL and QTL controlling the myrosinase/glucosinolate system in Arabidopsis thaliana. Genetics 161(1):325-332. (Pubmed link)


Lambrix, V.M., Reichelt, M., Mitchell-Olds, T., Kliebenstein, D.J., J. Gershenzon.. (2001) The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13(6):2793-2807. (Pubmed link)

Publications (Pubmed Search)

Rowe, H.C. Walley, J.W., Corwin, J.A., Chan, E.K.F., Corwin, J.A., Dehesh, K. and Kliebenstein, D.J. (2010) “Deficiencies in JA-mediated plant defense reveal quantitative genetic variation in Botrytis cinerea pathogenesis” PLoS Pathogens 6(4):e1000861. (Pubmed Link)


Rowe, H.C. and D.J. Kliebenstein. (2008) “Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea.” Genetics 180(4):2237-2250. (Direct Link)


Walley, J.W., Rowe, H.C., Xiao, Y., Chehab, E.W., Kliebenstein, D.J., Wagner, D. and K. Dehesh. (2008) “The chromatin remodeler SPLAYED regulates specific stress signaling pathways. PLoS Pathogens 4(12):e1000237. (Pubmed link)(Direct Link)


Kliebenstein, D.J. and H.C. Rowe (2008) “Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction.” Plant Science 174(6)551-6. (Pubmed link)(draft)


Chehab, E.W., Kaspi, R., Savchenko, T., Rowe, H., Negre-Zakharov, F., Kliebenstein, D.J., and K. Dehesh.  (2008) “Distinct roles of jasmonates and aldehydes in plant-defense responses”. PLoS ONE 3(4)e1904 (Free Access)(Pubmed link)


Rowe, H.C and D.J. Kliebenstein. (2007) “Elevated genetic variation within virulence-associated Botrytis cinerea polygalacturonase loci.” Molecular Plant Microbe Interactions (20)9:1126-37. (Pubmed link)


Kliebenstein, D.J., Rowe, H.C. and K.J. Denby. (2005) Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen susceptibility. Plant Journal 44(1):25-36. (Pubmed link)


Murray, S.L., Adams, N., Kliebenstein, D.J., Loake, G.J. and K.J. Denby. (2005) A constitutive PR-1::Luciferase expression screen identifies Arabidopsis mutants with differential disease resistance to biotrophic and necrotrophic pathogens. Molecular Plant Pathology 6(1):31-41. (Journal link)


Denby, KJ, Kumar, P. and Kliebenstein, D.J. (2004) Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant Journal 38(3):473-486. (Pubmed link)




Paul-Victor, C., Züst, T. Rees, M., Kliebenstein, D.J. and L.A. Turnbull (2010). “A new method for measuring RGR can uncover the costs of defensive compounds in Arabidopsis thaliana.” New Phytologist 187(4)1102-11. (Pubmed link)


Kliebenstein, D.J. (2010). “Genetic and functional modularity: How does an organisms solve a nearly infinite genetic/environmental problem space?”. Heredity v(i)pp-pp.(Pubmed link)


Kliebenstein, D.J. and H.C. Rowe (2009) “Anti-Rust Antitrust.” Science 323:1301-2 (Direct link)


Whittall, J.B., Voelckel, C., Kliebenstein, D.J. and S.A. Hodges. (2006) “Convergence, constraint and the role of regulatory genes during adaptive radiation: Floral anthocyanins in Aquilegia.” Molecular Ecology  15(14):4645-58. (Pubmed link)


Brown, B.A., Cloix, C., Jiang, G.H., Kaiserli, E., Herzyk, P., Kliebenstein, D.J. and G.I. Jenkins. (2005) A UV-B-specific signaling component orchestrates plant UV-protection.  Proc. Natl. Acad. Sci. USA. 102(50):18225-30. (Pubmed link)


Kliebenstein, D.J., Lim, J.E., Landry, L.G. and R.L. Last. (2002) Arabidopsis UVR8 regulates Ultraviolet-B signal transduction and tolerance and contains sequence similarity to Human Regulator of Chromatin Condensation 1. Plant Physiology 130(1):234-243. (Pubmed link)


Kliebenstein, D.J., Dietrich, R.A., Martin, A.C., Last, R.L. and J.L. Dangl. (1999) LSD1 Regulates salicylic acid induction of Copper Zinc Superoxide Dismutase in Arabidopsis thaliana. Molecular Plant Microbe Interactions 12(11):1022-26. (Pubmed link)


Kliebenstein, D.J., Monde, R.-A. and R.L. Last. (1998) Superoxide dismutase in Arabidopsis: An eclectic enzyme family with disparate regulation and protein localization. Plant Physiology. 118:637-650. (Pubmed link)


Kliebenstein, D.J., Conklin, P.L., Landry, L.G., Williams, E.H. and R.L. Last. (1997) Arabidopsis mutants altered in antioxidant enzyme accumulation. Plant Physiology. 114(suppl):56.


Jiang, C.-Z., Kliebenstein, D., Ke, N. and S. Rodermel (1994) Destabilization of rbcS sense transcripts by antisense RNA. Plant Molecular Biology 25(3):569-576. (Pubmed link)


Jiang, C.-Z., Quick, W.P., Alred, R., Kliebenstein, D. and S.R. Rodermel (1994) Antisense RNA inhibition of Rubisco Activase expression. Plant Journal 5(6):787-798.

Other References

Chan, E.K.F., Rowe, H.C., Hansen, B.G, and  Kliebenstein, D.J. (2010) “The complex genetic architecture of the metabolome”. PLoS Genetics 6(11)e1001198. (Pubmed link)


Chan, E.K.F., Rowe, H.C. and  Kliebenstein, D.J. (2010) “Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping” Genetics 185(3)991-1007. (Pubmed link)


Kliebenstein, D.J.  (2009) “Advancing genetic theory and application by metabolic QTL analysis.” Plant Cell v(i)pp-pp. (Direct Link)


Kliebenstein, D.J.  (2009) “Quantitative Genomics; analyzing intra-specific variation using global gene expression polymorphisms or eQTLs.” Annual Reviews Plant Biology 60(1)93-114. (Direct Link)


H.C. Rowe, Hansen, B.G., Halkier, B.A. and D.J. Kliebenstein. (2008) “Biochemical networks and epistasis shape the Arabidopsis metabolome.The Plant Cell 20(5)1199-1216. (Free Access)(Pubmed link)


Kliebenstein, D.J. (In press) “Quantification of variation in expression networks” in Plant Systems Biology, edited by D. Belostotsky. Humana Press. (draft).


Hansen, B.G., Halkier, B.A. and D.J. Kliebenstein (2008) “Identifying the molecular basis of QTLs: eQTLs add a new dimension.” Trends in Plant Sciences 13(2):72-77. (Pubmed link)


Wentzell, A.M., Rowe, H.C, Hansen, B.G., Ticconi, C., Halkier, B.A., and D.J. Kliebenstein. (2007) Linking metabolic QTL with network and cis-eQTL controlling biosynthetic pathways. PLOS Genetics 3(9):e162. (Free Access) note—Rowe and Wentzell are co-first authors. (Research highlight in Nature Genetics)


Van Leeuwen, H. Kliebenstein, D.J., West, M.A.L., Kim, K., van Poecke, R., Katagiri, F., Michelmore, R.W., Doerge, R.W. and D.A. St. Clair. (2007) Natural variation among Arabidopsis thaliana accessions for transcriptome response to exogenous salicylic acid. Plant Cell 19(7)2099-110. (Free Access)


West, M.A.L., Kim, K., Kliebenstein, D.J., van Leeuwen, H., Michelmore, R.W., Doerge, R.W., and D.A. St. Clair. (2007). Global eQTL mapping reveals the complex genetic architecture of transcript level variation in Arabidopsis. Genetics 175(3):1441-50. (Pubmed link)


Kliebenstein, D.J., West, M.A.L, van Leeuwen, H., Loudet, O., Doerge, R.W., and D.A. St. Clair. (2006) Identification of QTLs controlling gene expression networks defined a priori. BMC Bioinformatics 7(1):308.  (Pubmed link) (BMC Bioinformatics Link)


West, M.A.L, van Leeuwen, H., Kozik, A., Kliebenstein, D.J., Doerge, R.W., St. Clair, D.A. and R.W. Michelmore. (2006) High-density haplotyping with microarray-based expression and single feature polymorphism markers in Arabidopsis. Genome Research 16(6):787-95.

(Pubmed link)


Kliebenstein, D.J., West, M.A.L., van Leeuwen, H., Kim, K., Doerge, R.W., Michelmore, R.W. and D.A. St.Clair. (2006) Genomic survey of gene expression diversity in Arabidopsis thaliana.  Genetics 172(2):1179-89. (Pubmed link)


Kliebenstein, D.J., Figuth, A., and T. Mitchell-Olds. (2002) Genetic architecture of plastic methyl jasmonate responses in Arabidopsis thaliana. Genetics 161(4):1685-1696. (Pubmed link)


Kliebenstein, D.J., Gershenzon, J. and T. Mitchell-Olds. (2001) Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 159(1):359-370. (Pubmed link)








Botrytis cinerea Resistance

Glucosinolate Hydrolysis

Quantitative Genetics

Glucosinolate Biosynthesis

Other References


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