Faculty
Joseph P. Noel
Professor
Jack H. Skirball Center for Chemical Biology and Proteomics & Howard Hughes Medical Institute

Mechanistic, Structural and Evolutionary Basis for Chemical Complexity in Nature
Research Goals
The focus of the research in our laboratory is to decipher the core principles influencing evolutionary change in proteins and protein networks particularly enzymes and metabolic pathways underlying the emergence and rapid expansion of chemical diversity in living systems. We ultimately hope to understand the chemical, structural and evolutionary tenets governing this extraordinary form of biodiversity and biocomplexity. In addition to probing the fundamental nature of molecular evolution, we also aim to exploit what we learn to direct our efforts at harnessing and altering these pathways to generate chemical "scaffolds" for the development of small molecule tools modulating proteins, cells and organisms.
Evolutionary Rationale
We study sessile organisms such as plants and microbes and the molecular basis for how they acquired and evolved specialized biosynthetic networks classified as secondary metabolic pathways, the output of which are regio- and stereo-chemically complex small molecule natural products including isoprenoids, flavonoids, polyketides and alkaloids. These chemicals of secondary metabolism, or more appropriately specialized metabolism, serve as chemical languages in ecosystems and impart a species-specific chemical "signature" on the parent organism. Functionally, these natural chemicals often confer protective or symbiotic characteristics on their hosts allowing sessile organisms to survive and prosper in a multitude of challenging ecological niches.
So why are these metabolic pathways useful for understanding the molecular roots of biodiversity, biocomplexity and evolution? The means by which organisms acquire, improve and exploit diverse metabolic systems to generate a rich repertoire of chemically complex natural products play key roles in the rapid expansion of many ecosystems, and therefore, hold incredible adaptive significance for the diversity of life. While seemingly insignificant, specialized metabolites often serve as key mediators of intra- and interspecies interactions resulting in speciation, survival and ecological homeostasis. Under the evolutionary restraints of chemically established adaptation, diverse molecular changes associated with specialized metabolism are often preserved genetically in a particular species' genome and are discerned at a functional and structural level. These often ecotype specific genomes are the direct result of the increased fitness of host organisms "chemically" adapted to specific ecological niches. Therefore, these specialized metabolic pathways and their "chemical output" present us with a rich evolutionary record of where biosynthetic pathways, natural chemicals and biosynthetic enzymes have been (vestigial biochemical traits), what adaptive advantages these complex enzymatic systems hold in the present (emergent function), and ultimately where these pathways may be heading in the future (functional plasticity).
Metabolic Adaptation, Synthetic Evolutionary Lineages and Natural Chemicals
Currently, we are mapping the adaptive molecular changes that have occurred in enzymes and metabolic pathways of specialized metabolism as these enzymes and enzyme networks emerged and subsequently evolved from their ancestral roots in primary metabolism billions of years ago. Unlike enzymes of specialized metabolism, the modern day versions of these ancestral proteins are little changed in a functional sense since the primeval split with specialized metabolic enzymes. In short, functional change in primary metabolism is generally counter productive or even lethal since these enzyme networks often fulfill little changed catalytic roles pivotal for producing universally conserved primary metabolites essential to life. Our work to date has concentrated instead on specialized metabolites and their biosynthetic machinery encompassing three classes of natural chemicals with ancestral origins in primary metabolism, namely polyketides, isoprenoids and hybrid polyketide-isoprenoids.
Moreover, while these specialized metabolic pathways are ideal systems for exploring fundamental principles of natural selection including evolutionary landscapes linking structurally related proteins during the course of enzyme evolution, they also provide novel and rare chemical scaffolds for use in drug development and for engineering the metabolism of organisms. The structural and mechanistic foundation for evolutionary change in these systems provides us with a more cogent starting point to harness and alter biosynthetic pathways for the production of regio- and stereo-chemically complex molecular scaffolds. Notably, these natural products often possess diverse and extant bioactivities selected for over billions of years, a fact historically exploited during the search for new pharmaceuticals.
Genetically Encoded Medicinal Chemistry and Healthy Plant Based Diets
More recently, we have turned our attention to genetically encoding rationally designed "synthetic" metabolic pathways to facilitate our experimental search for definitive health related roles associated with natural plant compounds (nutraceuticals) including flavonoids and stilbenes (resveratrol) found in plant-rich diets. By genetically encoding existing and newly designed pathways, we can employ model organisms such as worms, flies and mice as heterologous hosts for our newly assembled metabolic pathways. In this way, understanding the detailed structures and functions of the enzymes that produce these compounds, how these enzyme structures change during the course of evolution, and how these enzymes organize themselves spatially and temporally in cells, we can judiciously engineer "synthetic" versions of the biosynthetic pathways now linked to an artificial gene or a set of genes. These "synthetic" and genetically encoded pathways can then be introduced and precisely regulated in new hosts to locally produce bioactive compounds starting from universal metabolic building blocks available in all organisms. With this level of control, we can then rigorously address, in a cellular and tissue specific context, the role played by these dietary compounds in slowing the progression of human maladies such as aging, aberrant fat metabolism, diabetes and various neurodegenerative diseases, all of which have been circumstantially curbed by plant derived flavonoids and stilbenes. Moreover, by harnessing a repository of biosynthetic reactions that alter these compounds in cells, we can genetically encode the chemical modification of existing compounds to improve their potency and activity entirely in living animals.
Education
- University of Pittsburgh at Johnstown, B.S., Chemistry, 1982-1985
- The Ohio State University, Ph.D., Chemistry and Biochemistry, 1985-1990
- Yale University, Postdoctoral Fellow, Structural Biology, 1990-1994
Awards and Honors
- Sohio and Philips Petroleum Company Fellow, 1985
- University Fellow, The Ohio State University, 1985-1986
- Presidential Fellow, 1988-1989
- Monsanto Biotechnology Fellow, 1989-1990
- National Science Foundation Chemistry Postdoctoral Fellow, 1990-1992
- National Institutes of Heath Postdoctoral Fellow, 1993-1994
- Howard Hughes Medical Institute Investigator, 2005
Selected Publications
- Starks, C.M., Back, K., Chappell, J., and Noel, J.P. (1997) Structural Basis for Cyclic Terpene Biosynthesis by Tobacco 5-Epi-Aristolochene Synthase. Science 277: 1815-1820.
- Ferrer, J.-L., Jez, J.M., Bowman, M.E., Dixon, R.A., and Noel, J.P. (1999) Structure of Chalcone Synthase and the Molecular Basis of Plant Polyketide Biosynthesis. Nat. Struct. Biol. 6: 775-783.
- Jez, J.M., Bowman, M.E., Dixon, R.A., and Noel, J.P. (2000) Structure and mechanism of the evolutionarily unique plant enzyme chalcone isomerase. Nat. Struct. Biol. 7: 786-791.
- Zubieta, C., He, X-Z., Dixon, R.A., and Noel, J.P. (2001) Structures of two natural product methyltransferases reveal the basis for substrate specificity in plant O-methyltransferases. Nat. Struct. Biol. 8: 271-279.
- Zubieta, C., Kota, P., Ferrer, J.-L., Dixon, R.A., and Noel, J.P. (2002) Structural Basis for the Modulation of Lignin Monomer Methylation by Caffeic Acid / 5-Hydroxyferulic Acid 3/5-O-Methyltransferase. Plant Cell 14:1265-1277.
- Zubieta, C., Ross, J.R., Koscheski, P., Yang, Y., Pichersky, E., and Noel, J.P. (2003) Structural Basis for Substrate Recognition in the Salicylic Acid Carboxyl Methyltransferase Family. Plant Cell 15: 1704-1716.
- Austin, M.B., Bowman, M.E., Ferrer, J.-L., Schröder, J., and Noel, J.P. (2004) An Aldol Switch Discovered in Stilbene Synthases Mediates Cyclization Specificity of Type III Polyketide Synthases. Chem. Biol. 11: 1179-1194.
- Kuzuyama, T., Noel, J.P., and Richard, S.B. (2005) Structural basis for the promiscuous biosynthetic prenylation of aromatic natural products. Nature 435: 983-987.
- Pichersky, E., Noel, J.P., and Dudareva, N. (2006) Biosynthesis of Plant Volatiles: Nature's Diversity and Ingenuity. Science 311: 808-811.
- Koeduka, T., Fridman, E., Gang, D.R., Vassao, D.G., Jackson, B.L., Kish, C.M., Orlova, I., Spassova, S.M., Lewis, N.G., Noel, J.P., Baiga, T.J., Dudareva, N. and Pichersky, E. (2006) From the Cover: Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. Proc. Natl. Acad. Sci. USA 103: 10128-10133. Epub 2006 Jun 16.
- Zhang, Y., Kim, Y., Genoud, N., Gao, J., Kelly, J.W., Pfaff, S.L., Gill, G.N., Dixon, J.E. and Noel, J.P. (2006) Determinants for Dephosphorylation of the RNA Polymerase II C-terminal domain by Scp1. Mol. Cell 24: 759-770.
- Liu, C.J., Deavours, B.E., Richard, S.B., Ferrer, J.L., Blount, J.W., Huhman, D., Dixon, R.A. and Noel, J.P. (2006) Structural basis for dual functionality of isoflavonoid O-methyltransferase in the evolution of plant defense responses. Plant Cell 18: 3656-3669. Epub 2006 Dec 15.
- Louie, G.V., Bowman, M.E., Moffitt, M.C., Baiga, T.J., Moore, B.S. and Noel, J.P. (2006) Structural determinants and modulation of substrate specificity in phenylalanine - tyrosine ammonia-lyases. Chem. Biol. 13: 1327-1338.
- Moffitt, M.C., Louie, G.V., Bowman, M.E., Pence, J., Noel, J.P. and Moore, B.S. (2007) Discovery of two cyanobacterial phenylalanine ammonia lyases: kinetic and structural characterization. Biochemistry 46: 1004-1012. Epub 2007 Jan 5.
- Varbanova. M., Yamaguchi, S., Yang, Y., McKelvey, K., Hanada, A., Borochov, R., Yu, F., Jikumaru, Y., Ross, J., Cortes, D., Ma, C.J., Noel, J.P., Mander, L., Shulaev, V., Kamiya, Y., Rodermel, S., Weiss, D. and Pichersky, E. (2007) Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19: 32-45. Epub 2007 Jan 12.
- Zhang, Y., Daum, S., Wildemann, D., Zhou, X.Z., Verdecia, M.A., Bowman, M.E., Lücke, C., Hunter, T., Lu, K.-P., Fischer, G. and Noel, J.P. (2007) Structural basis for high-affinity peptide inhibition of human Pin1. ACS Chem. Biol. 2: 320-328.
- Haagen, Y., Unsold, I., Westrich, L., Gust, B., Richard, S.B., Noel, J.P. and Heide, L. (2007) A soluble magnesium-independent prenyltransferase catalyzes the reverse and regular C-prenylations and O-prenylations of aromatic substrates. FEBS Lett. 581: 2889-2893. Epub 2007 May 22.
- Takahashi, S., Yeo, Y.S., Zhao, Y., O'Maille, P.E., Greenhagen, B.T., Noel, J.P., Coates, R.M. and Chappell, J. (2007) Functional characterization of premnaspirodiene oxygenase, a cytochrome P450 catalyzing regio- and stereo-specific hydroxylations of diverse sesquiterpene substrates. J. Biol. Chem. 282: 31744-31754. Epub 2007 Aug 22.
- Louie, G.V., Baiga, T.J., Bowman, M.E., Koeduka, T., Taylor, J.H., Spassova, S.M., Pichersky, E. and Noel, J.P. (2007) Structure and reaction mechanism of eugenol synthase from Ocimum basilicum. PLoS ONE. 10: e993.
- Noel, J.P. (2007) Digging for answers, smelling a hint of success and tasting triumph. Nat. Chem. Biol. 3: 690-691.
- Eustaquio, A.S., Pojer, F., Noel, J.P. and Moore, B.S. (2008) Discovery and characterization of a marine bacterial SAM-dependent chlorinase. Nat. Chem. Biol. 4: 69-74. Epub 2007 Dec 2.
- Zhao, N., Ferrer, J.-L., Ross, J., Guan, J., Yang, Y., Pichersky, E., Noel, J.P. and Chen, F. (2008) Structural, Biochemical and Phylogenetic Analyses Suggest that Indole-3-acetic Acid Methyltransferase Is An Evolutionarily Ancient Member of the SABATH Family. Plant Physiol. 146: 455-467. Epub 2007 Dec 27.
- Austin, M.B., O'Maille, P.E. and Noel, J.P. (2008) Evolving biosynthetic tangos negotiate mechanistic landscapes. Nat. Chem. Biol. 4: 217-222.
- Koeduka, T., Louie, G.V., Orlova, I., Kish, C.M., Ibdah, M., Wilkerson, C.G., Bowman, M.E., Baiga, T.J., Noel, J.P., Dudareva, N. and Pichersky, E. (2008) The multiple phenylpropene synthases in both Clarkia breweri and Petunia hybrida represent two distinct protein lineages. Plant J. 54: 362-374. Epub 2008 Jan 16.
- Baiga, T.J., Guo, H., Xing, Y., O'Doherty, G.A., Dillin, A., Austin, M.B., Noel, J.P. and La Clair, J.J. (2008) Metabolite induction of Caenorhabditis elegans dauer larvae arises via transport in the pharnyx. ACS Chem. Biol. 3: 294-304. Epub 2008 Apr 1.
- Tao, Y., Ferrer, J.-L., Pojer, F., Hong, F., Ljung, K., Long, J.A., Li, L., Moreno, J.E., Bowman, M.E., Ivans, L.J., Lim, J., Ballare, C.L., Sandberg, G., Noel, J.P. and Chory, J. (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for the shade avoidance response of plants. Cell 133: 164-176.
- Kumano, T., Richard, S.B., Noel, J.P., Nishiyama, M. and Kuzuyama, T. (2008) Chemoenzymatic syntheses of prenylated aromatic small molecules using Streptomyces prenyltransferases with relaxed substrate specificities. Bioorg. Med. Chem. ##: ###-###. Epub 2008 Jul 24.
- Eustaquio, A.S., Harle, J., Noel, J.P. and Moore, B.S. (2008) S-Adenosyl-L-Methionine Hydrolase (Adenosine-Forming), a Conserved Bacterial and Archeal Protein Related to SAM-Dependent Halogenases. Chembiochem. ##: ###-###. Epub 2008 Aug 21.
- O'Maille, P.E., Malone, A., Dellas, N., Hess, B.A., Smentek, L., Sheehan, I., Greenhagen, B.T., Chappell, J., Manning, G. and Noel, J.P. (2008) Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nat. Chem. Biol. (in press).
- Bomati, E.K., Dixon, R.A. and Noel, J.P. (2008) Crystal structure of the first dedicated monolignol biosynthetic enzyme cinnamoyl-CoA reductase. Phytochemistry (in press).
Links
- for more information about our laboratory associated with the Howard Hughes Medical Institute please click here - http://hhmi.org/research/investigators/noel.html.
Salk News Releases
- How plants fine-tune their natural chemical defenses, September 8, 2008
- A place in the sun, April 3, 2008
- How basil gets its zing, October 3, 2007
- Detailed 3-D image catches a key regulator of neural stem cell differentiation in action, December 7, 2006
- When the going gets tough, slime molds start synthesizing, August 16, 2006
- New Target for Anti-Cholesterol Drugs, Antibiotics, July 18, 2006
- Prestigious HHMI appointments go to two Salk Institute Researchers, March 21, 2005
- Promiscuous Catalytic Activity Possessed by Novel Enzyme Structure, June 15, 2005
- Puzzle of "French Paradox" Natural Product Solved, September 21, 2004
- Cancer "Survival" Structure Deciphered By Salk Scientists, June 29, 2000
- Plant Enzyme Important For Nutraceuticals Deciphered By Salk Scientists, July 28, 1999

