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Publications Citing NIH T32 Training Grant Support:


Miller, G.P., Waheed Bhat, W., Lanier, E.R., Johnson, S.R., Mathieu, D.T. and Hamberger, B., The biosynthesis of the anti‐microbial diterpenoid leubethanol in Leucophyllum frutescens proceeds via an all‐cis prenyl intermediate. The Plant Journal. doi:

Lybrand, D.B., Xu, H., Last, R.L. and Pichersky, E., 2020. How Plants Synthesize Pyrethrins: Safe and Biodegradable Insecticides. Trends in Plant Science. doi:

Fan, P., P. Wang, Y.-R. Lou, B.J. Leong, B.J. Moore, C.A. Schenck, R. Combs, P. Cao, F. Brandizzi, S.-H. Shiu and R.L. Last. 2020. Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity. eLife. doi:

Medina-Cucurella, A.V., Bammert, G.F., Dunkle, W., Javens, C., Zhu, Y., Mutchler, V.T., Teel, J.T., Stein, C.A., Dunham, S.A. and Whitehead, T.A., 2020. Feline Interleukin-31 shares overlapping epitopes with Oncostatin M Receptor and IL-31RA. Biochemistry. doi:

Sudhakaran, M. and Doseff, A.I., 2020. The Targeted Impact of Flavones on Obesity-Induced Inflammation and the Potential Synergistic Role in Cancer and the Gut Microbiota. Molecules25(11), p.2477. doi:

Takeuchi, T., Sears, B.B., Lindeboom, C., Lin, Y.T., Fekaris, N., Zienkiewicz, K., Zienkiewicz, A., Poliner, E. and Benning, C., 2020. Chlamydomonas CHT7 is required for an effective quiescent state by regulating nutrient-responsive cell cycle gene expression. The Plant Cell32(4), pp.1240-1269. doi:

García-Cerdán, J.G., Schmid, E.M., Takeuchi, T., McRae, I., McDonald, K.L., Yordduangjun, N., Hassan, A.M., Grob, P., Xu, C.S., Hess, H.F. and Fletcher, D.A., 2020. Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and affects carotenoid accumulation in Chlamydomonas. Proceedings of the National Academy of Sciences. DOI:

Li, W., Lybrand, D.B., Xu, H., Zhou, F., Last, R.L. and Pichersky, E., 2020. A Trichome-Specific, Plastid-Localized Tanacetum cinerariifolium Nudix Protein Hydrolyzes the Natural Pyrethrin Pesticide Biosynthetic Intermediate trans-Chrysanthemyl Diphosphate. Frontiers in Plant Science11, p.482. doi:

Havko, N.E., Das, M.R., McClain, A.M., Kapali, G., Sharkey, T.D. and Howe, G.A., 2020. Insect herbivory antagonizes leaf cooling responses to elevated temperature in tomato. Proceedings of the National Academy of Sciences, 117(4), pp.2211-2217. doi:

Pardo, J., Wai, C.M., Chay, H., Madden, C.F., Hilhorst, H.W., Farrant, J.M. and VanBuren, R., 2020. Intertwined signatures of desiccation and drought tolerance in grasses. Proceedings of the National Academy of Sciences, 117(18), pp.10079-10088. doi:

Leong, B.J., Hurney, S.M., Fiesel, P.D., Moghe, G.D., Jones, A.D. and Last, R.L., 2020. Specialized metabolism in a nonmodel nightshade: trichome acylinositol biosynthesis. Plant physiology183(3), pp.915-924. doi:

McClain, A.M. and Sharkey, T.D., 2020. Building a better equation for electron transport estimated from Chl fluorescence: accounting for non-photosynthetic light absorption. New Phytologist225(2), pp.604-608. doi:


Takeuchi, T. and Benning, C., 2019. Nitrogen-dependent coordination of cell cycle, quiescence and TAG accumulation in Chlamydomonas. Biotechnology for Biofuels12(1), pp.1-20. doi: 10.1186/s13068-019-1635-0

Duhl, K.L. and TerAvest, M., 2019. Shewanella oneidensis NADH dehydrogenase mutants exhibit an amino acid synthesis defect. Frontiers in Energy Research7, p.116. doi:

Sharkey, T.D., Weise, S.E., Childs, K., Preiser, A.L., Katulski, H.M., Perrin-Porzondek, C. and Liu, T., 2019. Transcriptional regulation of the glucose-6-phosphate/Phosphate translocator 2 is related to carbon exchange across the chloroplast envelope. Frontiers in plant science10, p.827. doi:

Longley, R., Benucci, G.M.N., Mills, G. and Bonito, G., 2019. Fungal and bacterial community dynamics in substrates during the cultivation of morels (Morchella rufobrunnea) indoors. FEMS microbiology letters366(17), p.fnz215. doi:

Benucci, G.M.N., Longley, R., Zhang, P., Zhao, Q., Bonito, G. and Yu, F., 2019. Microbial communities associated with the black morel Morchella sextelata cultivated in greenhouses. PeerJ7, p.e7744. doi: 

McCoy, A.G., Roth, M.G., Shay, R., Noel, Z.A., Jayawardana, M.A., Longley, R.W., Bonito, G. and Chilvers, M.I., 2019. Identification of Fungal Communities Within the Tar Spot Complex of Corn in Michigan via Next-Generation Sequencing. Phytobiomes Journal, pp.PBIOMES-03. doi:

Li, W., Lybrand, D.B., Zhou, F., Last, R.L. and Pichersky, E., 2019. Pyrethrin biosynthesis: The cytochrome P450 oxidoreducatse CYP82Q3 converts jasmolone to pyrethrolone. Plant Physiology, pp.pp-00499. doi:

Preiser, A.L., Fisher, N., Banerjee, A. and Sharkey, T.D., 2019. Plastidic glucose-6-phosphate dehydrogenases are regulated to maintain activity in the light. Biochemical Journal476(10), pp.1539-1551. doi:

McClain, A.M. and Sharkey, T.D., 2019. Triose phosphate utilization and beyond: from photosynthesis to end product synthesis. Journal of Experimental Botany70(6), pp.1755-1766. doi:

Li, L., Lavell, A., Meng, X., Berkowitz, O., Selinski, J., van de Meene, A., Carrie, C., Benning, C., Whelan, J., De Clercq, I. and Wang, Y., 2019. Arabidopsis DGD1 SUPPRESSOR 1 is a Subunit of the Mitochondrial Contact Site and Cristae Organizing System and Affects Mitochondrial Biogenesis. The Plant Cell, pp.tpc-00885. doi:

Lavell, A., Froehlich, J.E., Baylis, O., Rotondo, A. and Benning, C., 2019. A Predicted Plastid Rhomboid Protease Affects Phosphatidic Acid Metabolism in Arabidopsis thaliana. The Plant Journal. doi:

Fan, P., Leong, B.J. and Last, R.L., 2019. Tip of the trichome: evolution of acylsugar metabolic diversity in Solanaceae. Current Opinion in Plant Biology49, pp.8-16. doi:

Leong, B.J., Lybrand, D.B., Lou, Y.R., Fan, P., Schilmiller, A.L. and Last, R.L., 2019. Evolution of metabolic novelty: a trichome-expressed invertase creates specialized metabolic diversity in wild tomato. Science Advances5(4), p.eaaw3754. doi:

Lavell, A.A. and Benning, C., 2019. Cellular organization and regulation of plant glycerolipid metabolism. Plant and Cell Physiology60(6), pp.1176-1183. doi:

Jack, C.N., Rowe, S.L., Porter, S.S. and Friesen, M.L., 2019. A high‐throughput method of analyzing multiple plant defensive compounds in minimized sample mass. Applications in Plant Sciences, p.e01210. doi:

Moore, B.M., Wang, P., Fan, P., Leong, B., Schenck, C.A., Lloyd, J.P., Lehti-Shiu, M.D., Last, R.L., Pichersky, E. and Shiu, S.H., 2019. Robust predictions of specialized metabolism genes through machine learning. Proceedings of the National Academy of Sciences116(6), pp.2344-2353. doi:

Wrenbeck, E.E., Bedewitz, M.A., Klesmith, J.R., Noshin, S.R., Barry, C. and Whitehead, T.A., 2019. An automated data-driven pipeline for improving heterologous enzyme expression. ACS Synthetic Biology. doi:

Clark, T.J., Friel, C.A., Grman, E., Friesen, M.L. and Shachar‐Hill, Y., 2019. Unfair trade underground revealed by integrating data with Nash bargaining models. New Phytologist. doi:

Medina-Cucurella, A.V., Steiner, P.J., Faber, M.S., Beltrán, J., Borelli, A.N., Kirby, M.B., Cutler, S.R. and Whitehead, T.A., 2019. User-defined single pot mutagenesis using unamplified oligo pools. Protein Engineering, Design and Selection32(1), pp.41-45. doi:


Agostoni, M., Logan-Jackson, A.R., Heinz, E.R., Severin, G.B., Bruger, E.L., Waters, C.M. and Montgomery, B.L., 2018. Homeostasis of second messenger cyclic-di-AMP is critical for cyanobacterial fitness and acclimation to abiotic stress. Frontiers in microbiology9. doi:

Angelos, E. and Brandizzi, F., 2018. NADPH oxidase activity is required for ER stress survival in plants. The Plant Journal96(6), pp.1106-1120. doi:

Xu, H., Lybrand, D., Bennewitz, S., Tissier, A., Last, R.L. and Pichersky, E., 2018. Production of trans-chrysanthemic acid, the monoterpene acid moiety of natural pyrethrin insecticides, in tomato fruit. Metabolic engineering47, pp.271-278.

Rowe, S.L., Norman, J.S. and Friesen, M.L., 2018. Coercion in the evolution of plant–microbe communication: A perspective. Molecular Plant-Microbe Interactions31(8), pp.789-794..

Duhl, K.L., Tefft, N.M., TerAvest, M.A. 2018. Shewanella oneidensis MR-1 utilizes both sodium- and proton-pumping NADH dehydrogenases during aerobic growth. Appl. Environ. Microbiol. 84:e00415-1810. doi: 1128/AEM.00415-18.

Medina-Cucurella, A., Zhu, Y., Bowen, S.J., Bergeron, L.M. and Whitehead, T.A. 2018. Pro region engineering of nerve growth factor by deep mutational scanning enables a yeast platform for conformational epitope mapping of anti-NGF monoclonal antibodies, Biotech. and Bioeng. doi: 10.1002/bit.26606.

Poliner E., Takeuchi T., Du, Z.Y., Benning, C., Farré, E.M. 2018.“Nontransgenic Marker-Free Gene Disruption by an Episomal CRISPR System in the Oleaginous Microalga, Nannochloropsis oceanica CCMP1779.” ACS Synth. Biol.  Mar 14. doi: 10.1021/acssynbio.7b00362

Medina-Cucurella A. and Whitehead, T.A. 2018. Characterizing Protein-Protein Interactions Using Deep Sequencing Coupled to Yeast Surface Display, Methods Mol. Biol.,1764:101-121, doi: 10.1007/978-1-4939-7759-8_7


Leong, B.J. and Last, R.L. Promiscuity, impersonation and accommodation: evolution of plant specialized metabolism. 2017. Curr. Opin. Struct. Biol., 47:105–112

Wrenbeck E.E., Azouz L.R., Whitehead T.A. 2017. Single-mutation fitness landscapes for an enzyme on multiple substrates reveal specificity is globally encoded, Nature Comm. 8, Article number: 15695. doi:10.1038/ncomms15695

Moghe, G.D., Leong, B.J., Hurney, S. Jones, A.D. and Last, R.L. 2017. Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant defense related specialized metabolic pathway. eLife 2017;6:e28468 DOI: 10.7554/eLife.28468.

Clark, T.J., Friel, C.A., Grman, E., Shachar-Hill, Y. and Friesen, M.L. 2017. Modelling nutritional mutualisms: challenges and opportunities for data integration. Ecol. Letts. doi: 10.1111/ele.12810

Angelos, E., Ruberti, C., Kim, S.J., and Brandizzi, F. 2017. Maintaining the factory: the roles of the unfolded protein response in cellular homeostasis in plants. Plant J. 90:671-682. doi:10.1111.tpj.13449

Wrenbeck E. E., Faber, M. S., Whitehead, T. A. 2017. Deep sequencing methods for protein engineering and design. Curr. Opin. Struct. Biol., 45:36-44, doi: 10.1016/

Klesmith, J.R., Bacik, J.P., Wrenbeck, E.E., Michalczyk, R., Whitehead, T.A. 2017. Trade-offs between enzyme fitness and solubility illuminated by deep mutational scanning. Proc. Natl. Acad. Sci. U.S.A., 114:2265-2270, doi: 10.1073/pnas.1614437114

Panchy NL, Azodi C.B., Winship EF, O'Malley RC, Shiu SH. 2017. Asymmetric evolution of the transcription profiles and cis-regulatory sites contributes to the retention of transcription factor duplicates. bioRxiv DOI:10.1101/115857

Yang, Y., Zienkiewicz, A., Lavell, A. and Benning, C. 2017. Coevolution of Domain Interactions in the Chloroplast TGD1, 2, 3 Lipid Transfer Complex Specific to Brassicaceae and Poaceae Plants. Plant Cell, 29:1500–1515. DOI:


Wrenbeck, E.E., Klesmith, J.R., Stapleton, J.A., Adeniran, A., Tyo, K.E.J. and Whitehead T.A. 2016. Plasmid-based one-pot saturation mutagenesis. Nature Methods, 13:928–930. doi:10.1038/nmeth.4029.

Ning, J., Moghe, G., Leong, B.J., Kim, J., Ofner, I., Wang, Z., Adams, C., Jones, A., Zamir, D., Last, RL. 2015.  A feedback insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato. Plant Physiol. 169:1821-1835. doi:10.1104/pp.15.00474

Tsai, C.H., Warakanont, J., Takeuchi, T., Sears, B.B., Moellering, E.R., Benning, C. 2014. The protein Compromised Hydrolysis of Triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas. Proc. Natl. Acad. Sci. U.S.A. 111:15833–15838. doi:/10.1073/pnas.1414567111.

Other Publications from our Trainees:

Fan, P., Wang, P., Lou, Y.R., Leong, B.J., Moore, B.J., Schenck, C.A., Combs, R., Cao, P., Brandizzi, F., Shiu, S.H. and Last, R.L., 2020. Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity. bioRxiv. doi:

Sudhakaran, M., Sardesai, S. and Doseff, A.I., 2019. Flavonoids: new frontier for immuno-regulation and breast cancer control. Antioxidants8(4), p.103. doi:

Panchy, N.L., Azodi, C.B., Winship, E.F., O’Malley, R.C. and Shiu, S.H., 2019. Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication. BMC evolutionary biology, 19(1), p.77. doi:

Li, J., Weraduwage, S.M., Peiser, A.L., Tietz, S., Weise, S.E., Strand, D.D., Froehlich, J.E., Kramer, D.M., Hu, J. and Sharkey, T.D., 2019. A Cytosolic Bypass and G6P Shunt in Plants Lacking Peroxisomal Hydroxypyruvate Reductase. Plant physiology, pp.pp-00256. doi:

Johnson, S.R., Bhat, W.W., Sadre, R., Miller, G.P., Garcia, A.S. and Hamberger, B., 2019. Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution. New Phytologist. doi:

Lantz, A.T., Solomon, C., Gog, L., McClain, A.M., Weraduwage, S.M. and Sharkey, T.D., 2019. Isoprene suppression by CO2 is not due to triose phosphate utilization (TPU) limitation. Frontiers in Forests and Global Change2, p.8. doi:

Zuo, Z., Weraduwage, S.M., Lantz, A.T., Sanchez, L.M., Weise, S.E., Wang, J., Childs, K.L. and Sharkey, T.D., 2019. Isoprene acts as a signaling molecule in gene networks important for stress responses and plant growth. Plant physiology180(1), pp.124-152. doi: 

Medina-Cucurella, A.V., Mizrahi, R.A., Asensio, M.A., Edgar, R.C., Leong, J., Leong, R., Lim, Y.W., Nelson, A., Niedecken, A.R., Simons, J.F., Spindler, M.J., Stadtmiller, K., Wayham, N., Adler, A.S., Johnson, D.S. 2019. Preferential Identification of Agonistic OX40 Antibodies by Using Cell Lysate to Pan Natively Paired, Humanized Mouse-Derived Yeast Surface Display libraries. Antibodies.  doi:

Hoopes, G.M., Hamilton, J.P., Kim, J., Zhao, D., Wiegert-Rininger, K., Crisovan, E. and Buell, C.R., 2018. Genome assembly and annotation of the medicinal plant Calotropis gigantea, a producer of anticancer and antimalarial cardenolides. G3: Genes, Genomes, Genetics8(2), pp.385-391. doi: 10.1534/g3.117.300331

Hurlock, A.K., Wang, K., Takeuchi, T., Horn, P.J. and Benning, C., 2018. In vivo lipid ‘tag and track’approach shows acyl editing of plastid lipids and chloroplast import of phosphatidylglycerol precursors in Arabidopsis thaliana. The Plant Journal95(6), pp.1129-1139. doi:

Dums, J.T., Murphree, C.A., Vasani, N., Young, D. and Sederoff, H., 2018. Metabolic and Transcriptional Profiles of Dunaliella viridis Supplemented with Ammonium Derived from Glutamine. Frontiers in Marine Science5, p.311. doi:

Johnson, S.R., Bhat, W.W., Bibik, J., Turmo, A., Hamberger, B., Hamberger, B., Boachon, B., Buell, C.R., Crisovan, E., Dudareva, N. and Garcia, N., 2019. A database-driven approach identifies additional diterpene synthase activities in the mint family (Lamiaceae). Journal of Biological Chemistry294(4), pp.1349-1362. doi:

Hoopes, G.M., Hamilton, J.P., Wood, J.C., Esteban, E., Pasha, A., Vaillancourt, B., Provart, N.J. and Buell, C.R., 2018. An updated gene atlas for maize reveals organ‐specific and stress‐induced genes. The Plant Journal. doi:

Li, J., Weraduwage, S.M., Preiser, A.L., Weise, S.E., Strand, D.D., Froehlich, J.E., Kramer, D.M., Hu, J. and Sharkey, T.D., 2018. Loss of Peroxisomal Hydroxypyruvate Reductase Inhibits Triose Phosphate Isomerase but Stimulates Cyclic Photosynthetic Electron Flow and the Glc-6P-Phosphate Shunt. bioRxiv, p.278580. doi: 10.1101/278580

Uygun, S., Seddon, A.E., Azodi, C.B. and Shiu, S.H., 2017. Predictive models of spatial transcriptional response to high salinity. Plant physiology174(1), pp.450-464. doi: 10. 1104/ pp. 16. 01828

Dowdell, A.S., Murphy, M.D., Azodi, C., Swanson, S.K., Florens, L., Chen, S. and Zückert, W.R., 2017. Comprehensive spatial analysis of the Borrelia burgdorferi lipoproteome reveals a compartmentalization bias toward the bacterial surface. Journal of bacteriology199(6), pp.e00658-16. doi: 10.1128/JB.00658-16

Murphree, C.A., Dums, J.T., Jain, S.K., Zhao, C., Young, D.Y., Khoshnoodi, N., Tikunov, A., Macdonald, J., Pilot, G. and Sederoff, H., 2017. Amino acids are an ineffective fertilizer for Dunaliella spp. growth. Frontiers in plant science8, p.847. doi: 10.3389/fpls.2017.00847

Malmstrom, C.M., Bigelow, P., Trębicki, P., Busch, A.K., Friel, C., Cole, E., Abdel-Azim, H., Phillippo, C. and Alexander, H.M., 2017. Crop-associated virus reduces the rooting depth of non-crop perennial native grass more than non-crop-associated virus with known viral suppressor of RNA silencing (VSR). Virus research241, pp.172-184..

Banerjee A., Preiser A.L., Sharkey, T.D. Engineering of Recombinant Poplar Deoxy-D-xylulose-5-phosphate Synthase (PtDXS) by Site-directed Mutagenesis Improves Its Activity. 2016. PLoSOne. 11(8). 

Yang J., Preiser A.L., Li Z, Weise S.E., Sharkey T.D. 2016. Triose phosphate use limitation of photosynthesis short-term and long-term effects. Planta. 243(3): 687-98. doi:10.1007/s00425-015-2436-8

Clark, T.J. and Lu, Y., 2015. Analysis of loss-of-function mutants in aspartate kinase and homoserine dehydrogenase genes points to complexity in the regulation of aspartate-derived amino acid contents. Plant physiology168(4), pp.1512-1526. doi: 

Lantz, A.T., Cardiello, J.F., Gee, T.A., Richards, M.G., Rosenstiel, T.N. and Fisher, A.J., 2015. Biochemical characterization of an isoprene synthase from Campylopus introflexus (heath star moss). Plant Physiology and Biochemistry94, pp.209-215.. doi: 10.1016/j.plaphy.2015.06.008

Brasher, M.I., Surmacz, L., Leong, B., Pitcher, J., Swiezewska, E., Pichersky, E. and Akhtar, T.A., 2015. A two‐component enzyme complex is required for dolichol biosynthesis in tomato. The Plant Journal82(6), pp.903-914. doi: 10.1111/tpj.12859

Thireault, C., Shyu, C., Yoshida, Y., St. Aubin, B., Campos, M.L. and Howe, G.A., 2015. Repression of jasmonate signaling by a non‐TIFY JAZ protein in Arabidopsis. The Plant Journal82(4), pp.669-679. doi: 10.1111/tpj.12841, 25846245

Takeuchi, T., Newton, L., Burkhardt, A., Mason, S. and Farré, E.M., 2014. Light and the circadian clock mediate time-specific changes in sensitivity to UV-B stress under light/dark cycles. Journal of experimental botany65(20), pp.6003-6012. doi:

Bienick, M.S., Young, K.W., Klesmith, J.R., Detwiler, E.E., Tomek, K.J. and Whitehead, T.A., 2014. The interrelationship between promoter strength, gene expression, and growth rate. PloS one9(10). doi: 10.1371/journal.pone.0109105.

How to make sure publications are compliant with NIH guidelines for open access:

The easiest way to make sure that publications are compliant is to publish gold open access in journals indexed on PubMed.

If the journal does not offer gold OA, or it is more expensive than you wish to pay, make sure that you inform the journal that the work was funded in part by NIH. They should provide you with info on how they will submit to PubMed Central (no more than 12 months after the publication date) or instructions for you to submit the manuscript to NIH PubMed Central.

The MSU PBHS Biotechnology Training Program is supported by grant number NIH T32-GM110523.