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Research in my laboratory concerns the biochemistry and control of metabolism in plants, algae, and photosynthetic bacteria. Current areas of focus are: 1. Regulation of photosynthetic membrane lipid assembly; 2. Lipid trafficking between the endoplasmic reticulum (ER) and the plastid; and 3. Regulation of storage lipid biosynthesis in plants and algae.

Studying lipid metabolism is inherently challenging due to the complexity of lipid pathways in photosynthetic organisms. To meet this challenge we apply genetic and genomic approaches in suitable model organisms. The nature of the problems studied also demands the application of state-of-the-art techniques of enzyme biochemistry, analytical chemistry, and cell biology.

The discoveries made by students and postdoctoral researchers in my group encompass novel proteins and their biochemical function in plant lipid metabolism. Examples are proteins involved in sulfolipid [1, 2], phospholipid [3, 4], betaine lipid [5] and galactolipid [6] biosyntheses, transport proteins involved in ER-to-plastid lipid trafficking [7-11], and transcription factors [12] and enzymes [13, 14] critical for storage lipid biosynthesis. These findings have advanced our general understanding of lipid metabolism [15-17].

On occasion, Ph.D. students in my group make big discoveries "on the side". For example, Karen Bohmert first described the founding member of the now famous Argonaute protein family, AGO1 [18]. Her work was acknowledged in the 2006 Nobel speeches by Mello and Fire [19, 20]. Most recently, Eric R. Moellering "connected the dots" discovering an important mechanisms of freezing tolerance in plants. He identified the gene for an enigmatic enzyme involved in the remodeling of chloroplast membranes and showed that loss of this enzyme causes plants to be sensitive to freezing. This work has been published in Science [21].

Aside from these advancements in basic science and the broad training of students and postdoctoral researchers, our research routinely leads to the development of patentable tools and methods that will be useful for the engineering of pharmaceutically relevant lipids, e.g. therapeutic liposomes, or the engineering of improved oil yield in crop plants and algae for the purpose of biofuel production. To enable the translation of basic research findings and to identify job opportunities for graduating students and postdoctoral researchers, extensive contacts and collaborations with biotech companies have been established. MORE

[1] Essigmann B, Guler S, Narang RA, Linke D, Benning C. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 1998;95:1950-1955. Link to PubMed

[2] Yu B, Xu C, Benning C. Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci U S A 2002;99:5732-5737. Link to PubMed

[3] Xu C, Hartel H, Wada H, Hagio M, Yu B, Eakin C, Benning C. The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerol synthase with impaired activity. Plant Physiol 2002;129:594-604. Link to PubMed

[4] Xu C, Cornish AJ, Froehlich JE, Benning C. Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3-phosphate acyltransferase. Plant J 2006;47:296-309. Link to PubMed

[5] Riekhof WR, Sears BB, Benning C. Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Eukaryot Cell 2005;4:242-252. Link to PubMed

[6] Dormann P, Balbo I, Benning C. Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 1999;284:2181-2184. Link to PubMed

[7] Awai K, Xu C, Tamot B, Benning C. A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc Natl Acad Sci USA 2006;103:10817-10822. Link to PubMed

[8] Lu B, Xu C, Awai K, Jones AD, Benning C. A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J Biol Chem 2007;282:35945-35953. Link to PubMed

[9] Xu C, Fan J, Riekhof W, Froehlich JE, Benning C. A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBO J 2003;22:2370-2379. Link to PubMed

[10] Xu C, Fan J, Froehlich J, Awai K, Benning C. Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 2005;17:3094-3110. Link to PubMed

[11] Xu C, Fan J, Cornish AJ, Benning C. (2008) Lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis requires the extraplastidic TGD4 protein. Plant Cell. 20:2190-204. Link to PubMed

[12] Cernac A, Benning C. WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 2004;40:575-585. Link to PubMed

[13] Andre C, Froehlich JE, Moll MR, Benning C. A heteromeric plastidic pyruvate kinase complex involved in seed oil biosynthesis in Arabidopsis. Plant Cell 2007;19:2006-2022. Link to PubMed

[14] Wakao S, Benning C. Genome-wide analysis of glucose-6-phosphate dehydrogenases in Arabidopsis. Plant J 2005;41:243-256. Link to PubMed

[15] Benning C, Ohta H. Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 2005;280:2397-2400. Link to PubMed

[16] Benning C. Mechanisms of lipid transport involved in organelle biogenesis in plant cells. 2009. Annu Rev Cell Dev Biol. 25:71-91 Link to PubMed

[17] Benning C. Questions remaining in sulfolipid biosynthesis: a historical perspective. Photosynth Res 2007;92:199-203. Link to PubMed

[18] Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 1998;17:170-180. Link to PubMed

[19] Mello CC. Return to the RNAi world: rethinking gene expression and evolution (Nobel Lecture).

[20] Fire AZ. Gene silencing by double-stranded RNA (Nobel Lecture).

[21] Moellering ER, Muthan B, Benning C. 2010. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science. 330(6001):226-8. Abstract Reprint

Recent Publications

Zäuner S, Jochum W, Bigorowski T, Benning C. A cytochrome b5-containing plastid-located fatty acid desaturase from Chlamydomonas reinhardtii. Eukaryot Cell. 11:856-863. Link to article

Roston RL, Gao J, Murcha MW, Whelan J, Benning C. 2012. Trigalactosyldiacylglycerol (TGD) 1, 2 and 3 proteins involved in lipid trafficking form an ATP-binding cassette (ABC) transporter with multiple substrate binding proteins. J Biol Chem. 287(25):21406-15. Link to article

Wang Z, Xu C, Benning C. 2012. TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J. 70(4):614-23. Link to publication

Boyle NR, Page MD, Liu B, Blaby IK, Casero D, Kropat J, Cokus SJ, Hong-Hermesdorf A, Shaw J, Karpowicz SJ, Gallaher SD, Johnson S, Benning C, Pellegrini M, Grossman A, Merchant SS. 2012. Three Acyltransferases and Nitrogen-responsive Regulator Are Implicated in Nitrogen Starvation-induced Triacylglycerol Accumulation in Chlamydomonas. J Biol Chem. 287(19):15811-25. Link to publication

Li Z, Gao J, Benning C, Sharkey TD. 2012. Characterization of photosynthesis in Arabidopsis ER-to-plastid lipid trafficking mutants. 2012. Photosynth Res. 112(1):49-61. Link to publication

Wang Z, Benning C. 2012. Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochem Soc Trans. 40(2):457-63. Link to publication

Vieler A, Brubaker SB, Vick B, Benning C. 2012. A lipid droplet protein of nannochloropsis with functions partially analogous to plant oleosins. Plant Physiol. 158(4):1562-9. Link to publication

Chan CX, Zäuner S, Wheeler G, Grossman AR, Prochnik SE, Blouin NA, Zhuang Y, Benning C, Berg GM, Yarish C, Eriksen RL, Klein AS, Lin S, Levine I, Brawley SH, Bhattacharya D. 2012. Analysis of Porphyra membrane transporters demonstrates gene transfer among photosynthetic eukaryotes and numerous sodium-coupled transport systems. Plant Physiol. 158(4):2001-12. Link to publication

Ajjawi I, Coku A, Froehlich JE, Yang Y, Osteryoung KW, Benning C, Last RL. 2011. A J-like protein influences fatty acid composition of chloroplast lipids in Arabidopsis. PLoS One. 6(10):e25368. Link to publication

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