April 2010

What Can Plant Models Teach Us About Lipid Trafficking?

 

Lipid-NewsPlants are important to most life forms on Earth, because they produce the oxygen in the atmosphere, fix carbon dioxide and provide reduced carbon to sustain heterotrophic organisms, including humans. Plants are even the source of fossil and renewable fuels that power our cars, all courtesy of photosynthesis. To accomplish this feat, plant cells harbor chloroplasts, which have one of the most extensive membrane systems found in nature, the photosynthetic membrane. What may surprise people is that these membranes contain mostly nonphosphorous galactoglycerolipids, because sessile plants need to conserve phosphorus (1). Given that plant, algal and photosynthetic bacterial biomass is greater than that of heterotrophic organisms, these galactoglycerolipids are more prevalent in the global biosphere than phospholipids.

To make the lipids of the photosynthetic membrane, there is a division of labor between the endoplasmic reticulum and the chloroplast, requiring the exchange of lipid precursors across multiple membranes (2). Arabidopsis, which had its genome published 10 years ago (3), has promised to be a model for the discovery of components of the underlying transport machinery. Already, mutants of Arabidopsis have led to the identification of an ATP-binding cassette transporter hypothesized to carry phosphatidic acid (2), because one of the subunits specifically binds this phospholipid (4). This protein contains a mammalian cell-entry domain present in mycobacterial cell surface proteins. Most Gram-negative bacteria also have orthologs of the transporter, which, in Escherichia coli, was recently proposed to be involved in maintaining the asymmetry of the outer cell membrane (5).

Is this an isolated example for discoveries in Arabidopsis that can advance our general understanding of fundamental cell biological processes? Hardly so, as recently pointed out by Alan Jones and his colleagues (6). A noticeable example is the ago1 mutant of Arabidopsis, isolated by my former graduate student Karen Bohmert. She discovered the founding member of the ARGONAUTE family (7) now known to be involved in gene-silencing pathways guided by small RNAs. The protein was named by our collaborators, Michel Caboche and his co-workers, after a cephalopod inspired by the Arabidopsis ago1 mutant phenotype. For those interested in learning more about the promise of Arabidopsis as a model, a special issue of The Plant Journal entitled “Arabidopsis: A Rich Harvest 10 Years after Completion of the Genome Sequence” was published March 2010 (Vol. 61, issue 6). Articles in the issue are freely available for downloading at www.theplantjournal.com and are accompanied by a podcast on the Web site with testimonials from scientists that illustrate why Arabidopsis has emerged as a model equal to E. coli, yeast, Drosophila or Caenorhabditis.

Mechanisms of nonvesicular transfer of lipids between membranes of different organelles are poorly understood in any organism, yet they are essential to the development, maintenance and health of all eukaryotic cells. Any eukaryotic model that promises new insights is welcome, including the little weed that has already proven it could.

References

1. Benning, C., and Ohta, H. (2005) Three Enzyme Systems for Galactoglycerolipid Biosynthesis Are Coordinately Regulated in Plants. J. Biol. Chem. 2397–2400.
2. Benning, C. (2009) Mechanisms of Lipid Transport Involved in Organelle Biogenesis in Plant Cells. Annu. Rev. Cell. Dev. Biol. 25, 71–91.
3. The Arabidopsis Genome Initiative (2000) Analysis of the Genome Sequence of the Flowering Plant Arabidopsis thaliana. Nature 408, 796–815.
4. Lu, B., and Benning, C. (2009) A 25-Amino Acid Sequence of the Arabidopsis TGD2 Protein Is Sufficient for Specific Binding of Phosphatidic Acid. J. Biol. Chem. 284, 17420–17427.
5. Malinverni, J. C., and Silhavy, T. J. (2009) An ABC Transport System that Maintains Lipid Asymmetry in the Gram-negative Outer Membrane. Proc. Natl. Acad. Sci. U.S.A. 106, 8009-8014.
6. Jones, A. M. et al. (2008) The Impact of Arabidopsis on Human Health: Diversifying our Portfolio. Cell 133, 939-943.
7. Bohmert K et al. (1998) AGO1 Defines a Novel Locus of Arabidopsis Controlling Leaf Development. EMBO J 17, 170-180.

Christoph Benning (benning@msu.edu) is a professor of biochemistry and molecular biology at Michigan State University. He is also the editor-in-chief of The Plant Journal.


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