Phosphoinositides play important roles in both environmental response and metabolism in plants. This article looks at some of these molecules and the parts they play. (Titled "Phosphoinositide Signaling: Getting to the Root of the Matter" in print version.)
|Tomatoes (Micro-toms) transformed with genes from Pyrococcus furiosus, an Archaeal hyperthermophile. Photo credit Yang Ju Im.
Plants are totipotent, sessile organisms that must adapt to a changing environment in order to survive. Although plant phosphoinositide (PI) metabolism changes rapidly in response to environmental cues, PIs also appear to regulate fundamental metabolism.
The biosynthesis of phosphatidylinositol (4,5)bisphosphate (PtdInsP2) is regulated tightly, suggesting that it may function as a signaling molecule. The ratio of PtdInsP2 to PtdInsP is approximately 1:10, and there are no reports of PtdInsP3.
Biochemical and genetic comparisons in plants and mammals support the hypothesis that plants use only select aspects of PI signaling. In contrast to mammals, which have five distinct families of PtdInsP2-phospholipase Cs, plants only have one family, which is most similar to the mammalian zeta family of “sperm-specific” calcium regulated PLCs (1, 2). This is very different from phospholipase D signaling, in which plants have six different families of PLDs with distinct functions (3).
Although the additional types of PLCs are not essential for plant growth and development, PLC-mediated signaling and the polyphosphorylated inositol lipids affect fundamental processes such as differential cell growth, vascularization, cell polarity, asymmetric division during stem cell development, tip growth and basal metabolism.
Tip growing cells such as root hairs and pollen tubes have provided a platform for dissecting the selective functions of the type III PtdIns 4-kinase and PtdInsP 5-kinase isoforms in polar growth (4). Developmental studies of plant stem cells also recently revealed that PtdIns4P can activate POLTERGEIST, which is essential for the maintenance of asymmetric division during stem cell development (5). Proteins that regulate carbon portioning and the energy balance of the cell directly interact with PtdInsP kinases and inositol polyphosphate 5Ptases (6, 7).
It is not surprising then, that genetically altering InsP3 signaling has provided a new approach for engineering drought tolerant plants. Dampening the InsP3 signal by increasing the hydrolysis of InsP3 decreases the rate of gravitropic response, enhancing drought tolerance (8).
These are just a few examples of the insights gained from studying plant PI metabolism. Comparative analyses of the functions of PIs and PI binding proteins in diverse systems should continue to reveal insights into the regulation of fundamental metabolism. Although plant PI signaling may seem somewhat limited in scope because of the inherent differences in the regulation of their PI pathway, plants provide an excellent eukaryotic platform to build and test novel synthetic signaling systems.
1. Mueller-Roeber, B., and Pical, C. (2002) Inositol Phospholipid Metabolism in Arabidopsis. Characterized and Putative Isoforms of Inositol Phospholipid Kinase and Phosphoinositide-Specific Phospholipase C1. Plant Physiol. 130, 22 – 46.
2. Nomikos, M., et al. (2005) Role of Phospholipase C-ζ Domains in Ca2+-dependent Phosphatidylinositol 4,5-Bisphosphate Hydrolysis and Cytoplasmic Ca2+ Oscillations. J. Biol. Chem. 280, 31011 – 31018.
3. Wang, X., Devaiah, S. P., Zhang, W., and Welti, R. (2006) Signaling Functions of Phosphatidic Acid. Prog. Lipid Res. 45, 250 – 278.
4. Thole, J. M., and Nielsen, E. (2008) Phosphoinositides in Plants: Novel Functions in Membrane Trafficking. Curr. Opin. Plant Biol. 11, 620 – 631.
5. Gagne, J. M., and Clark, S. E. (2010) The Arabidopsis Stem Cell Factor POLTERGEIST Is Membrane Localized and Phospholipid Stimulated. Plant Cell 22, 729 – 743.
6. Lou, Y., Gou, J.-Y., and Xue, H.-W. (2007) PIP5K9, an Arabidopsis Phosphatidylinositol Monophosphate Kinase, Interacts with a Cytosolic Invertase to Negatively Regulate Sugar-Mediated Root Growth. Plant Cell 19, 163 – 181.
7. Ananieva, E. A., Gillaspy, G. E., Ely, A., Burnette, R. N., and Erickson, F. L. (2008)Interaction of the WD40 Domain of a Myoinositol Polyphosphate 5-Phosphatase with SnRK1 Links Inositol, Sugar, and Stress Signaling. Plant Physiol. 148, 1868 – 1882.
8. Perera, I. Y., Hung, C. Y., Brady, S., Muday, G. K., and Boss, W. F. (2006) A Universal Role for Inositol 1,4,5-Trisphosphate-Mediated Signaling in Plant Gravitropism. Plant Physiol. 140, 746 – 750.
Wendy F. Boss (firstname.lastname@example.org) is the William Neal Reynolds distinguished professor in the department of plant biology at North Carolina State University.