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Title: Synergism between inositol polyphosphates and TOR kinase signaling in nutrient sensing, growth control, and lipid metabolism in Chlamydomonas

item COUSO, INMACULADA - Danforth Plant Science Center
item EVANS, BRADLEY - Danforth Plant Science Center
item LI, JIA - Danforth Plant Science Center
item LIU, YU - Danforth Plant Science Center
item MA, FANGFANG - Danforth Plant Science Center
item DIAMOND, SPENCER - University Of California
item Allen, Douglas - Doug
item UMEN, JAMES - Danforth Plant Science Center

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/18/2016
Publication Date: 9/2/2016
Citation: Couso, I., Evans, B., Li, J., Liu, Y., Ma, F., Diamond, S., Allen, D.K., Umen, J.G. 2016. Synergism between inositol polyphosphates and TOR kinase signaling in nutrient sensing, growth control, and lipid metabolism in Chlamydomonas. The Plant Cell. 28(5):2026-2042. doi: 10.1105/tpc.16.00351.

Interpretive Summary: Carbon metabolism in photosynthetic systems is poorly understood; however to meet a growing population will require increased productivity from plant systems that are the primary source of food, feed and many renewable chemical feed stocks. Growth regulators that govern carbon partitioning and the balance between growth and allocation to storage reserves such as lipids like triacylglycerol (TAG) or starch are important to describe as they control the biomass compositions produced by plants and for example, the yield of vegetable oil that can be obtained. Through genetic screening we identified one mutant that had adverse effects on carbon partitioning including the production of enhanced levels of TAG. This mutant was further characterized through a series of growth studies where the amount of lipid produced was monitored under different circumstances and the production of primary metabolites as well as inositol polyphosphates were quantified with liquid chromatography linked to a tandem mass spectrometer. The analyses indicated that inositol polyphosphates that were altered in the mutant are important to the tradeoff between allocation of resources for growth versus the production of storage metabolites such as lipids. The findings are important because changes in growth and altered composition that include enhanced levels of lipids can lead to higher production of vegetable oils; demand for which is expected to double within the next 20-25 years.

Technical Abstract: The networks that govern carbon metabolism and control intracellular carbon partitioning in photosynthetic cells are poorly understood. Target of rapamycin (TOR) kinase is a conserved growth regulator that integrates nutrient signals and modulates cell growth in eukaryotes, though the TOR signaling pathway in plants and algae has yet to be completely elucidated. We screened the unicellular green alga Chlamydomonas using insertional mutagenesis to find mutants that conferred hypersensitivity to the TOR inhibitor rapamycin. We characterized one mutant, vip1-1, that is predicted to encode a conserved inositol hexakisphosphate kinase from the VIP family that pyrophosphorylates phytic acid (IP6) to produce the low abundance signaling molecules IP7 and IP8. Unexpectedly, the rapamycin hypersensitive growth arrest of vip1-1 cells was dependent on the presence of external acetate which normally has a growth-stimulatory effect on Chlamydomonas. vip1-1 mutants also constitutively overaccumulated triacylglycerols (TAGs) in a manner that was additive with other TAG inducing stimuli such as starvation. vip1-1 cells had reduced IP7 and IP8, both of which are dynamically modulated in wild-type cells by TOR kinase activity and the presence of acetate. Our data uncover a new interaction between the TOR kinase and inositol polyphosphate signaling systems that we propose govern carbon metabolism and intracellular pathways that lead to storage lipid accumulation.