Download Carbon metabolism in Chlamydomonas: inositol

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Plant Cell Advance Publication. Published on September 7, 2016, doi:10.1105/tpc.16.00702
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Carbon metabolism in Chlamydomonas: inositol polyphosphates and TORInsP
signaling
center IP6
stage
IP3 3 InsP
IP4take
IP5
4 InsP5 InsP
6
TOR (TARGET OF RAPAMYCIN) kinase
is a conserved regulator of cell growth that
directs protein synthesis, metabolic outputs,
and other growth-related processes in
response to developmental and external
nutrient cues (reviewed in Rexin et al., 2015).
In Arabidopsis, glucose activates TOR and
stimulates cell division in root meristems
(Xiong et al., 2013); however, little is known
about the downstream targets of TOR and
how TOR signaling integrates with other
metabolic pathways to control carbon
allocation and growth in photosynthetic
organisms.
In a Breakthrough Report, Couso et al.
(2016) reveal a link between TOR signaling
and inositol polyphosphates in the model
unicellular green alga Chlamydomonas
reinhardtii,
which
toggles
between
phototrophic (obtaining energy from light
sources), heterotrophic (obtaining energy
from carbon sources), and mixotrophic
(obtaining energy from light and carbon
sources) modes of growth.
To decipher the TOR signaling network
in Chlamydomonas, the authors screened for
mutants that were hypersensitive to the
antibiotic rapamycin (RAP), an established
inhibitor of TOR in this organism and others.
They identified the vip1-1 mutant, which
harbors a mutation in a gene predicted to
encode a diphosphoinositol phosphate kinase
that pyrophosphorylates phytic acid to
produce the inositol phosphate (InsP)7 and
InsP8 signaling molecules. To test if the vip11 mutant has defects in InsP7 and InsP8
accumulation, the authors developed a
sensitive liquid chromatography and mass
spectrometry (LC-MS/MS)-based method for
detecting these molecules, which are present
in eukaryotic cells at such low concentrations
that they are difficult to detect. The vip1-1
mutant indeed had reduced levels of InsP7
and InsP8, accumulating just 20-30% of wildtype levels. Therefore, VIP1 appears to
function in InsP7 and InsP8 biosynthesis,
linking TOR signaling to InsPs.
To investigate the relationship between
TOR and InsPs, the authors next examined
the effect of inhibiting TOR signaling. Growth
of both wild-type and vip1-1 cells was blocked
soon after RAP treatment, and wild-type, but
not vip1-1, cells acclimated to RAP by 12 h
0.03
0.02
10
IN BRIEF
7
IP7
InsP
7
IP8
InsP
8
IP8
InsP8
after treatment. Interestingly, InsP7 and InsP8
nutrients
B
levels dipped in both wild-type and vip1-1 cells
acetate
after treatment with RAP and gradually
increased in the wild-type cells as they
VIP1
?
acclimated to the treatment. These findings
show that inhibiting TOR signaling alters
InsP7 and InsP8 levels and suggest that the
InsPs
TOR
InsPs function downstream of TOR signaling.
In a surprising twist, the authors found
?
that RAP completely blocked growth under
mixotrophic conditions (in the presence of light
and acetate), but that phototrophic conditions
relieved RAP hypersensitivity. This prompted
the authors to examine whether the two main
cell growth
TAGs
carbon pools present in Chlamydomonas,
TCA
cycle
starch and neutral lipids, are affected by the
vip1-1 mutation. No Figure
differences
in InsP
starch
8. TOR and
interact to control cell growth, acetate metabolism and neutral lipid accumu
of intracellular InsP levels
by carbon
source.
Graphs
labeled as
in Fig. 3 showing
Model
linking
carbon
source
(acetate)
with InsP levels fr
content were observedModulation
between
vip1-1
and
(WT) and vip1-1 growing in the presence or absence of acetate (TAP and TP, respectively). B. Summary fi
TOR
kinase
and
inositol
phosphates.
InsPs
wild-type cells. However,
in contrast
to wildproposed
relationships
between carbon source (acetate), TOR, and InsPs produced by VIP1. Black arrows
interactions shown in this work (TOR
signalingby
andVIP1
carbon
source
levels)
while dashed gray
act
withinfluence
TOR toInsP
block
TAG
type cells, which typically
only
exhibit
lipid produced
question marks are possibilities that were not directly tested. TOR and the InsPs produced by VIP1 synerg
accumulation
and
stimulate
cell
growth.
Black
TAG accumulation
(repression bar) and promote cell growth (arrow).
bodies under nitrogen-starvation
conditions,
vip1-1 cells contained lipids in both the lines show interactions deduced from this
presence and absence of nitrogen, and the study and gray dashed lines show interactions
that remain to be confirmed. [Adapted from
mutant contained higher levels of total lipids
Couso et al. (2016), Figure 8B.]
than the wild type. Further analysis showed
that vip1-1 constitutively accumulated
triacylglycerols. In addition, the mutant had REFERENCES
reduced levels of some Krebs cycle
metabolites (citrate, aconitate, and malate) Couso, I., Evans, B.S., Li, J., Liu, Y., Ma, F.,
under mixotrophic conditions, and elevated
Diamond, S., Allen, D.K., and Umen, J.G.
levels of others (succinate, fumarate, and
(2016). Synergism between Inositol
aconitate) under phototrophic conditions,
Polyphosphates and TOR Kinase Signaling
further linking VIP1 with metabolic flux.
in Nutrient Sensing, Growth Control and
Finally, the authors showed that InsP7 and
Lipid Metabolism in Chlamydomonas. Plant
InsP8 profiles change dramatically in
cell 10.1105/tpc.15.00351.
response to acetate, supporting the notion Rexin, D., Meyer, C., Robaglia, C., and Veit,
that InsP7 and InsP8 are signals that respond
B. (2015). TOR signalling in plants.
to and/or control carbon metabolism.
Biochem. J. 470: 1–14.
This work (summarized in figure) is likely Xiong, Y., McCormack, M., Li, L., Hall, Q.,
to open new research frontiers in carbon
Xiang, C., and Sheen, J. (2013). Glucosemetabolism and partitioning in photosynthetic
TOR
signalling
reprograms
the
cells, and could have exciting applications in
transcriptome and activates meristems.
the field of biofuel production.
Nature 496: 181–6.
Kathleen L. Farquharson
Science Editor
[email protected]
http://orcid.org/0000-0002-8032-0041
©2016 American Society of Plant Biologists. All Rights Reserved
Carbon metabolism in Chlamydomonas: inositol polyphosphates and TOR signaling take center
stage
Kathleen L Farquharson
Plant Cell; originally published online September 7, 2016;
DOI 10.1105/tpc.16.00702
This information is current as of June 17, 2017
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