From the Department of Plant Biology, Carnegie Institution of Washington, Stanford, California 94305
In nature photosynthetic organisms cope with
fluctuating light conditions. Light intensity and quality vary
dramatically during the day or from one habitat to another.
Photosynthetic organisms sense intensities and wavelengths of light
both directly and indirectly. Because light fuels photosynthetic
electron transport and CO2 fixation, it is the primary
determinant of levels of NADP/NADPH, ATP, and carbon metabolites, all
of which can serve to modulate cellular processes. Light is also
absorbed by photoreceptors that link light cues to cellular metabolism.
However, light represents a single environmental cue, and other signals
interact with light through a web of regulatory circuits that result in
dynamic acclimatory responses. This review focuses on two specific
aspects of light-influenced processes in Cyanobacteria; both concern
changes in light harvesting structure and biosynthesis. The first part
of this review discusses effects of changing wavelengths of light on
the biosynthesis of the phycobilisomes
(PBS),1 dominant light
harvesting complexes of Cyanobacteria. The other discusses how
Cyanobacteria tune light harvesting and photosynthetic function to both
light intensity and nutrient availability and how the two responses are integrated.
Phycobilisome Structure
PBS are peripheral membrane complexes in Cyanobacteria that
efficiently harvest light energy and transfer the energy to
photosynthetic reaction centers. PBS, which can comprise 30% of the
cellular protein, are organized into two structural domains, the core
and rods (Fig. 1). Each of these domains
contains pigmented and nonpigmented polypeptides.
All PBS have the chromoproteins (phycobiliproteins) allophycocyanin
(AP) and phycocyanin (PC), and many also contain phycoerythrin (PE) or
phycoerythrocyanin. Phycobiliprotein colors are a consequence of
light absorption by linear tetrapyrrole chromophores that covalently associate with the apoproteins (1, 2). Phycobiliproteins are composed
of
PBS cores contain AP trimers along with pigmented and L polypeptides. A
high molecular mass core polypeptide, or LCM, has homology
to both phycobiliproteins and L polypeptides (3). The
phycobiliprotein-like domain of LCM binds a tetrapyrrole
chromophore and can serve as a PBS terminal energy acceptor. Generally,
six rods, each composed of stacks of PC and PE hexamers, radiate from the core, giving PBS a fanlike appearance (Fig. 1) (see Ref. 2 for details).
Complementary Chromatic Adaptation
It was noted over a century ago that Cyanobacteria pigmentation
changes with environmental light quality. This light control of
pigmentation, shown in the lower half of Fig. 1,
was termed complementary chromatic adaptation (CCA). Bennett and
Bogorad (4) showed that CCA was the result of altered PBS
pigment-protein composition. Development of molecular tools in the
1970s created new opportunities for elucidating PBS regulation, and by
the end of the 1980s most genes encoding PBS structural polypeptides
were characterized (5).
Genes of the PBS--
In the Cyanobacterium Fremyella
diplosiphon (similar to Calothrix PCC7601) the
PE:PC ratio reflects the spectral distribution of light in the
environment (6). In red light (RL) the organism has almost no PE, and
each PBS rod can have three PC hexamers (and specific L polypeptides).
If the Cyanobacterium is moved to green light (GL), new PBS are
synthesized with rods having single PC hexamers (core proximal hexamer)
and up to three PE hexamers. As the cells replicate in GL,
blue-pigmented PBS of RL-grown cells are gradually diluted, and the
cells begin to appear red. These light-responsive changes are
reversible, and because PC absorbs RL (
Knowledge of genes encoding phycobiliprotein and linker polypeptide has
been critical for understanding CCA (see Refs. 5 and 7)). Genes
encoding
Three distinct operons encode
The cpeBA operon encodes Expression during CCA--
Action spectra for the synthesis of PC
and PE in the Cyanobacteria have been measured (18). Maximum PE
synthesis and minimum PC synthesis occurred following exposure to 550 nm GL, and maximal PC synthesis and minimal PE synthesis occurred
following exposure to 640 nm RL. Hence, photoreceptor(s) controlling
CCA absorb RL and GL but elicit different responses in the two light
qualities. PC synthesis dominates in RL whereas PE synthesis dominates
in GL. Exposure of cells to natural sunlight, a mixture of RL and GL,
results in the synthesis of PBS with intermediate PC and PE levels.
Photocontrol of PE and PCi levels is primarily a
consequence of transcriptional regulation of cpeBA and
cpcB2A2 operons (19-21).
Mutants in CCA--
The dissection of regulatory circuits
involving CCA has exploited mutants abnormal for CCA. Several classes
of CCA mutants have been isolated (5, 22-24), including the red (FdR),
blue (FdB), green (FdG), and black (FdBk) strains. FdR mutants are red
under all conditions of illumination and constitutively synthesize PE
whereas PCi is never synthesized. These mutants are fixed
in a response normally exhibited only in GL, with aberrant regulation of both the cpeBA and cpcB2A2 operons (22). FdB
strains are bluer than wild-type cells in RL and require more GL to
suppress PCi synthesis (25). FdG mutants show normal
PCi expression, but the cpeBA genes never become
active. FdBk mutants have moderate levels of both PE and
PCi, which remain the same in RL and GL (7, 24).
Initially, an FdR mutant was complemented by rcaC, which
encodes a polypeptide of 651 amino acids with sequence similarities to
response regulators of two-component regulatory systems (26). It is
twice as large (73 kDa) as most response regulators and has two
conserved, aspartate-containing receiver domains, one at the N terminus
(Asp-51) and the other at the C terminus (Asp-576). The Asp-51 residue
is likely phosphorylated in RL-grown cells, and the phosphorylation
results in high level PCi and little PE synthesis. In GL
wild-type cells likely dephosphorylate Asp-51, which triggers elevated
PE synthesis and depressed PCi synthesis. Contiguous to the
N-terminal receiver domain of RcaC is a sequence predicted to bind DNA.
Between the putative DNA binding domain and the C-terminal receiver
domain is a motif that resembles an H block of some unorthodox sensor
proteins (27).
The FdBk class of mutants was complemented by rcaE, which
encodes a polypeptide of 74 kDa (24). The C-terminal region of RcaE has
motifs typical of bacterial sensor kinases (with a typical H block).
The N-terminal half of the polypeptide has a domain of about 140 amino
acids with similarity to the tetrapyrrole chromophore attachment domain
of phytochromes. The central region of the protein contains a
PAS domain (28), which may be involved in protein-protein interactions or binding of a redox-active prosthetic group. Recently RcaE was shown to covalently bind a linear tetrapyrrole chromophore at
a cysteine within the phytochrome-like
domain.2 The phenotype of the
FdBk mutant and similarity of RcaE to sensor kinases and eukaryotic
phytochrome photoreceptors are consistent with a photoreceptor role for
RcaE (7, 24).
Two FdR mutants were not complemented by rcaC (29). One was
complemented by the putative photoreceptor gene rcaE, and
the second by rcaF, which is immediately downstream of
rcaE on the F. diplosiphon genome and encodes
a small response regulator. RcaF may act as an intermediate in the
phosphorelay pathway controlling CCA and facilitate phosphate transfer
from its cognate sensor (presumably RcaE) to other response regulators
such as RcaC.
Because rcaE is sufficient for complementing both FdBk (24)
and FdR mutants, different lesions in rcaE can generate
different phenotypes. Furthermore, an FdR phenotype can result from
lesions in at least three distinct genes (rcaC,
rcaE, and rcaF). The lesions that caused the
mutant phenotype in these strains were the result of gene disruption by
in vivo transposition (22). Each of the FdBk
(rcaE-FdBk) and FdR (rcaE-FdR,
rcaF-FdR) mutants characterized contained insertion
sequences in the rcaE/rcaF operon (29). In
rcaE-FdBk mutants the inserts were located within 200 base pairs of the putative translation start site, and no RcaE protein was
detected in mutant cells.2 The rcaE-FdR mutants
contained insertions positioned between the H block and the four
conserved motifs critical for histidine kinase activity; this strain
appears to synthesize truncated RcaE. The rcaF-FdR mutants
contained insertions located ~200 base pairs downstream of the
rcaF translation initiation codon.
Constitutive PE and PC synthesis in rcaE-FdBk mutants
reflect an intermediate activation state of the system as a consequence of low level phosphorylation of regulatory elements that are no longer
under RcaE control. Hence, RcaF likely undergoes low level phosphorylation in the absence of RcaE; this phosphorylation is not
controlled by light quality and may result from cross-talk between RcaF
and other sensors or phosphoryl transfer from small molecule
phosphodonors. It is not unusual that a null mutation in a sensor
kinase leads to an intermediate, constitutive activation of the
phosphorelay system. In the rcaE-FdR mutants, although the
truncated RcaE cannot undergo autophosphorylation, it may bind RcaF and
block its phosphorylation by other molecules and/or retain phosphatase
activity, which would maintain RcaF in a dephosphorylated state.
Model for CCA--
Three regulatory elements critical for CCA are
RcaE, RcaF, and RcaC. Although these polypeptides have features of
bacterial two-component regulators, the CCA phosphorelay (Fig.
2) is unique because it includes five
potential phosphoacceptor domains among these polypeptides. RcaE, the
putative photoreceptor, perceives the light signal. RL causes RcaE to
undergo an autophosphorylation followed by transfer of the phosphoryl
groups to the response regulator RcaF. In the absence of RcaE, RcaF may
interact with other phosphoryl donors. RcaF then may transfer
phosphoryl groups to the conserved histidine of the H block within
RcaC, which can pass it to either the N- or C-terminal receiver domain.
The N-terminal receiver domain of RcaC is critical for CCA, whereas the
role of the C-terminal receiver domain is unclear. In GL RcaE acts as a
phosphatase or blocks phosphotransfer by binding to RcaF; this
inhibition causes activation of cpeBA and suppression of cpcB2A2.
Not surprisingly, other regulatory components also appear to be
involved in controlling CCA. A class of mutants that only affects
cpeBA expression has been identified and is designated turquoise (FdTq). These mutants exhibit normal regulation of
cpcB2A2 but cannot activate cpeBA in GL.
Complementation of the FdTq strains uncovered two genes,
trqA and trqB, encoding polypeptides related to
protein phosphatases3; this
finding is interesting, especially because phosphorylation of the
putative regulatory protein RcaA has been implicated in the control of
cpeBA expression (21).
Specific Nutrient Limitation Responses--
Responses of organisms
to nutrient availability may be classified as those specific to the
limiting nutrient and those that are more general, occurring during any
of a number of different nutrient limitation conditions. Specific
responses include metabolic changes enabling organisms to efficiently
scavenge the limiting nutrient; these responses may include synthesis
of high affinity transport systems (30) and production of hydrolytic
enzymes that facilitate utilization of alternate forms of the limiting nutrient (31).
General Responses--
General responses to nutrient-limited
growth include changes in cell morphology and metabolism.
Synechococcus cells starved for iron, nitrogen, or sulfur
accumulate low levels of thylakoid membrane, PBS, and ribosomes (32,
33). Nutrient deprivation also causes a rapid loss of O2
evolving activity, reflecting a decline in PSII function (34). A
visually dramatic, general response of Cyanobacteria to
nutrient-limited growth is the decrease in cellular pigmentation or
bleaching (35), which includes an almost complete loss of PBS (36).
Degradation of the PBS could provide amino acids or carbon skeletons
for production of other cellular constituents required during nutrient
deprivation and reduce absorption of excitation energy, making cells
less susceptible to photodamage.
Mutants of Synechococcus were isolated that could not
degrade their PBS during nutrient deprivation. Some of these mutants, designated nbl (nonbleaching), only
survived in relatively low light. Complementation of one nbl
mutant led to the isolation of nblA
(nonbleaching), which encodes a 59-amino acid
polypeptide. The nblA transcript only accumulates to high
levels in cells starved for nitrogen or sulfur; low levels of the
nblA mRNA are observed in cells maintained in
phosphorus-free or complete medium. Under all conditions tested,
nblA expression correlated with decreased PBS levels, even
under conditions that do not normally provoke PBS degradation (37).
nblA may be the primary (only) gene whose activity must be
elevated to provoke bleaching during sulfur- or nitrogen-limited
growth. Although NblA is probably not a protease itself, it may
function to activate or alter the specificity of a protease or somehow
tag PBS for degradation.
A second nbl mutant was complemented by nblB.
NblB has homology to subunits (e.g. CpcE, CpeZ) of lyases
that catalyze covalent attachment of phycochromobilin chromophores to
apophycobiliprotein subunits (38). This finding suggests that NblB
interacts directly with tetrapyrrole chromophores attached to
phycobiliproteins. Because nblB mutants do not degrade PBS
during nutrient limitation, it is reasonable to propose that NblB
catalyzes removal of chromophores from holophycobiliprotein subunits
and that only after the chromophore is removed can phycobiliprotein
subunits be degraded.
A third mutant, nblR, was complemented by a gene encoding a
response regulator (39). Cyanobacteria strains null for NblR (a) have ~150% the level of PBS as wild-type cells during
nutrient-replete growth, (b) fail to degrade PBS during
sulfur or nitrogen limitation, and (c) cannot properly
modulate PBS levels during exposure to high light (HL). The
(a), (b), and (c) phenotypes probably
reflect the fact that the nblR mutant (d) cannot
activate nblA during nutrient limitation. The mutant also
dies rapidly when starved for either sulfur or nitrogen or when exposed
to HL (39). Hence, in addition to controlling PBS degradation, NblR
modulates functions critical for cell survival during nutrient-limited
and HL conditions. The presence of the photosynthetic electron
transport inhibitor DCMU slows the death of the nblR
mutant during sulfur and nitrogen starvation, suggesting that death of
the mutant is a consequence of its inability to properly down-regulate
photosynthesis upon exposure to stress conditions. Hence, NblR appears
to have a pivotal role in regulating some general stress responses and
is critical for integrating various environmental signals with cellular metabolism.
The most recently characterized nbl mutant is
nblS. Like nblR, the nblS mutant is
sensitive to HL and nutrient limitation and cannot properly activate
nblA. Furthermore, the nblS strain cannot
activate hliA (gene encoding a polypeptide with similarity to chlorophyll a- and b-binding proteins of
plants that helps Cyanobacteria acclimate to HL (40)),
psbAII, and psbAIII during exposure of
Synechococcus to HL or blue/UV-A
light.4 NblS is also
important for the down-regulation of the psbAI and cpcBA genes in HL.
The nblS gene encodes a sensor histidine kinase of
two-component regulatory systems, with two predicted N-terminal
membrane-spanning domains followed by a region bearing a PAS domain.
PAS domains often bind flavin or heme prosthetic groups and may respond
to light or redox conditions (28). Preliminary work suggests that NblS
binds a flavin.5 Because NblS
controls nutrient stress responses and accumulation of nblA
mRNA (like NblR), we assume that NblS and NblR constitute a
sensor-response regulator pair, although this has not been proven. Interestingly, induction of hliA, psbAII, and
psbAIII in HL does not appear to be under the control of
nblR, suggesting that NblS modulates regulatory pathways
that are distinct from those controlled by NblR. Overall, the results
suggest that NblS serves to link the light environment and cellular
redox to global modulation of metabolic processes.
Model--
The integration of light and nutrient limitation
responses are presented in Fig. 3. NblS
is critical for integrating these responses, which include modulation
of PBS levels and controlling the activities of nblA,
hliA, psbAI, psbAII,
psbAIII, and cpcBA. It is not yet clear if NblS
is critical for regulating transcription of other genes that rapidly
respond to changes in light conditions. During nutrient limitation, as
cells generate reduced photosynthetic electron carriers, NblS initiates
a phosphorylation cascade in which NblR is activated. NblR turns on the
nblA gene, and NblA in conjunction with NblB (constitutively
expressed) actively degrades PBS. NblR must also activate other
processes in the cell (e.g. modification of the
photosynthetic apparatus) that favor survival during nutrient stress
and HL conditions. During HL exposure, NblS modulates the activity of
many genes encoding components of the photosynthetic apparatus.
Regulation of a number of these genes does not require NblR. Hence, in
addition to interacting with NblR, NblS must associate with other
response regulators that have not yet been identified.
A major question remaining is how may NblS be sensing the redox state
of the cell. During nutrient limitation, when the anabolism of the cell
is slowed down or completely arrested, NADP+, the final
electron acceptor of the photosynthetic electron transport chain, is
not recycled as fast as under nutrient-replete conditions and the
electron carriers are maintained in a relatively reduced state.
Similarly, under HL conditions the electron carriers may be reduced
faster than they are re-oxidized. Thus, nutrient limitation and HL
result in absorption of excess light energy by photosynthetic pigments,
and the overall cellular environment would become highly reduced. The
redox state of photosynthetic electron carriers is known to modulate
cellular transcription (41), translation (42), state transitions, and
changes in the stoichiometry of the photosystems (43). The results
discussed above suggest that NblS/NblR control is linked to the redox
state of the cells and possibly couples to the degree of reduction of
specific photosynthetic electron carriers. Furthermore, both DCMU,
which prevents photosynthetic electron flow beyond QA, and
DBMIB, which inhibits electron flow through the cytochrome
b6f complex, inhibit PBS degradation and the
accumulation of nblA mRNA during sulfur and nitrogen
stress. Like PBS degradation and nblA expression, expression
of hliA is altered by both DCMU and DBMIB. Interestingly,
upon treatment of Synechocystis PCC6803 with cyanide (which
inhibits both respiration and photosynthetic electron flow at
plastocyanin) hliA is activated in low light. Similarly, in
a PSI mutant of Synechocystis PCC6803, there is elevated
expression of hli genes even in moderate
light.6 These results suggest
that hyper-reduction of an electron transport carrier prior to PSI may
strongly affect acclimation during HL and nutrient limitation
conditions. Factors in addition to the redox state of the
photosynthetic apparatus may be important for tuning the activity of
NblS. For example, NblS control seems to promote PBS degradation during
nutrient limitation, but in HL it biases control toward activation of
hliA/psbAII/psbAIII/cpcBA. Interactions with a blue light
photoreceptor or the direct absorption of blue/UV-A light by NblS may
also bias NblS action toward the hliA/psbAII/psbAIII regulatory pathway over the
nblA pathway. Reactive oxygen species may also serve as
regulatory signals that modulate the activity of the nbl
system. Several aspects of the model are speculative and/or incomplete.
However, it represents an attractive unifying view that predicts global
metabolic effects in response to redox status of photosynthetic
electron carriers and links nutrient conditions, growth potential,
and light to overall regulation of cellular metabolism.
INTRODUCTION
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INTRODUCTION
Light Harvesting and...
Integration of Light and...
REFERENCES
Light Harvesting and Fluctuating Light Signals
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INTRODUCTION
Light Harvesting and...
Integration of Light and...
REFERENCES
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Fig. 1.
Cyanobacteria PBS. Top,
structure of PBS in RL and GL. Each disc in the rod substructure
represents a phycobiliprotein hexamer; red-pigmented discs represent PE
hexamers and blue-pigmented disks represent PC hexamers.
Bottom, cyanobacterial cells on solid medium in RL
(left) and GL (right).
and
subunits associated into heterodimers (termed
"monomers" in the literature) that aggregate into trimers (
)3 and hexamers (
)6.
Nonchromophorylated linker (L) polypeptides stabilize PBS, facilitate
assembly of phycobiliprotein aggregates, and modulate the absorption
characteristics of phycobiliproteins, promoting unidirectional energy
flow to photosynthetic reaction centers (1).
max = 620 nm) and
PE absorbs GL (
max = 560 nm), these changes facilitate
efficient absorption of prevalent wavelengths of light in the environment.
and
subunits of each phycobiliprotein are contiguous
on the cyanobacterial genome and are cotranscribed. Often,
polycistronic transcripts encode phycobiliprotein subunits and their
associated L polypeptides. In F. diplosiphon,
and
AP
subunits (
AP and
AP, respectively),
encoded by the apcA1B1 genes, are in an operon that also
contains the apcC1 and apcE1 genes; the latter
genes encode the core linker polypeptide and the LCM,
respectively (8).
PC and
PC
subunits (cpcBA genes) in F. diplosiphon (9-12).
The cpcB1A1 genes are constitutively transcribed and encode
PCc subunits (subscript indicates
constitutive). This operon also contains cpcE
and cpcF, which encode a lyase that attaches the
tetrapyrrole chromophores to the
subunit of PC (13). The
cpcB2A2 operon is specifically active in RL (inactive in GL)
and encodes PCi (subscript indicates
inducible), which is critical for CCA. Hexamers of
PCi comprise the majority of PBS rods when cyanobacterial
cells are grown in RL. The genes cpcH2, cpcI2,
and cpcD2 (14), encoding L polypeptides associated with
PCi, are cotranscribed with cpcB2A2.
Furthermore, the cpcB2A2H2I2D2 operon is clustered on the
F. diplosiphon genome with cpcB1A1 and
apcE1A1B1C1 (10). A third PC operon, cpcB3A3 plus
genes encoding associated L polypeptides, is only active during
sulfur-limited growth (12).
and
subunits of PE (15). In
contrast to the situation for cpc and apc
operons, genes encoding L polypeptides associated with PE are not
contiguous on the genome to cpeBA; they are encoded by the
cpeCDE operon (16). However, GL activation and RL
suppression of cpeBA and cpeCDE are coordinated. Also, cpeBA genes are linked to cpeY and
cpeZ, which encode the lyase that attaches tetrapyrrole
chromophores to PE subunits (17).
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Fig. 2.
Phosphorelay regulation of CCA. The
left side depicts RL-stimulated phosphorylation
of components of the signal transduction pathway, activation of
cpcB2A2, and suppression of cpeBA. The
right side depicts dephosphorylation of signal
transduction components in GL and the suppression of cpcB2A2
and activation of cpeBA. Pigmentation of cells under the
different light conditions is shown.
Integration of Light and Nutrient Signals in PBS Biosynthesis
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INTRODUCTION
Light Harvesting and...
Integration of Light and...
REFERENCES
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Fig. 3.
Model depicting the role of NblS in
controlling both HL and nutrient stress responses. The genes shown
in the figure are discussed in the text. HL, -N,
-S, -P, and -Ci represent conditions
in which the cells are exposed to HL or are deprived of nitrogen,
sulfur, phosphorus, or inorganic carbon, respectively. The model
suggests that these conditions cause a change in cellular redox and/or
in the level of reactive oxygen species, which is sensed by NblS. NblS
may also control some process through direct absorption of blue/UV-A
light.
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FOOTNOTES |
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* This minireview will be reprinted in the 2001 Minireview Compendium, which will be available in December, 2001. This is the first article of three in the "Light Minireview Series." Work in this laboratory is supported by NSF Grants 0084189 and 9727836 (to A. R. G.) and USDA Grants 97-35301-4575 and 98-35301-6445. We also acknowledge NSF for fostering genome-wide studies of Chlamydomonas (MCB 9976765). This is Carnegie Institution Publication 1457.
To whom correspondence should be addressed: Dept. of Plant
Biology, Carnegie Institution of Washington, 260 Panama St., Stanford, CA 94305. Tel.: 650-325-1521 (ext. 212); Fax: 650-325-6857; E-mail: arthur@andrew2.stanford.edu.
Published, JBC Papers in Press, February 16, 2001, DOI 10.1074/jbc.R100003200
2 D. M. Kehoe and A. R. Grossman, unpublished data.
3 D. M. Kehoe, personal communication.
4 L. van Waasbergen, N. Dolganov, and A. R. Grossman, submitted for publication.
5 J. Christie, L. van Waasbergen, W. Briggs, and A. R. Grossman, unpublished data.
6 W. Vermaas, personal communication.
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ABBREVIATIONS |
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The abbreviations used are: PBS, phycobilisome(s); AP, allophycocyanin; PC, phycocyanin; PE, phycoerythrin; L polypeptide, linker polypeptide; CCA, complementary chromatic adaptation; RL, red light; GL, green light; HL, high light; PAS, PER/ARNT/SIM; DCMU, 3-(3,4-dichlorophenyl)-1, 1-dimethylurea; DBMIB, 2,5-Dibromo-3-methyl-6-isopropyl-p-benzoquinone.
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