International Journal of
Molecular Sciences
Letter
The Chlorophyll a Fluorescence Modulated by
All-Trans-β-Carotene in the Process of Photosystem II
Tianyu Li 1 , Ye Zhang 2 , Nan Gong 1 , Zuowei Li 1 , Chenglin Sun 1 and Zhiwei Men 1, *
1
2
*
Coherent Light and Atomic and Molecular Spectroscopy Laboratory, College of Physics, Jilin University,
Changchun 130012, China; [email protected] (T.L.); [email protected] (N.G.);
[email protected] (Z.L.); [email protected] (C.S.)
College of Plant Science, Jilin University, Changchun 130062, China; [email protected]
Correspondence: [email protected]; Tel.: +86-431-8516-6787
Academic Editor: Dr.-Habil. Mihai V. Putz
Received: 11 May 2016; Accepted: 16 June 2016; Published: 21 June 2016
Abstract: Modulating the chlorophyll a (Chl-a) fluorescence by all-trans-β-Carotene (β-Car) in the
polarity and non-polarity solutions was investigated. The fluorescence intensity of Chl-a decreased as
the concentration of β-Car increased. The excited electronic levels of Chl-a and β-Car became much
closer owing to the solvent effect, which led to the electron transfer between both two molecules.
A electron-separated pair Chl´ ¨ Chl+ that is not luminous was formed due to electron transfer.
The solution of Chl-a and β-car in C3 H6 O was similar to the internal environment of chloroplast. We
conclude that the polar solvent is good for the fluorescent modulation in photosystem II.
Keywords: chlorophyll a; fluorescence; all-trans-β-carotene; electron transfer
1. Introduction
Photosynthesis is the biological basis of all material and energy metabolism, and it is very
important for the growth and development of plants. Fluorescence plays a much more important
role in avoiding the chloroplasts absorption of light compared with photosynthesis digestion to
reduce to a minimum loss of strong light. The chlorophyll a (Chl-a) fluorescence and photosynthetic
rate were negatively correlated with each other under natural conditions [1,2]. Chlorophyll and
carotenoids are both light-harvesting pigments, but chlorophyll plays an important role in the process
of photosynthesis. Carotenoid is an alkene molecule that contains π-electron conjugated double bonds,
and it has the function of light collection and protection, which is closely related to the chlorophyll
molecules in the chloroplast structure [3]. The chemical structure of chlorophyll is such that it may gain
or lose electrons easily, can absorb photons, and can transfer the excitation energy to the photosynthetic
reaction center [4]. All-trans-β-Carotene (β-Car) plays a role in regulating the energy flow of Chl-a
excited states in the photosynthetic antenna, being used in an energy dissipation route [5,6].
In this paper, we investigate the fluorescence characteristics of Chl-a and the function of β-Car
on the quenching process of Chl-a fluorescence. The UV-visible absorption and fluorescence spectra
for different concentrations of β-Car and Chl-a in organic solvents were measured. At a certain
concentration range, the fluorescence quenching effect of Chl-a becomes better with the increase of the
concentration of β-Car. The interactional mechanism between the π-electrons of β-Car and the Chl-a
singlet state are discussed in terms of the process of quenching of Chl-a singlet electronic excited state.
2. Results and Discussion
Chl-a has two strong absorption bands: one is located within 640–660 nm in the red area, the
other is located within 410–430 nm in the blue-violet light area. The absorption peaks of β-Car appear
Int. J. Mol. Sci. 2016, 17, 978; doi:10.3390/ijms17060978
www.mdpi.com/journal/ijms
Int.J.J.Mol.
Mol.Sci.
Sci.2016,
2016,17,
17,978
978
Int.
of66
22of
2. Results
Results and
and Discussion
Discussion
2.
Int. J. Mol. Sci. 2016, 17, 978
2 of 6
Chl-a has
has two
two strong
strong absorption
absorption bands:
bands: one
one is
is located
located within
within 640–660
640–660 nm
nm in
in the
the red
red area,
area, the
the
Chl-a
otheris
islocated
locatedwithin
within410–430
410–430nm
nmin
inthe
theblue-violet
blue-violetlight
lightarea.
area.The
Theabsorption
absorptionpeaks
peaksof
ofβ-Car
β-Carappear
appear
other
1 Ag
´ (S
11Bu++(S )
1Ag
−(S0)) Ñ
at
426,
453,
and
485
nm.
They
are
produced
by
allowing
transitions
of
1
1
1
−
1
+
at
426,
453,
and
485
nm.
They
are
produced
by
allowing
transitions
of
1
→
1
Bu
2
[3,7].
0
2
at 426, 453, and 485 nm. They are produced by allowing transitions of 1 Ag (S0) → 1 Bu (S2)) [3,7].
Markings
as
shown
in
Figure
1
from
left
to
right
are
0-2,
0-1,
and
0-0.
Markings as
as shown
shown in
in Figure
Figure 11 from
from left
left to
to right
right are
are 0-2,
0-2, 0-1,
0-1, and
and 0-0.
0-0.
Markings
Figure 1.1. The
The
absorption
spectra
of
chlorophyll
(Chl-a and
and all-trans-β-Carotene
all-trans-β-Carotene β-Car
β-Car in
in
Figure
all-trans-β-Carotene
The absorption
absorption spectra
spectra of
of chlorophyll
chlorophyll aaa (Chl-a
(Chl-a
β-Car
H
6O
O
solution.
6
solution.
CC33H
H O solution.
3
6
Figure 22 shows
shows the
the absorption
absorption and
and the
the fluorescence
fluorescence positions
positions of
of Chl-a
Chl-a change
change along
along with
with the
the
Figure
Figure 2 shows the absorption and the fluorescence positions of Chl-a change along with the
concentration
in
polarity
and
non-polarity
solvents.
From
Figure
2a,
it
shows
that
the
absorption
concentration in polarity and non-polarity solvents. From Figure 2a, it shows that the absorption
concentration in polarity and non-polarity solvents. From Figure 2a, it shows that the absorption
wavelength of
of Chl-a
Chl-a increases
increases with
with the
the increased
increased concentration
concentration of
of β-Car.
β-Car. Absorption
Absorption band
band of
of Chl-a
Chl-a
wavelength
wavelength of Chl-a increases with the increased concentration of β-Car. Absorption band of Chl-a at
at
410
nm
arises
red-shifted
because
of
the
solvent
effect,
which
results
in
the
excited
electronic
levels
at 410 nm arises red-shifted because of the solvent effect, which results in the excited electronic levels
410 nm arises red-shifted because of the solvent effect, which results in the excited electronic levels
of Chl-a
Chl-a and
and β-car
β-car becoming
becoming much
much closer,
closer, there
there is
is the
the lower
lower electron
electron energy
energy level
level in
in the
the solute
solute [8].
[8].
of
of Chl-a and β-car becoming much closer, there is the lower electron energy level in the solute [8].
C
3
H
6
O
appears
to
have
the
most
obvious
frequency
shift.
The
wavelength
of
fluorescence
decrease
for
C3H6O appears to have the most obvious frequency shift. The wavelength of fluorescence decrease for
C3 H6 O appears to have the most obvious frequency shift. The wavelength of fluorescence decrease
C
3
H
6
O
is
illustrated
in
Figure
2b.
Although
the
ground
state
and
the
excited
state
energy
are
both
C3H6O is illustrated in Figure 2b. Although the ground state and the excited state energy are both
for C3 H6 O is illustrated in Figure 2b. Although the ground state and the excited state energy are
decreased, the
the effect
effect of
of polar
polar solvents
solvents on
on the
the excited
excited states
states is
is stronger
stronger than
than that
that of
of the
the ground
ground state.
state.
decreased,
both decreased, the effect of polar solvents on the excited states is stronger than that of the ground
The
energy
difference
between
both
levels
becomes
small
[3,9].
Polar
solvents
should
cause
a
red
shift
The energy difference between both levels becomes small [3,9]. Polar solvents should cause a red shift
state. The energy difference between both levels becomes small [3,9]. Polar solvents should cause a
for
π
→
π
*
transitions
and
a
blue
shift
for
n
→
π
*
transitions,
especially
for
ketones
[10,11].
The
for π → π * transitions and a blue shift for n → π * transitions, especially for ketones [10,11]. The
red shift for π Ñ π * transitions and a blue shift for n Ñ π * transitions, especially for ketones [10,11].
electron distribution
distribution in
in the
the molecule
molecule is
is asymmetric,
asymmetric, and
and the
the intrinsic
intrinsic dipole
dipole moment
moment is
is generated.
generated.
electron
The electron distribution in the molecule is asymmetric, and the intrinsic dipole moment is generated.
Between
the
two
molecules
with
intrinsic
dipole
moments,
there
will
be
intermolecular
electrostatic
Between the two molecules with intrinsic dipole moments, there will be intermolecular electrostatic
Between the two molecules with intrinsic dipole moments, there will be intermolecular electrostatic
interactions [12].
[12].
interactions
interactions [12].
Figure 2.Cont.
Cont.
Figure
Figure 2.
2. Cont.
Int. J. Mol. Sci. 2016, 17, 978
Int. J. Mol. Sci. 2016, 17, 978
Int. J. Mol. Sci. 2016, 17, 978
3 of 6
3 of 6
3 of 6
Figure 2.2.The
The
dependence
of Chl-a
absorption
(a) and fluorescence
(b) wavelength
on the
Figure
dependence
of Chl-a
absorption
(a) and fluorescence
(b) wavelength
on the concentration
Figure 2. The dependence of Chl-a absorption (a) and fluorescence (b) wavelength on the
concentration
of
β-Car
in
different
solvents.
of β-Car in different solvents.
concentration of β-Car in different solvents.
Figure 3 shows that the levels is critical in energy transfer. It is believed that β-Car does not
Figure
Figure 33 shows
shows that
that the
the levels
levels isis critical
critical in
in energy
energy transfer.
transfer. ItIt is
is believed
believed that
that β-Car
β-Car does
does not
not
fluoresce [13] when excited in visible range. It is accepted that, instead of the strongly allowed
1 Bu
fluoresce
[13]
when
excited
in
visible
range.
It
is
accepted
that,
instead
of
the
strongly
allowed
fluoresce
[13]
when
excited
in
visible
range.
It
is
accepted
that,
instead
of
the
strongly
allowed
1Bu state, the lowest excited singlet electronic state of β-Car is a dipole forbidden 1Ag state at about
11
state,
the lowest
excited
singlet
electronic
state
of of
β-Car
is is
a dipole
1Bu state,
the lowest
excited
singlet
electronic
state
β-Car
a dipoleforbidden
forbidden Ag
Agstate
stateat
at about
about
- 1 lower in energy [14]. The vibronic transition from the excited singlet state of 1Ag to the
3450 cm´
1
11Ag to the
3450
cm
lower
in
energy
[14].
The
vibronic
transition
from
the
excited
singlet
state
of
1
3450 cm lower in energy [14]. The vibronic transition from the excited singlet state of Ag to the
ground singlet state of β-car has an overlap with the absorption band of the Chl-a [15,16].
ground
ground singlet
singlet state
state of
of β-car
β-car has
has an
an overlap
overlap with
with the
the absorption
absorption band
band of
ofthe
theChl-a
Chl-a[15,16].
[15,16].
Figure 3. Scheme of excited electronic levels of Chl-a and β-Car.
Figure
β-Car.
Figure 3.
3. Scheme
Scheme of
of excited
excited electronic
electronic levels
levels of
of Chl-a
Chl-a and
and β-Car.
Figure 4 shows the fluorescence spectra of Chl-a in polarity and non-polarity solvents. It is
Figure 4 shows the fluorescence spectra of Chl-a in polarity and non-polarity solvents. It is
obvious
that4 the
fluorescence
intensityspectra
of Chl-a
with theand
increase
of the concentration
Figure
shows
the fluorescence
of decreases
Chl-a in polarity
non-polarity
solvents. It of
is
obvious that the fluorescence intensity of Chl-a decreases with the increase of the concentration of
β-Car. On
interaction
of the excited
singlet
statedecreases
of β-Car with
the energy
be partitioned
obvious
that
the fluorescence
intensity
of Chl-a
with Chl-a,
the increase
of thecan
concentration
of
β-Car. On interaction of the excited singlet state of β-Car with Chl-a, the energy can be partitioned
between
transfer
andexcited
an electron
[17]. Chl-a,
For thethe
fact
that the
level of
β-Car.
Onenergy
interaction
of the
singlettransfer
state ofprocess
β-Car with
energy
canenergy
be partitioned
between energy transfer and an electron transfer process [17]. For the fact that the energy level of
Chl-a
is
lower
than
that
of
β-Car,
the
electron
transfer
will
dominate
in
the
center
of
the
reaction.
between energy transfer and an electron transfer process [17]. For the fact that the energy level of
Chl-a is lower than that of β-Car, the electron transfer will dominate in the center of the reaction.
Moreover,
β-Car
hasthat
a lower
ionization
potential.
As a result,
is likely to
the of
electron
donor,
Chl-a
is lower
than
of β-Car,
the electron
transfer
will it
dominate
inbecome
the center
the reaction.
Moreover, β-Car has a lower ionization potential. As a result, it is likely to become the electron donor,
and Chl− and Car+ generate during the whole process of electron transfer. The Chl+ is generated
and Chl− and Car+ generate during the whole process of electron transfer. The Chl+ is generated
through a fast ground state reaction (charge transfer) between the Car+ and its nearby Chl-a.
through a fast ground state reaction (charge transfer) between the Car+ and its nearby Chl-a.
Int. J. Mol. Sci. 2016, 17, 978
4 of 6
Moreover, β-Car has a lower ionization potential. As a result, it is likely to become the electron donor,
and Chl´ and Car+ generate during the whole process of electron transfer. The Chl+ is generated
Int. J. Mol. Sci. 2016, 17, 978
4 of 6
through
a fast ground state reaction (charge transfer) between the Car+ and its nearby Chl-a. Therefore,
+
´
the consequence
of the process is a generation of the separated change pair Chl ¨ Chl [18,19]. The
Therefore, the consequence of the process is a generation of the separated change pair Chl+·Chl− [18,19].
energy
levels
of
the
are close
in theinsolution,
so that
thethe
electron
The energy levelscompound
of the compound
are close
the solution,
so that
electronininthe
theupper
upper level
level will
easilywill
undergo
non-radiative
transition
to the lower
the fluorescence
is associated
easily aundergo
a non-radiative
transition
to thelevel.
lowerTherefore,
level. Therefore,
the fluorescence
is
with associated
a red shift.
Thea product
theproduct
experiment
non-emissive,
which leads
to the
quenching
with
red shift. of
The
of the isexperiment
is non-emissive,
which
leads
to the of
of Chl-a fluorescence.
Chl-aquenching
fluorescence.
Figure 4. Fluorescence spectra of Chl-a in polar and non-polar β-Car solutions. ((A) are the polar
Figure 4. Fluorescence spectra of Chl-a in polar and non-polar β-Car solutions. ((A) are the polar
solvets; (B) is the non-polar solvents. (a) C3H6O (b) CHCl3 (c) CH3COOC2H5 (d) C2H4Cl2 (e) C6H6
solvets; (B) is the non-polar solvents. (a) C3 H6 O (b) CHCl3 (c) CH3 COOC2 H5 (d) C2 H4 Cl2 (e) C6 H6
(f) CCl4).
(f) CCl4 ).
A more intuitive trend is shown in Figure 5, where the slope of C3H6O is the steepest. Polar
solvent
on the quenching
effect in
is Figure
more obvious.
of3 H
organic
solvents used in the
A more intuitive
trend is shown
5, whereThe
the polarity
slope of C
6 O is the steepest. Polar solvent
experiment
from
large
to
small
is:
C
3H6O > CHCl3 > C4H8O2 > C2H4Cl2 > C6H6 > CCl4. Therefore, C3H6O
on the quenching effect is more obvious. The polarity of organic solvents used in the experiment
a relatively effective quenching agent in these organic solvents because the effect of polar solvents
fromislarge
to small is: C3 H6 O > CHCl3 > C4 H8 O2 > C2 H4 Cl2 > C6 H6 > CCl4 . Therefore, C3 H6 O is a
on the excited states is stronger than that of the ground state [20]. Quenching of fluorescence by
relatively effective quenching agent in these organic solvents because the effect of polar solvents on
β-Car protects the plants from strong light radiation. In a certain concentration range, the Chl-a
the excited
states is stronger than that of the ground state [20]. Quenching of fluorescence by β-Car
fluorescence intensity decreases with the increase in the concentration of carotene, which improves
protects
the
plantsoffrom
strong lightInradiation.
In a transfer
certain concentration
the Chl-aoccurs
fluorescence
the efficiency
photosynthesis.
lower plants,
from β-carotenerange,
to chlorophyll
in
intensity
decreases
with the increase
the concentration
carotene,
which
improves the
efficiency
Photosystem
I exclusively.
In higherinplants
energy transferof
from
β-carotene
to chlorophyll
occurs
in
of photosynthesis.
In lower
plants,
β-carotene
to chlorophyll
occurs inwith
Photosystem
I
both Photosystem
I and II.
Light transfer
absorbed from
by β-carotene
is transferred
to chlorophyll
nearly
100%
efficiency
[21].
In
addition,
there
is
a
huge
quantity
of
inorganic
salt
and
polar
lipids
in
the
exclusively. In higher plants energy transfer from β-carotene to chlorophyll occurs in both Photosystem
Int. J. Mol. Sci. 2016, 17, 978
5 of 6
Mol. Sci. 2016, 17, 978
5 of 6
I and Int.
II. J.Light
absorbed by β-carotene is transferred to chlorophyll with nearly 100% efficiency
[21].
In addition, there is a huge quantity of inorganic salt and polar lipids in the chloroplast, and the polar
chloroplast, and the polar environment is similar to the C3H6O solution that we used in the
environment
is similar
experiment
[22,23]. to the C3 H6 O solution that we used in the experiment [22,23].
Figure 5. The dependence of fluorescence intensity on the concentration of β-Car in different solvents.
Figure 5. The dependence of fluorescence intensity on the concentration of β-Car in different solvents.
3. Experimental Section
3. Experimental Section
All samples contained the same Chl-a concentration of 6.7 × 10−5 M. The concentrations of β-Car
−5 M,Chl-a
All
same
concentration
of 6.7 solvents
ˆ 10´5 M.
The
concentrations
β-Car
are samples
0.6 × l0−5, contained
1 × l0−5, andthe
2 × 10
respectively.
The nonpolar
used
include
C6H6, CCl4, of
and
´
5
´
5
´
5
C
2
H
4
Cl
2
,
and
the
polar
solvents
used
include
C
3
H
6
O
CHCl
3
,
and
CH
3
COOC
2
H
5
.
The
exciting
laser
are 0.6 ˆ l0 , 1 ˆ l0 , and 2 ˆ 10 M, respectively. The nonpolar solvents used include C6 H6 , CCl4 ,
was fixed at 30 mW with wavelengths of 532 nm. The quartz cell size is 100 × 10 × 45 mm. The
and Cpower
2 H4 Cl2 , and the polar solvents used include C3 H6 O CHCl3 , and CH3 COOC2 H5 . The exciting
fluorescent
is 30
collected
perpendicular
to the
incident
laserquartz
beam and
is recorded
laser power was signal
fixed at
mW with
wavelengths
of 532
nm. The
cell size
is 100 ˆby10Ocean
ˆ 45 mm.
Optics (Maya 2000, Ocean optical Corporation, Dunedin, FL, USA). Absorption spectra were
The fluorescent signal is collected perpendicular to the incident laser beam and is recorded by Ocean
recorded on a double-beam UV-Vis spectrophotometer (TU-1901, Persee Co., Ltd., Beijing, China)
Optics (Maya 2000, Ocean optical Corporation, Dunedin, FL, USA). Absorption spectra were recorded
with a step of 0.5 nm at room temperature.
on a double-beam UV-Vis spectrophotometer (TU-1901, Persee Co., Ltd., Beijing, China) with a step of
0.5 nm
room temperature.
4. at
Conclusions
In conclusion, β-Car can modulate the fluorescence of Chl-a in the solutions. The excited
4. Conclusions
electronic levels of Chl-a and β-car became much closer owing to the solvent effect, which led to the
+ that isin
In
conclusion,
can an
modulate
the fluorescence
of Chl-a
the
solutions.
The excited
electron
transfer β-Car
producing
electron-separated
pair Chl−·Chl
not
luminous.
The effect
of
polar levels
solvents
the excited
statesbecame
is stronger
than
that ofowing
the ground
in C3H
6O solution,
electronic
ofon
Chl-a
and β-car
much
closer
to thestate
solvent
effect,
whichwhich
led to the
results
in a better
quenching
effect, and the polar
very
to the internal
electron
transfer
producing
an electron-separated
pairenvironment
Chl´ ¨ Chl+isthat
is similar
not luminous.
The effect
environment
of
chloroplast.
The
results
provide
references
for
optical
protection
of
plants
during
the
of polar solvents on the excited states is stronger than that of the ground state in C3 H6 O solution,
photosynthesis process.
which results in a better quenching effect, and the polar environment is very similar to the internal
environment
of chloroplast.
The results
provide
references
for optical
of Natural
plants Science
during the
Acknowledgments:
The authors
acknowledge
the financial
contribution
fromprotection
the National
photosynthesis
Foundation process.
of China (NSFC) (11574113, 11104106, and 11374123); the International Postdoctoral Exchange
Fellowship Program (20150030); and the Science and Technology Planning Project of Jilin Province
The authors acknowledge
the financial contribution from the National Natural Science
Acknowledgments:
(20130101017JC, 20140101173JC,
and 20140204077GX).
Foundation of China (NSFC) (11574113, 11104106, and 11374123); the International Postdoctoral Exchange
Author
Contributions:
Zhiwei
and Zuowei
Li conceived Planning
and designed
theof
experiments;
Tianyu
Li and
Fellowship
Program
(20150030);
andMen
the Science
and Technology
Project
Jilin Province
(20130101017JC,
Ye Zhang and
performed
the experiments; Tianyu Li and Nan Gong analyzed the data; Chenglin Sun and
20140101173JC,
20140204077GX).
Zhiwei Men contributed reagents/materials/analysis tools; Tianyu Li wrote the paper.
Author Contributions: Zhiwei Men and Zuowei Li conceived and designed the experiments; Tianyu Li and
Conflicts
of Interest:
The authors declare
of interest.
Ye Zhang
performed
the experiments;
Tianyuno
Liconflict
and Nan
Gong analyzed the data; Chenglin Sun and Zhiwei Men
contributed reagents/materials/analysis tools; Tianyu Li wrote the paper.
References
Conflicts of Interest: The authors declare no conflict of interest.
1.
Genty, B.; Briantais, J.M.; Baker, N.R. The relationship between the quantum yield of photosynthetic
electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 1989, 990, 87–92.
References
1.
Genty, B.; Briantais, J.M.; Baker, N.R. The relationship between the quantum yield of photosynthetic electron
transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 1989, 990, 87–92. [CrossRef]
Int. J. Mol. Sci. 2016, 17, 978
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
6 of 6
Schreiber, U.; Bilger, W.; Neubauer, C. Chlorophyll fluorescence as a non-destructive indicator for rapid
assessment of in vivo photosynthesis. Ecol. Stud. 1994, 100, 49–70.
Xu, S.N.; Liu, T.Y.; Sun, M.J.; Li, Z.W. Solvent effects on the electron-vibration coupling constant of β-Carotene.
Acta Phys. Sin. 2014, 63. [CrossRef]
Kopczynski, M.; Ehlers, F.; Lenzer, T.; Oum, K. Evidence for an intramolecular charge transfer state in
121 -apo-β-caroten-121 -al and 81 -apo-β-caroten-81 -al: Influence of solvent polarity and temperature. J. Phys.
Chem. A 2007, 111, 5370–5381. [CrossRef] [PubMed]
Garab, G. Photosynthesis: Mechanisms and Effects; Springer Science & Business Media: Berlin, Germany;
Heidelberg, Germany, 1998.
Gazdaru, D.M.; Iorga, B. Characterization of the quenching of chlorophyll a fluorescence by β-carotene using
the non-linear analysis. Photosynthetica 2001, 39, 607–609. [CrossRef]
Niedzwiedzki, D.M.; Enriquez, M.M.; LaFountain, A.M.; Frank, H.A. Ultrafast time-resolved absorption
spectroscopy of geometric isomers of xanthophylls. Chem. Phys. 2010, 373, 80–89. [CrossRef] [PubMed]
Lu, L.; Ma, B.; Wei, L.; Luo, X.; Ni, X. How does the β-ionone effect the spectra of chlorophyll and the
excitation energy transfer in solution. Opt. Spectrosc. 2014, 117, 545–551. [CrossRef]
Nagy, L.; Kiss, V.; Brumfeld, V.; Osvay, K.; Börzsönyi, Á.; Magyar, M.; Szabó, T.; Dorogi, M.; Malkin, S.
Thermal effects and structural changes of photosynthetic reaction centers characterized by wide frequency
band hydrophone: Effects of carotenoids and terbutryn. Photochem. Photobiol. 2015, 91, 1368–1375. [CrossRef]
[PubMed]
Fiedor, J.; Fiedor, L.; Winkler, J.; Scherz, A.; Scheer, H. Photodynamics of the bacteriochlorophyll-carotenoid
system. 1. Bacteriochlorophyll-photosensitized oxygenation of β-carotene in acetone. Photochem. Photobiol.
2001, 74, 64–71. [CrossRef]
Gribov, L.A. Introduction to Molecular Spectroscopy; Moscow Izdatel Nauka: Moscow, Russia, 2010.
Mahanty, J.; Ninham, B.W. Dispersion Forces; Academic Press: London, UK, 1976.
Song, P.S.; Moore, T.A. On the photoreceptor pigment for phototropism and phototaxis: Is a carotenoid the
most likely candidate? Photochem. Photobiol. 1974, 19, 435–441. [CrossRef] [PubMed]
Białek-Bylka, G.E.; Shkuropatov, A.Y.; Kadoshnikov, S.I.; Frhckowiak, D. Excitation energy transfer between
β-carotene and chlorophyll-a in various system. Photosynth. Res. 1982, 3, 241–254. [CrossRef] [PubMed]
Naqvi, K.R. The mechanism of singlet-singlet excitation energy transfer from carotenoids to chlorophyll.
Photochem. Photobiol. 1980, 31, 523–524. [CrossRef]
Sineshchekov, V.A.; Litvin, F.F.; Das, M. Chlorophyll-a and carotenoid aggregates and energy migration in
monolayers and thin films. Photochem. Photobiol. 1972, 15, 187–197. [CrossRef] [PubMed]
Frank, H.A.; Cogdell, R.J. Carotenoids in photosynthesis. Photochem. Photobiol. 1996, 63, 257–264. [CrossRef]
[PubMed]
Forti, G., Avron, M., Melandri, A., Eds.; Photosynthesis, Two Centuries after Its Discovery by Joseph Priestley:
Proceedings of the IInd International Congress on Photosynthesis Research Volume I Primary Reactions and Electron
Transport; Springer Science & Business Media: Berlin, Germany; Heidelberg, Germany, 2012.
Beddard, G.S.; Davidson, R.S.; Trethewey, K.R. Quenching of chlorophyll fluorescence by β-carotene. Nature
1977, 267, 373–374. [CrossRef]
Paraschuk, D.Y.; Arnautov, S.A.; Shchegolikhin, A.N.; Kobryanskii, V.M. Temperature evolution of electronic
and lattice configurations in highly ordered trans-polyacetylene. J. Exp. Theor. Phys. Lett. 1996, 64, 658–663.
[CrossRef]
Goedheer, J.C. Energy transfer from carotenoids to chlorophyll in blue-green, red and green algae and
greening bean leaves. Biochim. Biophys. Acta Bioenerg. 1969, 172, 252–265. [CrossRef]
Dirks, G.; Moore, A.L.; Gust, D. Light absorption and energy transfer in polyene-porphyrin esters.
Photochem. Photobiol. 1980, 32, 277–280. [CrossRef]
Heemskerk, J.W.M.; Bögemann, G.; Scheijen, M.A.M.; Wintermans, J.F.G.M. Separation of chloroplast
polar lipids and measurement of galactolipid metabolism by high-performance liquid chromatography.
Anal. Biochem. 1986, 154, 85–91. [CrossRef]
© 2016 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC-BY) license (http://creativecommons.org/licenses/by/4.0/).