Rational design of far red to near-infrared rhodamine analogues with huge Stokes shifts for single-laser excitation multicolor imaging

Article abstract of DOI:10.1016/j.cclet.2021.06.038

Rhodamine dyes have been widely employed in biological imaging and sensing. However, it is always a challenge to design rhodamine derivatives with huge Stokes shift to address the draconian requirements of single-excitation multicolor imaging. In this work, we described a generally strategy to enhance the Stokes shift of rhodamine dyes by completely breaking their electronic symmetry. As a result, the Stokes shift of novel rhodamine dye DQF-RB-Cl is up to 205 nm in PBS, which is the largest in all the reported rhodamine derivatives. In addition, we successfully realized the single excitation trichromatic imaging of mitochondria, lysosomes and cell membranes by combining DQF-RB-Cl with commercial lysosomal targeting probe Lyso-Tracker Green and membrane targeting dye Dil. This is the organic synthetic dyes for SLE-trichromatic imaging in cells for the first time. These results demonstrate the potential of our design as a useful strategy to develop huge Stokes shift fluorophore for bioimaging.

Full text of DOI:10.1016/j.cclet.2021.06.038

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Contents lists available at ScienceDirect
Chinese Chemical Letters
journal homepage: www.elsevier.com/locate/cclet
Communication
Rational design of far red to near-infrared rhodamine analogues with
huge Stokes shifts for single-laser excitation multicolor imaging
∗
∗
Xingxing Zhang, Tianbing Ren , Feiyu Yang, Lin Yuan
State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Chemistry and Chemical Engineering, Hunan University, Changsha 410082, China
a r t i c l e i n f o
a b s t r a c t
Article history:
Rhodamine dyes have been widely employed in biological imaging and sensing. However, it is always a
challenge to design rhodamine derivatives with huge Stokes shift to address the draconian requirements
of single-excitation multicolor imaging. In this work, we described a generally strategy to enhance the
Stokes shift of rhodamine dyes by completely breaking their electronic symmetry. As a result, the Stokes
shift of novel rhodamine dye DQF-RB-Cl is up to 205 nm in PBS, which is the largest in all the reported
rhodamine derivatives. In addition, we successfully realized the single excitation trichromatic imaging
of mitochondria, lysosomes and cell membranes by combining DQF-RB-Cl with commercial lysosomal
targeting probe Lyso-Tracker Green and membrane targeting dye Dil. This is the organic synthetic dyes
for SLE-trichromatic imaging in cells for the first time. These results demonstrate the potential of our
design as a useful strategy to develop huge Stokes shift fluorophore for bioimaging.
Received 21 March 2021
Revised 1 June 2021
Accepted 14 June 2021
Available online xxx
Keywords:
Fluorescent dyes
Rhodamine analogues
Huge stokes shifts
Single-laser excitation
Multicolor imaging
©
2021 Published by Elsevier B.V. on behalf of Chinese Chemical Society and Institute of Materia
Medica, Chinese Academy of Medical Sciences.
Fluorescence imaging has been widely used for interrogating
living systems owing to its superior sensitivity, fine spatiotem-
poral resolution, non-invasiveness and low cost [1–6]. In partic-
ular, multicolor fluorescence imaging has become a key method
to observe the interaction between intramolecular structures and
biomolecules and to track different organelles in the same cell
Compared to other typies of fluorophores, organic synthetic
dyes, owing to their easy modification and excellent biocompati-
bility, have received considerable attention for biomolecule detec-
tion [17–21] and labeling [7,22,23]. Among them, rhodamine and
its derivatives are highly popular because of their outstanding pho-
tophysical properties, including high extinction coefficients, good
quantum yields, excellent water solubility and resistance to pho-
tobleaching [24,25]. However, the traditional rhodamine dyes usu-
ally suffered from short emission wavelength (< 600 nm) togerther
with small Stokes shifts (< 30 nm), thus makes them difficult for
SLE-multicolor imaging. Although rencently many novel rhodamine
derivatives with large Stokes shifts (> 60 nm) have been developed
and some of them have been used for two-color imaging [14,26–
29], there is no reported work with more than two colors imag-
ing. In addition, the excitation wavelengthes do not well match the
laser of existing microscope also weakens the value of these new
rhodamines. Therefore, it remains an urgent need to design novel
rhodamine dyes with excellent photophysical properties for SLE-
multicolor imaging.
[
7–9]. Generally, the more colors of multicolor imaging, the more
information can be obtained with less experimental through-
put [10,11]. However, due to lack of suitable fluorophores with
matched excitation wavelength and huge Stokes shifts (> 180 nm),
most of the multicolor imaging experiments are multi-laser excita-
tion, and only a few can achieve multi-color imaging with single-
laser excitation (SLE) [12–14]. Compared with multi-excitation,
single-laser excitation multicolor imaging greatly saves resources
and reduces damage to biological samples, especially when there
are three or more colors. Up to date, almost all of the multicolor
images (more than two colors imaging) with single-laser excitation
are based on the Qdots [15] and fluorescent proteins [16]. How-
ever, because of the unadjustable targeting and poor stability, their
bioimaging applications are seriously restricted. Thus, it is signif-
icant and necessary to develop other fluorophores with excellent
photophysical properties for SLE-multicolor imaging.
In this study, by completely breaking the symmetry of tradi-
tional rhodamine, we described a strategy to develop rhodamines
analogues (DQF-RB-OMe, DQF-RB-H and DQF-RB-Cl) with huge
Stokes shift (> 150 nm) and far red to near-infrared emission (FR-
NIR, > 650 nm). Especially, DQF-RB-Cl, which was equipped with
1,4-dimethyl-decahydro-quinoxaline (DQ) group and chlorine to
∗
the xanthene skeleton, displayed the largest Stokes shift (205 nm
in PBS) among all the reported FR-NIR dyes based on rhodamine
Corresponding authors.
E-mail addresses: rentianbing@hnu.edu.cn (T. Ren), lyuan@hnu.edu.cn (L. Yuan).
https://doi.org/10.1016/j.cclet.2021.06.038
1001-8417/© 2021 Published by Elsevier B.V. on behalf of Chinese Chemical Society and Institute of Materia Medica, Chinese Academy of Medical Sciences.
Please cite this article as: X. Zhang, T. Ren, F. Yang et al., Rational design of far red to near-infrared rhodamine analogues with huge
Stokes shifts for single-laser excitation multicolor imaging, Chinese Chemical Letters, https://doi.org/10.1016/j.cclet.2021.06.038

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Table 1
Calculated absorption wavelengths, emission wavelengths and oscillator strengths
of rhodamine B, DQF-RB, DQF-RB-OMe, DQF-RB-H and DQF-RB-Cl.
Compd.
Absorption
Oscillator strength
Emission
Rhodamine B
478 nm (S0→S1)
0.9712
0.0101
0.664
504
nm
675
nm
703
nm
711
nm
720
nm
4
03 nm (S0→S2)
DQF-RB
545 nm (S0→S1)
36 nm (S0→S2)
539 nm (S0→S1)
28 nm (S0→S2)
537 nm (S0→S1)
28 nm (S0→S2)
547 nm (S0→S1)
31 nm (S0→S2)
4
0.3949
0.3175
0.5972
0.2558
0.5625
0.2925
0.647
DQF-RB-OMe
DQF-RB-H
DQF-RB-Cl
4
4
4
Note: Absorption wavelength, oscillator strength and emission wavelength were ob-
tained from Gaussian 09 programs at the B3LYP/6–31+G(d) level using a CPCM sol-
vation model with water as the solvent.
Fig. 1. (A) Rational engineering principle of novel rhodamine dyes. (B) Chemical
structures of rhodamine derivatives.
Table 2
frameworks (Table S1 in Supporting information). DFT calculations
indicate that the traditional rhodamines usually are excited to the
first excited state and then emit photons. In contrast, DQF-RB-Cl
first transits to the second excited state (SES) by absorbing high-
energy photons, then jumps from SES to first excited state (FES)
through internal conversion (IC) and then, emits photons through
the first excited state. This feature makes DQF-RB-Cl have signif-
icant blue shifted absorption (485 nm) and red shifted emission
Photo-physical properties of DQF-RB-OMe, DQF-RB-H and DQF-RB-Cl in EtOH.
−1
−1
Comp.
λ
abs/nm
λ
em/nm Stokes shift/nm ε (L mol cm )
ꢀ
f
DQF-RB-OMe 543
680
680
685
137
193
194
76,000
66,000
67,000
11%
3.5%
1.4%
DQF-RB-H
DQF-RB-Cl
487
491
(
690 nm). As a result, its Stokes shift is deeply expanded. Benefit-
of the substituents, the HOMO energy decreased faster than that
of LUMO. As a result, their calculated HOMO-LUMO energy gap
of these novel rhodamines gradually increased (from 2.53 eV to
2.67 eV) (Fig. 2I), thus resulting the blueshift of their absorption
wavelengths. It should also be noted that unlike DQF-RB, which
displayed a sharp absorption peak at 584 nm, all of the new rho-
damines (DQF-RB-OMe, DQF-RB-H & DQF-RB-Cl) showed broad ab-
sorption with two peaks (peak A & peak B) (Figs. 2A-D). This in-
dicated that there may be two absorbed states of the new rho-
damines, that is, the absorption from S →S transition (peak A)
ing from its large Stokes shift, we successfully realized the SLE-
trichromatic imaging of mitochondria, lysosomes and cell mem-
branes by combining DQF-RB-Cl with commercial lysosomal target-
ing probe Lyso-Tracker Green and membrane targeting dye Dil. We
believe that this strategy may not only provide a means to con-
struct dyes with huge Stokes shifts, but also reignite interest in
multicolor imaging, especially more than two colors imaging with
single-laser excitation.
Our previous work has indicated that when an amino group
of traditional rhodamine (e.g. RhB) is replaced by 1,4-dimethyl-
decahydro-quinoxaline (DQ) with stronger electron donor group,
the Stokes shift (up to 85 nm in PBS) of rhodamine derivative
DQF-RB increases significantly (Fig. 1A and Table S2 in Support-
ing information) [26]. However, for SLE-multicolor imaging, this
moderate Stokes shift is not sufficient. Considering that enhanced
intramolecular charge transfer (ICT) can effectively increase the
Stokes shift of D-A dye and breaking the electronic symmetry
could strengthen the rhodamines’ ICT process [30–32], here we
intend to replace another one diethylamino group of rhodamine
0
1
and the absorption from S →S transition (peak B). However, due
0
2
to the weaker electron-donating ability of hydrogen and chlorine
than methoxyl, DQF-RB-H and DQF-RB-Cl exhibited much stronger
S →S transition than S →S transition (Table 1), whereas the two
0
2
0
1
transitions for DQF-RB-OMe are comparable. This result indicated
that with the electronic symmetry of traditional rhodamine further
or completely breaked, the absorption of rhodamine dyes gradually
changed from S →S transition to S →S transition (Table 1).
0
1
0
2
Thus, the maximum absorption of these new rhodamines un-
dergoes a great blue shift. On the other hand, owing to the asym-
metry ICT in the rhodamine skeleton was further enhanced by the
weaker electron-donating substituents, the three new rhodamines
(DQF-RB-OMe, DQF-RB-H & DQF-RB-Cl) also exhibited a slight red-
shift emission (λem > 685 nm in PBS) compared to their origi-
nal dye DQF-RB (λem = 671 nm in PBS) (Fig. S1 and Table S2 in
Supporting information). As a result, the calculated Stokes shifts of
them are further expanded (> 150 nm), in particular, the Stokes
shift of DQF-RB-Cl is up to 205 nm (Table S2), which is the largest
Stokes shift among all the rhodamine frameworks (Table S1). It
should be also noting that, when completely breaking the sym-
metry of traditional rhodamine, the fluorescence quantum yields
of new rhodamines gradually decreased with the electron-donating
ability of substituent weaked (Table 2 and Table S2). This may be
due to that as the absorption of the novel rhodamines changed
from S →S transition (DQF-RB & DQF-RB-OMe) to S →S tran-
(
DQF-RB) with a weaker electron-donating group or electron-
withdrawing substituent. We expect that this change will further
enhance the electronic asymmetry of rhodamine dyes and continue
to enhance its unidirectional ICT, thus increasing the Stokes shift of
rhodamine derivatives to a greater extent (Fig. 1A). As proof of con-
cept, we designed and synthesized three new rhodamine B deriva-
tives, named as DQF-RB-OMe, DQF-RB-H and DQF-RB-Cl (Fig. 1B).
As described in Scheme S2 (Supporting information), all these new
rhodamines were synthesized with a simple one-step procedure.
And then they were carefully characterized by NMR and ESI analy-
ses.
With the new dyes in hand, we first investigated their photo-
physical properties in different solvents. As shown in Fig. 2 and
Table S2, compared to the original dye DQF-RB, with decreasing
electron-donating ability of the donor group, the maximum ab-
sorption wavelength of new rhodamine derivatives gradually de-
creased from 584 nm (DQF-RB) to 534 nm (DQF-RB-OMe) and
then to 483 nm (DQF-RB-H) and 485 nm (DQF-RB-Cl). A closer
look at the electronic structures in ground state indicates that:
Although both the HOMO and LUMO energy levels of the novel
rhodamines reduced with the decrease of electron-donating ability
0
1
0
2
sition (DQF-RB-H & DQF-RB-Cl), their vibration relaxation and in-
ternal conversion were enhanced. As a result, the photons emitted
from the excited state back to the ground state greatly decreased.
Furthemore, the solvatochromic behaviors showed that the new
rhodamine DQF-RB-Cl and DQF-RB-H displayed much more serious
fluorescence quenching than that of DQF-RB-OMe, when the sol-
2

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Fig. 2. The normalized absorption spectra of (A) DQF-RB, (B) DQF-RB-OMe, (C) DQF-RB-H, (D) DQF-RB-Cl. Fluorescence emission spectra of (E) DQF-RB, (F) DQF-RB-OMe,
G) DQF-RB-H, (H) DQF-RB-Cl in different solvent. (I) Optimized frontier molecular orbitals and orbital energies of DQF-RB, DQF-RB-OMe, DQF-RB-H and DQF-RB-Cl in the
(
ground state. Water was used as the solvent for calculations at the B3LYP/6–31+G(d) level.
vent polarity is increasing (Figs. 2E-H and Fig. S1g). All these data
indicated that further breaking the electronic symmetry of rho-
damine derivative DQF-RB by the weaker electron-donating group
indeed can increase its asymmetry ICT and prepare new rho-
damines with greater Stokes shift (Figs. S3 and S4 in Supporting
information). Such discoveries have expanded our understanding
of the fluorescent scaffold and allowed us to readily design fluo-
rophores with huge Stokes shift.
Considering that DQF-RB-Cl has the largest Stokes shift (Fig. S3
in Supporting information), we chose it as a representative dye
for follow-up experiments. Firstly, we carried out the MTT assay
and the result confirmed that even a concentration as high as
Fig. 3. (A) Confocal fluorescence images of live HeLa cells cultured with DQF-RB-Cl
and Cy5 with continuous irradiation using confocal microscope. (B) Quantification
of the relative mean fluorescence levels of cells from the images of DQF-RB-Cl and
Cy5. Scale bar = 50 μm. For DQF-RB-Cl, λex = 488 nm, λem = 663−738 nm; for
Cy5, λex = 640 nm, λem = 663−738 nm. Laser power is 3 mW.
10 μmol/L of DQF-RB-Cl would not affect cell viability (Fig. S5
in Supporting information). Next, we tested the photostability of
DQF-RB-Cl and the performance was compared with Cy5. DQF-RB-
Cl and Cy5 in PBS (25 mmol/L, pH 7.4, containing 1% DMSO) were
irradiated continuously by a Xe lamp under the same irradiation
conditions. It was observed that DQF-RB-Cl remained highly emis-
sive after continuous irradiation for up to 1 h (99% initial values),
whereas the fluorescence intensity of Cy5 decreased to approxi-
mately 84% of its initial value under the same power energy (Fig.
S6 in Supporting information). To further test the stability of DQF-
RB-Cl, we then incubated it with the cells. It can be clearly seen
that although the fluorescence of DQF-RB-Cl in the pure PBS was
very weak, it still displayed a bright image in living cells. We rea-
son that this significant enhancement may be attributed to the
binding between some proteins in the cell with DQF-RB-Cl (Fig.
S2 in Supporting information). In addtion, similar to the result in
vitro, DQF-RB-Cl incubated within the cells exhibited superior pho-
tostability than the contrast dye Cy5 over continuous excitation.
Cy5 near completely bleached after 10 min of excitation, whereas
DQF-RB-Cl still preserved 70% of initial value (Fig. 3 and Fig. S7
in Supporting information). These results indicated that DQF-RB-
Cl possessed more superior photostability than Cy5, and had a
3

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Fig. 4. (A) The colocalization of DQF-RB-Cl in HeLa cells. (A1) Red channel: DQF-
RB-Cl (2 μmol/L) stain (λex = 488 nm, λem = 663–738 nm); (A2) green chan-
nel: Mito-Tracker Green (200 nmol/L) stain (λex = 488 nm, λem = 500–550 nm);
Fig. 5. Confocal SLE-multicolor images in HeLa cells. (A) Red channel: DQF-RB-
Cl (λex = 488 nm, λem = 663–738 nm); (B) Lyso-Tracker Green (λex = 488 nm,
λ
em = 500–550 nm); (C) plasma membrane fluorescent probe: Dil (λex = 488 nm,
em = 570–620 nm); (D) the merged image of A, B; (E) the merged image of A,
(A3) yellow: overlay; (A4) Pearson’s correlation coefficient (r) = 0.96). (B) The colo-
λ
calization of DQF-RB-Cl in HeLa cells. (B1) Red channel: DQF-RB-Cl (2 μmol/L)
stain (λex = 488 nm, λem = 663–738 nm); (B2) blue channel: Lyso-Tracker Green
C; (F) the merged image of B, C; (G) the merged image of A, B, C. (H) Line profile:
Intensity profile of the white line in image overlap 4. Scale bar: 20 μm.
(
50 nmol/L) stain (λex
=
488 nm, λem
=
500–550 nm); (B3) yellow: overlay;
(
B4) Pearson’s correlation coefficient (r) = 0.32). (C) The colocalization of DQF-RB-
Cl in HeLa cells. (C1) Red channel: DQF-RB-Cl (2 μmol/L) stain (λex = 488 nm,
λ
λ
(
em = 663–738 nm); (C2) green channel: Dil (100 nmol/L) stain (λex = 560 nm,
em = 570–620 nm); (C3) yellow: overlay; (C4) Pearson’s correlation coefficient
that DQF-RB-Cl has great potential in the two-color imaging of or-
ganelles with single laser excitation.
r) = 0.28). (D) The colocalization of DQF-RB-Cl in HeLa cells. (D1) Red channel:
Encouraged by the above results and huge Stokes shift of DQF-
RB-Cl (> 200 nm), we next examined whether it can be used
for SLE-trichromatic imaging in cells. Here we choose Lyso-Tracker
Green and Dil to image together with DQF-RB-Cl, since they not
only have no spectral interference with each other but also ex-
hibit different organelle targeting abilities (Fig. S10 in Supporting
information). As shown in Figs. 5A-F, incubation of living HeLa cells
with DQF-RB-Cl (2.0 μmol/L), Lyso-Tracker Green (50 nmol/L) and
Dil (100 nmol/L) at 37 °C for 15 min, and then collected the red
channel (663–738 nm) for DQF-RB-Cl, green channel (570–620 nm)
for Dil and blue channel (500–550 nm) for Lyso-Tracker Green. It
can be clearly seen that with the 488-nm laser excited, all of the
imaging reagents display bright fluorescence in the cells and mark
the corresponding organelles very well. From their overlapping im-
ages, we can also observe that the fluorescence of the three chan-
nels does not seriously overlap, indicating that there is no obvious
spectral crosstalk between DQF-RB-Cl and the other two labeling
reagents (Figs. 5G and H). These results demonstrated DQF-RB-Cl
with huge Stokes shifts can indeed be used for SLE-trichromatic
imaging. As far as we know, this is the first case of organic syn-
thetic dye for SLE-trichromatic imaging in cells. From the L02 cells
(normal hepatocyte) imaging, we once again confirmed the excel-
lent SLE-trichromatic imaging ability of DQF-RB-Cl (Fig. S11 in Sup-
porting information).
DQF-RB-Cl (2 μmol/L) stain (λex = 488 nm, λem = 663–738 nm); (D2) green chan-
nel: ER-Tracker Red (100 nmol/L) stain (λex = 560 nm, λem = 570–620 nm); (D3)
yellow: overlay; (D4) Pearson’s correlation coefficient (r) = 0.24). Scale bar: 20 μm.
great potential as an excellent organic fluorophore for the long-
term imaging applications.
Given that the positively charged dyes tend to accumulate in
the mitochondria [33], we then investigated the viability of DQF-
RB-Cl as a mitochondrial targeting reagent. As shown in Fig. 4A
and Fig. S8 (Supporting information), after incubation of living
HeLa cells with DQF-RB-Cl (2.0 μmol/L) and commercially avail-
able Mito-Tracker Green (200 nmol/L) at 37 °C for 15 min, the
red fluorescence emitted from DQF-RB-Cl can be well covered with
the green fluorescence from Mito-Tracker Green. The high Pear-
son’s coefficient (0.96) of the overlay image indicated that DQF-
RB-Cl has a good mitochondrial targeting ability. To further prove
its selectivity to mitochondria, DQF-RB-Cl was then incubated with
other organelle targeting reagents such as Lyso-Tracker Green, Dil
(
commercially available membrane targeting dye) and ER-Tracker
Red. Figs. 4B-D and Fig. S8 showed that the area marked by DQF-
RB-Cl in the cells is significantly distinguished from the lysosomes,
membranes and endoplasmic reticulum, and the Pearson’s coeffi-
cients of their overlapping images are only 0.32, 0.28 and 0.24, re-
spectively. These results indicated that DQF-RB-Cl indeed can lo-
calize selectively in mitochondria and could serve as a new kind of
mitochondrial trackers. Notably, due to its suitable excitation wave-
length (λabs = 485 nm) and large Stokes shift (205 nm), DQF-RB-
Cl and three commercially organelle targeting reagents can be ef-
fectively excited by 488-nm laser of the confocal microscope and
are collected in different fluorescence channels with no crosstalk
In summary, we report in this study a strategy to develop large
Stokes shift rhodamines with far red to near-infrared emission
(> 650 nm). With the electronic asymmetry and unidirectional
ICT process increases, the novel rhodamine dye DQF-RB-Cl exhib-
ited largest Stokes shift which is up to 205 nm in PBS. Benefit-
ing from its excellent mitochondrial targeting and photostability,
DQF-RB-Cl can be applied for the long-term mitochondrial labeling
imaging. In addtion, due to its suitable excitation wavelength and
(
Figs. 4A and B, Fig. S9 in Supporting information). This indicates
4

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huge Stokes shift, DQF-RB-Cl was successfully applied to the SLE-
multicolor imaging (including two-color imaging & trichromatic
imaging) in different cells combined with the commercially avail-
able Lyso-Tracker Green and membrane targeting dye (Dil) for the
first time. We believe that our strategy not only can be used to
develop large Stokes shifts rhodamine dyes, but also largely con-
tributes to future improvements of SLE-multicolor imaging .
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