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Excited-State Dynamics of DNA Duplexes with Different H-Bonding Motifs Yuyuan Zhang, Kimberly de La Harpe, Ashley A. Beckstead, Lara Martinez-Fernandez, Roberto Improta, and Bern Kohler J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.6b00074 • Publication Date (Web): 17 Feb 2016 Downloaded from http://pubs.acs.org on February 18, 2016

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The Journal of Physical Chemistry Letters

Excited-State Dynamics of DNA Duplexes with Different H-Bonding Motifs

Yuyuan Zhang,† Kimberly de La Harpe,‡ Ashley A. Beckstead,† Lara Martínez-Fernández,§ Roberto Improta,*,§ and Bern Kohler*,† †

Department of Chemistry and Biochemistry, Montana State University, Bozeman, MT 59717, USA ‡

Department of Physics, United States Air Force Academy, USAF Academy, CO 80840, USA

§

Consiglio Nationale delle Ricerche, Istituto di Biostrutture e Bioimmagini, 80136 Naples, Italy

Figures: 4

* Corresponding Authors: Bern Kohler: [email protected], Tel: +1 406-994-7931 Roberto Improta: [email protected], Tel: +39 081 2532036

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Abstract The excited-state dynamics of three distinct forms of the d(GC)9·d(GC)9 DNA duplex were studied by combined time-resolved infrared experiments and quantum mechanical calculations. In the B- and Z-forms, bases on opposite strands form Watson-Crick (WC) base pairs, but stack differently due to salt-induced changes in backbone conformation. At low pH, the two strands associate by Hoogsteen (HG) base pairing. UV-induced intrastrand electron transfer (ET) triggers interstrand proton transfer (PT) in the B- and Z-forms, but the PT pathway is blocked in the HG duplex. Despite the different decay mechanisms, a common excited-state lifetime of ~30 ps is observed in all three duplex forms. The ET-PT pathway in the WC duplexes and the solely intrastrand ET pathway in the HG duplex yield the same pair of π-stacked radicals on one strand. Back ET between these radicals is proposed to be the rate-limiting step behind excited-state deactivation in all three duplexes.

TOC Graphic

Keywords Watson-Crick base pair, Hoogsteen base pair, time-resolved vibrational spectroscopy, DNA photophysics, proton-coupled electron transfer

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A recent experimental and computational study revealed that the long-lived excited state with a lifetime of ~30 ps in a DNA duplex with alternating Watson-Crick (WC) G·C base pairs is formed via a multi-site proton-coupled electron transfer (PCET) mechanism.1 UV excitation of the duplex transfers an electron from G to its π-stacked neighbor C, forming a guanine radical cation (G•+) and a cytosine radical anion (C•−). Intrastrand electron transfer (ET) is an important decay pathway in single-stranded DNA sytems.2-7 In double-stranded DNA, base pairing provides the necessary reaction coordinate for interstrand proton transfer (PT), which is much more favorable in the radical ion base pairs created by intrastrand charge separation on account of the greatly enhanced acidity/basicity of the nucleobase radical ions.1 Because C•− is a strong base, it acquires the N1-proton from G along the middle H-bond, forming a C(+D3)• neutral radical, which is base paired with G(−D1)−, a closed shell deprotonated guanine anion (Figure 1a).1 As a result, a distonic radical ion base pair is formed in which spin and charge reside on opposite DNA strands. Excited-state PCET in DNA duplexes should therefore be exquisitely sensitive to both base stacking and pairing interactions. The structures of G·C DNA duplexes can be tuned by adjusting

the

solution

conditions.

At

neutral

pH

and

low

salt

concentration,

poly(dGdC)·poly(dGdC) adopts the right-handed B-DNA conformation, but converts to the lefthanded Z-form at high salt concentration (e.g., 5 M NaCl).8-9 At low pH, the C residues are protonated at the N3 position and WC base pairs (Figure 1a) are replaced by Hoogsteen (HG) base pairs (Figure 1b).10 A previous UV-pump/UV-probe transient absorption study on B-, Zand HG forms of d(GC)9·d(GC)9 reported identical excited-state lifetimes within experimental uncertainty.11 In this study, we seek to understand why excited-state relaxation occurs on similar

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time scales in all three duplexes despite significant differences in base stacking and pairing motifs.

Figure 1. (a) UV-induced proton-coupled electron transfer (PCET) in an alternating G·C duplex with the Watson-Crick base pairing motif. The bottom base pair on the right is distonic. (b) UVinduced electron transfer (ET) between π-stacked bases in an alternating G·C duplex with Hoogsteen base pairing. Ring numbering is shown for convenience. All labile protons have been substituted by deuterons.

By combining time-resolved infrared spectroscopy (TRIR) and quantum chemical calculations, the long-lived transient species formed by UV excitation of B-, Z- and HG-forms of d(GC)9·d(GC)9 are identified through the distinct patterns of vibrational bands in the doublebond stretching region. We show that UV excitation triggers intrastrand ET in all three duplexes, but interstrand PT takes place only when WC base pairs are present. Interestingly, the same pair 4


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of radicals, a G•+ π-stacked with C(+D3)•, is formed on one strand in both the WC and HG duplexes although they are hydrogen bonded differently to different closed-shell partners (Figure 1). Our results suggest that back ET between these common π-stacked radicals is the ratelimiting step in excited state deactivation.

Figure 2. (a,b) TRIR spectra of B- and Z-form d(GC)9·d(GC)9 in buffered D2O solution recorded from 1 ps (purple) to 1 ns (red) after 265-nm excitation. (c,d) The DADS for the long-lived excited state obtained from global fitting (see text), compared with the inverted FTIR spectra. The FTIR spectrum of G(−D1)− of GMP in basic D2O solution is shown for comparison. (e,f) PCM/M052X/6-31G(d) calculated frequencies for the radical ion pairs depicted in Figure 1a.

The duplexes were excited at 265 nm and probed by a broadband mid-IR pulse centered at 1626 cm-1 (6150 nm) with a bandwidth of ~200 cm-1. All experiments were carried out in D2O to minimize absorption of the probe pulse by the solvent. Sample preparation and the TRIR setup are discussed in Supporting Information (SI). It is noteworthy that the stability of the HG form of the d(GC)9·d(GC)9 duplex is extremely sensitive to pD (pD = −log([D3O+]) and NaCl

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concentration, and thus was carefully characterized by UV-visible, circular dichroism (CD) and FTIR spectroscopy (see Figure S1 in the SI and accompanying discussion). Panels a and b of Figure 2 display the TRIR spectra of B- and Z-form d(GC)9·d(GC)9, respectively. The positive bands originate from excited-state and/or transient species, whereas the negative bands, which align well with the inverted FTIR spectrum, are due to ground state bleaching (GSB). The FTIR spectrum of the Z-form duplex differs significantly from that of the B-form. The carbonyl stretching modes of G (GC=O, band 1 in Figure 2) and C (CC=O, band 2) shift by approximately 15 cm-1 to lower frequency in response to the B → Z transition. This agrees with observations by Taboury et al.9 and Doorley et al.,12 confirming that our sample is Band Z-form at 100 mM and 5 M NaCl concentrations, respectively. The TRIR signals for the B-form of d(GC)9·d(GC)9 decay bi-exponentially with time constants τ1 = 7.4 ± 0.4 ps and τ2 = 31 ± 1 ps in excellent agreement with literature values.1, 12 The TRIR signals for the Z-form decay similarly (τ1 = 9 ± 1 ps and τ2 = 34 ± 2 ps). Previously, Doorley et al. observed biexponential decays for the B-form of poly(dGdC)⋅poly(dGdC), but monoexponential dynamics for the Z-form of the same substrate.12 The TRIR signals for both duplexes disappear by approximately 150 ps, indicating that virtually all excited-state population returns to the ground state within this time. A featureless, negative offset is observed at t > 150 ps that does not evolve in time. This weak signal originates from spectral shifts of D2O after heating by the UV pump pulses.13-14 Global analysis15-16 was used to extract excited-state lifetimes and the decay-associated difference spectrum (DADS) of the state with the longest lifetime (see Figure S2 and associated text in the SI for details). Note that the TRIR spectra at t > 30 ps (i.e. after the fast component has decayed away) are identical in shape to the long-lived DADS shown in Figures 2c and 2d.

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The focus of this study is on this long-living excited state and details of the dynamics on shorter time scales when multiple states are present is the subject for a future study. We note that a comparison of the GSB recovery dynamics of the GC=O mode (band 1 in Figures 2a and 2b) reveals identical kinetics for both forms of the 18-mer within experimental uncertainty (see Figure S3 in the SI). This is consistent with an earlier UV/UV and UV/vis transient absorption study, which found identical excited-state lifetimes for B- and Z-form d(GC)9·d(GC)9 in H2O solution.11 The TRIR signal in the ~1620 cm-1 region appears to decay faster in the B-form duplex than in the Z-form (compare Figure 2a with 2b). However, this difference arises because the short-lived component absorbs more strongly in the B- vs. Z-form (see Figure S4a in the SI). The long-lived transient species, which is the subject of this study, decays with the same kinetics in both forms. In alternating G·C duplexes, the intrastrand CT state consisting of G•+ and C•− is the lowest-energy excited state in the Franck-Condon region.17-18 Furthermore, PT from G to C•− along the middle H-bond is thermodynamically favorable, yielding a distonic base pair C(+D3)•·G(−D1)− stacked with G•+·C (see Figure 1a).1 Indeed, geometry optimization of the distonic base pair C(+D3)•·G(−D1)− leads to a minimum that is approximately 0.1 eV more stable than the non-distonic form (see Computational Details in the SI). The calculated frequencies of the marker bands for the transient products (panels e and f of Figure 2) formed via the multi-site PCET mechanism shown in Figure 1a are compared to the frequencies of the positive features observed in the ~30-ps DADS (panels c and d of Figure 2). The vibrational spectrum of the excited state (see Figure 1) is approximated as the sum of the ground-state spectra of two oppositely charged tetramers (whether distonic or not). All calculated frequencies

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have been multiplied by 0.95 for comparison with experiment. The computational approach is discussed in detail in the SI and ref. 1. The frequencies of the positive bands in the ~30-ps DADS of the B- and Z-form d(GC)9·d(GC)9 duplexes are very similar (see Figure S4a). Comparison of theory and experiment supports the conclusion that these positive signals originate from identical species. Bands b and a in Figures 2c and 2d are assigned to carbonyl stretching modes of C(+D3)• and G•+, respectively (see sticks in Figures 2e and 2f). These bands occur at nearly the same frequencies in B- and Zforms in contrast to the carbonyl stretches of neutral C and neutral G (bands 2 and 1, respectively in Figures 2a and 2b), which are more sensitive to helix conformation. The key evidence supporting a PCET mechanism (Figure 1a) is the observation of the deprotonated guanine G(−D1)− base paired with the neutral cytosine radical C(+D3)•. The IR signature of the closed-shell G(−D1)− was obtained from the FTIR spectrum of guanosine monophosphate at pD > 9.25 (Figure 2c, d).19 The same deuteron is transferred to C•− formed by UV-induced intrastrand ET. The FTIR spectrum of G(−D1)− has two bands at 1595 and 1585 cm1

, in excellent agreement with bands c and d, respectively, observed in the long-lived DADS of

both WC duplexes. Calculations indicate that these two bands are due to in-plane stretching modes, and their frequencies are insensitive to base stacking and pairing, justifying use of the monomer marker bands to assign the positive bands seen in the TRIR spectra of the B- and Zform duplexes. The calculated frequencies for these two bands differ by only 10 cm-1 in the two stacking conformations. The weakly exoergic G•+ → C PT does not appear to take place because vibrational signatures for G(−D)• and C(+D)+ are not evident in the TRIR spectrum.1 However, Parker et al. observed deuteron transfer from N1 of G•+ to N3 of C following UV excitation at 77 K.20 If PT

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were to take place in the cationic base pair in addition to the anionic one, then one electron moving “vertically” along the base stack would result in the transfer of two protons “horizontally” in neighboring base pairs. This interesting possibility warrants further experimental and theoretical investigation. Intrastrand ET triggers interstrand PT in the two WC d(GC)9·d(GC)9 duplexes along the middle H-bond joining the N1 of G to the N3 of C. HG base pairs lack this middle H-bond, providing an excellent test of our mechanism. Protonation of the C residues in the d(GC)9·d(GC)9 duplex induces the transition from the WC base pairing motif to HG. The latter motif preserves the C6=O···D−N4 H-bond, but N1−D of G no longer participates in base pairing. Instead, the extra deuteron acquired by C at N3 is H-bonded to N7 of G (Figure 1b). The inverted FTIR spectrum of the HG d(GC)9·d(GC)9 (Figure 3a) differs from the FTIR spectra of the WC duplexes. The spectrum exhibits a broad feature at ~1715 cm-1 (band 1ʹ) and a strong band at 1657 cm-1 (band 2ʹ), which are assigned to the carbonyl stretch and ring in-plane vibration of protonated C, C(+D3)+, respectively. Note that protonation shifts the carbonyl stretch of C by 60 cm-1 to higher frequency (compare band 2 in Figure 2a with band 1ʹ in Figure 3a). Also note that bands 1ʹ and 2ʹ of protonated C hardly shift on going from the monomer to the duplex (see Figure S5 in the SI).

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Figure 3. (a) TRIR spectra of Hoogsteen d(GC)9·d(GC)9 in pD = 3.6 solution recorded from 1 ps (purple) to 1 ns (red) after 265-nm excitation. (b) Comparison of the long-lived DADS for the Hoogsteen (blue trace) and the B-form (purple trace) duplex. (c) The DADS of the long-lived excited state compared with the inverted FTIR spectrum. (d) PCM/M052X/6-31G(d) calculated frequencies for the radical ion pairs shown in Figure 1b.

The TRIR spectra of the HG d(GC)9·d(GC)9 are shown in Figure 3a. Global fitting reveals that the long-lived component has essentially the same lifetime observed for the WC duplexes (τ2 = 28 ± 1 ps for HG vs 31 ± 1 ps for B-form and 34 ± 2 ps for Z-form). GSB recovery kinetics monitored at 250 nm also show very little difference between the B- and HG duplexes.11 Interestingly, despite the similar lifetimes, Figure 3b shows that the shape of the long-lived DADS of the HG duplex differs significantly compared to the WC duplexes (also see panel b of Figure S4 in the SI). The positive features at 1595 cm-1 (band c in Figure 2) and 1585 cm-1 (band d in Figure 2) seen in the WC duplexes, which are assigned to ring in-plane vibrations of G(−D1)−, are no longer observed in the HG duplex. The absence of positive signals in this region results in a pronounced negative signal that corresponds to GSB of band 3ʹ (shaded area in Figure 3b). This confirms that G(−D1)− is not formed in the excited-state HG duplex where the N1−D···N3 H-

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bond is absent, and lends further support to PT from N1 of G to N3 of C upon UV-excitation of the WC duplexes. The absence of PT in the HG duplex is consistent with our calculation predicting that the CT state consisting of G•+ and C(+D3)•, formed by transferring an electron from G to its πstacked neighbor C(+D3)+, is the lowest-energy excited state. Geometry optimization of this CT state also leads to a stable minimum (see Computational Details in the SI). Calculations further predict that the positions and intensities of the marker bands for the G•+·C and C(+D3)•·G base pairs in the HG duplex (Figure 3d) are quite different from those in the WC duplexes (Figures 2e and 2f). The C=O stretching mode of G•+ is calculated at 1720 cm-1, but is predicted to be six times weaker in the HG duplex. This makes it difficult to detect due to overlap with the bleach of the carbonyl stretch of C(+D3)+ (band 1ʹ in Figure 3a). On the other hand, the ring in-plane vibration of G•+ becomes stronger in the HG base pair and is responsible for the broad feature observed in the 1600 – 1650 cm-1 region (band a in Figure 3c). The signature of C(+D3)• in the HG base pair is blue-shifted by ~30 cm-1 compared to the WC base pair. The C(+D3)• marker band (band b in Figure 3c) is assigned to C=O stretching. It overlaps the GSB of the ring in-plane vibration of C(+D3)+, decreasing the intensity of the latter (green shaded area in Figure 3c). The C(+D3)• band is accompanied by bleaching of the carbonyl stretch mode of C(+D3)+ above 1700 cm-1 as expected when a C radical is formed from C(+D3)+. Evidence thus suggests that an electron is transferred from C to its π-stacked neighbor C(+D3)+, forming G•+ and C(+D3)•. Interstrand PT from C(+D3)• to N7 of G is not energetically feasible, because the former is a very weak acid (pKa > 13).21 Comparing the transient species seen in the WC and HG duplexes is the key to elucidating the excited-state deactivation mechanisms. Although the distonic radical ion base pair

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G(−D1)−·C(+D3)• is not formed in the HG duplex, G•+ π-stacked with C(+D3)• is observed in both the HG and WC duplexes upon UV excitation (Figures 1 and 4). In the HG duplex, G and C(+D3)+ are re-formed from G•+ and C(+D3)• via back ET that takes place on a time scale of 28 ± 1 ps (Figure 4b). For excited-state decay in the WC duplexes, in addition to the “vertical” movement of an electron, “horizontal” movement of a deuteron along the middle H-bond must also take place (Figure 4a). This back PCET reaction moves an electron and a proton from a common origin to two different destinations. Because the excited-state lifetimes of the WC and HG duplexes are similar (~30 ps), we propose that intrastrand back ET in the WC duplex occurs first between G•+ and C(+D3)• followed by ultrafast PT in the resulting C(+D3)+·G(−D1)− base pair. It seems unlikely that concerted proton-electron transfer in the WC duplex would occur at the same rate as intrastrand ET in the HG duplex, but further work is needed to investigate the question of concerted vs. stepwise transfers.

Figure 4. Excited-state deactivation pathways for (a) Watson-Crick and (b) Hoogsteen duplexes.

Bucher et al.22 used the TRIR technique to observe the bleach recovery kinetics of ground state vibrations of the four canonical bases in calf thymus DNA. Vibrations of G and C bases recovered with a 40 ps time constant in reasonable agreement with the dynamics observed here, while those associated with A and T bases recovered on a longer, 210 ps time scale. The authors

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asserted that the common decay rates observed for complementary bases indicate that excitedstate deactivation takes place in base pairs as additional decay times would be expected for intrastrand pathways because of the large number of base doublets. Here, similar lifetimes are observed in all three alternating G·C duplexes, but the TRIR spectra indicate quite different deactivation mechanisms, revealing subtle interactions among base stacking and base pairing. In summary, the results of this study argue that the common lifetimes seen for the B-, Zand HG-forms of the d(GC)9⋅d(GC)9 duplex do not indicate common decay mechanisms. In the case of the HG d(GC)9·d(GC)9 duplex, intrastrand ET forms G•+ stacked with C(+D3)• and interstrand PT is not observed. Intrastrand ET also takes place in the WC d(GC)9·d(GC)9 duplexes, forming G•+ stacked with C•−. However, the latter is a strong base and acquires the N1 deuteron from G along the middle H-bond, yielding a distonic C(+D3)•·G(−D1)− base pair. PCET in the WC duplexes and intrastrand ET in the HG duplex both form G•+ stacked with C(+D3)• on one strand. The observation of identical decay times suggests that back ET between these two species is the rate-limiting step in excited-state deactivation.

Acknowledgments Work at Montana State University was supported by the NSF (CHE-1112560). The TRIR spectrometer was constructed with funding from the M. J. Murdock Charitable Trust. R. I. and L. M.-F. were supported by the Italian Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR Grants PRIN-2010ERFKXL), and French Agency for Research Grant ANR-12-BS080001-01 and LR. Campania num 5/2002 – Annualità 2007.

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Supporting Information Experimental methods, supplementary results, and computational details. This material is available free of charge via the Internet at http://pubs.acs.org.

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References (1) Zhang, Y.; de La Harpe, K.; Beckstead, A. A.; Improta, R.; Kohler, B. UV-Induced Proton Transfer between DNA Strands. J. Am. Chem. Soc. 2015, 137, 7059-7062. (2) Doorley, G. W.; Wojdyla, M.; Watson, G. W.; Towrie, M.; Parker, A. W.; Kelly, J. M.; Quinn, S. J. Tracking DNA Excited States by Picosecond-Time-Resolved Infrared Spectroscopy: Signature Band for a Charge-Transfer Excited State in Stacked Adenine-Thymine Systems. J. Phys. Chem. Lett. 2013, 4, 2739-2744. (3) Stuhldreier, M. C.; Temps, F. Ultrafast Photo-Initiated Molecular Quantum Dynamics in the DNA Dinucleotide d(ApG) Revealed by Broadband Transient Absorption Spectroscopy. Faraday Discuss. 2013, 163, 173-188. (4) Bucher, D. B.; Pilles, B. M.; Carell, T.; Zinth, W. Charge Separation and Charge Delocalization Identified in Long-Living States of Photoexcited DNA. Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 4369-4374. (5) Pilles, B. M.; Bucher, D. B.; Liu, L. Z.; Gilch, P.; Zinth, W.; Schreier, W. J. Identification of charge separated states in thymine single strands. Chem. Commun. 2014, 50, 15623-15626. (6) Zhang, Y.; Dood, J.; Beckstead, A. A.; Li, X. B.; Nguyen, K. V.; Burrows, C. J.; Improta, R.; Kohler, B. Efficient UV-Induced Charge Separation and Recombination in an 8Oxoguanine-Containing Dinucleotide. Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 11612-11617. (7) Zhang, Y.; Dood, J.; Beckstead, A. A.; Li, X. B.; Nguyen, K. V.; Burrows, C. J.; Improta, R.; Kohler, B. Photoinduced Electron Transfer in DNA: Charge Shift Dynamics Between 8-Oxo-Guanine Anion and Adenine. J. Phys. Chem. B 2015, 119, 7491-7502. (8) Pohl, F. M.; Jovin, T. M. Salt-Induced Cooperative Conformational Change of a Synthetic DNA: Equilibrium and Kinetic Studies with Poly(dG-dC). J. Mol. Biol. 1972, 67, 375396. (9) Taboury, J. A.; Liquier, J.; Taillandier, E. Characterization of DNA Structures by Infrared-Spectroscopy: Double Helical Forms of Poly(dG-dC)·Poly(dG-dC), Poly(dD8GdC)·Poly(dD8G-dC), and Poly(dG-dm5C)·Poly(dG-dm5C). Can. J. Chem. 1985, 63, 1904-1909. (10) Segers-Nolten, G. M. J.; Sijtsema, N. M.; Otto, C. Evidence for Hoogsteen GC Base Pairs in the Proton-Induced Transition From Right-Handed to Left-Handed poly(dGdC)·poly(dG-dC). Biochemistry 1997, 36, 13241-13247. (11) de La Harpe, K.; Crespo-Hernández, C. E.; Kohler, B. The Excited-State Lifetimes in a G·C DNA Duplex Are Nearly Independent of Helix Conformation and Base-Pairing Motif. Chemphyschem 2009, 10, 1421-1425. (12) Doorley, G. W.; McGovern, D. A.; George, M. W.; Towrie, M.; Parker, A. W.; Kelly, J. M.; Quinn, S. J. Picosecond Transient Infrared Study of the Ultrafast Deactivation

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Excited-State Dynamics of DNA Duplexes with ... - ACS Publications

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