Dynamics of Charge Injection and Charge Recombination in DNA Mini

Article

Dynamics of Charge Injection and Charge Recombination in DNA Mini-Hairpins Ashutosh Kumar Mishra, Michelle A. Harris, Ryan M. Young, Michael R. Wasielewski, and Frederick D. Lewis J. Phys. Chem. B, Just Accepted Manuscript • Publication Date (Web): 19 Jun 2017 Downloaded from http://pubs.acs.org on June 20, 2017

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The Journal of Physical Chemistry

Dynamics of Charge Injection and Charge Recombination in DNA Mini-Hairpins

Ashutosh Kumar Mishra, Michelle A. Harris, Ryan M. Young, Michael R. Wasielewski,* and Frederick D. Lewis* Department of Chemistry. Argonne-Northwestern Solar Energy Research (ANSER) Center, and Institute for Sustainability and Energy at Northwestern, Northwestern University, Evanston, Illinois 60208-3113

Abstract

Steady state spectroscopy, femtosecond transient absorption spectroscopy (fsTA), and femtosecond stimulated Raman spectroscopy (FSRS) of DNA mini-hairpins possessing a diphenylacetylenedicarboxamide (DPA) linker and 1-3 adenine-thymine (A-T) or guaninecytosine (G-C) base pairs have been investigated. Ultraviolet and circular dichroism (UV and CD) spectra are consistent with ground state conformations that are predominantly base-paired and π-stacked for conjugates possessing two or three base pairs; however, they offer no information concerning the conformation of conjugates possessing a single base pair. fsTA

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spectra are indicative of π-stacked structures excepted in the case of the conjugate possessing a single G-C base pair. All of the conjugates display transient absorption bands characteristic of the DPA-. anion radical. Conjugates possessing two or three G-C base pairs display a transient absorption band characteristic of the short-lived G+. cation radical. The mini-hairpins with 1-3 A-T base pairs do not display the transient absorption band characteristic of the (An+.) polaron. This implies that an A-tract with three base pairs is too short to support polaron formation.

Introduction

Recent experimental and theoretical investigations have led to substantial progress in understanding the mechanism of photoinduced charge separation mediated both by duplexes1-4 and higher order DNA structures such as three-way junctions,5-6 G-quadruplexes7-8 and i-motifs.9 We have recently studied of the femtosecond dynamics of the initial steps in exergonic charge separation using the singlet excited states of both electron donor10-11 and electron acceptor12 chromophores adjacent to a DNA base pair in synthetic DNA hairpins. The rate constant for the initial charge injection process is determined mainly by the free energy for this process. For example, electron injection from the electron donor stilbenediether (Sd) to a pyrimidine base is more rapid for thymine than for cytosine10 and hole injection from the electron acceptor diphenylacetylenedicarboxamide (DPA) to guanine is more rapid than for adenine (Scheme 1).11, 13-14

The behavior of the resultant contact radical ion pair is not simply correlated with the base

redox potentials, the thymine anion radical and adenine cation radical undergoing slower charge recombination than their pyrimidine and purine counterparts, resulting in more efficient charge electron and hole transport for A-tracts adjacent to either an electron donor or acceptor.


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Scheme 1. Mechanisms for (a) electron injection and charge recombination from a Sd linker to a thymine base and for (b) hole injection and charge recombination from a DPA linker to a adenine base in chromophore-linked poly(A-T) hairpins.

The DPA chromophore has several desirable features for the investigation of hole injection and charge recombination in DNA hairpins in aqueous solution. These include conversion of a relatively narrow 525 nm transient absorption band for

1*

DPA into two bands at 500 nm and

1130 nm assigned to DPA-. anion radical upon photoinduced electron transfer.11 The kinetics of charge injection and charge recombination (Scheme 1) can be readily determined either by global analysis of the transient absorption spectrum or by monitoring the single-wavelength rise and decay of the 1130 nm band.11 Analysis of the transient absorption and stimulated Raman spectra for a family of DPA-linked hairpins in which a single G-C base pair is separated from DPA by a variable number of A-T base pairs recently provided evidence for both the formation of G+. as hole trap and the adenine polaron (An+.) as hole carrier.11 Another attractive feature of the DPA chromophore is its rigid-rod geometry and excellent match to the dimensions of the DNA base pair, which result in the formation of stable DPA-


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linked hairpins.15 In this respect, it resembles Sd which is known to form stable mini-hairpins.16 The solution 1H NMR structure of a Sd-linked mini-hairpin possessing 3 G-C base pairs (Sd-G3) has been reported.17 This hairpin and its analog having 3 A-T base pairs have CD spectra consistent with B-DNA structures and UV spectra consistent with stacked purine bases.16 The CD and UV evidence for base paired structures for the lower homologs G2-Sd-C2 and A2-Sd-T2 is suggestive but not convincing, and the CD and UV spectra of G-Sd-C and A-Sd-T by themselves own provide no evidence base-paired structures.

Chart 1. Structures for (a) the DPA-Linked Mini-Hairpins and (b) Longer Hairpins used for Purposes of Comparison

It occurred to us that femtosecond transient absorption (fsTA) and/or stimulated Raman spectroscopy (FSRS) might prove to be sensitive methods for investigating the presence of basepaired vs. non-base-paired ground state conformations of DPA-linked mini-hairpin. That is, charge separation and charge recombination are expected to be more rapid for base-paired conformations in which the DPA chromophore is π-stacked with the adjacent base pair than for extended conformations in which DPA and the adjacent purine base are separated by one or more water molecules. Furthermore, unlike UV and CD, fsTA and FSRS do not require the


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presence of two or more stacked bases for the observation of exciton coupling. We report here an investigation of the UV and CD spectra and femtosecond transient absorption and Raman spectroscopy of mini-hairpins possessing a DPA linker and 1, 2, or 3 A-T or G-C base pairs (Chart 1, A1-3 and G1-3). Several longer hairpins have also been prepared for purposes of comparison of their transient spectra with those of the mini-hairpins. As expected, the UV and CD spectra of A3 and G3 are similar to those of the corresponding Sd-linked mini-hairpins.16-17 fsTA proves to be a powerful tool for distinguishing between base-paired and extended conformations of the mini-hairpins as well as for determining the dependence of charge separation and charge recombination dynamics on choice of purine base and the extent of πstacking. Materials and Methods Diphenylacetylene-4,4'-dicarboxylic acid was prepared and converted to its N,N'-dihydroxypropylamide (DPA, Chart 1) as previously described.11 The dihydroxypropylamide linker was incorporated into the hairpins in Chart 1 by the method of Letsinger and Wu.18 The hairpins were purified to a single peak (>98%) by reverse phase HPLC and characterized by MALDITOF mass spectrometry, (Table S1), UV and CD spectrometry (Figures 1 and 2). All spectroscopic studies were conducted at room temperature (23 oC, except as noted) in 10 mM phosphate buffer, with added 0.1M NaCl, pH ~7.2. For UV and CD spectra absorbance at 330 nm in a 1 cm cuvette was adjusted to 0.16-0.17 O.D. For transient absorption and Raman spectra absorbance in a 2 mm cuvette at 330 nm was also 0.16-0.17. Femtosecond transient absorption (fsTA) spectra were obtained using an apparatus reported previously.19 Samples were prepared in 2 mm cuvettes and excited with a 0.7 µJ laser pulse at 330 nm using a commercial non-collinear optical parametric amplifier (TOPAS-White, Light-


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Conversion LLC). Samples were stirred to reduce the effects of local heating and sample degradation.

Femtosecond stimulated Raman spectroscopy (FSRS) was performed using a

Ti:sapphire based apparatus previously described.20 The spectra are acquired after exciting DPA with a 330 nm actinic pump and using a 575 nm Raman pump on resonance with the G+. absorption. Methods for analysis of the transient spectroscopic data are described in Supporting Information. Results and Discussion The DPA-linked hairpins were prepared, purified, and characterized as described in the Methods and Materials section.11 The UV spectra of the A1-3 and G1-3 hairpins are shown in Figure 1a and 1b, respectively. The spectra of A2-3 and G2-3 display DPA vibronic maxima at 312 and 327 nm; whereas, the spectra of A1 and G1 display maxima at 308 nm and shoulders around 323 nm.

The UV spectra also have maxima or shoulders at shorter wavelengths

attributed to the base pairs. In the case of A1-3 there are small blue shifts in the shorterwavelength maxima upon addition of the second and third A-T base pairs (ca. 2 nm and 1 nm, respectively). The larger effect of the second vs. third base pair is consistent with the requirement of two stacked purines for the occurrence of exciton coupling and for stronger coupling between nearest neighbors than for second nearest neighbors.21 The short-wavelength bands for G1-3 (Figure 1b) resemble those of the analogous stilbenediether (Sd)-linked hairpins in that the maximum for G1 is not resolved.17 The blue shift upon addition of a third G-C base pair is the same as for A3.


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0.3

Absorbance (au)

0.3

(a)

(b)

A1 A2 A3

0.2

G1 G2 G3

0.2

0.1

0.1

0.0 200

250

300

250

350

Wavelength (nm)

300

0.0 400

350

Wavelength (nm)

Figure 1. UV spectra of hairpins (a) A1-3 and (b) G1-3 at 23 oC in aqueous buffer.

3 2

(a)

(b)

1

A1 A2 A3

G1 G2 G3

2 1

0

0

-1

-1 -2

-2 200

θ (mdeg)

θ (mdeg)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


250

300

350

Wavelength (nm)

250

300

350

-3 400

Wavelength (nm)

Figure 2. Circular dichroism spectra of hairpins (a) A1-3 and (b) G1-3 at 23 oC in aqueous buffer. The CD spectra of the A1-3 and G1-3 hairpins are shown in Figure 2a and 2b, respectively. The spectra of A2-3 resemble those of the corresponding Sd-linked hairpins; however the spectra of G2-3 do not do so.16-17 Reduction of the number of base pairs results in significant changes in


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the CD spectra which are most pronounced for A1 and G1, for which exciton coupling between stacked bases cannot occur. The strongest features in the spectrum of G1 resemble those of dGMP; whereas there are no strong features in the spectra of either A1 or dAMP.22 The CD spectra of A2-3 and G2-3 recorded at 0 oC and 23 oC are compared in Figure S1 and show only minor differences.

This indicates that these hairpins exist predominantly in base-paired

conformations at room temperature and 0 oC. CD spectra provide no information about the conformation of A1 or G1. The solution 1H NMR structure of the Sd-linked hairpin having three G-C base pairs shows it to have a slightly overwound B-DNA conformation with minimal endfraying.17 We assume that G3 and A3 have conformations similar to that of the Sd-linked hairpin. The fsTA spectra of hairpins A1-3 and G1-3 were obtained as previously described.11 The broad band spectra (440-1400 nm) of A2 and G2 and the expanded short wavelength region of the spectra of G1 and G3 are shown in Figure 3 and the broad-band spectra of A1-3, G1-3 are shown in Figure S2. The spectra of A1-3 are essentially the same, other than their charge recombination times. At short times they display a single band at 525 nm assigned to

1*

DPA

which is formed during the ca. 250 fs instrument response function (IRF) and decays within several ps accompanied with the formation of a band at 500 nm having a shoulder at 475 nm and a broad, long-wavelength band at 1130 nm. The two successor bands are assigned to DPA-..11 The kinetic Scheme 2a is proposed to account for the time-dependent transient absorption spectra of A1-3 based on singular value decomposition (SVD) global fitting. The resulting kinetic plots and species associated spectra (SAS) shown in Figures S3-S5 and time constants for charge separation and charge recombination are reported in Table 1. The values for τcs for A1-3 are the same within the experimental error, as is also the case for the longer hairpin A6.11 The values of


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τcs for hairpin AGA5 and AG3A3 (Figure S9) which have an AG purine base sequence are somewhat shorter, indicative of faster hole injection (Table 1).

Scheme 2. Mechanisms for photoinduced hole injection and charge recombination from singlet DPA to adjacent A-T and G-C base pairs in folded conformations of (a) A1-A3 and (b) G1-G3 and in the extended conformation of G1. Neighboring ground state purine shown in red.

The values of τcr for A1-3 increase upon the addition of each A-T base pair, indicative of hole delocalization within the A-tract. The value of τcr for A3 is the same as that previously reported for A6.11 One notable difference between the transient spectra of A3 and A6 is the absence in the former of a broad absorption band at 565 nm attributed to the A polaron (An+.). Plausibly, the number of stacked adenines in A3 is too small to support polaron formation.11 The values of τcr for AGA5 and AG3A3 are an order of magnitude shorter than that for A3 or A6 and faster even than for A1. This is consistent with the hole in the AG hairpins residing predominantly on G,23


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resulting in a shorter distance and/or smaller free energy for charge recombination than for the

∆A x 103

80

(a)

60

A2

40

0.2 ps 1 ps 2 ps 5 ps 10 ps 20 ps 50 ps

100 ps 200 ps 500 ps 1 ns 2 ns 5 ns 7 ns

0.2 ps 1 ps 2 ps 5 ps 10 ps 20 ps 50 ps

(c) G2

100 ps 200 ps 0.04 500 ps 1 ns 0.03 2 ns 5 ns 7 ns

0.02

20

0.01

0

0.00 1000 1200

500 600 700

Wavelength (nm) 100

(b) G1

0.1 ps 1 ps 2 ps 5 ps 10 ps 20 ps 50 ps

75

1000 1200 1400

Wavelength (nm) 100 ps 200 ps 500 ps 1000 ps 2000 ps 5000 ps 7500 ps

(d)

0.2 ps 1 ps 2 ps 5 ps 10 ps 20 ps 50 ps

G3

50

100 ps 200 ps 0.03 500 ps 1 ns 2 ns 0.02 5 ns 7 ns

∆A x 103

500 600 700

125

∆A x 103

A-tract hairpins.

∆A x 103

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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0.01

25

0.00

0 500

600

700

Wavelength (nm)

450

500

550

600

650

700

Wavelength (nm)

Figure 3. Femtosecond transient absorption spectra for hairpins (a) A2, (b) G1, (c) G2 and (d) G3 in aqueous buffer at the indicated delay times following a 330 nm laser pump pulse in aqueous solution (note different wavelength scale for A2 and G2 vs. G1 and G3).


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Table 1. Charge separation and charge recombination times for hairpins A1-A3 and G1-G3 from the current study and for related hairpins. Conjugate

τcs, ps

τcr, ps

A1

2.7 ± 0.24

830 ± 190

A2

2.8 ± 0.52

1100 ± 160

A3

3.2 ± 0.14

2500 ± 150

A6a

2.8

2500

AGA5a

1.6

130

AG3A3

1.7 ± 0.01 b

300 ± 8.0

0.33 ± 0.01 b G1

(340 ± 40) c

16.0 ± 0.8

G2

0.25 ± 0.02 b

21.0 ± 0.7

G3

0.23 ± 0.03 b

24.0 ± 0.9

a

Data from ref 11. b The error of the instrument is ~ 0.2 ps and is the minimum possible error regardless of smaller errors calculated. c Value in parentheses assigned to 1*DPA in extended conformation of G1. Uncertainties represent the standard error of the fit; the resolution of the instrument is ~ 0.2 ps and is the minimum possible error regardless of smaller errors calculated.

The fsTA spectra of G2 and G3 (Figure 3c,d) resemble those of A2 and A3 (Figure 3a and Figure S2) aside from the more rapid conversion of the 525 nm

1*

DPA band to the short- and

long-wavelength DPA-. bands. SVD global fits according to Scheme 2b provide the SAS (Figure S6 and S7) and the rate constants reported in Table 1. In the case of G1 (Figures S2 and S8), the transient spectra display a persistent 525 nm shoulder that is absent in the spectra of G2 and G3 (Figure 3c and Figure S2). The 525 nm single wavelength decay of 1*DPA for G1 is best fit as a biexponential with a fast component similar to those of G2 and G3 and a slow component similar to that that of the DPA linker diol singlet state in methanol ( 340 vs. 350 ps).16 Since


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there is no slow component of DPA-. formation or decay, we attribute the slow component of 1*

DPA decay to the non-radiative decay of extended ground state conformations of G1 which do

not undergo photoinduced electron transfer (Scheme 2b). Observation of dual exponential decay for singlet G1 but not for A1 appears to be inconsistent with the stronger hydrogen bonding expected for a G-C vs. A-T base pair.24 Furthermore, the intrinsic solubility of adenine in pH 7 phosphate buffer at 25 oC is an order of magnitude larger than that of guanine.25 The π-stacking interaction of the A-T base pair with DPA may be stronger than that of the G-C base pair; however, no information is available concerning the relative strength of these hydrophobic interactions. In addition to the strong 500 nm band and 475 nm shoulder the short-wavelength region of the fsTA spectra of G3 displays a band at 575 nm (Figure 3d). We have previously observed a 575 nm band in the transient spectra of the hairpins GA6 and AGA5.11 The FSRS data supports the assignment of these bands to the guanine cation radical, G+.. The stronger 575 nm band for G3 than for G2 is consistent with the essential role of terminal base pairs in stabilizing mini-hairpins and in delocalizing the positive charge on an adjacent purine. We previously reported that the FSRS spectra for DPA-linked hairpins display transient bands at 1125, 1600, and 2105 cm-1 characteristic of DPA-..11, 26 In addition, hairpins GA6 and AGA5 display transient Raman bands at 1260 and 1565 cm-1 similar to the frequencies calculated by Sevilla et al. for G+..27 The FSRS data for hairpins G3 and AG3A3 shown in Figure 4a and 4b, respectively, and G1 and G2 (Figure S10) all have strong DPA-. Raman bands, but G+• bands that are either weak or absent. The weak Raman bands for G+. may be attributed to rapid solvent relaxation or proton transfer following charge separation in the case of G1 and to delocalization of the hole over two or three guanines in the case of G2 or G3. Stacking of chromophores is known to result in loss of


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intensity as well as frequency shifts in the vibrational spectra of neutral chromophores and their radical ions.28-29 The FSRS for A1-A3 (Figure S11) also display strong bands for DPA-. but not for A+., as was the case in our previous study of DPA-linked hairpins.11

1.5

G3 (a)

-1 ps 1 ps 5 ps 20 ps 50 ps 200 ps

1

AG3A3

(b)

0.5

0.0

0 1000

-1 ps 1 ps 5 ps 20 ps 200 ps 1 ns

1.0

∆Gain (%)

2

∆Gain (%)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


1200

1400

1600

1800

2000

2200

1000

-1

1200

1400

1600

1800

2000

2200

-1

Raman Shift (cm )

Raman Shift (cm )

Figure 4. FSRS spectra of hairpins (a) G3 and (b) AG3A3 in aqueous solution acquired with a 575 nm Raman pump following 330 nm excitation. Conclusions In summary, we have investigated the dynamics of charge separation and charge recombination in mini-hairpins possessing three or fewer base pairs connected by a chromophore linker (Chart 1). Global analysis of the fsTA spectra for hairpins possessing two or three A-T or G-C base pairs and a DPA linker is consistent with the simple kinetic scheme shown in Scheme 2a according to which the hairpins exist predominantly in base paired conformations. The same conclusion applies to the minimal conjugate A1 which possesses a single A-T base pair. Thus hairpins A1-3 and A6 have similar charge separation times indicative of the formation of DPA-•/A+• contact radical ion pairs following absorption of UV light by the DPA chromophore. Replacement of the second A by guanine results in somewhat faster charge separation, as a result of stabilization of A+• by a neighboring G. Charge recombination times increase as the size of


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the hairpin increases from A1 to A3; however, no further increase is observed for A6. Plausibly A+• can delocalize over the first few adenines; however the extent of delocalization is limited by Coulomb attraction to DPA-•. The broad weak absorption characteristic of the (An+•) polaron is not observed in the fsTA spectra of A1-3.11, 23 Unlike A1, the transient absorption spectra of G1 are not consistent with a single base-paired ground state conformation, but rather the presence of base-paired and open conformations (Scheme 2b). This results in both fast and slow decay of the 1*

DPA singlet state, the fast component of having a value of τcs similar to that for G2 and the

slow component similar to that for the hairpin linker. Fast charge recombination for the G1-3 charge separated states (Table 1) is consistent with fast charge delocalization within the oxidized G-tract. The fsTA spectra of G2 and G3 display the 575 nm band that is the signature of the short-lived G+• cation radical.11 ASSOCIATED CONTENT Supporting Information Conjugate mass spectral data, femtosecond transient absorption spectra and data analysis, femtosecond stimulated Raman spectra. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Authors [email protected] [email protected] The authors declare no competing financial interests.


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ACKNOWLEDGMENT This research was funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division under Awards DEFG02-96ER14604 (F.D.L.) and DE-FG02-99ER14999 (M.R.W). References (1) Lewis, F. D. Distance-Dependent Electronic Interactions across DNA Base Pairs. Charge Transport, Exciton Coupling, and Energy Transfer. Israel J. Chem. 2013, 53, 350-365. (2) Kawai, K.; Majima, T. Hole Transfer Kinetics of DNA. Acc. Chem. Res. 2013, 46, 26162625. (3) Renaud, N.; Berlin, Y. A.; Lewis, F. D.; Ratner, M. A. Between Superexchange and Hopping: An Intermediate Charge-Transfer Mechanism in Poly(A)-Poly(T) DNA Hairpins. J. Am. Chem. Soc. 2013, 135, 3953-3963. (4) Zhang, Y.; Liu, C.; Balaeff, A.; Skourtis, S. S.; Beratan, D. N. Biological Charge Transfer via Flickering Resonance. Proc. Nat. Acad. Sci. USA 2014, 111, 10049-10054. (5) Young, R. M.; Singh, A. P. N.; Thazhathveetil, A. K.; Cho, V. Y.; Zhang, Y.; Renaud, N.; Grozema, F. C.; Beratan, D. N.; Ratner, M. A.; Schatz, G. C. et al. Charge Transport across DNA-Based Three-Way Junctions. J. Am. Chem. Soc. 2015, 137, 5113-5122. (6) Zhang, Y.; Young, R. M.; Thazhathveetil, A. K.; Singh, A. P. N.; Liu, C.; Berlin, Y. A.; Grozema, F. C.; Lewis, F. D.; Ratner, M. A.; Renaud, N. et al. Conformationally Gated Charge Transfer in DNA Three-Way Junctions. J. Phys. Chem. Lett. 2015, 6, 2434-2438. (7) Choi, J.; Park, J.; Tanaka, A.; Park, M. J.; Jang, Y. J.; Fujitsuka, M.; Kim, S. K.; Majima, T. Hole Trapping of G-Quartets in a G-Quadruplex. Angew. Chem. Internat. Ed. 2013, 52, 11341138.


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(8) Thazhathveetil, A. K.; Harris, M. A.; Young, R. M.; Wasielewski, M. R.; Lewis, F. D. Efficient Charge Transport via DNA G-Quadruplexes. J. Am. Chem. Soc. 2017, 139, 1730-1733. (9) Choi, J.; Tanaka, A.; Cho, D. W.; Fujitsuka, M.; Majima, T. Efficient Electron Transfer in i-Motif DNA with a Tetraplex Structure. Angew. Chem. Internat. Ed. 2013, 52, 12937-12941. (10) Gorczak, N.; Fujii, T.; Mishra, A. K.; Houtepen, A. J.; Grozema, F. C.; Lewis, F. D. Mechanism and Dynamics of Electron Injection and Charge Recombination in DNA. Dependence on Neighboring Pyrimidines. J. Phys. Chem. B 2015, 119, 7673-7680. (11) Harris, M. A.; Mishra, A. K.; Young, R. M.; Brown, K. E.; Wasielewski, M. R.; Lewis, F. D. Direct Observation of the Hole Carriers in DNA Photoinduced Charge Transport. J. Am. Chem. Soc. 2016, 138, 5491-5494. (12) Renaud, N.; Harris, M. A.; Singh, A. P. N.; Berlin, Y. A.; Ratner, M. A.; Wasielewski, M. R.; Lewis, F. D.; Grozema, F. C. Deep-Hole Transfer Leads to Ultrafast Charge Migration in DNA Hairpins. Nat. Chem. 2016, 8, 1015-1021. (13) Lewis, F. D.; Liu, X.; Miller, S. E.; Hayes, R. T.; Wasielewski, M. R. Dynamics of Electron Injection in DNA Hairpins. J. Am. Chem. Soc. 2002, 124, 11280-11281. (14) Takada, T.; Kawai, K.; Fujitsuka, M.; Majima, T. High-Yield Generation of a Long-Lived Charge-Separated State in Diphenylacetylene-Modified DNA. Angew. Chem., Internat. Ed. 2006, 45, 120-122. (15)

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Dynamics of Charge Injection and Charge Recombination in DNA Mini

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