This journal is c the Owner Societies 2011 Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 6145 Cite this: Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 Photodynamical simulations of cytosine: characterization of the ultrafast bi-exponential UV deactivationw Mario Barbatti,* ab Ade´lia J. A. Aquino, ac Jaroslaw J. Szymczak,z a Dana Nachtigallova´ d and Hans Lischka* a Received 27th July 2010, Accepted 27th January 2011 DOI: 10.1039/c0cp01327g Deactivation of UV-excited cytosine is investigated by non-adiabatic dynamics simulations, optimization of conical intersections, and determination of reaction paths. Quantum chemical calculations are performed up to the MR-CISD level. Dynamics simulations were performed at multiconfigurational level with the surface hopping method including four electronic states. The results show the activation of four distinct reaction pathways at two different subpicosecond time scales and involving three different conical intersections. Most trajectories relax to a minimum of the S 1 state and deactivate with a time constant of 0.69 ps mainly through a semi-planar conical intersection along the n O p* surface. A minor fraction deactivate along pp* regions of the S 1 surface. Sixteen percent of trajectories do not relax to the minimum and deactivate with a time constant of only 13 fs. 1. Introduction Upon UV excitation, the five naturally occurring nucleobases return to the ground state by internal conversion at an ultrafast time scale ranging from half a picosecond to few picoseconds. 1–5 In general, ultrafast decay depends on the existence of reaction pathways connecting the Franck–Condon region to the seam of conical intersections between the excited and ground states where radiationless processes can occur. The characterization of these pathways has led to a large amount of theoretical work not only for the five nucleo- bases, 1–14 but also for their isomers, 6,15 substituted species, 7,16,17 and base models. 18,19 Significant progress has been achieved with photodynamical simulations, 20–22 which describe the excited-state time evolution and the most accessed reaction pathways explicitly. Excited-state dynamics simulations are still a major challenge in computational chemistry requiring a proper description of multiple electronic excited states and their non-adiabatic couplings. At the same time, they should keep computational costs under strict control as to allow dynamics propagation for thousands of femtoseconds. Despite the difficulties, ab initio 21–25 and semiempirical 20,26–31 non-adiabatic dynamics simulations have been recently reported for all nucleobases. In the gas phase, the excited-state lifetime of cytosine measured by different groups present somewhat divergent results. Kang et al. 32 (pump: 267 nm; probe: 800 nm) reports a single time constant decay of 3.2 ps. Canuel et al. 33 (pump: 267 nm; probe: 2 400 nm) reports two time constants, 0.16 ps and 1.86 ps. Ullrich et al. 34 (pump: 250 nm; probe: 200 nm) distinguishes three time constants, a very fast decay occurring in less than 0.05 ps, another component of 0.82 ps and a third component of 3.2 ps. Recently, Kosma and co-workers have shown that the excited-state lifetime strongly depends on the excitation wavelength, varying from 3.8 ps to 1.1 ps for pump wavelengths spanning the range from 260 to 290 nm. 35 In common, all these sets of results indicate that cytosine relaxation takes place within one to three picoseconds after the excitation. Additionally, Ullrich et al. 34 have measured the time dependent photoelectron spectra of cytosine and other nucleobases in gas phase. The comparison between the pyrimidine bases cytosine, uracil and thymine clearly indicates that cytosine deactivates in a distinct way producing more energetic photoelectrons. As typical for species deactivating by internal conversion, cytosine fluorescence quantum yield is very small in neutral a Institute for Theoretical Chemistry, University of Vienna, Waehringerstrasse 17, A 1090 Vienna, Austria. E-mail: Mario [email protected], Hans [email protected]b Max-Planck-Institut fu ¨r Kohlenforschung, Kaiser-Wilhelm-Platz 1, D-45470 Mu ¨lheim an der Ruhr, Germany c Institute of Soil Research, University of Natural Resources and Applied Life Sciences Vienna, Peter-Jordan-Straße 82, A-1190 Vienna, Austria d Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Flemingovo nam. 2, CZ-16610 Prague 6, Czech Republic w Electronic supplementary information (ESI) available: Experimental time constants, conical intersection notations, molecular orbitals, geometries and pathways at CASSCF level, Cartesian coordinates. See DOI: 10.1039/c0cp01327g z Present address: Department of Chemistry, University of Basel, Klingelbergstrasse 80, 4056 Basel, Switzerland. PCCP Dynamic Article Links www.rsc.org/pccp PAPER Downloaded by Texas Technical University on 04 May 2011 Published on 24 February 2011 on http://pubs.rsc.org | doi:10.1039/C0CP01327G View Online
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This journal is c the Owner Societies 2011 Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 6145
Photodynamical simulations of cytosine: characterization of the ultrafast
bi-exponential UV deactivationw
Mario Barbatti,*ab
Adelia J. A. Aquino,ac
Jaroslaw J. Szymczak,zaDana Nachtigallova
dand Hans Lischka*
a
Received 27th July 2010, Accepted 27th January 2011
DOI: 10.1039/c0cp01327g
Deactivation of UV-excited cytosine is investigated by non-adiabatic dynamics simulations,
optimization of conical intersections, and determination of reaction paths. Quantum chemical
calculations are performed up to the MR-CISD level. Dynamics simulations were performed at
multiconfigurational level with the surface hopping method including four electronic states.
The results show the activation of four distinct reaction pathways at two different subpicosecond
time scales and involving three different conical intersections. Most trajectories relax to a
minimum of the S1 state and deactivate with a time constant of 0.69 ps mainly through a
semi-planar conical intersection along the nOp* surface. A minor fraction deactivate along pp*regions of the S1 surface. Sixteen percent of trajectories do not relax to the minimum and
deactivate with a time constant of only 13 fs.
1. Introduction
Upon UV excitation, the five naturally occurring nucleobases
return to the ground state by internal conversion at an
ultrafast time scale ranging from half a picosecond to few
picoseconds.1–5 In general, ultrafast decay depends on the
existence of reaction pathways connecting the Franck–Condon
region to the seam of conical intersections between the excited
and ground states where radiationless processes can occur.
The characterization of these pathways has led to a large
amount of theoretical work not only for the five nucleo-
bases,1–14 but also for their isomers,6,15 substituted species,7,16,17
and base models.18,19 Significant progress has been achieved
with photodynamical simulations,20–22 which describe the
excited-state time evolution and the most accessed reaction
pathways explicitly.
Excited-state dynamics simulations are still a major
challenge in computational chemistry requiring a proper
description of multiple electronic excited states and their
non-adiabatic couplings. At the same time, they should keep
computational costs under strict control as to allow dynamics
propagation for thousands of femtoseconds. Despite the
difficulties, ab initio21–25 and semiempirical20,26–31 non-adiabatic
dynamics simulations have been recently reported for all
nucleobases.
In the gas phase, the excited-state lifetime of cytosine
measured by different groups present somewhat divergent
results. Kang et al.32 (pump: 267 nm; probe: 800 nm) reports
a single time constant decay of 3.2 ps. Canuel et al.33 (pump:
267 nm; probe: 2 � 400 nm) reports two time constants, 0.16 ps
and 1.86 ps. Ullrich et al.34 (pump: 250 nm; probe: 200 nm)
distinguishes three time constants, a very fast decay occurring
in less than 0.05 ps, another component of 0.82 ps and a third
component of 3.2 ps. Recently, Kosma and co-workers have
shown that the excited-state lifetime strongly depends on the
excitation wavelength, varying from 3.8 ps to 1.1 ps for pump
wavelengths spanning the range from 260 to 290 nm.35
In common, all these sets of results indicate that cytosine
relaxation takes place within one to three picoseconds after the
excitation. Additionally, Ullrich et al.34 have measured the
time dependent photoelectron spectra of cytosine and other
nucleobases in gas phase. The comparison between the pyrimidine
bases cytosine, uracil and thymine clearly indicates that
cytosine deactivates in a distinct way producing more energetic
photoelectrons.
As typical for species deactivating by internal conversion,
cytosine fluorescence quantum yield is very small in neutral
a Institute for Theoretical Chemistry, University of Vienna,Waehringerstrasse 17, A 1090 Vienna, Austria.E-mail: Mario [email protected],Hans [email protected]
bMax-Planck-Institut fur Kohlenforschung,Kaiser-Wilhelm-Platz 1, D-45470 Mulheim an der Ruhr, Germany
c Institute of Soil Research, University of Natural Resources andApplied Life Sciences Vienna, Peter-Jordan-Straße 82,A-1190 Vienna, Austria
d Institute of Organic Chemistry and Biochemistry,Academy of Sciences of the Czech Republic, Flemingovo nam. 2,CZ-16610 Prague 6, Czech Republic
w Electronic supplementary information (ESI) available: Experimentaltime constants, conical intersection notations, molecular orbitals,geometries and pathways at CASSCF level, Cartesian coordinates.See DOI: 10.1039/c0cp01327gz Present address: Department of Chemistry, University of Basel,Klingelbergstrasse 80, 4056 Basel, Switzerland.
This journal is c the Owner Societies 2011 Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 6149
that, cytosine should present other S0/S1 crossings for NH
stretching and CN ring opening. The intersection along the
NH stretching should occur by a crossing between the p3s andthe closed shell states.82 Because of its high vertical excitation
energy, the p3s state in cytosine is not expected to play a
relevant role in the photodynamics following excitation into
the first pp* state. In the case of the ring-opening conical
intersections, their activation usually involves the overcoming
of high energy barriers.83 Dynamics simulations will also show
that they also do not play any role in the deactivation of
cytosine excited into the first absorption band.
The geometries of the MXSs optimized at the MR-CISD
level are rather similar to the ones optimized at the CASSCF
level (Table 3). The differences are, however, large enough
to change the conformation classification. Thus, while the
oop-NH2 MXS has a 3S4 conformation at the CASSCF level,
it has an envelope 3E at the MR-CISD level, which implies a
smaller degree of C4 puckering. Similarly, the puckering of the
N1 atom in C6-puckered MXS decreases when it is optimized
at the MR-CISD level. Because of this, the conformation
changes from 6S1 to6E.
The energetic order of the MXSs also changes at the
MR-CISD level, although the state character remains
the same as in CASSCF (Table 2). At MR-CISD + Q level,
the semi-planar MXS is destabilized by about 0.6 eV while
the C6-puckered is stabilized by about 0.3 eV in comparison
to the CASSCF level. Because of this, the energetic order
is altered and the oop-NH2 and C6-puckered MXSs appear
first with very close energies followed by the semi-planar at
higher energy. The implications of this change will be
discussed later. (Note that because the MXSs were optimized
at the MR-CISD level and the energies were computed at
the MR-CISD+Q level, there is a small energy split between
S0 and S1.)
Table 2 Vertical excitation energies (eV), energies at the S1 minimum and at the S1/S0 MXSs for cytosine obtained with CASSCF and MR-CISDmethods. Values with Davidson correction are given in parentheses. cs—closed shell
a E0 = �392.671177 au. b E0 = �393.153516 au. c E0 = �393.234586 au.
Fig. 3 Geometry of four minima on the S1/S0 crossing seam of
cytosine optimized at MR-CISD level. Geometries optimized at
CASSCF level are shown in the Supplementary Information.
Table 3 Characterization of the S1/S0 minima on the crossing seamoptimized at CASSCF and MRCI levels in terms of the Cremer-Popleparameters Q (A), y (1), and f (1) and of selected bond distances (A)
This journal is c the Owner Societies 2011 Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 6151
conical intersection. As it has been discussed by Blancafort42
the differences between barriers along CASSCF pathways and
pathways computed at higher levels, in this case CASPT2, are
of about 0.2 eV, which are in the accuracy limit of not only
CASSCF but also of most of the other methods.
3.2 Dynamics results
Fig. 6 shows the time evolution of the occupation of each
adiabatic state. At time zero, cytosine is in the pp* state, whoseintensity is distributed as 29% to S1, 61% to S2 and 10% to S3(see discussion about initial conditions in the ‘‘Computational
details’’ section). Non-adiabatic events take place already in
the first 10 fs. S2, the initially most strongly occupied state,
transfers part of the population to S1 and to S3, reflecting the
exchange of the diabatic character of the three states. S3 is
quickly depopulated within 20 fs. The occupation of the first
excited state reaches a maximum of about 60% in 20 fs and
remains oscillating around this level during the first 100 fs.
After 100 fs, the transfer to the ground state is intensified.
The ground state is populated bi-exponentially. Its
occupation can be fitted with the three-parameter function:
f2(t) = 1 � a exp(�t/t1) � (1 � a)exp(�t/t2),
where t is the time and t1 and t2 are the two time constants.
The amplitude a is the fraction of the initial excited state
population following the pathways with time constant t1,while (1 � a) is the fraction following the pathways with t2.The fitting procedure results in a very fast t1 = 13 fs decay
component followed by a = 16% of the population and a
slower t2 = 0.7 ps component followed by (1 � a) = 84% of
the population (Table 4). This gives an average lifetime of
hti = at1 + (1 � a)t2 = 0.58 ps.
In this analysis, we assumed that trajectories that were still
in the excited state at the end of the simulation (1.2 ps) should
deactivate within the exponential decay t2. An alternative
interpretation is that these trajectories are not part of the
second exponential decay and they will deactivate with a
longer time constant. In this case, the ground state population
6152 Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 This journal is c the Owner Societies 2011
The trajectories that remained in the excited state after this
first encounter with S0 were transferred to the nOp* state
within the next 100 fs. They relaxed to the energy minimum
of this state and remained there for an average time of about
0.6 ps before being finally deactivated. During this time,
small energy gaps to the ground state often occurred. The
non-adiabatic transition probability is small enough to
guarantee that multiple of such encounters occur without
returning to the ground state. The reason for this rests on
the shape of the potential energy surface in the region between
the S1 minimum and the semi-planar conical intersection. The
sloped conical intersection is reached in an up-hill motion,
which decreases the efficiency of the non-adiabatic transitions.
Because of this, other pathways to the ground state through
pp*/cs conical intersections (oop-NH2 and C6-puckered
conical intersections) start to compete with the nOp*/cspathway. As discussed in section ‘‘Reaction paths,’’ the
activation of the pp*/cs pathways starting from the nOp*minimum depends on overcoming energetic barriers to the
biradical pp* states. When this is achieved, the conical inter-
section to the ground state can be easily accessed because of its
peaked shape and the internal conversion occurs quickly,
usually in less than 100 fs after the barrier is overcome.
The occurrence of a conical intersection with the ground
state as soon as 10 fs after the photoexcitation is an unexpected
feature for a large molecule like cytosine. It is certainly one of
the fastest internal conversion processes among organic
molecules, even faster than the exceptionally fast decay of
ethylene whose lifetime is about 38 fs.84 To check whether this
was not an artifact of the CASSCF method induced by
artificially large energy gradients in the Franck–Condon
region, we have simulated the initial relaxation of cytosine
with dynamics simulations performed with the RI-CC2/SVP
method. Exactly as predicted at CASSCF level, all CC2
trajectories moved into the semi-planar S1/S0 crossing within
about 10 fs. The average potential energy over all trajectories
plotted as a function of time is shown in Fig. 8. This figure also
shows the shortening of the C2-N3 bond length in the beginning
of the dynamics typical for the semi-planar conical intersection.
3.3 Photophysics of cytosine
Fig. 9 schematically illustrates our main findings concerning
the photodynamics of cytosine excited into the first singlet pp*
Table 4 Time constants for cytosine relaxation after UV excitation in gas phase. SH—surface hopping; MS—multiple spawning. Results fromref. 35 are those for pump wavelength 280 nm, which has the closest correspondence to the spectral region excited in the present work
a Bi-exponential fitting: a = 0.16, (1 � a) = 0.84. b Tri-exponential fitting: a1 = 0.13, a2 = 0.74, (1 � a1 � a2) = 0.13.
Table 5 Main conical intersections accessed for S1/S0 deactivation. Conical intersection energies computed at same level as the dynamicssimulations are given in parentheses. SH—surface hopping; MS—multiple spawning; nr—not reported
6154 Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 This journal is c the Owner Societies 2011
CASSCF(2,2) multiple spawning simulations, the C6-puckered
was the unique conical intersection observed in the OM2
surface hopping simulations (Table 5).
The remaining 17% of trajectories did not deactivate within
the 1.2 ps simulation time. They may still be part of the t2exponential decay or at least a fraction of them may decay
with a third and longer time constant of 3 ps. The duration
of our dynamics simulation is not sufficiently extended to
distinguish between the two possibilities. If the longer decay
time constant is assumed, the previous discussion is still valid,
but the numerical values for the time constants are slightly
modified to t1 = 9 fs and t2 = 0.53 ps (Table 4).
Different from our results, the analysis of reaction pathways
performed in ref. 42 at CASPT2 level disfavored the
semi-planar intersection and indicated a dominance of the
C6-puckered and oop-NH2 conical intersections. However,
comparison of the energy of the semi-planar conical inter-
section not only with present results based on full optimiza-
tion, but also with those of other CASPT2 and MRCI
investigations44,46 shows that the semi-planar structure is
probably computed too high in energy in ref. 42.
The different results obtained by several simulations are
expression of the discrepancies between the potential energy
surfaces computed at diverse levels. All of them predict
internal conversion occurring in sub-picosecond time scale
but with different populations of each deactivation pathway.
The CAS(2,2) employed in the multiple spawning dynamics is
likely a too small space to adequately describe the potential
energy surfaces of cytosine and it should be especially taken
with care for the description of the three state region of the
crossing seam, leading to a underestimation of the role of the
semi-planar conical intersection. Nevertheless, similar to our
results, it predicts a dominant trend of relaxation to the S1minimum from where cytosine escapes to different conical
intersections. In the case of the OM2 method, the lack of
activation of different conical intersections in any proportion
may be an indication of an overstabilization of the pathway
leading to the C6-puckered conical intersection. In comparison
to our results, a qualitatively different mechanism is predicted,
with direct deactivation along the pp* state without relaxing tothe S1 minimum. The CAS(14,10) active space used in our
simulations tends to predict the energy of the pp* state
relatively too high in comparison with the np* state. Because
of this, we believe that the proper stabilization of the pp* stateby inclusion of dynamical electron correlation should bring to
an increase of deactivation at the pp* channels.
4. Conclusions
We have investigated the photophysics of cytosine by non-
adiabatic dynamics simulations, optimization of stationary
points and conical intersections, and determination of reaction
paths. Optimizations have been performed at CASSCF and
MR-CISD levels and the dynamics simulations were performed
at CASSCF level with the surface hopping method including
four electronic states.
The results show the activation of multiple reaction
pathways in up to three different time scales, which correlates
well with the experimental results. Most of trajectories relax to
the np* S1 minimum. From this minimum, cytosine deactivates
mainly via a semi-planar conical intersection between the nOp*and the ground state in a region of the crossing seam near
a triple degeneracy. In fewer cases, it deactivates via two
different conical intersections involving crossings between
pp* states and the ground state. Dynamics of cytosine presents
a singular feature that is a semi-instantaneous internal
conversion of a minor fraction of the population within only
10 fs. The competition between reaction paths is controlled by
excited state barriers, and comparison to results of other
dynamics simulations shows that details of the potential
energy surfaces are important for the exact determination of
the role of each deactivation path.
Acknowledgements
This work has been supported by the Austrian Science Fund
within the framework of the Special Research Programs F41
(ViCoM) and of the German Research Foundation, Priority
Program SPP 1315, project No. GE 1676/1-1. This work was
part of the research project Z40550506 of the Institute of
Organic Chemistry and Biochemistry of the Academy of
Sciences of the Czech Republic. Support by the grant from
the Ministry of Education of the Czech Republic (Center for
Biomolecules and Complex Molecular Systems, LC512) and
Computer time at the Vienna Scientific Cluster (project nos.
70019 and 70151) is gratefully acknowledged.
References
1 L. Blancafort, J. Am. Chem. Soc., 2006, 128, 210.2 H. Chen and S. H. Li, J. Phys. Chem. A, 2005, 109, 8443.3 W. C. Chung, Z. G. Lan, Y. Ohtsuki, N. Shimakura, W. Domckeand Y. Fujimura, Phys. Chem. Chem. Phys., 2007, 9, 2075.
4 C. M. Marian, J. Chem. Phys., 2005, 122, 104314.5 S. Perun, A. L. Sobolewski and W. Domcke, J. Am. Chem. Soc.,2005, 127, 6257.
6 L. Serrano-Andres, M. Merchan and A. C. Borin, Proc. Natl.Acad. Sci. U. S. A., 2006, 103, 8691.
7 T. Gustavsson, A. Banyasz, E. Lazzarotto, D. Markovitsi,G. Scalmani, M. J. Frisch, V. Barone and R. Improta, J. Am.Chem. Soc., 2006, 128, 607.
8 S. Perun, A. L. Sobolewski and W. Domcke, J. Phys. Chem. A,2006, 110, 13238.
9 G. Zechmann and M. Barbatti, J. Phys. Chem. A, 2008, 112, 8273.10 M. Z. Zgierski, S. Patchkovskii, T. Fujiwara and E. C. Lim,
J. Phys. Chem. A, 2005, 109, 9384.11 N. Ismail, L. Blancafort, M. Olivucci, B. Kohler and M. A. Robb,
J. Am. Chem. Soc., 2002, 124, 6818.12 S. Matsika, J. Phys. Chem. A, 2004, 108, 7584.13 C. M. Marian, J. Phys. Chem. A, 2007, 111, 1545.14 M. Barbatti, A. J. A. Aquino, J. J. Szymczak, D. Nachtigallova,
P. Hobza and H. Lischka, Proc. Natl. Acad. Sci. U. S. A., 2010,107, 21453.
15 S. Perun, A. L. Sobolewski andW. Domcke,Mol. Phys., 2006, 104,1113.
16 L. Blancafort, B. Cohen, P. M. Hare, B. Kohler and M. A. Robb,J. Phys. Chem. A, 2005, 109, 4431.
17 S. B. Nielsen and T. I. Solling, ChemPhysChem, 2005, 6, 1276.18 M. Barbatti and H. Lischka, J. Phys. Chem. A, 2007, 111, 2852.19 J. A. Frey, R. Leist, C. Tanner, H. M. Frey and S. Leutwyler,
J. Chem. Phys., 2006, 125, 114308.20 E. Fabiano and W. Thiel, J. Phys. Chem. A, 2008, 112, 6859.21 M. Barbatti and H. Lischka, J. Am. Chem. Soc., 2008, 130, 6831.22 H. R. Hudock, B. G. Levine, A. L. Thompson, H. Satzger,
D. Townsend, N. Gador, S. Ullrich, A. Stolow andT. J. Martinez, J. Phys. Chem. A, 2007, 111, 8500.
This journal is c the Owner Societies 2011 Phys. Chem. Chem. Phys., 2011, 13, 6145–6155 6155
23 G. Groenhof, L. V. Schafer, M. Boggio-Pasqua, M. Goette,H. Grubmuller and M. A. Robb, J. Am. Chem. Soc., 2007, 129,6812.
24 H. R. Hudock and T. J. Martinez, ChemPhysChem, 2008, 9,2486.
25 J. J. Szymczak, M. Barbatti, J. T. Soo Hoo, J. A. Adkins,T. L. Windus, D. Nachtigallova and H. Lischka, J. Phys. Chem.A, 2009, 113, 12686.
26 H. Langer, N. L. Doltsinis and D. Marx, ChemPhysChem, 2005, 6,1734.
27 Y. Lei, S. Yuan, Y. Dou, Y. Wang and Z. Wen, J. Phys. Chem. A,2008, 112, 8497.
28 R. Mitric, U. Werner, M. Wohlgemuth, G. Seifert andV. Bonacic-Koutecky, J. Phys. Chem. A, 2009, 113, 12700.
29 Z. G. Lan, E. Fabiano and W. Thiel, ChemPhysChem, 2009, 10,1225.
30 Z. Lan, E. Fabiano and W. Thiel, J. Phys. Chem. B, 2009, 113,3548.
31 A. N. Alexandrova, J. C. Tully and G. Granucci, J. Phys. Chem. B,2010, 114, 12116.
32 H. Kang, K. T. Lee, B. Jung, Y. J. Ko and S. K. Kim, J. Am.Chem. Soc., 2002, 124, 12958.
33 C. Canuel, M. Mons, F. Piuzzi, B. Tardivel, I. Dimicoli andM. Elhanine, J. Chem. Phys., 2005, 122, 074316.
34 S. Ullrich, T. Schultz, M. Z. Zgierski and A. Stolow, Phys. Chem.Chem. Phys., 2004, 6, 2796.
35 K. Kosma, C. Schroter, E. Samoylova, I. V. Hertel and T. Schultz,J. Am. Chem. Soc., 2009, 131, 16939.
36 M. Daniels and W. Hauswirth, Science, 1971, 171, 675.37 J. W. Longworth, R. O. Rahn and R. G. Shulman, J. Chem. Phys.,
1966, 45, 2930.38 R. J. Malone, A. M. Miller and B. Kohler, Photochem. Photobiol.,
2003, 77, 158.39 L. Blancafort, M. J. Bearpark and M. A. Robb, in Radiation
Induced Molecular Phenomena in Nucleic Acid, ed. M. K. Shuklaand J. Leszczynski, Springer, Netherlands, 2008.
40 M. Z. Zgierski, T. Fujiwara and E. C. Lim, Chem. Phys. Lett.,2008, 463, 289.
41 K. Tomic, J. Tatchen and C. M. Marian, J. Phys. Chem. A, 2005,109, 8410.
42 L. Blancafort, Photochem. Photobiol., 2007, 83, 603.43 M. Merchan, R. Gonzalez-Luque, T. Climent, L. Serrano-Andres,
E. Rodriuguez, M. Reguero and D. Pelaez, J. Phys. Chem. B, 2006,110, 26471.
44 M.Merchan and L. Serrano-Andres, J. Am. Chem. Soc., 2003, 125,8108.
45 K. A. Kistler and S. Matsika, J. Chem. Phys., 2008, 128, 215102.46 K. A. Kistler and S. Matsika, J. Phys. Chem. A, 2007, 111, 2650.47 L. Blancafort andM. A. Robb, J. Phys. Chem. A, 2004, 108, 10609.48 A. L. Sobolewski and W. Domcke, Phys. Chem. Chem. Phys.,
2004, 6, 2763.49 J. C. Tully, Faraday Discuss., 1998, 110, 407.50 W. J. Hehre, R. Ditchfield and J. A. Pople, J. Chem. Phys., 1972,
56, 2257.51 R. Shepard, H. Lischka, P. G. Szalay, T. Kovar and M. Ernzerhof,
J. Chem. Phys., 1992, 96, 2085.52 R. Shepard, in Modern Electronic Structure Theory, ed.
D. R. Yarkony, World Scientific, Singapore, 1995, vol. 1, p.345.
53 H. Lischka, M. Dallos and R. Shepard, Mol. Phys., 2002, 100,1647.
54 H. Lischka, M. Dallos, P. G. Szalay, D. R. Yarkony andR. Shepard, J. Chem. Phys., 2004, 120, 7322.
55 M. Dallos, H. Lischka, R. Shepard, D. R. Yarkony andP. G. Szalay, J. Chem. Phys., 2004, 120, 7330.
56 W. C. Swope, H. C. Andersen, P. H. Berens and K. R. Wilson,J. Chem. Phys., 1982, 76, 637.
57 J. Butcher, J. Assoc. Comput. Mach., 1965, 12, 124.58 J. Pittner, H. Lischka and M. Barbatti, Chem. Phys., 2009, 356,
147.59 G. Granucci and M. Persico, J. Chem. Phys., 2007, 126, 134114.60 J. C. Tully, J. Chem. Phys., 1990, 93, 1061.61 S. Hammes-Schiffer and J. C. Tully, J. Chem. Phys., 1994, 101,
4657.62 D. Cremer and J. A. Pople, J. Am. Chem. Soc., 1975, 97, 1354.63 J. C. A. Boeyens, J. Chem. Crystallogr., 1978, 8, 317.64 V. Subramanian, K. Chitra, K. Venkatesh, S. Sanker and
T. Ramasami, Chem. Phys. Lett., 1997, 264, 92.65 M. Barbatti, A. J. A. Aquino and H. Lischka, Phys. Chem. Chem.
Phys., 2010, 12, 4959.66 A. Sharonov, T. Gustavsson, V. Carre, E. Renault and
D. Markovitsi, Chem. Phys. Lett., 2003, 380, 173.67 L. B. Clark, G. G. Peschel and I. Tinoco, J. Phys. Chem., 1965, 69,
3615.68 O. Christiansen, H. Koch and P. Jorgensen, Chem. Phys. Lett.,
1995, 243, 409.69 C. Hattig and F. Weigend, J. Chem. Phys., 2000, 113, 5154.70 C. Hattig and A. Kohn, J. Chem. Phys., 2002, 117, 6939.71 A. Bunge, J. Chem. Phys., 1970, 53, 20.72 S. R. Langhoff and E. R. Davidson, Int. J. Quantum Chem., 1974,
8, 61.73 P. J. Bruna, S. D. Peyerimhoff and R. J. Buenker, Chem. Phys.
Lett., 1980, 72, 278.74 H. Lischka, R. Shepard, F. B. Brown and I. Shavitt, Int. J.
Quantum Chem., 1981, S15, 91.75 H. Lischka, R. Shepard, R. M. Pitzer, I. Shavitt, M. Dallos,
T. Muller, P. G. Szalay, M. Seth, G. S. Kedziora, S. Yabushitaand Z. Y. Zhang, Phys. Chem. Chem. Phys., 2001, 3, 664.
76 H. Lischka, R. Shepard, I. Shavitt, R. M. Pitzer, M. Dallos,T. Muller, P. G. Szalay, F. B. Brown, R. Ahlrichs, H. J. Boehm,A. Chang, D. C. Comeau, R. Gdanitz, H. Dachsel, C. Ehrhardt,M. Ernzerhof, P. Hochtl, S. Irle, G. Kedziora, T. Kovar,V. Parasuk, M. J. M. Pepper, P. Scharf, H. Schiffer,M. Schindler, M. Schuler, M. Seth, E. A. Stahlberg, J.-G. Zhao,S. Yabushita, Z. Zhang, M. Barbatti, S. Matsika, M. Schuurmann,D. R. Yarkony, S. R. Brozell, E. V. Beck, J.-P. Blaudeau,M. Ruckenbauer, B. Sellner, F. Plasser and J. J. Szymczak,COLUMBUS, an ab initio electronic structure program, release5.9.2, 2008, www.univie.ac.at/columbus.
77 M. Barbatti, G. Granucci, M. Persico, M. Ruckenbauer,M. Vazdar, M. Eckert-Maksic and H. Lischka, J. Photochem.Photobiol., A, 2007, 190, 228.
78 M. Barbatti, G. Granucci, M. Ruckenbauer, J. Pittner, M. Persicoand H. Lischka, NEWTON-X: a package for Newtonian dynamicsclose to the crossing seam, 2007, www.newtonx.org.
79 R. Ahlrichs, M. Bar, M. Haser, H. Horn and C. Kolmel, Chem.Phys. Lett., 1989, 162, 165.
80 A. L. Spek, J. Appl. Crystallogr., 2003, 36, 7.81 C. Angeli, J. Comput. Chem., 2009, 30, 1319.82 A. L. Sobolewski and W. Domcke, Chem. Phys., 2000, 259, 181.83 S. Perun, A. L. Sobolewski and W. Domcke, Chem. Phys., 2005,
313, 107.84 K. Kosma, S. A. Trushin, W. Fuss and W. E. Schmid, J. Phys.
Chem. A, 2008, 112, 7514.85 J. Gonzalez-Vazquez and L. Gonzalez, ChemPhysChem, 2010, 11,