Precision neutron diffraction structure determination of protein and nucleic

acid components. X. A comparison between the crystal and molecular

structures of Ltyrosine and Ltyrosine hydrochloride
Michel N. Frey, Thomas F. Koetzle, Mogens S. Lehmann, and Walter C. Hamilton
Citation: The Journal of Chemical Physics 58, 2547 (1973); doi: 10.1063/1.1679537
View online: http://dx.doi.org/10.1063/1.1679537
View Table of Contents: http://scitation.aip.org/content/aip/journal/jcp/58/6?ver=pdfcov
Published by the AIP Publishing
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THE JOURNAL OF CHEMICAL PHYSICS

VOLUME 58, NUMBER 6

15 MARCH 1973

Precision neutron diffraction structure determination of protein and nucleic acid

components. X. A comparison between the crystal and molecular
structures of L-tyrosine and L-tyrosine hydrochloride*
Michel N. Frey,t Thomas F. Koetzle,t Mogens S. Lehmann, and Walter C. Hamilton
Chemistry Department, Brookhaven National Laboratory, Upton, New York 11973

(Received 26 October 1972)

The amino acid L-tyrosine (C 9HllNOa) and its salt L-tyrosine hydrochloride (C 9HllNOaHCl) crystallize
respectively in the space groups P2 12121, a=6.913(3) A, b=21.118(1O) A, &=5.832(3) A, and P2 1, a=
11.083(5) A, b=9.041 (4) A, c=5.099(3) A, ~=91.82(3) A. Both structures have been refined by neutron
diffraction techniques, and all the hydrogen atoms have been located precisely. The tyrosine molecule occurs
in the zwitterion form in pure L-tyrosine while both the amino group and the carboxyl group are protonated
in the hydrochloride. In both crystalline compounds there is a three-dimensional network of hydrogen
bonds. Statistical tests show no significant differences between the bond lengths and valence angles in
the compounds except for those atoms involved in hydrogen bonds. The conformational angles of the
main chain (C, Ca, N, 0 1, 0 2) and those of the side chain differ only slightly in the two compounds while
the mutual orientations of the main chain and of the side chain differ completely; in L-tyrosine N is gauche
with respect to C~ of the phenyl group while in the hydrochloride N is nearly trans to C~. The barriers
to rotation of the ammonium groups are estimated to be 8.3 kcal/mole in L-tyrosine and 5.0 kcal/mole
in the more weakly hydrogen bonded hydrochloride. Detailed statistical tests for L-tyrosine show very
good agreement between the heavy atom structural parameters obtained from our work and those found
in previous x-ray diffraction studies [A. Mostad, H. M. Nissen, and C. Rmming, Tetrahedron Lett.
1971,2131, and Acta Chern. Scand. (to be published) ; J. Donohue and R. Bogg (private communication) J.
Such tests also show that the standard deviations are quite well estimated in both the neutron and one
of the x-ray studies (Mostad et at.).

INTRODUCTION

Crystal Data

The crystal data are summarized in Table 1.

Both sets of neutron diffraction data were collected
at room temperature on an automatic four-circle diffractometer at the Brookhaven High Flux Beam Reactor
using the Multiple Spectrometer Control System.s The
cell dimensions were refined by least-squares techniques
from the setting angles of 30 well-centered reflections
evenly distributed in the reciprocal lattice. For L-tyrosine these values were averaged with the x-ray results
to get the final parameters. As previously determined
cell parameters for L-tyrosine hydrochloride were far
EXPERIMENTAL
less precise than ours, we used only the neutron results.
Intensities were measured by the fJ-20 step scan techCrystal Growth
nique. The scan length was varied according to the
Crystals of L-tyrosine large enough for neutron formula t:.20= 1.0(1+8 tanO) , and the step size was
diffraction were grown by the method of Mostad et al.' chosen so that there were approximately 40 points in
A needle-shaped crystal 1.4 mm3 in volume, elongated each scan.
Background corrections were made, using a method6
in the c direction and bounded by seven major faces,
was used for data collection.
which divides the peak and the background in such a
A crystal of L-tyrosine hydrochloride 3.1 mm3 in way that rr(I)/I is minimized. I is the integrated involume was obtained by evaporation of a saturated tensity and 0'(1) its e.s.d. based on counting statistics.
solution of L-tyrosine in concentrated HCI. The crystal Squared structure amplitudes were obtained as F02=
proved to be hygroscopic and was enclosed in a sealed I sin20, and were corrected for absorption by the
quartz tube during the data collection. The sample was Gaussian integration method using a grid of 256
a prism elongated in the c direction and bounded by sampling points for L-tyrosine and 512 points for
six major planes.
L-tyrosineHCI. The linear absorption coefficient was
Both crystals were mounted with the c axis near the calculated assuming the incoherent scattering cross
axis of the goniometer head.
section for hydrogen to be 40 barn and using the values
2547

The structures of L-tyrosine and L-tyrosine hydrochloride have been solved previously from x-ray diffraction data. 1- 3 The refinements of both structures by
neutron diffraction techniques have been carried out
as part of a series of studies in this laboratory, the primary purpose of which is to provide detailed information about hydrogen atom stereochemistry in the
principal commonly occurring amino acids.

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2548

FREY,

KOETZLE, LEHMANN,

AND

HAMILTON

T ABLE I. Crystal data.

Mol. wt.
Space group
a

c
(3

Z
Peale

(flotation)
Absorption coefficien t J.I.
Neutron wavelength A
d* max
Total number of reflections
Number of independent reflections
Rc= T. 1F02-F021 /l:Fo"

Poba

L-Tyrosine
CgHllNO,

L-Tyrosine H CI
CgHllNO,HCI

181.2
Orthorhombic, P2 12121
6.913(3) X
21.118(10)
5.832(3)
90.000
4
1. 413 g/cm 3
1. 41
2.09 cm-1
1.0142(4) A
1. 36 A-I

217.7
Monoclinic, P2[
11.083(5) X
9.041(4)
5.099(3)
91. 82(3)0
2
1. 415 g/cm'
1.41
1. 96 cm- I
1.0142(4) X
1.36 X-I
3299 (hkl, hiil, hkl, hkl)
1341
0.049

2561 (hkl, hkl)

1283
0.040

Fo' is the mean value for symmetry related reflections.

of (/L/p) for C, Cl, N, 0 tabulated in the International

Tables for X-Ray Crystallography.7 Finally the corrected
F02 were averaged over symmetry-related reflections.
Structure Refinement
The starting parameters for the refinement of L-tyrosine were the final coordinates from the x-ray analysis.l
For L-tyrosineHCl a few cycles of refinement were
carried out including only the coordinates and isotropic
temperature factors of the nonhydrogen atoms as obtained from the x-ray analysis. 3 The locations of the
hydrogen atoms were then determined from a difference
Fourier synthesis.
Least-squares full-matrix refinements of the atomic
coordinates, anisotropic temperature factors and an
isotropic extinction factor as given by Zachariasen8

TABLE

were then carried out until the shifts in the parameters

were less than 10% of the estimated standard deviations. Neutron scattering lengths were taken to be
bc =0.6626; bCl=0.958; bN=0.940; bo =0.575 and
bH = -0.372 (X 10-12 cm). The function minimized
was L: w \ F02-\ Fc2 \\2; weights were chosen as w=
1/u2(Fo2) with 0"2(Fo2) = O"count2(Fo2) + (O.01Fo2) 2, where
O"oount is based on counting statistics.
Details concerning the refinement are provided in
Table II. Only the reflections with Fo2>30"count(Fo2)
were included in the refinement process, and thus
values of the agreement factors RF2 are slightly smaller
than the corresponding Rc values given in Table 1.
The refined atomic parameters are listed in Table IILA
and IILB and F02, 0" (F02) , I Fe2 I are tabulated in Table
IV.A and IV.B.

n. Refinement data.
L-Tyrosine

L-Tyrosine HCI

No = Number of reflections included

Fo'> 3rrcount (Fo) ,

RF2 =

l: 1FoL 1Fe I' 1/2:Fo'

Rw= (T.w
RF=l:

1FoL 1Fe l'I'/2:wFo'}I12

1Fo- 1Fe 11/l:Fo

s= (l:w 1FoL 1Fe I' I'/(No-N,.) }II' a

1078

1091

0.033

0.043

0.036

0.039

0.026

0.041

1.35

1. 47

Extinction coefficient g

0.50(3) XIO'

0.05(2) X 10'

Smallest extinction factor

0.83 [refl. (200) ]

0.97 [refl. (111)]

Standard deviation of an observation of unit weight where N v is the number of refined parameters in the model.
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STRUCTURE OF PROTEINS AND

NUCLEIC

ACIDS.

2549

TABLE III. Fractional coordinates and temperature parameters. The form of the anisotropic Debye-Waller factor is exp{ -2rX
[ull(ha*)2+u,,(kb*)'+uaa(lc*)'+2ul,ha*kb*+2u13ha*lc*+2u'3kb*lc*Jf. The Ui/S are multiplied by 104
Atom

Ull

U"

UlS

Uaa

Ul'

165(6)
157(6)
247(7)
185(7)
188(7)
205(7)
216(7)
194(7)
215(7)
184( 5)
259(9)
179(8)
303 (10)
423 (18)
247(15)
330(17)
368(17)
633(22)
392(18)
315(16)
400(18)
379(18)
302 (17)
374(17)

-5(6)
21(5)
18(6)
-3(5)
-26(5)
0(6)
8(6)
-2(6)
3(6)
-1(5)
48(8)
25(9)
37(8)
99(14)
-19(16)
-78(14)
44(12)
72(15)
-16(16)
-59(17)
45(16)
64(16)
-6(16)
56(14)

22(6)
15(6)
38(7)
5(6)
-35(6)
-39(7)
-45(7)
-32(7)
-3(6)
-15(5)
37(8)
-17(8)
-22(9)
-35(15)
-26(14)
-8(14)
-8(16)
-116(16)
203(17)
-115(17)
-174(17)
-151(17)
-159(17)
-30(17)

-4(6)
-9(5)
-4(6)
23(6)
20(6)
13(6)
22(6)
-6(6)
1 (6)
6(5)
-59(8)
30(7)
0(8)
-37(15)
2(14)
53 (14)
-5(12)
14(17)
-75(15)
-34(14)
45(16)
70(15)
-87(15)
9(14)

605(10)
415(12)
377(11)
395(13)
333(10)
407(11)
396(12)
413(13)
432(11)
373(10)
573(12)
558(16)
523(16)
567(16)
686(31)
1077(47)
951 (39)
510(25)
918(38)
383(23)
727(31)
634(31)
679(30)
819(35)
719(28)
709(30)

-5(6)
21 (8)
-21 (8)
46(9)
16(8)
-26(8)
-33(9)
-17(8)
-76(9)
6(7)
-46(8)
30(10)
53 (12)
-40(11)
26(22)
-127(28)
-125(31)
-33(19)
56(22)
98(25)
-188(22)
-83(25)
-60(23)
-259(25)
-77(20)
32(19)

-54(6)
-72(8)
-70(8)
-101(10)
-20(8)
12(9)
-24(10)
4(9)
-17(9)
7(8)
-183(8)
-123(13)
-205(12)
-84(12)
-249(22)
-541(36)
-77(25)
-54(19)
-188(26)
-8(20)
33(23)
-106(25)
-113(23)
11 (23)
-50(20)
-177(21)

141 (8)
-40(10)
14(10)
-135(13)
-7(10)
23(9)
62(10)
81 (10)
101 (10)
18(9)
21 (10)
23(13)
-105(14)
133(14)
43(28)
-31(32)
403(43)
93(22)
-317(29)
0(26)
203(27)
329(28)
332(29)
357(30)
43(24)
-200(24)

U'3

A. L-tyrosine
C
Ca

cP
C7
C81
C8'
Cd
C"

cr

N
01
0'
O'
HI
H'
HS
Ha
HPI
HP'
H81
H8'
Hd
H"
H.

0.32432(21)
0.39973(19)
0.57492(20)
0.54120(19)
0.45884(21)
0.59696(21)
0.43361 (21)
0.57407 (21)
0.49446(20)
0.24177(16)
O. 16707 (25)
0.42880(25)
0.48075(27)
O. 18562 (46)
0.29598(45)
0.12887(44)
0.44365(42)
0.69394(43)
0.61862(47)
0.41781(53)
0.66334(49)
0.37025(53)
0.62154(52)
O. 42734 (47)

0.30508(6)
0.29320(6)
0.33568(6)
0.40544(6)
0.44429(6)
0.43323(6)
0.50894(6)
0.49781(6)
0.53565(6)
0.30408(5)
0.33308(8)
0.28577(8)
0.59924(8)
0.34833(15)
0.29829(15)
0.27260(14)
0.24362(12)
0.31953(14)
0.32750(15)
0.42432(15)
0.40411(14)
0.53835(14)
0.51921(15)
0.62156(13)

0.60788(23)
0.36514(22)
0.31199(26)
0.35374(23)
O. 18600(24)
0.56031 (24)
0.22266(25)
0.59906(24)
0.42882(23)
0.19631(18)
0.62569(30)
0.77039(27)
0.46966(33)
0.20901(59)
0.02977 (50)
O. 22250 ( 55)
0.34946(49)
0.41932(64)
0.13399(56)
0.02148(53)
0.69275(58)
0.09021(58)
0.75871 (52)
0.33636(55)

296(7)
254(7)
253(7)
239(7)
300(8)
281 (7)
285(7)
294(7)
241 (7)
306(5)
325(8)
393(10)
421 (11)
457(17)
471 (20)
382(16)
443(17)
385(17)
563(20)
658(22)
616(20)
702(23)
693 (22)
508(18)

194(6)
189(6)
238(7)
227(6)
251 (7)
250(7)
248(7)
240(7)
216(6)
259(6)
322(9)
350(9)
231 (8)
381(17)
466(18)
462(17)
262(13)
421(17)
457(17)
451(18)
405(17)
391 (16)
447(17)
336(15)

B. L-tyrosine.HCI

CI
C
Ca
CP
C7

0'

cn

Cd
Cd

cr
N
01
0'
O'
HI
H'
H3
Ha
HPI
HP2
H82
H81
H"
Hoi
H'
JIll'

0.41280(11)
-0.32987 (15)
-0.34781 (15)
-0.24003(17)
-0.12254(15)
-0. 10323 (16)
-0.02941(17)
0.00593(17)
0.08105(18)
0.09794(14)
-0.45969(15)
-0.36134(21)
-0.27318(20)
0.20367 (21)
-0.46427(39)
-0. 46559 (48)
-0.53334(42)
-0.36159(32)
-0.26145(44)
-0.23182(36)
-0.17443 (37)
-0.04317(40)
0.02026(39)
O. 15366(37)
0.26416(34)
. -0. 25425(37)

0.25000
0.25640(29)
0.09429(27)
0.03494(32)
0.03849(28)
-0.05312(28)
0.13160(28)
-0.05027 (28)
0.13338(29)
0.04359(26)
0.08123(29)
0.35444(30)
0.27195(34)
0.04224(35)
0.15613 (55)
-0.02071 (67)
0.09767 (84)
0.02877(52)
-0.07718(53)
0.09936(61)
-0.12759(60)
0.20257(60)
-0.12124(59)
0.20546(61)
O. 1131O( 55)
0.38038(56)

0.40927(30)
0.14766(37)
0.07735(39)
-0.07299(43)
0.08458(33)
0.30162 (37)
0.01061(41)
0.44399(42)
0.14934(41)
0.36668(35)
-0.09173 (39)
0.00066(52)
0.37392(49)
0.51494(50)
-0.23797 (95) .
-0.17541(113)
0.01958(122)
0.25575(79)
-0.13459(108)
-0.24998(85)
0.36337 (89)
-0. 15649(93)
0.61397 (95)
0.08706(91)
0.45200(87)
0.40968(91)

336(6)
307(8)
319(9)
402(12)
336(9)
310(10)
431 (11)
312(9)
364(10)
327(10)
370(9)
515(14)
491(13)
339(12)
572(26)
880(39)
307(22)
541 (23)
692(27)
647(26)
479(24)
752(30)
553(26)
560(25)
411(21)
552(25)

497(9)
305(10)
,111(10)
393(12)
296(10)
312(11)
384(12)
341(12)
363(12)
258(9)
441 (10)
316(12)
389(15)
415(14)
533 (28)
545(32)
1667(69)
476(24)
527(29)
896(34)
657(29)
761 (38)
716(32)
777(37)
544(27)
469(27)

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2550

FREY, KOETZLE,

LEHMANN,

AND HAMILTON

~i~ij::i3~;~!;~~Sia~~~;:5.5!~;:!~;;;!E~;5!;;;E~~i;!Es~a~5~~i~~.~~B~E;~;~~::~:~5E:~;E~~i.~S;:~:!;:;

~~~~~~~~:~~~~=~~t~~~~:!~:t~~~~~~!:~:~~~~l~~!:~~~!::~~~ ~~~N!N::=:~~~:~~Z~!:'2.!=~~=::.~::~:::!~~~:

:o~;~~~~~~:~~!:~;!~:~:~$!:~!'~~~~;::!~:~:~=:~:;~~:~~~ ~~~~!=;~~=!~~~~~~=~:~=;~!:~~~:=~!:a:~:~::~.:
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:~::::::::::::~:::::=::::::~:~:::==~::::~~~::::::::~~:::::::::::::~:::~::::~:::::::::::::~:~::~::
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~~~i~O-~~~7~O-~~i~~70-C-:7~C~~~7~~O-N~i~~70-N~.~~0.N~.7i~O-~M70-~~i~-~i7C_O-:~01~i~O-~~~~770-~~.i

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... ... ............ ...

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2551

STRUCTURE OF PROTEINS AND NUCLEIC ACIDS. X

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2552

FREY,

KOETZLE, LEHMANN,

AND

HAMILTON

DESCRIPTION AND DISCUSSION

Molecular Structure
The tyrosine molecule is shown schematically in
Fig. 1, and the two molecular structures are illustrated
in Fig. 2(a) and 2(b). Intramolecular bond lengths and
TABLE VI. Angles (deg) within the molecule.

OLC-o'
()I-C-C"
O"-C-C"
C-C"-H"
C-C"-N
C-C"-CP

H"-C"-N
H"-C"-CP
N-C"-CP

C"-N-HI
C"-N-H'
C"-N-H3
HLN-H'
HLN-H3
H"-N-H3
C"-CJi-C~

TABLE V. Distances

U\)

C"-CJi-HP'
C"-CP-HPI

within the molecule.

HP"-CJi-C~

HP"-CJi-HPI
Corrected
Corrected
for thermal
for thermal
motion L-Tyrosine. HCl motion
L-Tyrosine

C~-CJi-Wl
CP-C~-C!L

CJi-C~-C6'
C!LC~-C8'

C-ol
C-O'
C-C"
C"-H"
C"-N
N-HI
N-H'
N-fl3
C"-CJi
CJi-Cr
CJi-flPl
CJi-W2
Cr-cn
C6LH&1
Cr-C"
C&"-H8'
OLCd
C,LHd
C6,,-C"
C'''-H''
c,Ler
c'''-er
C,-oOll-HO"-Ho,

1.242(2)
1.259(2)
1. 529(2)
1. 094(3)
1. 488(2)
1.015(4)
1.048(3)
1.037(3)
1. 539(2)
1.511 (2)
1. 088( 4)
1.094( 4)
1. 398(2)
1.085(4)
1.394(2)
1.088(4)
1.393(2)
1.083(4)
1. 391 (2)
1.085(3)
1. 393(2)
1. 388(2)
1. 367(2)
0.981(4)

1. 250
1.266
1.535
1.097
1.496
1.018
1.050
1.039
1. 514
1.095
1.100
1.402
1.091
1.399
1.094
1.395
1.089
1.393
1.092
1.397
1.393
1.369
0.982

1.205(3)
1.304(3)
1.520(3)
1.100(5)
1.492(2)
1. 007(8)
1.017(8)
1.020(6)
1.536(3)
1.509(3)
1. 085(6)
1.080(6)
1.393(3)
1.074(6)
1.393(3)
1. 091 (5)
1. 394(3)
1. 091 (5)
1.391(3)
1. 086(6)
1.382(3)
1.393(3)
1.374(3)
0.988(6)
1. 018(6)

1. 215
1.313
1.530
1.103
1.504
1.009
1.026
1.038
1. 512
1.092
1.087
1.401
1.081
1.402
1.098
1.398
1.099
1.395
1.093
1.391
1.401
1.378
0.989
1.019

C~-C6LH!1

C~-C!LCd

H!LC8LCd
C~-O"-C"
C~-C!"-H&'

C'''-0''-H8'
C6LC'LHd
OLC'LC'
H,LC,LC'
O"-C'''-C'
C8"-C'''-H''
C'-C'''-H''
c'Ler-o
C,Lcr-c,
O'-C'-C<2
C-OII-H'
C-O"-Ho,

L-Tyrosine

L-TyrosineHCl

126.4(2)
117.0(1)
116. 6( 1)
109.2(2)
109.7(1)
111.1(1)
107.2(2)
108.8(2)
110.8(1)
112.0(2)
109.4(2)
110.9(2)
108.2(3)
107.0(3)
109.3(3)
114.5(1)
108.4(2)
107.3(2)
110.4(2)
106.7(3)
109.2(2)
121.5(1)
120.5(1)
118.0(1)
119.8(2)
121.3(1)
118.9(2)
121. 4(1)
119.4(2)
119.1(2)
120.2(2)
119.4(1)
120.3(2)
119.6(1)
120.9(2)
119.6(2)
121.8(1)
120.2(1)
117.9(1)
111.1(2)

126.4(2)
122.0(2)
111. 6(2)
110.2(3)
108.2(1)
110.9(2)
107.5(2)
110.8(3)
109.2(2)
113.3(3)
110.8(3)
109.4(3)
107.3(4)
107.0(4)
108.9(5)
113.5(2)
108.4(3)
107.7(3)
109.8(3)
106. 6( 4)
110.6(3)
120.2(2)
121.2(2)
118.5(2)
119.2(3)
121.0(2)
119.7(3)
120.8(3)
120.1(3)
119.1 (3)
120.2(3)
119.6(2)
120.1(3)
119.7(2)
120.5(3)
119.7(3)
122.5(2)
120.2(2)
117.3(2)
113.0(3)
110.7(3)

angles are given in Tables V and VI. The general features of the nonhydrogen atom backbone found in
earlier x-ray diffraction studies of L-tyrosine1. 2 are confirmed, and the molecule is verified to be a zwitterion.
In L-tyrosineHCI the carboxyl group is protonated.
The two bonds C-Ol and C-02 differ by 0.10 A in

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2553

STRUCTURE OF PROTEINS AND NUCLEIC ACIDS. X

FIG. 2. Stereoscopic drawing of

the molecules. The thermal ellipsoids include areas with an
atomic density greater than 50%.
A=a, B={3, G=-y, D=6, E=E,
Z=t, H='I/: (a) L-tyrosine; (b)
L-tyrosine HC!.

(a)

till

till

(b)

length; C-01 is a double bond and the extra hydrogen

atom is bonded to 0 2 In the x-ray work3 the C-0 1 and
C-02 bond lengths were found to be apparently equal
leading to the false conclusion that in this compound
the tyrosine molecule is the usual zwitterion. In fact
the molecule is a positive ion with the charge formally
residing on the NHa+ group.
A comparison between the geometries of the tyrosine
molecule in the two compounds has been carried out.
x2 tests9 and normal probability plotsl0,1l of the parameter differences I llpi/O'(pi) I have been prepared to
compare the interatomic distances and angles. The
parameter sets Pi were chosen to include all covalent
bond distances and bond angles. If the atoms involved
in hydrogen bonds are excluded (HI, H2, H3, 01, 0 2,

o~, H~)

these comparisons show no significant differences between the two molecules at the 0.05 probability
level. The straight line obtained in the normal probability plot indicates that the errors are approximately
normally distributed; moreover the slope of this line
is 1.3 which indicates that the pooled standard deviations 0'= (0'12+0'22)1/2 are only slightly underestimated.
In the benzene ring the average C-H bond length is
1.085(2) it in L-tyrosine and 1.086(3) it in L-tyrosine
hydrochloride, and the average C-C distances are
1.393(1) and 1.391(1) it respectively. The deviations
of the atoms in the side chain from a least-squares plane
through the benzene carbon atoms are similar in the
two compounds and range from 0.001 to 0.009 it for
the carbons in the ring and from 0.004 to 0.040 it for

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2554

FREY,

KOETZLE,

LEHMANN,

AND

HAMILTON

FIG. 3. Stereoscopic view of

molecular packings. (a) LTyrosine; thermal ellipsoids as
in Fig. 2. (b) L-Tyrosine
HCI; the thermal ellipsoids include areas with an atomic
density greater than 80%.
Molecular bond, thick; hydrogen bond, thin.

raj

(b)

the hydrogens. The atoms O~, Cfl and H~ deviate significantly from the plane (0.020--0.100 A). Two short
intramolecular contacts are worth noticing, namely
Cd H~ 2.47 Ain L-tyrosine and 2.52 Ain the hydrochloride. These distances are shorter than the sum of
the Van der Waals radii (C-H""2.70 A)12; the near
coplanarity of OH with the ring may be due to special
requirements of the strong hydrogen-bonding system
in which it is involved.
The torsion angles (Table VII) have been calculated
according to the IUP AC-IUB conventions.13 The most
dramatic differences between the two molecular conformations occur for the angles XI and Xu describing
the linkage between the main chain and the side chain.
The configuration of N-C'"-OL02 is nearly planar,
which is common in the amino acids we have studied.

TABLE VII. Torsion angles (deg). The IUPAC-IUB conventions

have been used.
Angle

Atoms involved

L-Tyrosine

L-Tyrosine. HCI

cp1
cp2
cp3

C-Ca-N-H1
C-Ca-N-H2
C-C"--N-H2

+57.0(2)
+177.0(2)
-62.4(2)

+47.1(4)
+167.8(4)
-72.2(5)

1/1 1
1/1 2

OLC-Ca-N
OLC-C"--N

-14.2(2)
+166.3(1)

-31.8(3)
+151.1(2)

Xl
X2.1

N-Ca-O-C'I'
Ca_O-C'I'_CIl

x 1

C~LCLcr-o.

X6

CLcr-O'l-H

+69.1(1)
-86.0(2)
+177.1(2)
-1.4(3)

-178.1 (2)
-113.6(2)&
181.3(2)
1. 4( 4)

The labeling of the atoms in the phenyl ring in tyrosine

HCI, i.e., the assignment of 61, E1 vs 02, .2 violates rule 2.2.3 of
the IUPAC-IUB rules13 which assigns the lowest number to
the branch giving the smallest absolute value of the torsion
angle. This was done to keep the notation identical for the two
crystals and is in the spirit of the exception to rule 2.2.3. in
the footnote on p. 6 of the IUPAC-IUB rules.
&

Hydrogen Bonding

The hydrogen bonding networks as well as the molecular packing in one unit cell of each structure are
shown in Fig. 3. Hydrogen bond distances and angles
are summarized in Table VIII.

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STRUCTURE OF

PROTEINS

AND

NUCLEIC ACIDS.

2555

TABLE VIII. Distances (A) and angles (deg) in the hydrogen bonds.
A-H .. B-C

AB

H .. B

LA-H .. B

LC-B .. H

2.877(2)
2.826(2)
2.884(2)
2.666(3)

2. 120(4)
1. 789(4)
1.853(4)
1.689(4)

129.8(3)
169.8(3)
172.7(3)
173.8(3)

131.7(2)
107.1(2)
131.3 (2)
132.0(2)

3.251 (3)
3.452(3)
3.329(3)
3.045(3)
2.619(4)
2.901(5)

2.378(5)
2.471 (7)
2.505(8)
2.078(5)
1.609(5)
2.420(5)

144.5(3)
161.8(4)
137. 4( 4)
165.6(3)
170.7(4)
108.0(4)

115.1 (2)
109.4(3)

L-Tyrosine
N-H1 .. O'-Cl'
N-H3 .. 0LC
N-H3. OLC
O'l--HOLC
L-Tyrosine HCI
N-H1CI
N-H2 .. CI
N-H3CI
O-H .. CI
OLHo20'l--O
N-H301-C
&

&

Assumed to be a hydrogen bond from the x-ray work, although the present results belie this conclusion.

L-Tyrosine
Four hydrogen atoms are involved in hydrogen
bonding. The detailed geometries of the hydrogen
bonds are similar to those in most of the amino acids
we have studied. There is a good inverse correlation
between the N-H and HO distances in N-HO
hydrogen bonds; these bonds are considerably bent and
the C-OH angles differ significantly from 120.
There is no intramolecular hydrogen bond joining the
carboxyl and ammonium groups; the closest approach
of 2.453 A for 0 1. ff1 is equal to the appropriate sum
of Van der Waals radii assuming the radius for hydrogen
to be 1.0 A as proposed by BaurY A short intermolecular contact is OI .. H" (2.24 A).
L-Tyrosine Hydrochloride
The hydrogen bonding system consists of five hydrogen bonds. All three hydrogens of the ammonium
group are donated to chlorine atoms. The contact
H2 0 1 cannot be considered a hydrogen bond as was
assumed from the x-ray results3 ; the distance is 2.420(5)
A, about what is expected for a van der Waals contact.
TABLE IX. Statistical comparison for L-Tyrosine.
Atomic coordinates
Neutron
Expected
x-ray
values (M.N.R.)
Slope
Xz'

xu'
x.'

Xz.u

1.0
22.4
22.4
22.4
56.0

1.2
21.3
26.3
32.8
80.4

Neutron
x-ray
(D.B)

X-ray
(M.N.R.),
(D.B)

1.8
20.9
83.8
31.2
135.9

1.8
21. 7
68.8
42.9
133.3

The two hydrogen bonds involving H' and H02 are quite
strong. There is no evidence for an intramolecular hydrogen bond; the ff1 0 1 distance is equal to 2.420 A,
so this again is a normal van der Waals contact.
Some intermolecular contacts shorter than Van der
Waals distances l2 are Cl H~I (2.66 A),
H02
(2.52 A) and 0 2.. 0' (2.62 A).

cr

Thermal Motion
An attempt was made to fit the heavy atom thermal
parameters to rigid-body motions described in terms
of T, L, and S tensorsY; As in the x-ray workl,2 we
find that the thermal parameters of the main chain and
the side chain atoms in both crystals are best treated
in terms of the motions of two independent rigid bodies.
The largest principal libration axis of the main chain
is parallel to C-C" while the side chain librates
mainly around CY cr. The corresponding amplitudes
of libration for the main chain and the side chain are
5.7 (1.9), 4.5 (4) in L-tyrosine and 6.6 (1.3),
6.5 (4) in L-tyrosineHCI. The differences (t:.UiJ)Ay I/2
between the observed thermal parameters and those
calculated assuming only rigid-body motion are satisfactorily small in the range 0.0005-0.0015 A2. The effective screw translations are very small. Corrected
bond distances based on these rigid-body calculations
are included in Table V.
There is a substantial amount of nonrigid body motion involving the hydrogen atoms, but quite reasonable corrected C-H distances were obtained using the
minimum correction of Busing and Levy.16 The mean
corrected C-H distances in the benzene ring are 1.092 A
in L-tyrosine and 1.093 A in L-tyrosineHCI, slightly
larger than the spectroscopic value of Yo= 1.084(5)
found in benzeneY Additional partial rigid-body calculations were carried out for the ammonium group.
The rigid-body was defined by Ca, N, HI, H2, H3. These

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2556

FREY, KOETZLE, LEHMANN,

calculations give a good fit in the case of L-tyrosine,

(.6.Ui.r)A/ '2 =0.OO2 12. The largest principal axis L is
inclined 19 to the N-Ca bond and has an amplitude of
8.0 (8) 0. If we assume a threefold cosine poten tiaP8
this libration amplitude leads to an estimated barrier
to rotation of 8.8 kcal/mole, in the range 7-10 kcal/mole
found for the ammonium groups in most amino acids.
In the case of L-tyrosineHCI similar calculations
lead to a less satisfactory goodness of fit (.6.Ui.r)A/'2 =
0.006 12. The largest principal lib ration axis is parallel
to N-Ca and has an amplitude of 13.0 (1.3) leading to
a barrier of rotation of 5.1 kcal/mole, which is unusually
low. The second largest libration axis also has a relatively large amplitude of 9.0 (2.4). These lib rations
reflect the fact that the system of N-H 'CI hydrogen
bonds involving the ammonium group of L-tyrosine
HCI is relatively weak.
Interexperimental Comparisons
In addition to the comparisons of the neutron diffraction results for L-tyrosine and L-tyrosineHCI described
above we performed comparisons between our results
and those of the accurate x-ray studies of L-tyrosine of
Mostad, Nissen, and R~mming (x-ray M.N.R.) 1 and
of Donohue and Bogg (x-ray D.B.).2 Only the parameters for the nonhydrogen atoms were included in the
comparisons, as there are known systematic differences
between hydrogen atom positions as determined by
neutron diffraction and conventional x-ray diffraction
techniques. The comparisons were carried out by preparing half-normal probability plots10 ll of the parameter differences from each pair of studies and by the
use of the X2 test. 9 The results of these comparisons are
summarized in Table IX.
The normal plots are linear, indicating that the errors
are normally distributed. The slopes of the lines are
somewhat larger than unity, indicating that the pooled
standard deviations are underestimated by a factor
of 1.2 to 1.8.
The sum of the squares of the differences for each
structural parameter class (x, y, z, all atomic coordinates) was tested at the 0.05 probability level as x2
These tests reveal that the y coordinates from the x-ray
(D.B.) study are significantly different from those from
the x-ray (M.N.R.) study and from our neutron diffraction study. Similar calculations were performed to compare the thermal parameters from our neutron study

AND

HAMILTON

with those of the x-ray (M.N.R) study. The x2 tests

reveal significant differences between the two sets of
parameters, with the x-ray values of {311 and {322 systematically larger than the corresponding neutron values
and the inverse for {333. This anomaly may be related
to the fact that all the samples are elongated along c
or may partly reflect the influence of bonding electron
density on the x-ray thermal parameters.
ACKNOWLEDGMENTS
We are indebted to Dr. A. Mostad, Dr. H. M. Nissen,
and Dr. C. R~mming for supplying us with seed crystals,
information concerning crystal growth, and x-ray structural parameters for L-tyrosine. We also thank Dr.
J. Donohue and Dr. R. Bogg for supplying us with their
x-ray structural parameters.

* Research performed under the auspices of the U.S. Atomic

Energy Commission.
t Charge de Recherches au C.N.R.S. (France). Holder of a
N.A.T.O. grant. On leave from Laboratoire de Cristallographie
Universite, 14 Caen, France.
t U.S. National Institutes of Health Postdoctoral Fellow.
On leave from Kemisk Institut, Arhus Universitet, Denmark
and supported in part by a grant from StatensNaturvidenskabelige
Forskningsrad, Copenhagen, Denmark.
1 A. Mostad, H. M. Nissen, and C. Rmming, Tetrahedron
Letters 1971, 2131; Acta Chern. Scand (to be published).
J. Donohue and R. Bogg (private communication).
3 R. Srinivasan, Proc. Ind. Acad. Sci. A50, 19 (1959).
A. Mostad, H. M. Nissen, and C. Rmming, Acta Chern.
Scand. 25, 1145 (1971).
6 D. R. Beaucage, M. A. Kelley, D. Ophir, S. Rankowitz, R. J.
Spinrad, and R. Van Norton, Nucl. Instr. and Methods 40, 26
(1966).
6 M. S. Lehmann, W. C. Hamilton, and F. K. Larsen, American
Crystallographic Association Meeting Abstracts 09, Albuquerque,
New Mexico, 1972.
7 International Tables jor X-ray Crystallography, edited by C. H.
Macgillary, G. D. Riecks, and K. Lonsdale (Kynoch, Birmingham, England, 1962), Vol. 3, p. 197.
8 W. H. Zachariasen, Acta Cryst. 23, 558 (1967).
9 W. C. Hamilton, Acta Cryst. A 25, 194 (1969).
10 S. C. Abrahams and E. T. Keve, Acta Cryst. A 27, 157
(1971).
11 W. C. Hamilton and S. C. Abrahams, Acta Cryst. A 28,215
(1972) .
IA. Bondi, J. Phys. Chern. 68, 441 (1964).
13IUPAC-IUB Commission on Biochemical Nomenclature,
J. Mol. BioI. 52, 1 (1970).
14 W. H. Baur, Acta Cryst. B 28, 1456 (1972).
16 V. Schomaker and K. N. Trueblood, Acta. Cryst. B 24, 63
(1968) .
16W. R. Busing and H. A. Levy, Acta Cryst. 17,142 (1964).
17 A. Langseth and B. P. Stoichefi, Can. J. Phys. 34, 350
(1956) .
18 E. O. Schlemper, W. C. Hamilton, and S. J. La Placa, J.
Chern. Phys. 54, 3990 (1971).

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