Indications for a common evolutionary origin shown in the primary structure of three transfer RNAs

Vol.

24,

No. 5, 1966

BIOCHEMICAL

INDICATIONS

FOR

IN THE

PRIMARY

AND

BIOPHYSICAL

A COMMON

EVOLUTIONARY

STRUCTURE

OF THREE

Thomas

H.

RESEARCH

ORIGIN

COMMUNICATIONS

SHOWN

TRANSFER

RNAs.

divergence

of

Jukes

Space Sciences Laboratory University of California Berkeley, California’

Received

August

4, 1966

There

is

molecules

from

cation

followed

tiation

is

and

to

comparison of

polypeptide

with

the

as

The

present,

it

of

example It

some

as

a result

(sRNA) made

in

above. Supported

to

the

of two

partial

has

been

possible

to

indications

now

of

example, a,

them

the

p and

are

their

that

(1).

genetic

of

the

is

in

with

and

sequence

from

of

i nogen

point

mutations by

acid

sequences

been

and

archetype

by

tryps

direct

compared

hemoglobin,

and

its

changes

has

a common

Chymotryps

differen-

compatible

amino

chains

dupli-

secondary

these the

protein

the

deletions

myoglobin

origin

of

conserve

examine

y polypeptide

accepted

possible

for

related the

serine

to

(4), that

procedure

grant

NsG of

first

479

California,

base

and

tyrosine

the

for

the

to

compare

molecules,

the

used is

by

time

acid

of

sRNAs

similar

the

nucleic

discoveries

essential

University

the

widely

a manner

by

a manner

included

comparison

functionally

The

in

to

certain

diver-

i nogen

are

(2). is

(3),

molecule

not

means extent

necessary

has

of

is

by

process

For

this

place The

constraints

the

but

sequences

of

the

chains.

evolution

another

I

genes,

taken

differentiation.

of

role.

a result

gent

by

evolutionary has

functional

restricted

of

the

archetype

structure

the

that

a common by

tertiary

biological Up

evidence

all

sequences sRNA

the

protein

insertion

of

National Berkeley.

744

Aeronautics

the

primary

obtained

structures from

of

alanine

transfer

(5).

The

comparison

sequences arbitrary

RNA was

mentioned gaps

and

yeast,

Space

which

infer

Administration

Vol.

24, No.

5, 1966

BIOCHEMICAL

AND

BIOPHYSICAL

RESEARCH

COMMUNICATIONS

I

Figure I. Comparison of possible secondary structures,for yeast alanine, serine, and tyrosine sRNAs (see text). “indicates suggested deletion of bases in serine sRNA. The proposed anticodons are shown in each case in complementary juxtaposition to messenger coding triplets, in conformation with the “wobble” hvoothesis (12).

/

C-0

G

Me IL1 ’ : ‘u G--u I / ‘0-C ’ \

A--“-G

/

‘C

\ rxi

L& L ‘c

,U’“lA \ I;

:-G-G-c-c I ,I I 111 \ T.U2

‘G

’ Lln2-

A’

+A Cld /

\ Y \

lU ”

IMe \ I-T-C’

-C-C-G(U) (A)

‘t-o-

WryI

C

:=:

,un2’G‘A, GOMe ’

/ G I * \

AC

\/

,un,G

LFG

C-C-G II II G-G-C

0, ’ “t?=:-c-G-“-C-C 111 II 111

,u-G’A Y

,I,

\

TtI/C

* ‘e

-

Ii

p-u

I C3G I GSA , ‘GS l-E-“.-;-

,+“: -G-C 2-z

Y

:

\ T-*2

Al

“HZ ‘U”z-WI;

UH2.A

MO 1 MI\\ C-C-G “I ,,I G-G-C

1;

P

,I/

lA

/ GOY,

\ II

\

.A

U”2

A’

A-hop \G--Y-A

I-G-A’

-C-A-“-

--c-c--u-(U)

IUI

IA)

that by

deletions alignment

portions nature not

of

is of

yet

of

genetic

material

homologous

presumed

to

their

function,

sufficient

for

portions have or the

been because

have of

taken the

place sequences.

preserved

either

the

accumulation

time of

745

during

lapse

enough

The due

to

evolution identity the

following randomly-occurring

as of

shown these

essential duplication

is point

Vol. 24, No. 5, 1966

mutations are 5

to

produce

readily (7)

BIOCHEMICAL

differences

perceptible

are

structure

et

al.

provide

an

evolutionary

sRNAs.

The

in

each

18

to

of 2

includes The

is

that

below.

It

three

in

serine

all

the

this

loop

and to

these

chains

phenomena

of

to

enable the

2

cytochrome

following

41-45

84

f:47-50,

--54-57

5:60-64,

--72-76 and

the

UUU

sequence

and

tyrosine

alanine exists

in

place from

contained

draws

attention 2 pairing

loop

in

between

corresponding three

alanine

loops sRNAs

are

”2”

loop

the

compared

it

13 and

for

746

loops

the

system sites.

proposed

h:65-7

I

back

have

evolution

and

the

sRNA in

2

in 24

The

serine as

shown

two

sRNA,

homologous

portion. in

between

other

alanine

model:

2: 13-24

just

is

present

numbering

in

pair,

Loops

during

deleted

sRNA

base is

in

at

common

which

residues,

one

Holley

2: 34-40

the

residues in

made

g-2

homology

s The

j&

sRNAs

the 12

to

be

by by

Reqions

upon

of

to

tyrosyl

same

deletion

&

in

28,

and the

shortened

sRNA.

features

8-9,

includes

by

to

seryl

evolutionary

(sRNA)

used

conformation

tyrosine

Connecting

(8),was

model

been

to

RNA

alanyl,

residues

comparisons

g2J-a

f

one

in

al.

yeast

has

from

51-53,

The

The

48

et

transfer

“cloverleaP’

that

25-27 a-

originally

complementary

the

extending

Cantor

The

regions

suggested

a trinucleotide

and

the

l2,

region of

the

Reqions

from

molecules.

with

of

the

alanyl

1.

in

77-83

region

sRNAs,

or

yeast

the

Figure

shown of

is

possess

b: E-

connecting

one

by

comparing in

are

sRNA,

a$-~,

deleted

for

shown

sRNAs,

gaps,

sRNAs

deletion

Both

(6)

for

modified

that

He1 ical

been

chains

proposed

model

except

the

three

Helical

composition,

globin

subsequently

regions

( 3 1,

explained

(3),

comparison

helical

as

the

base

compared.

Holley,

et al

in

when

A secondary

four

AND BIOPHYSICAL RESEARCH COMMUNICATIONS

the loops

to

a short

postulated implies

case in

expanded (3),

evidently

that

of

the

all

three

form,

omitting

compare

it

more

other

two

sRNA the closely

sRNAs.

evolutionary

homology

in

their

base

Vol. 24, No. 5, 1966

sequences

in

regions,

Table

loops,

and

correspondence

in

sequence

that

where

the

(Figure

a region

of

tary cistrons sequent

the

the

a helical one

member

the

complement the

the

base

of

the

two

A much has

more

system

recent

apparently

a piece

led of

of the

to

the DNA

gene

three that

terminal

of

duplication, the

sRNAs contained -CCA-OH

in

in

in

84 that

base is

are

the

added

747

a time

to

evolution only

excluding

or

serine have

been from

transcription.

I) these

into

different

comparison archetype. changes,

sRNAs.

The

transcribed the

by

Such

evolve

an

“2’

replacement

3 single-base

yeast

the

of

The from

in

distance

(Figure

Replacement

complementarity.

to

some

region

sRNAs

pair

changing

in

about

following

sub-

inserting

mutations,

two

the

sRNA

base

point

by

of

alanine

indications

U.

1 appears pairs,

at

at

character.

divergent

complemen-

involves

2 helical

helical

of table

mutation

two

followed

separation

point

bring

their

concept

subsequently

another

regions

preserving the

to

helical

then

There

A)

in

sRNAs.

This

Each

however,

archetype

of

pair.

another

(C or

common

point

sRNAs

a complementary

and

a G or

is,

the

archetype

replacing

by an A would

U the

with

by

base

the

while

the

proceed.

Us opposite

in

separated

base

of

tyrosine

duplication

cistron.

could

and

gene

mutation

the

There

underwent

in

structure

reoccurring

i ne

Else-

incidence

the

tyros

the

sRNAs.

extensive

that

and

base in

enable

agreement

archetype

a point

this

opposite would

ne

yeast

secondary

serine

of

includes

(6,7).

and

region

zwhich

indicates

course,

replaced

the

of

22

complementary

by

how

compositions in

of

complementary

base

procedure

is

pair

appropriate

seri

another

the

or

probably

the

connecting obvious

all

evolution

to

which

exists,

of

2 This

of

of

to

to

in

sequences

residues

sRNAs

common

view

most

64

only

during

primary

replacement

one

the

in

duplication

by

first region

contains

of

of

surprising

archetype

region

be

appears

and -- 41-k

gene

to

three

the

two

residues

all

from

common

found

occur

regions, The

in

(9)

not

helical

aligned.

al,

in

A problem

helical

is

evidently

these

to

from

sRNAs

--IO-12

for

from

three

extending

sequences

the

all

is

can

which

are

homology

region

proposed

for

This that

in

et

homology

mutations

AND BIOPHYSICAL RESEARCH COMMUNICATIONS

deletions

all

Zamir

I).

the

I,

BIOCHEMICAL

from

numbering Analyses

a

Vol.

24, No.

5, 1966

Table

.L

I.

Homologous serine and

alignment tyrosine

Ala

PG G G C G u G >k,ku GMe

PG G c A A c U U G

PC U C u C G G U A GMe c 2

C C C U Y
G C

40

C

CAc G A G

A A G UHZ

;‘rGMe c 2

0

U

Aisop

A G G C GMe A 2 A

= 6-aminoisopentenyi

conventional the

(9)*

ones. proposed

The the A.

Base in

dupl

icat

ion,

could

be

(3, in

bases

changes

are that

parentheses;

of

sys tern

of bases

sRNAs,

presence

number

other

deletions,

indicated.

If

and

lead and

the

sRNAs

to if

G,

U,

comparisons

indeed

748

an

G G C G T Y

k(A)

k AMe C U C G c C C C C G G G A G A

:(A) U C C u G C A G U U G U C G

!H

gaps.

original evolved

the

and

--36-38 sequence

“invariant”

C,

by

e.g.

from

the

have

arisen

which

will length

from

are

Res idues

emphasized

second may

so,

C A G G T Y

Tv

C C

are is

the

C C G 9:G ;‘;T

abbreviations

the

differentiation

Ser

UH CM,2 G

64-68

A,

Ala

w W 3:i-i +:A U ?::;u SC C G G A C U C G U C C A

so

3 molecules from

alanine,

A G A C U G Y A AMe A2z Y C U U G A G A

includes

differentiate

may

yeast

4, 5).

(IO,ll);other

5)

formed

this

however,

4, all

in

COMMUNICATIONS

W

adenosine

anticodons

modified

are

other

The

identity

(.4)

of

kcUH2 U

60

sequences RNAs (3,

A G A Y U I G A Aisop A Y C U U U UOMe G G G C U U(C) U G C C C G CMe G

22

UH2 UH A2 A G G C GMe c 2 A

RESEARCH

Ser

Ziie G

G w

lH2

from

of base transfer

Vr

‘JH2

that

BIOPHYSICAL

Ser

C G U A G UH C2

are

AND

Ala

:kG 9:C G

lo

BIOCHEMICAL

*.

GMe2

It from

first

assumed and

serine

following

reveal

sRNA gene

the

greater

a common

is G,

than origin

this by

gene

l

Vol.

24,

No. 5, 1966

duplications,

BIOCHEMICAL

this

number

of

became

increased

might

anticodons

suggest

that by

AND

that

the

underwent

gene

dupl

BIOPHYSICAL

RESEARCH

genetic

code

differentiation

icat

Each

ions.

COMMUNICATIONS

evolved

as

the

duplication

from number

could

a small of

give

sRNAs rise

to

a new

anticodon. REFERENCES 1.

Ingram,

2.

1963.

v.M., Univ.

Press,

Hartley,

B.S., Nature

3.

4.

H.G., Edn.

5.

Madison,

Brown,

D.L.

0. 5 :422.

D;tting

Everett, and A.

and

H.

H.

1966

Abstracts,

Kung.

p.

1965, 221i

8.

Cantor,

C., press).

S.

Jaskunas

9.

Zamir,

A.,

R,W.

Halley

R-H., sot.

Il.

Biemann,

12.

Crick,

M.J.

Robins,

M.

L.

1965.

Marquisee, 147:1462. Chemie,

S.H.

international

Cold

Spring

31:43.

and E.L. Smith, Press, N.Y.),

and

M. Science

1965.

Angew.

Margoliash, E. (Academic

I.

Madison,

(Columbia

Smi 11 ie.

1966.

1965,

and

L.B.

Evolution

Feldman.

97.

Hall,

L.

and

and

J.T. Zamir.

p.

IO.

and Press,

Genetics 132.

Kauffmann

G.E. Everett and Symp. Quant. Biol. E.

in p.

Pauling. N.Y.),

7.

Zuckerkandl, (Academic

Hemoglobins Chapter 6,

J. Apgar, G.A. J.R. Penswick

J.T., Harbor

6.

J.R. 207:1157.

Ho1 ley, R.W., Merrell, Zachau,

The N.Y.)

in

in

Tinoco,

Evolving

Evolving

Genes

1966.

Jr..

1965.

Marquisee.

Stasiuk

and

Genes

R.

J.

J.

and

Proteins

and

Proteins

Mol.

Biol.

Biol.

Chem.

1966.

Thedford.

J.

(in

240:1267

Am.

88:2614. K.

F.H.C. manuscript.

and

S. 1965.

Tsunakawa.

1966.

Codon-anticodon

(cited pai ring

749

by -

Zachau, the

wobble

et

al.

the

1966).

hypothesis;

Chem.