RNA From Mathematical Models to Real Molecules
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2 RNA From Mathematical Models to Real Molecules 3. Optimization and Evolution of RNA Molecules Peter Schuster Institut für Theoretische hemie und Molekulare Strukturbiologie der Universität Wien IMPA enoma School Valdivia,
3 Web-Page for further information:
4 RNA molecules Bacteria Higher multicelluar organisms eneration time generations 10 6 generations 10 7 generations 10 sec 27.8 h = 1.16 d d 3.17 a 1 min 6.94 d 1.90 a a 20 min d a 380 a 10 h a a a 10 d 274 a a a 20 a a a a Time scales of evolutionary change
5 5' 3' Plus Strand Synthesis 5' 3' Plus Strand 3' Synthesis 5' 3' Plus Strand Minus Strand James Watson and Francis rick, ' 5' 5' Plus Strand 5' Minus Strand omplex Dissociation + 3' 3' omplementary replication as the simplest copying mechanism of RNA omplementarity is determined by Watson-rick base pairs: and A=U
6 (A) + I 1 f 1 I 2 + I 1 dx 1 / dt = f2 x 2 - x 1 Φ dx 2 / dt = f 1 x 1 - x 2 Φ (A) + I 2 f 2 I 1 + I 2 Φ =Σ i f x i ; Σ x = 1 ; i =1,2 i i i omplementary replication as the simplest molecular mechanism of reproduction
7 Equation for complementary replication: [I i ] = x i 0, f i > 0 ; i=1,2 Solutions are obtained by integrating factor transformation f x f x f x x f dt dx x x f dt dx = + = = = ,, φ φ φ () ( ) ( ) ( ) ( ) ( ) ( ) ( ) ( ) ( ) ,1 1,2 (0), (0) (0) (0), (0) (0) exp 0 ) ( exp 0 ) ( exp 0 exp 0 f f f x f x f x f x f t f f f t f f f t f t f f t x = = + = + + = γ γ γ γ γ γ 0 ) exp( as ) ( and ) ( ft f f f t x f f f t x
8 5' 3' Plus Strand Minus Strand Plus Strand Minus Strand 5' 3' 3' 5' Plus Strand 3' 5' + 5' 3' Minus Strand 3' 5' Direct replication of DNA is a higly complex copying mechanism involving more than ten different protein molecules. omplementarity is determined by Watson-rick base pairs: and A=T
9 (A) + I 1 f 1 I 1 + I 1 (A) + I 2 f 2 I 2 + I 2 dx / dt = f x - x i i i i Φ = x (f i - Φ i ) Φ =Σ j f j x j ; Σ x = 1 ; i,j =1,2,...,n j j (A) + I i f i I i + I i [I i] = x i 0 ; i =1,2,...,n ; [A] = a = constant f m = max { f j ; j=1,2,...,n} (A) + I m f m I m + I m x m (t) 1 for t (A) + I n f n I n + I n Reproduction of organisms or replication of molecules as the basis of selection
10 Selection equation: [I i ] = x i 0, f i > 0 n n ( f φ ), i = 1,2, L, n; x = 1; φ = f x f dx i = xi i i i j j j dt = = 1 = 1 Mean fitness or dilution flux, φ (t), is a non-decreasing function of time, n dφ = dt i= 1 f i dx dt i = f 2 ( ) 2 f = var{ f } 0 Solutions are obtained by integrating factor transformation ( 0) exp( f t) xi i xi () t = ; i = 1,2, L, n n x ( ) ( f jt) j = j 0 exp 1
11 s = ( f 2 -f 1 ) / f 1 ; f 2 > f 1 ; x 1 (0) = 1-1/N ; x 2 (0) = 1/N 1 Fraction of advantageous variant s = 0.1 s = 0.02 s = Time [enerations] Selection of advantageous mutants in populations of N = individuals
12 hanges in RNA sequences originate from replication errors called mutations. Mutations occur uncorrelated to their consequences in the selection process and are, therefore, commonly characterized as random elements of evolution.
13 5' 3' Plus Strand 5' 3' AAUAA AAUUAA Plus Strand Insertion 3' 5' 3' Minus Strand AAUAA AAUA Plus Strand 5' 3' Deletion Point Mutation The origins of changes in RNA sequences are replication errors called mutations.
14 Theory of molecular evolution M.Eigen, Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58 (1971), J. Thompson, J.L. McBride, On Eigen's theory of the self-organization of matter and the evolution of biological macromolecules. Math. Biosci. 21 (1974), B.L. Jones, R.H. Enns, S.S. Rangnekar, On the theory of selection of coupled macromolecular systems. Bull.Math.Biol. 38 (1976), M.Eigen, P.Schuster, The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. Naturwissenschaften 58 (1977), M.Eigen, P.Schuster, The hypercycle. A principle of natural self-organization. Part B: The abstract hypercycle. Naturwissenschaften 65 (1978), 7-41 M.Eigen, P.Schuster, The hypercycle. A principle of natural self-organization. Part : The realistic hypercycle. Naturwissenschaften 65 (1978), J. Swetina, P. Schuster, Self-replication with errors - A model for polynucleotide replication. Biophys.hem. 16 (1982), J.S. Mcaskill, A localization threshold for macromolecular quasispecies from continuously distributed replication rates. J.hem.Phys. 80 (1984), M.Eigen, J.Mcaskill, P.Schuster, The molecular quasispecies. Adv.hem.Phys. 75 (1989), Reidys,.Forst, P.Schuster, Replication and mutation on neutral networks. Bull.Math.Biol. 63 (2001), 57-94
15 hemical kinetics of molecular evolution M. Eigen, P. Schuster, `The Hypercycle, Springer-Verlag, Berlin 1979
16 I 1 + I j f j Q j1 I 2 + I j Σ dx / dt = f x - x i j jq ji j i Φ Φ = Σ f x j j i ; Σ x = 1 ; j j Σ Q i ij = 1 f j Q j2 f j Q ji I i + I j [I i ] = x i 0 ; i =1,2,...,n ; [A] = a = constant (A) + I j f j Q jj I j + I j Q = (1-) p ij l-d(i,j) p d(i,j) p... Error rate per digit f j Q jn I n + I j l... hain length of the polynucleotide d(i,j)... Hamming distance between I i and I j hemical kinetics of replication and mutation as parallel reactions
17 ... AU... d =2 d =1 H... A U UU... H d =1 H... UU... ity-block distance in sequence space 2D Sketch of sequence space Single point mutations as moves in sequence space
18 Mutation-selection equation: [I i ] = x i 0, f i > 0, Q ij 0 dx i n n n = f Q x x i n x f x j j ji j i φ, = 1,2, L, ; i i = 1; φ = j j j dt = = 1 = 1 = 1 f Solutions are obtained after integrating factor transformation by means of an eigenvalue problem x i () t = n 1 k n j= 1 ( 0) exp( λkt) c ( 0) exp( λ t) l = 0 ik ck ; i = 1,2, L, n; c (0) = n 1 k l k= 0 jk k k n i= 1 h ki x i (0) W 1 { f Q ; i, j= 1,2, L, n} ; L = { l ; i, j= 1,2, L, n} ; L = H = { h ; i, j= 1,2, L, n} i ij ij ij { λ ; k = 0,1,, n 1} 1 L W L = Λ = k L
19 oncentration Master sequence Mutant cloud Sequence space The molecular quasispecies in sequence space
20 Quasispecies as a function of the replication accuracy q
21 In evolution variation occurs on genotypes but selection operates on the phenotype. Mappings from genotypes into phenotypes are highly complex objects. The only computationally accessible case is in the evolution of RNA molecules. The mapping from RNA sequences into secondary structures and function, sequence structure function, is used as a model for the complex relations between genotypes and phenotypes. Fertile progeny measured in terms of fitness in population biology is determined quantitatively by replication rate constants of RNA molecules. Population biology Molecular genetics Evolution of RNA molecules enotype enome RNA sequence Phenotype Organism RNA structure and function Fitness Reproductive success Replication rate constant The RNA model
22 Optimized element: RNA structure
23 Hamming distance d (S,S ) = H (i) (ii) (iii) d (S,S) = 0 H 1 1 d (S,S ) = d (S,S ) H 1 2 H 2 1 d (S,S) d (S,S) + d (S,S) H 1 3 H 1 2 H 2 3 The Hamming distance between structures in parentheses notation forms a metric in structure space
24 Replication rate constant: f k = / [ + d S (k) ] d S (k) = d H (S k,s ) f 6 f 7 f5 f 0 f f 4 f 1 f 2 f 3 Evaluation of RNA secondary structures yields replication rate constants
25 Stock Solution Reaction Mixture Replication rate constant: f k = / [ + d S (k) ] d S (k) = d H (S k,s ) Selection constraint: # RNA molecules is controlled by the flow N ( t) N ± N The flowreactor as a device for studies of evolution in vitro and in silico
26 3'-End 5'-End Randomly chosen initial structure Phenylalanyl-tRNA as target structure
27 oncentration Master sequence Mutant cloud Off-the-cloud mutations Sequence space The molecular quasispecies in sequence space
28 enotype-phenotype Mapping I { S { = ( I { ) S { f = ƒ( S ) { { Evaluation of the Phenotype Mutation Q {j f 2 I 2 f 1 I1 I n I 1 f n I 2 f 2 f 1 I n+1 f n+1 f { Q f 3 I 3 Q f 3 I 3 f 4 I 4 I { f { I 4 I 5 f 4 f 5 f 5 I 5 Evolutionary dynamics including molecular phenotypes
29 50 S Average distance from initial structure 50 - d Evolutionary trajectory Time (arbitrary units) In silico optimization in the flow reactor: Trajectory (biologists view)
30 50 S Average structure distance to target d Evolutionary trajectory Time (arbitrary units) In silico optimization in the flow reactor: Trajectory (physicists view)
31 36 Relay steps Number of relay step 38 Evolutionary trajectory Time Average structure distance to target d S Endconformation of optimization
32 36 Relay steps Number of relay step 38 Evolutionary trajectory Time Average structure distance to target d S Reconstruction of the last step 43 44
33 36 Relay steps Number of relay step Average structure distance to target d S 42 Evolutionary trajectory Reconstruction of last-but-one step ( 44) Time
34 36 Relay steps Number of relay step Average structure distance to target d S Evolutionary trajectory Reconstruction of step ( 43 44) Time
35 36 Relay steps Number of relay step Average structure distance to target d S Evolutionary trajectory Reconstruction of step ( ) Time
36 Average structure distance to target d S 10 Relay steps Number of relay step Evolutionary trajectory Time Evolutionary process Reconstruction Reconstruction of the relay series
37 Transition inducing point mutations Neutral point mutations hange in RNA sequences during the final five relay steps 39 44
38 50 Relay steps S Average structure distance to target d Evolutionary trajectory Time (arbitrary units) In silico optimization in the flow reactor: Trajectory and relay steps
39 50 Relay steps Main transitions Average structure distance to target d S Evolutionary trajectory Time (arbitrary units) In silico optimization in the flow reactor: Main transitions
40 Three important steps in the formation of the trna clover leaf from a randomly chosen initial structure corresponding to three main transitions.
41 10-1 3'-End Frequency of occurrence '-End Frequent neighbors Rare neighbors Minor transitions Main transitions Rank Probability of occurrence of different structures in the mutational neighborhood of trna phe
42 Definition of an -neighborhood of structure S k Y(S k )... set of all structures occurring in the Hamming distance one neighborhood of the neutral network k of S k jk... number of contacts between the two neutral networks j and k jk = kj Probability of occurrence: ρ (S j ; S k ) = γ jk n( κ 1) k ; ρ (S k ; S j ) ρ (S j ; S k ) { S Υ(S ) ρ(s ;S ) ε } ε neighborhood of S : Ψε (S ) = > k k j k j k
43 AU Movies of optimization trajectories over the AU and the alphabet
44 Frequency Runtime of trajectories Statistics of the lengths of trajectories from initial structure to target (AU-sequences)
45 Main transitions 0.2 Frequency All transitions Number of transitions Statistics of the numbers of transitions from initial structure to target (AU-sequences)
46 Alphabet Runtime Transitions Main transitions No. of runs AU U Statistics of trajectories and relay series (mean values of log-normal distributions)
47 Number of relay step 28 neutral point mutations during a long quasi-stationary epoch Average structure distance to target d S Uninterrupted presence Evolutionary trajectory Time (arbitrary units) Transition inducing point mutations Neutral point mutations Neutral genotype evolution during phenotypic stasis
48 Variation in genotype space during optimization of phenotypes Mean Hamming distance within the population and drift velocity of the population center in sequence space.
49 Spread of population in sequence space during a quasistationary epoch: t = 150
50 Spread of population in sequence space during a quasistationary epoch: t = 170
51 Spread of population in sequence space during a quasistationary epoch: t = 200
52 Spread of population in sequence space during a quasistationary epoch: t = 350
53 Spread of population in sequence space during a quasistationary epoch: t = 500
54 Spread of population in sequence space during a quasistationary epoch: t = 650
55 Spread of population in sequence space during a quasistationary epoch: t = 820
56 Spread of population in sequence space during a quasistationary epoch: t = 825
57 Spread of population in sequence space during a quasistationary epoch: t = 830
58 Spread of population in sequence space during a quasistationary epoch: t = 835
59 Spread of population in sequence space during a quasistationary epoch: t = 840
60 Spread of population in sequence space during a quasistationary epoch: t = 845
61 Spread of population in sequence space during a quasistationary epoch: t = 850
62 Spread of population in sequence space during a quasistationary epoch: t = 855
63 Massif entral Examples of smooth landscapes on Earth Mount Fuji
64 Dolomites Examples of rugged landscapes on Earth Bryce anyon
65 Fitness End of Walk Start of Walk enotype Space Evolutionary optimization in absence of neutral paths in sequence space
66 Adaptive Periods End of Walk Fitness Random Drift Periods Start of Walk enotype Space Evolutionary optimization including neutral paths in sequence space
67 rand anyon Example of a landscape on Earth with neutral ridges and plateaus
68 Neutral ridges and plateus
69 Acknowledgement of support Fonds zur Förderung der wissenschaftlichen Forschung (FWF) Projects No , 10578, 11065, , and Universität Wien Jubiläumsfonds der Österreichischen Nationalbank Project No. Nat-7813 European ommission: Project No. EU Siemens A, Austria The Santa Fe Institute and the Universität Wien The software for producing RNA movies was developed by Robert iegerich and coworkers at the Universität Bielefeld
70 oworkers Walter Fontana, Santa Fe Institute, NM Universität Wien hristian Reidys, hristian Forst, Los Alamos National Laboratory, NM Peter Stadler, Bärbel Stadler, Universität Leipzig, E Ivo L.Hofacker, hristoph Flamm, Universität Wien, AT Andreas Wernitznig, Michael Kospach, Universität Wien, AT Ulrike Langhammer, Ulrike Mückstein, Stefanie Widder Jan upal, Kurt rünberger, Andreas Svrček-Seiler, Stefan Wuchty Ulrike öbel, Institut für Molekulare Biotechnologie, Jena, E Walter rüner, Stefan Kopp, Jaqueline Weber
71 Web-Page for further information:
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