×

Motif frequency and evolutionary search times in RNA populations. (English) Zbl 1397.92541

Summary: RNA molecules, through their dual identity as sequence and structure, are an appropriate experimental and theoretical model to study the genotype-phenotype map and evolutionary processes taking place in simple replicator populations. In this computational study, we relate properties of the sequence-structure map, in particular the abundance of a given secondary structure in a random pool, with the number of replicative events that an initially random population of sequences needs to find that structure through mutation and selection. For common structures, this search process turns out to be much faster than for rare structures. Furthermore, search and fixation processes are more efficient in a wider range of mutation rates for common structures, thus indicating that evolvability of RNA populations is not simply determined by abundance. We also find significant differences in the search and fixation processes for structures of same abundance, and relate them with the number of base pairs forming the structure. Moreover, the influence of the nucleotide content of the RNA sequences on the search process is studied. Our results advance in the understanding of the distribution and attainability of RNA secondary structures. They hint at the fact that, beyond sequence length and sequence-to-function redundancy, the mutation rate that permits localization and fixation of a given phenotype strongly depends on its relative abundance and global, in general non-uniform, distribution in sequence space.

MSC:

92D20 Protein sequences, DNA sequences
68T20 Problem solving in the context of artificial intelligence (heuristics, search strategies, etc.)
92D15 Problems related to evolution
92C40 Biochemistry, molecular biology

References:

[1] Ancel, L.W.; Fontana, W., Plasticity, evolvability, and modularity in RNA, J. exp. zool., 288, 242-283, (2000)
[2] Bartel, D.P.; Szostak, J.W., Isolation of new ribozymes from a large pool of random sequences, Science, 261, 1411-1418, (1993)
[3] Bonhoeffer, S.; McCaskill, J.S.; Stadler, P.F.; Schuster, P., RNA multi-structure landscapes, Eur. biophys. J., 22, 13-24, (1993)
[4] Briones, C.; Stich, M.; Manrubia, S.C., The dawn of the RNA world: toward functional complexity through ligation of random RNA oligomers, RNA, 15, 743-749, (2009)
[5] Carothers, J.M.; Oestreich, S.C.; Davis, J.H.; Szostak, J.W., Informational complexity and functional activity of RNA structures, J. am. chem. soc., 126, 5130-5137, (2004)
[6] Clote, P.; Kranakis, E.; Krizanc, D.; Salvy, B., Asymptotics of canonical and saturated RNA secondary structures, J. bioinform. comput. biol., 7, 869-893, (2009)
[7] Cowperthwaite, M.C.; Economo, E.P.; Harcombe, W.R.; Miller, E.L.; Ancel Meyers, L., The ascent of the abundant: how mutational networks constrain evolution, Plos comput. biol., 4, e1000110, (2008)
[8] Dirks, R.M.; Lin, M.; Winfree, E.; Pierce, N.A., Paradigms for computational nucleic acid design, Nucleic acids res., 32, 1392-1403, (2004)
[9] Fontana, W.; Griesmacher, T.; Schnabl, W.; Stadler, P.F.; Schuster, P., Statistics of landscapes based on free energies, replication and degradation rate constants of RNA secondary structures, Monatsh. chem., 122, 795-819, (1991)
[10] Fontana, W.; Konings, D.A.M.; Stadler, P.F.; Schuster, P., Statistics of RNA secondary structures, Biopolymers, 33, 1389-1404, (1993)
[11] Fontana, W.; Schuster, P., A computer-model of evolutionary optimization, Biophys. chem., 26, 123-147, (1987)
[12] Gan, H.H.; Pasquali, S.; Schlick, T., Exploring the repertoire of RNA secondary motifs using graph theory; implications for RNA design, Nucleic acids res., 31, 2926-2943, (2003)
[13] Gevertz, J.; Gan, H.H.; Schlick, T., In vitro RNA random pools are not structurally diverse: a computational analysis, RNA, 11, 853-863, (2005)
[14] Grüner, W.; Giegerich, R.; Strothmann, D.; Reidys, C.; Weber, J.; Hofacker, I.L.; Stadler, P.F.; Schuster, P., Analysis of RNA sequence structure maps by exhaustive enumeration. I. neutral networks, Monatsh. chem., 127, 355-374, (1996)
[15] Grüner, W.; Giegerich, R.; Strothmann, D.; Reidys, C.; Weber, J.; Hofacker, I.L.; Stadler, P.F.; Schuster, P., Analysis of RNA sequence structure maps by exhaustive enumeration. II. structures of neutral networks and shape space covering, Monatsh. chem., 127, 375-389, (1996)
[16] Held, D.M.; Greathouse, S.T.; Agrawal, A.; Burke, D.H., Evolutionary landscapes for the acquisition of new ligand recognition by RNA aptamers, J. mol. evol., 57, 299-308, (2003)
[17] Hofacker, I.L.; Fontana, W.; Stadler, P.F.; Bonhoeffer, L.S.; Tacker, M.; Schuster, P., Fast folding and comparison of RNA secondary structures, Monatsh. chem., 125, 167-188, (1994)
[18] Hofacker, I.L.; Schuster, P.; Stadler, P.F., Combinatorics of RNA secondary structures, Discr. appl. math., 88, 207-237, (1998) · Zbl 0918.05004
[19] Huynen, M.A.; Konings, D.A.M.; Hogeweg, P., Multiple coding and the evolutionary properties of RNA secondary structure, J. theor. biol., 165, 251-267, (1993)
[20] Huynen, M.A.; Stadler, P.F.; Fontana, W., Smoothness within ruggedness: the role of neutrality in adaptation, Proc. natl. acad. sci. USA, 93, 397-401, (1996)
[21] Joyce, G.F., Directed evolution of nucleic acid enzymes, Annu. rev. biochem., 73, 791-836, (2004)
[22] Kennedy, R.; Lladser, M.E.; Wu, Z.; Zhang, C.; Yarus, M.; de Sterck, H.; Knight, R., Natural and artificial RNAs occupy the same restricted region of sequence space, RNA, 16, 280-289, (2010)
[23] Kim, N.; Gan, H.H.; Schlick, T., A computational proposal for designing structured RNA pools for in vitro selection of rnas, RNA, 13, 478-492, (2007)
[24] Knight, R.; DeSterck, H.; Markel, R.; Smit, S.; Oshmyansky, A.; Yarus, M., Abundance of correctly folded RNA motifs in sequence space, calculated on computational grids, Nucleic acids res., 33, 5924-5935, (2005)
[25] Pedersen, J.S.; Bejerano, G.; Siepel, A.; Rosenbloom, K.; Lindblad-Toh, K.; Lander, E.S.; Kent, J.; Miller, W.; Haussler, D., Identification and classification of conserved RNA secondary structures in the human genome, Plos comput. biol., 2, e33, (2006)
[26] Petrillo, M.; Silvestro, G.; DiNocera, P.P.; Boccia, A.; Paolella, G., Stem-loop structures in prokaryotic genomes, BMC genomics, 7, 170, (2006)
[27] Pitt, J.N.; Ferré-D’Amaré, A.R., Rapid construction of empirical RNA fitness landscapes, Science, 330, 376-379, (2010)
[28] Puerta-Fernández, E.; Romero-López, C.; Barroso-delJesús, A.; Berzal-Herranz, A., Ribozymes: recent advances in the development of RNA tools, FEMS microbiol. rev., 27, 75-97, (2003)
[29] Rajamani, S.; Ichida, J.K.; Antal, T.; Treco, D.A.; Leu, K.; Nowak, M.A.; Szostak, J.W.; Chen, I.A., Effect of stalling after mismatches on the error catastrophy in nonenzymatic nucleic acid replication, J. am. chem. soc., 132, 5880-5885, (2010)
[30] Sabeti, P.C.; Unrau, P.J.; Bartel, D.P., Accessing rare activities from random RNA sequences: the importance of the length of molecules in the starting pool, Chem. biol., 4, 767-774, (1997)
[31] Schuster, P., Molecular insights into evolution of phenotypes, (), 163-215
[32] Schuster, P., Prediction of RNA secondary structures: from theory to models and real molecules, Rep. prog. phys., 69, 1419-1477, (2006)
[33] Schuster, P.; Fontana, W.; Stadler, P.F.; Hofacker, I.L., From sequences to shapes and back: a case study in RNA secondary structures, Proc. R. soc. London B, 255, 279-284, (1994)
[34] Stadler, P.F., Fitness landscapes arising from the sequence – structure maps of biopolymers, J. mol. struc. (theochem.), 463, 7-19, (1999)
[35] Stich, M.; Briones, C.; Manrubia, S.C., Collective properties of evolving molecular quasispecies, BMC evol. biol., 7, 110, (2007)
[36] Stich, M.; Briones, C.; Manrubia, S.C., On the structural repertoire of pools of short, random RNA sequences, J. theor. biol., 252, 750-763, (2008)
[37] Stich, M.; Lázaro, E.; Manrubia, S.C., Phenotypic effect of mutations in evolving populations of RNA molecules, BMC evol. biol., 10, 46, (2010)
[38] Stich, M.; Lázaro, E.; Manrubia, S.C., Variable mutation rates as an adaptive strategy in replicator populations, Plos one, 5, e11186, (2010)
[39] Tacker, M.; Stadler, P.F.; Bornberg-Bauer, E.G.; Hofacker, I.L.; Schuster, P., Algorithm independent properties of RNA secondary structure predictions, Eur. biophys. J., 25, 115-130, (1996)
[40] Waldispühl, J.; Devadas, S.; Berger, B.; Clote, P., Efficient algorithms for probing the RNA mutation landscape, Plos comput. biol., 4, e1000124, (2008)
[41] Waterman, M.S., Secondary structure of single-stranded nucleic acids, (), 167-212 · Zbl 0434.05007
[42] Watts, J.M.; Dang, K.K.; Gorelick, R.J.; Leonard, C.W.; Bess, J.W.; Swanstrom, R.; Burch, C.L.; Weeks, K.M., Architecture and secondary structure of an entire HIV-1 RNA genome, Nature, 460, 711-719, (2009)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.