Evolutionary Genomics
Evolutionary Change at Genome Scale
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Journal of Molecular Evolution
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Updated: 1 hour 26 min ago Evolution of Enzymatic Activities of Testis-Specific Short-Chain Dehydrogenase/Reductase in DrosophilaAbstract The testis-specific gene Jingwei (jgw) is a newly evolved short-chain dehydrogenase/reductase in Drosophila. Preliminary substrate screening indicated that JGW prefers long-chain primary alcohols as substrates, including several exotic alcohols such as farnesol and geraniol. Using steady-state kinetics analyses and molecular docking, we not only confirmed JGW’s substrate specificity, but also demonstrated that the new enzymatic activities of JGW evolved extensively after exon-shuffling from a preexisting enzyme. Analysis of JGW orthologs in sister species shows that subsequent evolutionary changes following the birth of JGW altered substrate specificities and enzyme stabilities. Our results lend support to a general mechanism for the evolution of a new enzyme, in which catalytic chemistry evolves first followed by diversification of substrate utilization.
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Genes Devoid of Full-Length Transposable Element Insertions are Involved in Development and in the Regulation of Transcription in Human and Closely Related SpeciesAbstract Transposable elements (TEs) are major components of mammalian genomes, and their impact on genome evolution is now well established. In recent years several findings have shown that they are associated with the expression level and function of genes. In this study, we analyze the relationships between human genes and full-length TE copies in terms of three factors (gene function, expression level, and selective pressure). We classified human genes according to their TE density, and found that TE-free genes are involved in important functions such as development, transcription, and the regulation of transcription, whereas TE-rich genes are involved in functions such as transport and metabolism. This trend is conserved through evolution. We show that this could be explained by a stronger selection pressure acting on both the coding and non-coding regions of TE-free genes than on those of TE-rich genes. The higher level of expression found for TE-rich genes in tumor and immune system tissues suggests that TEs play an important role in gene regulation.
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Classification of Nucleotide Sequences Using Support Vector MachinesAbstract Species identification is one of the most important issues in biological studies. Due to recent increases in the amount of genomic information available and the development of DNA sequencing technologies, the applicability of using DNA sequences to identify species (commonly referred to as “DNA barcoding”) is being tested in many areas. Several methods have been suggested to identify species using DNA sequences, including similarity scores, analysis of phylogenetic and population genetic information, and detection of species-specific sequence patterns. Although these methods have demonstrated good performance under a range of circumstances, they also have limitations, as they are subject to loss of information, require intensive computation and are sensitive to model mis-specification, and can be difficult to evaluate in terms of the significance of identification. Here, we suggest a new DNA barcoding method in which support vector machine (SVM) procedures are adopted. Our new method is nonparametric and thus is expected to be robust for a wide range of evolutionary scenarios as well as multilocus analyses. Furthermore, we describe bootstrap procedures that can be used to test the significances of species identifications. We implemented a novel conversion technique for transforming sequence data to real-valued vectors, and therefore, bootstrap procedures can be easily combined with our SVM approach. In this study, we present the results of simulation studies and empirical data analyses to demonstrate the performance of our method and discuss its properties.
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Sexual Selection and the Molecular Evolution of ADAM ProteinsAbstract Rapid evolution has been identified for many reproductive genes and recent studies have combined phylogenetic tests and information on species mating systems to test sexual selection. Here we examined the molecular evolution of the ADAM gene family, a diverse group of 35 proteins capable of adhesion to and cleavage of other proteins, using sequence data from 25 mammalian genes. Out of the 25 genes analyzed, all those expressed in male reproductive tissue showed evidence of positive selection. Positively selected amino acids within the protein adhesion domain were only found in sperm surface ADAM proteins (ADAMs 1, 2, 3, 4, and 32) suggesting selection driven by male × female interactions. We tested heterogeneity in rates of evolution of the adhesion domain of ADAM proteins by using sequence data from Hominidae and macaques. The use of the branch and branch-site models (PAML) showed evidence of higher d N/d S and/or positive selection linked to branches experiencing high postmating selective pressures (chimpanzee and macaque) for Adams 2, 18, and 23. Moreover, we found consistent higher proportion of nonsynonymous relative to synonymous and noncoding sequence substitutions in chimpanzee and/or macaque only for Adams 2, 18, and 23. Our results suggest that lineage-specific sexual selection bouts might have driven the evolution of the adhesion sperm protein surface domains of ADAMs 2 and 18 in primates. Adams 2 and 18 are localized in chromosome 8 of primates and adjacent to each other, so their evolution might have also been influenced by their common genome localization.
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Variable Numbers of Tandem Repeats in Plasmodium falciparum GenesAbstract Genome variation studies in Plasmodium falciparum have focused on SNPs and, more recently, large-scale copy number polymorphisms and ectopic rearrangements. Here, we examine another source of variation: variable number tandem repeats (VNTRs). Interspersed low complexity features, including the well-studied P. falciparum microsatellite sequences, are commonly classified as VNTRs; however, this study is focused on longer coding VNTR polymorphisms, a small class of copy number variations. Selection against frameshift mutation is a main constraint on tandem repeats (TRs) in coding regions, while limited propagation of TRs longer than 975 nt total length is a minor restriction in coding regions. Comparative analysis of three P. falciparum genomes reveals that more than 9% of all P. falciparum ORFs harbor VNTRs, much more than has been reported for any other species. Moreover, genotyping of VNTR loci in a drug-selected line, progeny of a genetic cross, and 334 field isolates demonstrates broad variability in these sequences. Functional enrichment analysis of ORFs harboring VNTRs identifies stress and DNA damage responses along with chromatin modification activities, suggesting an influence on genome mutability and functional variation. Analysis of the repeat units and their flanking regions in both P. falciparum and Plasmodium reichenowi sequences implicates a replication slippage mechanism in the generation of TRs from an initially unrepeated sequence. VNTRs can contribute to rapid adaptation by localized sequence duplication. They also can confound SNP-typing microarrays or mapping short-sequence reads and therefore must be accounted for in such analyses.
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Explosive Expansion of βγ-Crystallin Genes in the Ancestral VertebrateAbstract In jawed vertebrates, βγ-crystallins are restricted to the eye lens and thus excellent markers of lens evolution. These βγ-crystallins are four Greek key motifs/two domain proteins, whereas the urochordate βγ-crystallin has a single domain. To trace the origin of the vertebrate βγ-crystallin genes, we searched for homologues in the genomes of a jawless vertebrate (lamprey) and of a cephalochordate (lancelet). The lamprey genome contains orthologs of the gnathostome βB1-, βA2- and γN-crystallin genes and a single domain γN-crystallin-like gene. It contains at least two γ-crystallin genes, but lacks the gnathostome γS-crystallin gene. The genome also encodes a non-lenticular protein containing βγ-crystallin motifs, AIM1, also found in gnathostomes but not detectable in the uro- or cephalochordate genome. The four cephalochordate βγ-crystallin genes found encode two-domain proteins. Unlike the vertebrate βγ-crystallins but like the urochordate βγ-crystallin, three of the predicted proteins contain calcium-binding sites. In the cephalochordate βγ-crystallin genes, the introns are located within motif-encoding region, while in the urochordate and in the vertebrate βγ-crystallin genes the introns are between motif- and/or domain encoding regions. Coincident with the evolution of the vertebrate lens an ancestral urochordate type βγ-crystallin gene rapidly expanded and diverged in the ancestral vertebrate before the cyclostomes/gnathostomes split. The β- and γN-crystallin genes were maintained in subsequent evolution, and, given the selection pressure imposed by accurate vision, must be essential for lens function. The γ-crystallin genes show lineage specific expansion and contraction, presumably in adaptation to the demands on vision resulting from (changes in) lifestyle.
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Evolution of the Cinnamyl/Sinapyl Alcohol Dehydrogenase (CAD/SAD) Gene Family: The Emergence of Real Lignin is Associated with the Origin of Bona Fide CADAbstract Lignin plays a vital role in plant adaptation to terrestrial environments. The cinnamyl alcohol dehydrogenase (CAD) catalyzes the last step in monolignol biosynthesis and might have contributed to the lignin diversity in plants. To investigate the evolutionary history and functional differentiation of the CAD gene family, we made a comprehensive evolutionary analysis of this gene family from 52 species, including bacteria, early eukaryotes and green plants. The phylogenetic analysis, together with gene structure and function, indicates that all members of land plants, except two of moss, could be divided into three classes. Members of Class I (bona fide CAD), generally accepted as the primary genes involved in the monolignol biosynthesis, are all from vascular plants, and form a robustly supported monophyletic group with the lycophyte CADs at the basal position. This class is also conserved in the predicted three-dimensional structure and the residues constituting the substrate-binding pocket of the proteins. Given that Selaginella has real lignin, the above evidence strongly suggests that the earliest occurrence of the bona fide CAD in the lycophyte could be directly correlated with the origin of lignin. Class II comprises members more similar to the aspen sinapyl alcohol dehydrogenase gene, and includes three groups corresponding to lycophyte, gymnosperm, and angiosperm. Class III is conserved in land plants. The three classes differ in patterns of evolution and expression, implying that functional divergence has occurred among them. Our study also supports the hypothesis of convergent evolution of lignin biosynthesis between red algae and vascular plants.
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Was Wright Right? The Canonical Genetic Code is an Empirical Example of an Adaptive Peak in Nature; Deviant Genetic Codes Evolved Using Adaptive BridgesAbstract The canonical genetic code is on a sub-optimal adaptive peak with respect to its ability to minimize errors, and is close to, but not quite, optimal. This is demonstrated by the near-total adjacency of synonymous codons, the similarity of adjacent codons, and comparisons of frequency of amino acid usage with number of codons in the code for each amino acid. As a rare empirical example of an adaptive peak in nature, it shows adaptive peaks are real, not merely theoretical. The evolution of deviant genetic codes illustrates how populations move from a lower to a higher adaptive peak. This is done by the use of “adaptive bridges,” neutral pathways that cross over maladaptive valleys by virtue of masking of the phenotypic expression of some maladaptive aspects in the genotype. This appears to be the general mechanism by which populations travel from one adaptive peak to another. There are multiple routes a population can follow to cross from one adaptive peak to another. These routes vary in the probability that they will be used, and this probability is determined by the number and nature of the mutations that happen along each of the routes. A modification of the depiction of adaptive landscapes showing genetic distances and probabilities of travel along their multiple possible routes would throw light on this important concept.
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Actin Gene Family Dynamics in Cryptomonads and Red AlgaeAbstract Here we present evidence for a complex evolutionary history of actin genes in red algae and cryptomonads, a group that acquired photosynthesis secondarily through the engulfment of a red algal endosymbiont. Four actin genes were found in the nuclear genome of the cryptomonad, Guillardia theta, and in the genome of the red alga, Galdieria sulphuraria, a member of the Cyanidiophytina. Phylogenetic analyses reveal that the both organisms possess two distinct sequence types, designated “type-1” and “type-2.” A weak but consistent phylogenetic affinity between the cryptomonad type-2 sequences and the type-2 sequences of G. sulphuraria and red algae belonging to the Rhodophytina was observed. This is consistent with the possibility that the cryptomonad type-2 sequences are derived from the red algal endosymbiont that gave rise to the cryptomonad nucleomorph and plastid. Red algae as a whole possess two very different actin sequence types, with G. sulphuraria being the only organism thus far known to possess both. The common ancestor of Rhodophytina and Cyanidiophytina may have had two actin genes, with differential loss explaining the distribution of these genes in modern-day groups. Our study provides new insight into the evolution and divergence of actin genes in cryptomonads and red algae, and in doing so underscores the challenges associated with heterogeneity in actin sequence evolution and ortholog/paralog detection.
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Mutation Biases and Mutation Rate Variation Around Very Short Human Microsatellites Revealed by Human–Chimpanzee–Orangutan Genomic Sequence AlignmentsAbstract I have studied mutation patterns around very short microsatellites, focusing mainly on sequences carrying only two repeat units. By using human–chimpanzee–orangutan alignments, inferences can be made about both the relative rates of mutations and which bases have mutated. I find remarkable non-randomness, with mutation rate depending on a base’s position relative to the microsatellite, the identity of the base itself and the motif in the microsatellite. Comparing the patterns around (AC)2 with those around other four-base combinations reveals that (AC)2 does not stand out as being special in the sense that non-repetitive tetramers also generate strong mutation biases. However, comparing (AC)2 and (AC)3 with (AC)4 reveals a step change in both the rate and nature of mutations occurring, suggesting a transition state, (AC)4 exhibiting an alternating high–low mutation rate pattern consistent with the sequence patterning seen around longer microsatellites. Surprisingly, most changes in repeat number occur through base substitutions rather than slippage, and the relative probability of gaining versus losing a repeat in this way varies greatly with repeat number. Slippage mutations reveal rather similar patterns of mutability compared with point mutations, being rare at two repeats where most cause the loss of a repeat, with both mutation rate and the proportion of expansion mutations increasing up to 6–8 repeats. Inferences about longer repeat tracts are hampered by uncertainties about the proportion of multi-species alignments that fail due to multi-repeat mutations and other rearrangements.
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Accelerated Evolutionary Rate of Housekeeping Genes in TunicatesAbstract Phylogenomics has recently revealed that tunicates represent the sister-group of vertebrates in the newly defined clade Olfactores. However, phylogenomic and comparative genomic studies have also suggested that tunicates are characterized by an elevated rate of molecular evolution and a high degree of genomic divergence. Despite the recurrent interest in the group, the picture of tunicate peculiar evolutionary dynamics is still fragmentary, as it mainly lies in studies focusing on only a few model species. In order to expand the available genomic data for the group, we used the high-throughput 454 technology to sequence the partial transcriptome of a previously unsampled tunicate, Microcosmus squamiger. This allowed us to get further insights into tunicate-accelerated evolution through a comparative analysis based on pertinent phylogenetic markers, i.e., a core of 35 housekeeping genes conserved across bilaterians. Our results showed that tunicates evolved on average about two times faster than the other chordates, yet the degree of this acceleration varied extensively upon genes and upon lineages. Appendicularia and Aplousobranchia were detected as the most divergent groups which were also characterized by highly heterogeneous substitution rates across genes. Finally, an estimation of the d N/d S ratio in three pairs of closely related taxa within Olfactores did not reveal strong differences between the tunicate and vertebrate lineages suggesting that for this set of housekeeping genes, the accelerated evolution of tunicates is plausibly due to an elevated mutation rate rather than to particular selective effects.
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Functional Diversification and Evolution of Antifreeze Proteins in the Antarctic Fish Lycodichthys dearborniAbstract Antifreeze proteins (AFPs) have independently evolved in many organisms. AFPs act by binding to ice crystals, effectively lowering the freezing point. AFPs are often at high copy number in a genome and diversity exists between copies. Type III antifreeze proteins are found in Arctic and Antarctic eel pouts, and have previously been shown to evolve under positive selection. Here we combine molecular and proteomic techniques to understand the molecular evolution and diversity of Type III antifreeze proteins in a single individual Antarctic fish Lycodichthys dearborni. Our expressed sequence tag (EST) screen reveals that at least seven different AFP variants are transcribed, which are ultimately translated into five different protein isoforms. The isoforms have identical 66 base pair signal sequences and different numbers of subsequent ice-binding domains followed by a stop codon. Isoforms with one ice-binding unit (monomer), two units (dimer), and multiple units (multimer) were present in the EST library. We identify a previously uncharacterized protein dimer, providing further evidence that there is diversity between Type III AFP isoforms, perhaps driven by positive selection for greater thermal hysteresis. Proteomic analysis confirms that several of these isoforms are translated and present in the liver. Our molecular evolution study shows that paralogs have diverged under positive selection. We hypothesize that antifreeze protein diversity is an important contributor to depressing the serum freezing point.
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De Novo Evolution of Complex, Global and Hierarchical Gene Regulatory MechanismsAbstract Gene regulatory networks exhibit complex, hierarchical features such as global regulation and network motifs. There is much debate about whether the evolutionary origins of such features are the results of adaptation, or the by-products of non-adaptive processes of DNA replication. The lack of availability of gene regulatory networks of ancestor species on evolutionary timescales makes this a particularly difficult problem to resolve. Digital organisms, however, can be used to provide a complete evolutionary record of lineages. We use a biologically realistic evolutionary model that includes gene expression, regulation, metabolism and biosynthesis, to investigate the evolution of complex function in gene regulatory networks. We discover that: (i) network architecture and complexity evolve in response to environmental complexity, (ii) global gene regulation is selected for in complex environments, (iii) complex, inter-connected, hierarchical structures evolve in stages, with energy regulation preceding stress responses, and stress responses preceding growth rate adaptations and (iv) robustness of evolved models to mutations depends on hierarchical level: energy regulation and stress responses tend not to be robust to mutations, whereas growth rate adaptations are more robust and non-lethal when mutated. These results highlight the adaptive and incremental evolution of complex biological networks, and the value and potential of studying realistic in silico evolutionary systems as a way of understanding living systems.
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Insights into the Phylogeny or Arylamine N-Acetyltransferases in FungiAbstract Previous studies have shown that Eumycetes fungi can acylate arylamine thanks to arylamine N-acetyltransferases, xenobiotic-metabolizing enzymes also found in animals and bacteria. In this article, we present the results of mining 96 available fungal genome sequences for arylamine N-acetyltransferase genes and propose their phylogeny. The filamentous Pezizomycotina are shown to possess many putative N-acetyltransferases, whilst these are often lacking in other fungal groups. The evolution of the N-acetyltransferases is best explained by the presence of at least one gene in the opisthokont ancestor of the fungi and animal kingdoms, followed by recurrent gene losses and gene duplications. A possible horizontal gene transfer event may have occurred from bacteria to the basidiomycetous yeast Malassezia globosa.
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The Role of the Formamide/Zirconia System in the Synthesis of Nucleobases and Biogenic Carboxylic Acid DerivativesAbstract We describe the one-pot synthesis of a large variety of nucleic acid bases and related compounds from formamide in the presence of zirconium minerals as catalysts. The major products observed are: purine, 2-hydroxy pyrimidine, 5-hydroxy pyrimidine, isocytosine, adenine, urea, and carbodiimide. The synthesis of low molecular weight amides and carboxylic acid derivatives (intermediates of extant metabolism) was also observed: glyoxylamide, glycolic-, lactic-, succinic-, oxalic-, fumaric-, and maleic acids. As the major problem in the origin of informational polymers is the instability of their precursors, we also investigated the effects of zirconia minerals on the stability of ribooligonucleotides in formamide and in water. The relevance of these findings with respect to the origin of informational polymers and primordial metabolism is discussed.
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Evolutionary History and Functional Diversification of Phosphomannomutase GenesAbstract Phosphomannomutases (PMMs) catalyze the interconversion of mannose-6-phosphate to mannose-1-phosphate. In humans, two PMM enzymes exist—PMM1 and PMM2; yet, they have different functional specificities. PMM2 presents PMM activity, and its deficiency causes a Congenital Disorder of Glycosylation (PMM2-CDG). On the other hand, PMM1 can also act as glucose-1,6-bisphosphatase in the brain after stimulation with inosine monophosphate and thus far has not been implicated in any human disease. This study aims to refine the evolutionary time frame at which gene duplication gave rise to PMM1 and PMM2, and to identify the most likely amino acid positions underlying the proteins’ different functions. The phylogenetic analysis using available protein sequences, allowed us to establish that duplication occurred early in vertebrate evolution. In order to understand the molecular basis underlying the functional divergence, conserved and most likely functional divergence-related sites were identified, through the analysis of site-specific evolutionary rates. This analysis indicates that most of the sites known to be important in the homodimer formation and in the catalytic activity are conserved in both proteins. Among those potentially related to functional divergence, two positions (183 and 186 in human PMM1) emerge as the most interesting ones. The residues at these positions have different side-chain conformations in the protein structure in the unbound and bound states, and are highly but differently conserved in PMM1 and in PMM2 proteins. Altogether, these results provide new data into the evolutionary history of PMM1 and PMM2 duplicates and highlight the most probable sites that evolved to distinct functional specificities.
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Inferring the Evolutionary History of Mo-Dependent Nitrogen Fixation from Phylogenetic Studies of nifK and nifDKAbstract The ability to fix nitrogen is widely, but sporadically distributed among the Bacteria and Archaea suggesting either a vertically inherited, ancient function with widespread loss across genera or an adaptive feature transferred laterally between co-inhabitants of nitrogen-poor environments. As previous phylogenetic studies of nifH and nifD have not completely resolved the evolutionary history of nitrogenase, sixty nifD, nifK, and combined nifDK genes were analyzed using Bayesian, maximum likelihood, and parsimony algorithms to determine whether the individual and combined datasets could provide additional information. The results show congruence between the 16S and nifDK phylogenies at the phyla level and generally support vertical descent with loss. However, statistically significant differences between tree topographies suggest a complex evolutionary history with the underlying pattern of vertical descent obscured by recurring lateral transfer events and different patterns of evolution between the genes. Results support inheritance from the Last Common ancestor or an ancient lateral transfer of the nif genes between Bacteria and Archaea, ongoing gene transfer between cohabitants of similar biogeographic regions, acquisition of nitrogen-fixing capability via symbiosis islands, possible xenologous displacement of one gene in the operon, and possible retention of ancestral genes in heterocystous cyanobacteria. Analyses support the monophyly of the Cyanobacteria, αβγ-Proteobacteria, and Actinobacteria (Frankia) and provide strong support for the placement of Frankia nif genes at the base of combined the Cyanobacteria/Proteobacteria clades.
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Using Non-Reversible Context-Dependent Evolutionary Models to Study Substitution Patterns in Primate Non-Coding SequencesAbstract We discuss the importance of non-reversible evolutionary models when analyzing context-dependence. Given the inherent non-reversible nature of the well-known CpG-methylation-deamination process in mammalian evolution, non-reversible context-dependent evolutionary models may be well able to accurately model such a process. In particular, the lack of constraints on non-reversible substitution models might allow for more accurate estimation of context-dependent substitution parameters. To demonstrate this, we have developed different time-homogeneous context-dependent evolutionary models to analyze a large genomic dataset of primate ancestral repeats based on existing independent evolutionary models. We have calculated the difference in model fit for each of these models using Bayes Factors obtained via thermodynamic integration. We find that non-reversible context-dependent models can drastically increase model fit when compared to independent models and this on two primate non-coding datasets. Further, we show that further improvements are possible by clustering similar parameters across contexts.
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Understanding the Effect of Secondary Structures and Aggregation on Human Protein Folding Class EvolutionAbstract Using several model organisms it has been shown earlier that protein designability is related to contact density or fraction of buried residues and influence protein evolutionary rates dramatically. Here, using Homo sapiens as a model organism, we have analyzed two main folding classes (all-α and all-β) to examine the factors affecting their evolutionary rates. Since, secondary structures are the most fundamental components of the protein folding classes, we explored the effect of protein secondary structure composition on evolution. Our results show that sheet and helix fractions exhibit positive and negative correlations, respectively, with the rate of protein evolution. On dividing the secondary structure components according to solvent accessibility, linear regression model identified two factors namely buried sheet fraction and relative aggregation propensity. Both these factors together can explain about 13.4% variability in the rate of human protein evolution, while buried sheet residues can alone account to 9.9% variability.
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Enantiodifferent Proton Exchange in Alanine and Asparagine in the Presence of H 217 OAbstract Using Time Domain 1H Nuclear Magnetic Resonance with H217O (H217O-TD-1HNMR), we found [H217O]- and pH-controlled chiral differences in proton exchange properties in alanine (Ala) and asparagine (Asn). To minimize and equalize chemical impurities, Asn enantiomers were purified by crystallization from racemic solution. At <0.1 M H217O, a shift in isoelectric pH (pI) occurred, ~1.14 kJ mol−1 l-d-Asn ΔΔG o′ in the 5.91–6.42 pH range. One potential source for this asymmetry is the enantio-different magnetic moments (lμ↑ ≠ dμ↓) produced by neutral ring currents in the chiral center, leading to enantio-different nuclear spin organization and charge distribution in the amino group. At ≥pI, dissimilar interactions may occur in the hydration of the amino group with H217O (NH2/H217O ≠ NH2/H216O; NH3 +/H217O ≠ NH2/H217O; l-*C-NH2/H217O ≠ d-*C-NH2/H217O). As lμ↑ ≠ dμ↓, the l-*C-amino and the d-*C-amino groups are diastereo spin-isomers. The nuclear spin of 17O may be parallel or antiparallel with the ortho-1H1H pair; hence two ortho-H217O molecules exist, also diastereo spin-isomers. As the pK of H217O is different from H216O, dissimilarities between l-*C- and d-*C-amino groups are converted into proton exchange differences. During H217O-TD-1HNMR, the H217O molecule is a “probe” of the state of the amino group. Regarding prebiotic evolution: prebiotic chirality may not require stochastic symmetry breaking or preexisting chiral conditions; chemical chiral effects due to lμ↑ ≠ dμ↓ are small and need chiral amplification to generate an enantiomeric excess significant for prebiotic evolution; and prebiotic symmetry breaking was homochiral because the effect of lμ↑ and dμ↓ on the amino group should be similar in all alpha amino acids.
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Molecular Biology & EvolutionJournal of Molecular EvolutionBMC Evolutionary Biology
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