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Molecular Mechanism for Genetic Recombination (Protein-Nucleic Acid Symmetry/Protein Binding/Polarity/Gene Conversion) HENRY M

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Molecular Mechanism for Genetic Recombination (Protein-Nucleic Acid Symmetry/Protein Binding/Polarity/Gene Conversion) HENRY M Proc. Nat. Acad. Sci. USA Vol. 69, No. 9, pp. 2483-2487, September 1972 Molecular Mechanism for Genetic Recombination (protein-nucleic acid symmetry/protein binding/polarity/gene conversion) HENRY M. SOBELL Department of Chemistry, The University of Rochester, Rochester, New York 14627; and Department of Radiation Biology and Biophysics, The University of Rochester, School of Medicine and Dentistry, Rochester, New York 14620 Communicated by E. W. Montroll, June 8, 1972 ABSTRACT Symmetry considerations of protein- The binding of actinomycin to DNA and its specificity nucleic acid interaction suggest the existence of an alter- in inhibiting the RNA polymerase reaction suggest a primi- nate branched configuration for DNA induced by binding specific structural proteins to symmetricallyarranged poly- tive repressor-operator character for this complex that may nucleotide base sequences. The concept that such se- quences exist at the ends of genes or operons leads to a mo- lecular model for genetic recombination in eukaryotic cells. A B NUCLEASE SPECIFiCITY ACTINOMYCIN SPECIFICITY 3' 5' The molecular mechanism underlying genetic exchange in 5' 3' 5' 3' eukaryotic organisms is a subject that has received wide at- tention in recent years (1). It is generally thought that genetic I recombination begins with the pairing of two parental DNA duplexes on the nucleotide level (synapsis) to give a hybrid GC)3 *<G Au () & SI DNA structure containing both parental strands (2). Subse- 3' 5' 3' 5' quent events lead to the formation of recombinant molecules. poly d(G-C) Micrococcus /uteus DNA The phenomenon of gene conversion appears to be intimately BERNARDI (1968) KELLY & SMI'ITH (1970) connected with genetic recombination (3, 4); this most prob- A ably reflects excision and repair of regions of heteroduplex C 5' 3' DNA either during or immediately after recombination (5-7). Polarity in single-site conversion frequencies and coconver- sion events has been documented in a recent series of detailed S. v /d, C G studies of gene conversion in yeast (Saccharomyces cereviseae) CG (8, 9). Related data exists for Ascobolus immersus (10), Sor- AT AT TERNARDID196GC T A dariafimicola (11), and Neurospora crassa (12). TKASC G C D C C G CD The purpose of this paper is to present a simple unifying C G A T CG structural model for genetic recombination in eukaryotic C G A Ta Unomycin-DAATA bindAng cCs GCciTAaI p m GC G C organisms. The model is consistent with a large amount of G C TA D CGCDC CD data on genetic recombination in these organisms, and may A T CD ATC A T CDG AT have wider relevance in understanding the mechanism of T ~~~~~~TAT genetic recombination in viruses and bacteria. Because of * D~~~~~GC * D~~~~~GC space limitations, the theory will be presented in outline only. 15' ~~~~CG 3 A T 3c5 More complete discussions will appear shortly (13, 14). DIMER RECOGNITION wA i BERNARDI (1968) TERMEECAITO Symmetry in protein-nucleic acid interaction MONOD (1969) TTAE EONTO KELLY & SMITH (1970) 3,' GIERER (1966) The ideas presented here stem from the stereochemical model C that has been advanced for actinomycin-DNA binding (14- FIG. 1. A schematic diagram illustrating the general principle 18). Actinomycin is a cyclic polypeptide-containing anti- governing protein-nucleic acid recognition, as exemplified by biotic that binds to dG-dC sequences in DNA, this reflecting actinomycin-DNA binding specificity and endonuclease speci- intercalation of the phenoxazone ring system between adjacent ficity (A and B). If a protein molecule has identical subunits S-C base pairs and protein-nucleic acid hydrogen bonding. related by 2-fold symmetry when it binds to DNA-the 2-fold The latter interaction reflects the 2-fold symmetry relating axis coinciding with the dyad axis on DNA-then a necessary the two cyclic pentapeptide chains on actinomycin. This allows consequence is that the base sequence in the recognition site them to interact with both sugar-phosphate chains through have 2-fold symmetry. C. Extension of this general principle for numerous van der Waals contacts, and to hydrogen bond with dimer recognition to include tetramer recognition. One postulates deoxyguanosine residues on opposite DNA chains (shown a tandem genetic duplication of the DNA sequence involved in schematically in dimer recognition, followed by a hydrogen-bonding rearrange- Fig. 1A). A similar pattern of protein- ment. This nucleic acid structure can then be recognized by a nucleic acid recognition is used with two (19, 20), possibly tetrameric protein having identical subunits related by 4-fold three (21), nuclease enzymes (shown schematically in Fig. symmetry. Patterns of recognition such as these may exist 1B). between operators and repressors. 2483 Downloaded by guest on September 28, 2021 9AQA Ar-in-rx Genetics: SobeH Proc. Nat. Acad. Sci. USA 69 (1972) A A B B 5'63 563' 56 3' 5' 3' AT T A T A TA T A G C G C C G C G C G A AI C G A T 'GC T T A T T A I ACC GC G A GA A T C G C C G A T A T A T GA CT T A T A CG GC G C I-,;-- -1 A T X~~ Vs\ \ A T AT A T H F G C .. D G C AT A T 3' . T A 36 GCT A T TA AY TtK A TH T A T A A I G C G C TTATAGCCC G C A AG C G AACCG~~~~~ C G C G C G AT I(TAACGGT CCGTTA) FA A T T A GAT1 IATTGCCA TGGC AATI C T A G C A T C G C G C A GC G C C G 56 C G C G A T A T A T AT A T A T A_ A3' T A _T G G H A 3' B 3 TA 3 56 S' 3' GH '3 D DGD 5-A A T TA TA A T CG A T T A G C A 2T T A GC T A GC 3*3 * TAACGGTAC GTAC C G T T A *5'B CG T A C G 5'A- AATTGCCATGGcCATGGCAAT * 3' AA ~C G G C C GCT A C T A G c C G G TA T E TAACGGT AC C GGTA CCGT TA E TAG G ATTGCCA TG CA TGGCAAT FC G ^ t T GTA G G A AA C 3***TCGTAAT T T T A *A S GAT GC C G G C T S'* AT - A A T * *3 A T G C GT A T C G T A A T G C AT AT A T C G A T T A TA AT * T A AT * C t A C3'5 6A 3' 5' c 3t D C T 3' FIG. 2. A model for genetic recombination. Homologous chromosomes A-C and B-D possess specific regions (perhaps placed every cistron or operon length along the chromosome) capable of forming Gierer-like structures in the presence of a specific recombination structural protein. Regions such as E-G and H-F form single-stranded, denatured loops outside the immediate environment of the protein (which senses only the symmetry-related nucleic acid structure shown) and are, therefore, susceptible to nuclease attack (shown by the arrows). When complementary loops G, H are nicked and opened, Watson-Crick base pairing occurs; this is followed by extensive propa- gation of the heteroduplex (shown in the lower two figures). The final structural intermediate is shown in the center of Fig. 3. prove to have more general meaning with regard the recogni- that can be recognized by a tetrameric protein having identi- tion of naturally occurring operators by repressors. If a re- cal subunits related by 4-fold symmetry (222 symmetry is also pressor molecule has identical subunits related by two-fold possible; however, one must relax the requirement that the symmetry when it binds to DNA-the 2-fold axis coinciding nucleic acid structure possesses exact 222 symmetry. See with the dyad axis on DNA-then a necessary consequence refs. 13 and 14). is that the base sequence in the operator have 2-fold sym- Although no structural evidence is yet available concerning metry. This would be true regardless of precisely which the arrangement of subunits in the lac or the X repressors, groove (or grooves) the repressor binds. This general principle both proteins appear to bind DNA in tetrameric form (23, 24). for dimer recognition may be extended to include tetramer The precise symmetry relating subunits of these proteins will recognition in the following way (see Fig. 1C). One postulates eventually be revealed by x-ray crystallography; however, a tandem genetic duplication of the DNA sequence involved strong genetic evidence already points to the existence of two- in dimer recognition, followed by a hydrogen-bonding re- fold symmetry in the lac operator genetic map, with higher- arrangement (22). This generates a clover leaf-like structure order subdivision possible (25, 26). These findings, along with Downloaded by guest on September 28, 2021 Proc. Nat. Acad. Sci. USA 69 (1972) Molecular Mechanism for Genetic Recombination 2485 A 3. A B 5! 3' 5' G ~~~TA GH ~~AA 5- AGT TTGC A A T T A T C T A A T C G T A A T G C GC C G AT CG G C T A CG GC TA AT T A G C T A A T -- TAGTC G CC G C GGGTACCGTTA,::: B s. G CC G G C CG GC C G A T T A A T A T T A A T TA A T TA CG GC C G GC CG G C A T TA A T AT TA I +LIGASE -LIGASE E T AF GCAH cMMEEMEMMMEMMMM~gG' E G A F G C CG G C 'bb AT TA A TT TA A T A TA A T T A T A A T TA G C T A A T A G C TA A T 3,- **TAAC G T TA * - *5' G C C G * D C GG C A ATTG C AAT * *3' C GG C 3'-- *TAACGGTAC GTACCGTTA .
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