Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria - PubMed (original) (raw)

Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria

M Vulić et al. Proc Natl Acad Sci U S A. 1997.

Abstract

Speciation involves the establishment of genetic barriers between closely related organisms. The extent of genetic recombination is a key determinant and a measure of genetic isolation. The results reported here reveal that genetic barriers can be established, eliminated, or modified by manipulating two systems which control genetic recombination, SOS and mismatch repair. The extent of genetic isolation between enterobacteria is a simple mathematical function of DNA sequence divergence. The function does not depend on hybrid DNA stability, but rather on the number of blocks of sequences identical in the two mating partners and sufficiently large to allow the initiation of recombination. Further, there is no obvious discontinuity in the function that could be used to define a level of divergence for distinguishing species.

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Figures

Figure 1

Figure 1

Relationships between frequency of recombination and genomic sequence divergence. The global genomic sequence divergence is indicated as the fraction of two parental genomic DNAs that does not hybridize at 60°C. The scale on the upper _x_-axis is the approximate corresponding percentage of sequence divergence [conversion according to the formula given in ref. , and using 1.18% sequence mismatch per 1°C of Δ_T_m depression (31)]. Shown below are regressions with the corresponding coefficients of determination (_r_2). Frequencies of recombination in one-donor (E. coli K-12) crosses and one-recipient (E. coli K-12) crosses are represented by ○ and □, respectively.

Figure 2

Figure 2

Effect of MMR (A) and SOS (B) systems on frequency of recombination in one-recipient crosses. The recipient strain indicated as wild type was AB1157 nalR (○). All other recipients were AB1157 nalR derivatives carrying (A) MutS deficiency (□) or multicopy plasmids that overproduce wild-type MutS and MutL proteins (▵); or (B) a block to induction of the SOS regulon caused by the lexA1 allele, which encodes an uncleavable LexA repressor (□); constitutive overproduction of RecA conferred by the recAo98 allele (◊); or a plasmid carrying the lexA3(Ind−) gene (▵). In the case of plasmid-bearing strains, vectors were confirmed to have no relevant phenotypes of their own (data not shown). The log–linear regressions and corresponding coefficients of determination are given in Table 1. The Salmonella point in MutSL-overproducing background (A, ▵) was omitted from linear regression analysis (explanation in the text).

Figure 3

Figure 3

Maximal and minimal frequencies of recombination vs. sequence divergence in one-recipient crosses. The recipient strain indicated as wild type was AB1157 nalR (○). Other recipients were AB1157 nalR derivatives carrying either block to induction of the SOS regulon caused by the lexA3 allele, which encodes an uncleavable LexA repressor, and multicopy plasmids that overproduce wild-type MutS and MutL proteins (□), or MutS deficiency and constitutive overproduction of RecA (▵). The log–linear regressions and corresponding coefficients of determination are given in Table 1.

Figure 4

Figure 4

Increasing sequence identity requirement for recombination with increasing concentration of mismatch-binding proteins. (A) After the transfer into recipient cell and subsequent replication of the donor DNA, single-stranded tails are produced by the action of the RecBCD enzyme. The RecA protein (shaded ellipses) polymerizes on single-stranded DNA, which becomes the substrate for the homology search and subsequent strand-exchange reactions. L is the length of that nucleoprotein filament available for recombination. (B) Shown are heteroduplexes formed by strand transfer after the pairing of the short mismatch-free sequence (_H_0) at three different loci (a, b, and c). _H_0 corresponds to the minimal sequence identity sufficient to initiate recombination or MEPS (minimum efficient processing segment) as defined by Shen and Huang (34). If the concentration of functional mismatch-binding proteins is zero, all such products will give recombinant molecules (a, b, and c). If these proteins are functional, only a certain fraction of such heteroduplexes will yield recombinant molecules, depending on the average number of mismatched bases within the heteroduplex region. The higher the concentration of these proteins, the longer the segment of mismatch-free DNA required to complete the event. As a result only those heteroduplexes with high sequence identity will give rise to recombinant molecules (b and c with moderate concentration of MutSL, and only c with high concentration of MutSL) which is reflected in an apparent increase in the length of H (H*).

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