Duplication-Translocations of Tryptophan Operon Genes in Escherichia coli

Abstract

Mutants of Escherichia coli were selected in which a single mutational event had both relieved the polar effect of an early trpE mutation on trpB and simultaneously released the expression of trpB from tryptophan repression. The frequency at which these mutations appeared was roughly equal to the frequency of point mutations. In each of these mutants, the mutation increased the function of trpB and also increased the activity of some, but not all, of the other four tryptophan operon genes. Genetic analysis showed that the mutations were not located within the trp operon since in each case the parental trp operon could be recovered from the mutants. Each mutant was shown to carry a duplication of a trp operon segment translocated to a new position near the trp operon. Polarity is relieved since the trpB duplication-translocation is not in the same operon as the trpE polar mutation. The duplicated and translocated segments are fused to operons not regulated by tryptophan, so trpB function is no longer subject to tryptophan repression. The properties of the mutants indicate that the length of the duplicated segment and the position to which it is translocated differ in each of the seven mutants studied. The duplications are unstable, but the segregation pattern observed is not consistent with a single crossover model for segregation. That such duplication-translocation events generate a variety of new genetic arrangements at a frequency comparable with point mutations suggests they may play an important role in evolution.

Extrachromosomal elements as possible agents of adaptation and development.

“…In view of the universal distribution of recombinational systems, I propose that sequence reiterations represent the most common type of programmed mutation. The experimental evidence of Jackson and Yanofsky (125) suggests that "spontaneous" gene duplications may arise in bacteria almost as frequently as gene mutations. This is highly significant in view of the fact that the duplication of a sequence 1,000 or so nucleotides long (the calculated size for an average gene) is a much more complex event than a point mutation.…”

“…Duplication destabilizes genetic organization because it renders the DNA prone to recombination. Tandem reiterations are known to be unstable in prokaryotes (225,125) and in higher organisms (197). What has not been widely recognized is that duplication tends to create circular mini-DNAs by reciprocal crossover between any regions of repeated homology, i.e., reiterated DNA favors the formation of ECEs (209).…”

Promoter-like mutants with increased expression of the Escherichia coli uridine phosphorylase structural gene

“…To test this possibility, we plated the mutant strains AM257 and AM258 on nutrient agar and replicated more than 1,000 colonies of each strain to glucose minimal medium with thymine. In fact, all colonies tested were stable and did not segregate variants that could not grow on this agar, whereas duplication-translo-cation events in E. coli are characterized by instability (11,25).…”

Increased Gene Dosage Plays a Predominant Role in the Initial Stages of Evolution of Duplicate Tem-1 Beta Lactamase Genes

“…A fourth candidate mechanism for duplicate gene retention involves novel sequences that are created at the junctions between new duplicates. Such novel sequences can themselves be beneficial for cells and help spread gene duplicates through a population (Glansdorff and Sand 1968;Jackson and Yanofsky 1973;Ahmed 1975; Anderson andRoth 1977, 1978a,b;Kugelberg et al 2006Kugelberg et al , 2010. In addition to these main classes of hypotheses, theoretical studies have suggested various further scenarios for gene duplicate retention (Nowak et al 1997;Wagner 2000aWagner , 2002Gu et al 2003;Kafri et al 2006Kafri et al , 2008.…”