Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes.

Abstract

We have found that human and ape ribosomal genes undergo concerted evolution involving genetic exchanges among nucleolus organizers on nonhomologous chromosomes. This conclusion is based upon restriction enzyme analysis of the ribosomal gene families in man and five ape species. Certain structural features were found to differ among (but not within) species even though the ribosomal genes have a multichromosomal distribution. Genetic exchanges among nucleolus organizer regions may be related to the well-known phenomenon of acrocentric chromosome associations observed in man and apes. Length variation in a region of the nontranscribed spacer was found in both chimpanzee species we examined. The nature of this length variation was found to be identical to that previously described in man. The origin of the length variation and its polymorphism within these three species might be explained by unequal alignment and unequal crossing-over among the ribosomal genes. An especially surprising finding was a nucleotide sequence polymorphism present in each individual human and ape we examined. Some ribosomal genes of each individual have a HindIl site in the 28S gene about 800 base pairs from the EcoRI site in this gene. The remaining 28S genes lack this HindII site. The presence of this polymorphism within individuals of every species we examined suggests that it has been maintained by natural selection.

Ribosomal RNA genes in B chromosomes of Crepis capillaris detected by non-radioactive in situ hybridization

“…Multichromosomal distribution of rRNA genes and their genetic exchange among nonhomologous chromosomes are known to occur, e.g., in man and higher apes (Arnheim et al, 1980). Molecular and immunocytochemical techniques, such as those used in the present investigation, should help to solve some of the questions regarding the cytoevolution of "accessory" chromosomes.…”

A cytogenetical and molecular analysis of the ribosomal cistrons of Allium sphaerocephalon L. (Liliaceae)

“…These data are in agreement with those a. sphaerocephalon rDNA has gained another two targets for EcoRI that digest the 8.5 kb band and that have been propagated throughout the ribosomal gene family in this species. This degree of homogenization within ribosomal multigene families in A. sphaerocephalon, a species where rDNA are located in multiple chromosomes, may result from unequal genetic exchanges between rDNA from homologous and non-homologous chromosomes because if ribosomal genes on non-homologous chromosomes were genetically isolated from each other then it might be expected that each NOR would evolve independently (Arheim et a!., 1980). The same mechanism can also explain the intra- Fig.…”

“…(1990) for Mus musculus. The same process, which produces sequence homogenization, can also increase or decrease ribosomal RNA gene number, not only in homologues but also between 43 non-homologous chromosomes (Arheim et at., 1980;Suzuki etal., 1990).…”

Variation and inheritance of ribosomal DNA in Pinus sylvestris L. (Scots pine)

“…Therefore, frequent molecular interactions within chromosomes are able to create the observed within-individual linkage disequilibrium, homogenizing each rDNA array independently of others arrays located on other (homologous or nonhomologous) chromosomes. However, the occurrence of some polymorphic rDNA variants at more than one locus has been observed in primates (Arnheim et al, 1980;Krystal et a!., 1981) and Drosophila melanogasrer (Coen & Dover, 1983). Dover (1989) sampling is a more important source of sampling variance than population sampling, even when 20 restriction enzymes are used (Lynch & Crease, 1990).…”

“…Concerted evolution, also known as molecular drive (Dover, 1982), tends to reduce variability between gene copies by molecular, non-Mendelian mechanisms (e.g. gene conversion, unequal crossing-over), resulting in relatively homogeneous gene copies within a species (Arnheim et at., 1980;Dover, 1982;Ohta & Dover, 1983.…”