Polymorphism and concerted evolution in a tandemly repeated gene family: 5S ribosomal DNA in diploid and allopolyploid cottons

Abstract

5S RNA genes and their nontranscribed spacers are tandemly repeated in plant genomes at one or more chromosomal loci. To facilitate an understanding of the forces that govern 5S rDNA evolution, copy-number estimation and DNA sequencing were conducted for a phylogenetically well-characterized set of 16 diploid species of cotton (Gossypium) and 4 species representing allopolyploid derivatives of the diploids. Copy number varies over twentyfold in the genus, from approximately 1,000 to 20,000 copies/2C genome. When superimposed on the organismal phylogeny, these data reveal examples of both array expansion and contraction. Across species, a mean of 12% of nucleotide positions are polymorphic within individual arrays, for both gene and spacer sequences. This shows, in conjunction with phylogenetic evidence for ancestral polymorphisms that survive speciation events, that intralocus concerted evolutionary forces are relatively weak and that the rate of interrepeat homogenization is approximately equal to the rate of speciation. Evidence presented also shows that duplicated 5S rDNA arrays in allopolyploids have retained their subgenomic identity since polyploid formation, thereby indicating that interlocus concerted evolution has not been an important factor in the evolution of these arrays. A descriptive model, one which incorporates the opposing forces of mutation and homogenization within a selective framework, is outlined to account for the empirical data presented. Weak homogenizing forces allow equivalent levels of sequence polymorphism to accumulate in the 5S gene and spacer sequences, but fixation of mutations is nearly prohibited in the 5S gene. As a consequence, fixed interspecific differences are statistically underrepresented for 5S genes. This result explains the apparent paradox that despite similar levels of gene and spacer diversity, phylogenetic analysis of spacer sequences yields highly resolved trees, whereas analyses based on 5S gene sequences do not.

Evolution and structure of 5S rDNA loci in allotetraploid Nicotiana tabacum and its putative parental species

“…The data revealed: (i) the length of basic unit of the S-genome family of tobacco is the same as the length of basic unit in N. sylvestris, likewise the length of basic unit of the T-genome family of tobacco is the same as the full length unit in N. tomentosiformis; (ii) the T-genome family of tobacco and N. tomentosiformis 5S units have the same GC-rich sub-region that is absent in the S-genome family and N. sylvestris; and (iii) the non-coding spacer of S-genome family has high sequence similarity to the spacer of N. sylvestris while the non-coding spacer of Tgenome family has high sequence similarity to N. tomentosiformis. This organization of 5S units in tobacco in which parental 5S units can be distinguished by length polymorphisms resembles other well-studied plant allopolyploids in the genera Triticum (Scoles et al, 1988) and Gossypium (Cronn et al, 1996).…”

“…Thus interlocus gene conversion has not occurred for 5S rDNA as it did for 18-26S rDNA. Similarly, interlocus homogenisation at 18-26S rDNA, but not 5S rDNA, has been observed in allopolyploid Gossypium species (Cronn et al, 1996), suggesting similar evolutionary patterns.…”

“…(2) Cronn et al (1996) predicted that genetic recombination is influenced by chromosomal location. Perhaps sequences positioned near the telomere have a greater likelihood to interact with non-homologous chromosomes (eg, during end-to-end fusions) than interstitial or centromeric sequences.…”

“…It is possible that the two 5S rDNA families in N. tabacum and N. rustica have their origins in the diploid progenitor species. Certainly in the Triticeae (Scoles et al, 1988) and in the Gossypium allopolyploids, G. hirsutum and G. mustelinum (Cronn et al, 1996), two 5S rDNA families have been found that remained closely similar to the diploid progenitor species. In this paper we extend our analysis of 5S rDNA families in tobacco to determine: (i) the organization, location and copy numbers of the two 5S families;…”

Types, levels and patterns of low-copy DNA sequence divergence, and phylogenetic implications, for Gossypium genome types

“…The Gossypium genus is an attractive model for studying the genetic changes associated with polyploid evolution, with a natural interspecific cross between taxa that remain extant followed by chromosome doubling having spawned five extant tetraploid species. Substantial divergence among the diploid genomes provides a backdrop for polyploid cotton evolution-for example, a twofold difference in genome size between the A and D genome progenitors is due largely to differential accumulation of retroelements in the A genome (Zhao et al, 1995Grover et al, 2007) and biased accumulation of small deletions in the D genome (Grover et al, 2007), with intergenomic exchange of these elements following polyploid formation (Wendel et al, 1995;Cronn et al, 1996;Hanson et al, 1998;Zhao et al, 1998).…”