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Intraspecific and Interspecific Variation in 5S RNA Genes Are Decoupled in Diploid Wheat Relatives

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Intraspecific and Interspecific Variation in 5S RNA Genes Are Decoupled in Diploid Wheat Relatives Copyright 8 1995 by the Genetics Society of America Intraspecific and Interspecific Variation in 5s RNA Genes Are Decoupled in Diploid Wheat Relatives Elizabeth A. Kellogg * and Rudi Appels *Department of Organismic and Evolutionary Biology, Haward University, Cambridge, Massachusetts 02138, and +Division of Plant Industry, CSIRO, Canberra, ACT, Australia Manuscript received August20, 1994 Accepted for publication February 13, 1995 ABSTRACT 5s RNAs form part of the ribosome in most organisms. In some, e.g., prokaryotes and some fungi, the genes are part of the ribosomal operon, but in most eukaryotes theyare in tandem arrays of hundreds to thousands of copies separate from the main ribosomal array. 5s RNA genes can be aligned across kingdoms. We were therefore surprised to find that, for 28 diploid species of the wheat tribe (Triticeae) , nucleotide diversity within an array is up to 6.2% in the genes, not significantly different from that of the nontranscribed spacers. Rates of concerted evolution must therefore be insufficient to homogenize the entire array. Between species, there are significantly fewer fixed differencesin the gene than would be expected, given the high within-species variation. Incontrast, the amount of variation between species in the spacer is the same as or greater than that within individuals. This leads to a paradox. High variation within an individual suggests that there is little selection on any particular gene within an array. But conservation of the gene across species impliesthat polymorphisms are periodically eliminated at a rate approximately equal to or greater than that of speciation. Levels of intraspecific polymorphism and interspecific divergenceare thus decoupled. This implies that selective mechanisms exist eliminate to mutations in the gene without also affecting the spacer. S RNA is a small 120-bp molecule that forms part much, however, and those sites that do accumulate mu- 5 of the ribosome in most known organisms. In eu- tations do so rapidly enough that they are subject to karyotes, it forms a complex with the large subunit of multiple hits; evolution rapidly wipes out its own tracks ribosomal RNA and several ribosomal proteins. The ( HALANYCH 1991; STEELEet al. 1991 ) . precise function of the 5s RNA in the ribosome is un- At least some of the conserved regions can be ex- known. 5s RNA genes are part of the rRNA cistron plained by analysis of gene transcription. 5s RNA genes in some organisms, including most bacteria and some are transcribed by RNA polymerase I11 (pol 111) , a poly- fungi, and occur in the spacer between the large and merase that also transcribes WASand some small nu- small subunit genes. In all animals and green plants, clear RNAs. A convenient model for study of pol111 has however, the genes are in tandem arrays separate from been theXenopus oocyte, in which there arethousands the main rDNA array (LONG andDAWID 1980). There of 5s RNA genes. Pol111 does not bind to DNA directly, may be one (e.g., Drosophila (SAMSONand WEGNEZ but rather depends on interaction with transcription 1988), two (e.g., members of the Triticeae, see below), factor IIIA (TFIIIA) (HAYES and TULLIUS1992; PIELER or many [ e.g., Linum ( GOLDSBROUGH et aZ. 1981; et aZ. 1987). TFIIIA makes the initial contact with the SCHNEEBERGERand CULLIS 1992) ; Neurospora ( SELKER DNA, binding strongly to a sequence called box C and et al. 1981) ] such arrays, with copy number ranging somewhat less strongly to box A (Figure 1) . In Xeno- from several hundred to several thousand. pus, mutations in either Box A or Box C, prevent tran- The sequence and structure of 5s RNA genes and scription (HAYES and TULLIUS1992) and changes in their products are highly conserved, as might be ex- the distance between the boxes reduce transcription pected for a gene with such a wide distribution. The levels. It is thus no surprise to discover that these re- length varies little from 120 bp. Certain positions and gions contain highly conserved bases. regions of the gene are sufficiently conserved that it In Xenopus oocytes, TFIIIA alsobinds and sequesters can be aligned across broad taxonomic ranges. The the newly synthesized RNA molecule ( CLEMENSet al. alignment led to early hopes that the gene would be 1993). Thebinding sites for the gene product (RNA) useful for inferring phylogenetic relationships among differ from those for DNA (Figure 1) . If TFIIIA also deep branches of eukaryotes. Many sites do not vary binds the gene productin angiosperms, then mutations in these sites might result in a nonfunctional gene. In- Cmwingauthor: E. A. Kellogg, Harvard Unversity Herbaria, 22 Divinity Ave., Cambridge, MA 02138. teractions with TFIIIA may thus af€ect selection on 5s E-mail: [email protected] RNA genes, quite independent of any functional con- Genetics 140 325-343 (May, 1995) 326 Kellogg E. A. and R. Appels cxxx x xx FIGURE1.-Location of intraspecific polymorphisms in 5s RNA genes in the wheat tribe. Consensussequence for the XXXOOOC-GX Triticeae is mappedonto the secondary DNA - BOX A structure for Xenopus 5s RNA, which was determined by using solution data .C-A. and molecular modeling. Sites varying C-G OXX within individual plants marked: short- 1:: X XXG-U f xAAoe spacer units, x; long-spacer units, @. A-G Note that the variable sites are spread xG-U across the molecule. Box A and Box C A are highly conserved DNA binding do- x .G-C mains. Other lines markRNA binding XXXG-U 0 domains. The conserved sequence X U-A GGAUCC at the 3' end of the third loop xx C-G 0 X oC-GX is aBamHI site that was used forcloning; A ox p units with mutations inthis site were not u-u. ' sequenced. @C-G oxxx 2 C-GOX n A- -GOx GU straints imposed by binding with the ribosome. Because group 1 chromosomes and the array with long spacers of the strongsimilarity ofthe 5s genes across kingdoms, on group 5 ( SCOLESet al. 1988). This has been indi- functions identified in Xenopus may well be important cated by deletion mutations (LASSNER and DvoW for 5s genes in general. 1986) , nulli/ tetrasomic combinations ( DVO- et al. 5s RNA genes have been studied extensivelyin 1989), in situ hybridization (APPELS et al. 1980; KIM et plants, with sequences now in the literature for a gym- al. 1993), and pulsed field gel electrophoresis (PFGE; nosperm ( Pinus radiata; MORANet al. 1992) , and many RODER1992). However, in the genera Critesion and angiosperms including dicots, such as Acacia (Legu- Hordeum (both sometimes included in an expanded minosae; PLAYFORDet al. 1992), Linum (Linaceae; genus Hordeum), the short spacer array occurs on the GOLDSBOROUGH et al. 1982) , Arabidopsis (Brassica- group 2 chromosomes, a result that has been confirmed ceae; CAMPELL 1992), Pisum (Leguminosae; ELLISet by RFLP mapping and by in situ hybridization (KOL al. 1988), monocots of the grass family, such as rice CHINSKY et Ul. 1990; LAURIE et d. 1993). MUINet d. ( Oryza; MCINTYREet al. 1992 ) , and members of the ( 1993) found a long spacer array on chromosome 3. wheat tribe (Triticeae; &PELS et al. 1992; SCOLESet High resolution fluorescent in situ hybridization in bar- al. 1988). The data base for the Triticeae is uniquely ley indicates that there are 5s arrays on chromosomes powerful, because of its size and density. 2, 3, 4, and 7 ( LEITCHand HESLOP-HARRISON1993). The Triticeae (wheat tribe) is a group of diploid Other markers on the long armof 2 (2H) in H. vulgare and polyploid grasses.It contains -500 species, among indicate colinearity with Triticum aestivum (wheat) and them wheat, barley, rye and their wild progenitors. The Secab cereab (rye) . Hence, it appears that the short number of genera is a matter of contention, and de- spacer array from the group 1 chromosome has some- pending on the taxonomist consulted, ranges from l how "moved" onto chromosome 2 ( LAURIE et al. 1993) to 38; we recognize an intermediate number here. De- without disruption of other linkage groups. In the ge- cades of cytogenetic work have shown that the seven nus Dasypyrum (with the single species D. villosum) chromosomes of each haploidgenome are syntenic there is no short-spacer array at all. DVO- et al. ( 1989) throughout the group. Thus chromosomes numbered reported that the short units of T. umbellulatum are on 1 through 7 are presumed homologues. chromosome 5, and long units were not found. They Chromosomal locations of genes in the Triti- also noted that T. speltoides had only a long-spacer array, ceae: The genes for 5s RNA occur in large tandem confirming previous reports by PEACOCKet al. ( 1981 ) . arrays, in which genes alternate with nontranscribed REDDY and APPELS ( 1989) suggested that there may spacers. The arrays are at two distinct chromosomal be additional dispersed locations for 5s RNA genes, locations, and the two loci can be unambiguously distin- based on results of in situ hybridizations; however, their guished by both the length and the sequence of the observations were at the limits of resolution for the spacers ( GERLACHand DYER1980). For most members technique. Using higher resolution techniques, LEITCH of the tribe, the array with short spacers occurs on the and HESLOP-HARRISON( 1993) found only the two ma- Variation in 5s RNA Genes 327 jor arrays on chromosomes 1 and 5. In their studies of tion may be fairly uniform within a locus; GOLDSBO- nulli-tetrasomic and ditelosomic lines of diploid and ROUGH et al. (1982) found that genes andspacers were polyploid Triticeae, DVORAK et al. (1989) determined about equally methylated in Linum, but there are no the chromosomal location of 5s arrays by analyzing data on this in the Triticeae. presence/ absence of bands in Southern blots; they Direct sequencing of RNA has shown that the gene foundbands corresponding to the short-spacer and products are largely homogeneous, implying that there long-spacer arrays.
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