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Intra- and Interspecific DNA Variation and Codon Bias of the Alcohol

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Intra- and Interspecific DNA Variation and Codon Bias of the Alcohol Intra- and Interspeci®c DNA Variation and Codon Bias of the Alcohol Dehydrogenase (Adh) Locus in Arabis and Arabidopsis Species Naohiko T. Miyashita,* Akira Kawabe,* Hideki Innan,*1 and Ryohei Terauchi²2 *Laboratory of Plant Genetics, Graduate School of Agriculture, and ²Laboratory of Plant Systematics, Faculty of Science, Kyoto University, Japan Sequence variation at the alcohol dehydrogenase (Adh) locus was analyzed for six species each of the genera Arabis and Arabidopsis. Phylogenetic analysis showed that investigated species were grouped into three clusters, and the generic classi®cation did not correspond to the clusterings. The results indicated that the genera could not be distinguished on the basis of the Adh variation. A signi®cant difference in the ratio of silent to replacement sites was detected by MK test in two comparisons, with Arabidopsis thaliana polymorphism due to excess silent diver- gence. Silent changes were predominant in the evolution of the Adh locus in Arabis and Arabidopsis. To infer evolutionary signi®cance of silent substitutions, codon bias was studied. The degree of codon bias of the Adh region was relatively constant over Arabis and Arabidopsis species. ``Preferred'' codons of A. thaliana were determined. No evidence of natural selection on codon change was detected in the Adh regions of A. thaliana and Arabis gemmifera. Introduction Arabidopsis thaliana provides an excellent opportu- two loci were consistent with those of divergence be- nity to study DNA variation in natural plant populations. tween these species, except for an excess of replacement This species has been used as a model system for plant polymorphism in Arabis gemmifera. molecular biology (Meyerowitz and Somerville 1994). The purpose of this study was to investigate genetic Accumulating sequence information on various genes mechanisms acting on DNA variation in the Adh regions can be readily utilized to study sequence variation of A. of Arabidopsis and Arabis species by comparing pat- thaliana and its related species. terns and levels of intra- and interspeci®c DNA variation So far, only a few nuclear genes of this plant spe- in these two genera. Knowledge of the phylogenetic re- cies have been analyzed from the perspective of popu- lationship between species is important in interspeci®c lation and evolutionary genetics. In a worldwide sample comparisons, e.g., HKA (Hudson, Kreitman, and Agu- of A. thaliana, dimorphism of DNA variations was de- ade 1987) and MK (McDonald and Kreitman 1991) tected in the Adh region, i.e., two distinct arrays of DNA tests. Although Hanfstingl et al. (1994) compared a por- polymorphisms segregated throughout the region (Innan tion of exon 4 of the Adh to investigate the phylogenetic et al. 1996). Dimorphism was detected in the acidic chi- relationship between A. thaliana and related species, an tinase (ChiA) region as well (Kawabe et al. 1997). These analysis of a longer sequence is necessary to obtain a results suggest that dimorphism of DNA variations is a reliable phylogeny. At ®rst, we investigated the phylo- characteristic of the nuclear genome of this plant spe- genetic relationship of six species each of Arabis and cies. To explain the dimorphism, we hypothesized that Arabidopsis based on variation in the Adh region. We fusion of two divergent populations occurred in the his- found that synonymous changes were predominant in tory of A. thaliana. sequence evolution of the Adh regions of these plant Levels of nucleotide variation at the Adh and ChiA species. To investigate the evolutionary signi®cance of regions in A. thaliana were comparable with those re- synonymous changes, we analyzed codon bias of the ported for other plant and Drosophila nuclear genes. Adh region. The neutral mutation hypothesis (Kimura 1983) was not rejected in the Adh region, while signi®cant deviation Materials and Methods was detected in the ChiA region. We also compared in- Plant Materials tra- and interspeci®c variation at the two loci of A. thal- iana and related Arabis species to infer the genetic Six species each of the genera Arabis and Arabi- mechanism acting on DNA variation (Miyashita, Innan, dopsis were used (table 1). Some of species are poly- and Terauchi 1996; Kawabe et al. 1997). It was shown ploid, with a basic chromosome number of 16. The na- that the level and pattern of DNA polymorphism of the ture of polyploidy (auto- and alloploidy) and genome constitution have not been investigated. Arabidopsis 1 Present address: Department of Biological Sciences, Graduate suecica has been suggested to be amphiploid between School of Science, University of Tokyo, Japan. A. thaliana and Cardaminopsis arenosa (Hylander 2 Present address: Biocenter, University of Frankfurt, Germany 1957; ReÂdei 1972; O'Kane, Schaal, and Al-Shehbaz Key words: Adh, Arabis, Arabidopsis, phylogeny, codon bias. 1996). A. thaliana and A. gemmifera were described (Miyashita, Innan, and Terauchi 1996; Innan et al. Address for correspondence and reprints: Naohiko Miyashita, Laboratory of Plant Genetics, Graduate School of Agriculture, Kyoto 1996). Seeds of the other Arabidopsis species were ob- University, Sakyo-ku, Kyoto 606-01, Japan. E-mail: tained from Professor N. Goto, Sendai Arabidopsis Seed [email protected]. Stock Center, Miyagi University of Education. Plants Mol. Biol. Evol. 15(11):1420±1429. 1998 were grown in pots placed in an incubator under 24-h q 1998 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038 light conditions. The other Arabis species were sampled 1420 Adh Variation in Arabis and Arabidopsis 1421 Table 1 Arabidopsis and Arabis Species Studied Genus Species N Sampling Location 2n Distribution Arabidopsis .... A. thaliana 17 See Innan et al. (1996) 10 Eurasia, North Africa A. himalaica 1 Ganesh Himal, Nepal (JOS18)a 16 China, West Himalaya, Pakistan A. wallichii 1 Unknown (JS5)a 16 Afganistan, Central Asia, China, West Himalaya, Iran, Pakistan A. korshinskyi 1 Unknown (JS4)a 48 Central Asia A. grif®thiana 1 Unknown (JS3)a 32 Afganistan, Central and Southwest Asia, China, Iran, Pakistan, East Russia A. suecica 1 Finland (JS6)a 26 North Europe Arabis ........ A. gemmifera 1 Minou, Osaka Prefecture, 1994 16 East Asia (Japan, Korea) A. lyrata subsp. kawasakiana 1 Oyodo, Mie Prefecture, 1992 32 East Asia, North America A. glabra 1 Maiko, Shiga Prefecture, 1992 12 Eurasia (Europe, Asia) A. hirsuta subsp. japonica 1 Yushima, Yamanashi Prefecture, ? East Asia (Japan, Korea, Manchuria) 1994 A. stelleri 1 Hamakurosaki, Toyama Prefec- 32 East Asia (Japan, Korea, Kamchatka) ture, 1992 A. ¯agellosa 1 Kifune, Kyoto Prefecture, 1992 ? East Asia (Japan) NOTE.ÐN 5 the number accessions analyzed; 2n 5 diploid chromosome number. a Code number of the Sendai Arabidopsis Seed Stock Center. in Japan (table 1). As an outgroup for interspeci®c com- using PAUP 3.1.1 (Swofford 1993) with the heuristic parison, Brassica oleacea (cabbage) purchased at a mar- search option. To analyze codon bias and GC content, ket was used. MEGA and CODONS (Lloyd and Sharp 1992) were used. Codon usage data for A. thaliana were obtained DNA Sequencing from the CUTG (Codon Usage Tabulated from Gen- Total DNAs of the Arabis and Arabidopsis species Bank; Nakamura, Gojobori, and Ikemura 1997). After and B. oleacea were puri®ed by a modi®ed CTAB meth- eliminating cDNA sequences of unknown function and od (Terauchi and Konuma 1994) and used for PCR am- YAC and BAC ORF sequences determined by the Ara- pli®cation of about 1.7 kb of the Adh gene. Primers for bidopsis Genome Initiative (AGI), 1,491 nuclear coding PCR ampli®cation were 59-ACC ACC GGA CAG ATT sequences were analyzed. To determine ``preferred'' co- ATT CG-39 and 59-CAC CCA TGG TGA TGA TGC dons in synonymous families, we compared codon usage ACC-39, which were located in the ®rst and last (sev- frequencies in high- and low-biased genes, following the enth) exons of the A. thaliana Adh region, respectively method of Sharp and Lloyd (1993) and Akashi (1994). (Chang and Meyerowitz 1986). Because the number of For a synonymous family, codons showing signi®cant Adh genes in these species was not known, direct se- increases in frequency between low- and high-biased quencing was not possible. The PCR products were genes examined by the G-test were considered ``pre- cloned into plasmid pUC18. One clone was sequenced ferred.'' Signi®cance of the G-test was examined by the for each species and used only for interspeci®c com- sequential Bonferroni test (Rice 1989). parisons. The sequencing reaction followed the manu- facturer's protocol (Pharmacia ALFexpress, AutoRead). Results Nucleotide sequences were determined in both strands Phylogenetic Relationship of Arabis and Arabidopsis by a Pharmacia ALFred sequencer. Newly determined Species Adh sequences were deposited in the DDBJ/GenBank/ EMBL databases under accession numbers AB015498± In the investigated Arabis and Arabidopsis species, AB015508. the Adh genes have seven exons and six introns (table 2). Every intron starts with dinucleotide GT and ends Data Analyses with AG, which is typical of eukaryotes. Lengths of Program package DnaSP, version 2.5 (Rozas and introns, especially intron 1, vary among species. It was Rozas 1997), was used to analyze intra- and interspeci®c not straightforward to align each intron over the 12 spe- variation by estimation of nucleotide diversity (p; Nei cies. In A. thaliana, introns 2, 3, and 6 vary in length. and Li 1979) and the tests of Hudson, Kreitman, and This variation is associated with dimorphic indels (Innan Aguade (1987), Tajima (1989), McDonald and Kreitman et al. 1996). In A. gemmifera, the sizes of four introns (1991), and Fu and Li (1993). Phylogenetic analyses, vary, mainly owing to the variation in repeats of T (Mi- consisting of estimation of the number of nucleotide yashita, Innan, and Terauchi 1996). substitutions per site (Kimura 1980; Nei and Gojobori The number of nucleotide substitutions per site 1986) and construction and bootstrap probability esti- (Nei and Gojobori 1986) in the coding region of the Adh mation of the neighbor-joining (NJ) tree (Saitou and Nei gene between each pair of the 12 species was estimated 1987), were conducted with PHYLIP, version 3.57 (Fel- (table 3).
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