Summary
Mapping studies were performed with 18 cloned probes on mitochondrial DNA (mtDNA) from 15 species ofSuillus and four species from three related genera of fleshy pore mushrooms (Boletaceae). WithinSuillus, mtDNAs vary in size from 36 to 121 kb, differ in gene order by only one major rearrangement, and have diverged in nucleotide sequence within the large subunit ribosomal RNA gene region by up to 2.9%. Three additional gene orders exist in related genera. Two of the three can be transformed into the predominantSuillus order by either one or two rearrangements. The fourth requires two to three rearrangements to be converted to any of the others. The minimum estimates of nucleotide divergence within the large subunit ribosomal RNA gene region vary from 8.3% to 11% in comparisons betweenSuillus and these related species. Trees based on restriction-site and size differences within the mitochondrial ribosomal RNA genes were consistent with the hypothesized sequence of genome rearrangements and provide suggestive evidence for a major expansion of the mitochondrial genome withinSuillus. Structural and sequence changes in mtDNA provided information about phylogenetic relationships within the Boletaceae.
Similar content being viewed by others
References
Bonitz SG, Coruzzi G, Thalenfeld BE, Tzagoloff A, Macino G (1980) Assembly of the mitochondrial membrane system: structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrome oxidase. J Biol Chem 255:11927–11941
Bruns TD, Palmer JD, Shumard DS, Grossman GI, Hudspeth MES (1988) Mitochondrial DNAs ofSuillus: three-fold size change in molecules that share a common gene order. Curr Genet 13:49–56
Collins RA, Lambowitz AM (1983) Structural variations and optional intron in the mitochondrial DNA ofNeurospora species isolated from nature. Plasmid 9:53–70
Dujon B (1980) Sequence of the intron and flanking exons of the mitochondrial 21S rRNA gene of yeast strains having different alleles at the omega and rib-1 loci. Cell 20:185–187
Heckman JE, RajBhandary UL (1979) Organization of tRNA and rRNA genes inN. crassa mitochondria: intervening sequence in the large rRNA gene and strand distribution of the RNA genes. Cell 17:583–595
Heim R (1971) The interrelationships between the Agaricales and the Gastromycetes. In: Petersen RH (ed) Evolution in the higher Basidiomycetes. University of Tennessee Press, Knoxville, pp 505–534
Hensgens LAM, Bonen L, de Haan M, van der Horst G, Grivell LA (1983) Two intron sequences in yeast mitochondrial COX1 gene: homology among URF-containing introns and strain-dependent variation in flanking exons. Cell 32:379–389
Hillis DM, Davis SK (1987) Evolution of the 28S ribosomal RNA gene in anurans: regions of variability and their phylogenetic implications. Mol Biol Evol 4:117–125
Jacquier A, Dujon B (1983) The intron of the mitochondrial 21s rRNA gene: distribution in different yeast species and sequence comparison betweenKluyveromyces thermotolerans andSaccharomyces cerevisiae. Mol Gen Genet 192:487–499
Lazarus CM, Lunsdorf H, Han U, Stepien PP, Kuntzel H (1980) Physical map ofAspergillus nidulans mitochondrial gene coding for ribosomal RNA: an intervening sequence in the large rRNA cistron. Mol Gen Genet 177:389–397
Macino G, Tzagoloff A (1979) Assembly of the mitochondrial membrane system: the DNA sequence of a mitochondrial ATPase gene inSaccharomyces cerevisiae. J Biol Chem 254:4617–4623
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Springer Harbor NY
Marsh JL, Erfle M, Wykes EJ (1984) The pIC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation. Gene 32:481–485
Murray MC, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Nei M, Li W (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273
Palmer JD, Herbon LA (1986) Tricircular mitochondrial genomes ofBrassica andRaphanus: reversal of repeat configurations by inversion. Nucleic Acids Res 14:9744–9764
Pantidou ME, Groves JW (1966) Cultural studies of Boletaceae: some species ofSuillus andFuscoboletinus. Can J Bot 44:1371–1392
Pegler DN, Young TWK (1981) A natural arrangement of the Boletales with reference to spore morphology. Trans Br Mycol Soc 76:103–146
Pomerleau R, Smith AH (1962)Fuscoboletinus, a new genus in the Boletaceae. Brittonia 14:156–172
Rohlf FJ (1982) Consensus indices for comparing classifications. Math Biosci 59:131–144
Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Highuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491
Sanders JPM, Heyting C, Verbeet MP, Meijlink CPW, Borst P (1977) The organization of genes in yeast mitochondrial DNA. III. Comparison of the physical maps of the mitochondrial DNAs from three wild-typeSaccharomyces strains. Mol Gen Genet 157:239–261
Singer R (1986) The Agaricales in modern taxonomy, ed 4 Koeltz Scientific Books, Koenrgstein
Singer R, Snell WH, Dick E (1963) The genusFusoboletinus. Mycologia 55:352–357
Smith AH, Thiers HD (1971) The Boletaceae of Michigan. University of Michigan Press, Ann Arbor
Sor F, Fukuhara H (1982) Nature of an inserted sequence in the mitochondrial gene coding for the 15S ribosomal RNA of yeast. Nucleic Acids Res 10:1625–1633
Swofford DL (1985) PAUP-phylogenetic analysis using parsimony version 2.4. User's manual. University of Illinois, Urbana
Taylor JW, Smolich BD, May G (1986) Evolution and mitochondrial DNA inNeurospora crassa. Evolution 40:716–739
Templeton AR (1983a) Phylogenetic inferences from restriction endonuclease cleavage site maps with particular reference to evolution of humans and apes. Evolution 37:221–224
Templeton AR (1983b) Convergent evolution and nonparametric inferences from restiction data and DNA sequences. In: Weir BS (ed) Statistical analysis of DNA sequence data. Marcel Dekker, New York, pp 151–180
Watling R (1969) The genusParagyrodon. Notes R Bot Gard Edinb 29:67–73
Waring RB, Davies RW, Scazzacchio C, Brown TA (1982) Internal structure of a mitochondrial intron ofAspergillus nidulans. Proc Natl Acad Sci USA 79:6332–6336
Wright RM, Cummings DJ (1983) Mitochondrial DNA fromPodospora anserina IV. The large ribosomal RNA gene contains two long intervening sequences. Curr Genet 7:151–157
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bruns, T.D., Palmer, J.D. Evolution of mushroom mitochondrial DNA:Suillus and related genera. J Mol Evol 28, 349–362 (1989). https://doi.org/10.1007/BF02103431
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02103431