Summary
The mitochondrial genomes of wheat and rye each contain a three-member family of recombining repeat peat sequences (the “18S/5S repeat”) that encode genes for 18S and 5S rRNAs (rrn18 and rrn5) and tRNAfMet (trnfM). Here we present, for wheat and rye, the sequence and boundaries of the “common sequence unit” (CSU) that is shared between all three repeat copies in each species. The wheat CSU is 4,429 base-pairs long and contains (in addition to trnfM, rrn18 and rrn5) a putative promoter, three tRNA-like elements (“t-elements”), and part of a pseudogene (“ψatpA c”) that is homologous to chloroplast atpA, which encodes the α subunit of chloroplast F1 ATPase. The rye CSU is somewhat smaller (2,855 base pairs) but contains much the same genic and other sequence elements as its wheat counterpart, except that two of the three t-elements as well as ψatpA c are found in only one of the three downstream flanks of the 18S/5S repeat, outside the CSU boundaries. In interpreting the seuuence data in terms of the evolutionary history of the 18S/5S-repeat family of wheat and rye, we conclude that (1) the wheat-rye form of the 18S/5S repeat most likely originated between 3 and 14 million years ago, in a lineage that gave rise to wheat and rye but not to barley, oasts, rice or maize; (2) the close linkage (1-bp apart) between trnfM and rrn18 is similarly limited in its taxonomic distribution to the wheat/rye lineage; (3) the trnfM-rrn18 pair arose via a single mutation that inserted a sequence block containing trnfM immediately upstream of rrn18; and (4) the presence of a putative promoter upstream of rrn18 in all wheat and rye repeats is consistent with all three repeat copies being transcriptionally active. We discuss these conclusions in the light of the possible functional significance of recombining-repeats in plant mitochondrial genomes.
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References
André C, Levy A, Walbot V (1992) Trends Genet 8:128–132
Augustyniak, H (1991) EMBL Sequence Database, Accession Number Z11512
Bendich AJ (1985) In: Hohn B, Dennis ES (eds) Genetic flux in plants. Springer, Wien, pp 111–138
Bendich AJ (1987) BioEssays 6:279–282
Bendich AJ, Smith SB (1990) Curr Genet 17:421–425
Borsuk P, Sirko A, Bartnik E (1986) Nucleic Acids Res 14:7508
Chao S, Sederoff RR, Levings CS III (1983) Plant Physiol 71:190–193
Coulthart MB, Huh GS, Gray MW (1990) Curr Genet 17:339–346
Dale RMK, McClure BA, Houchins JP (1985) Plasmid 13:31–40
Falconet D, Lejeune B, Quetier F, Gray MW (1984) EMBO J 3:297–302
Falconet D, Delorme S, Lejeune B, Sévignac M, Delcher E, Bazetoux S, Quétier F (1985) Curr Genet 9:169–174
Folkerts O, Hanson MR (1989) Nucleic Acids Res 17:7345–7357
Gottschalk M, Brennicke A (1985) Curr Genet 9:165–168
Grabau EA (1985) Plant Mol Biol 5:119–124
Gray MW, Spencer DF (1983) FEBS Lett 161:323–327
Gray MW, Hanic-Joyce PJ, Covello PS (1992) Annu Rev Plant Physiol Plant Mol Biol 43:145–175
Hanic-Joyce PJ, Spencer DF, Gray MW (1990) Plant Mol Biol 15:551–559
Henikoff S (1984) Gene 28:351–359
Howe CJ, Fearnley IM, Walker JE, Dyer TA, Gray JC (1985) Plant Mol Biol 4:333–345
Joyce PBM, Spencer DF, Gray MW (1988) Plant Mol Biol 11:833–843
Jubier M-F, Lucas H, Delcher E, Hartmann C, Quétier F, Lejeune B (1990) Curr Genet 17:523–528
Lejeune B, Delorme S, Delcher E, Quétier F (1987) Plant Physiol Biochem 25:227–233
Lonsdale DM, Hodge TP, Fauron C M-R (1984) Nucleic Acids Res 12:9249–9261
Makaroff CA, Palmer JD (1989) J Biol Chem 264:11706–11713
Maloney AP, Walbot V (1990) J Mol Biol 213:633–649
Maxam AM, Gilbert W (1980) Methods Enzymol 65:499–560
Palmer DJ (1985) In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York London, pp 131–240
Palmer JD (1990) Trends Genet 6:115–120
Palmer JD (1991) In: Bogorad L, Vasil IK (eds) The molecular biology of plastids (vol 7A in Cell culture and somatic cell genetics of plants). Academic Press, San Diego, pp 5–53
Palmer JD, Herbon LA (1987) Curr Genet 11:565–570
Palmer JD, Herbon LA (1988) J Mol Evol 28:87–97
Palmer JD, Shields CR (1984) Nature 307:437–440
Quetier F, Lejeune B, Delorme S, Falconet D, Jubier MF (1985) In: van Vloten-Doting L, Groot GSP, Hall TC (eds) Molecular form and function of the plant genome. Plenum Press, New York, pp 413–420
Rodermel SR, Bogorad L (1987) Genetics 116:127–139
Runeberg-Roos P, Grienenberger JM, Guillemaut P, Marechal L, Gruber V, Weil JH (1987) Plant Mol Biol 9:237–246
Sanger F, Nicklen S, Coulson AR (1977) Proc Natl Acad Sci USA 74:5463–5467
Siculella L, Palmer JD (1988) Nucleic Acids res 16:3787–3799
Spencer DF, Bonen L, Gray MW (1981) Biochemistry 20:4022–4029
Spencer DF, Schnare MN, Gray MW (1984) Proc Natl Acad Sci USA 81:493–497
Spencer DF, Schnare MN, Coulthart MB, Gray MW (1992) Plant Mol Biol (in press)
Stern DB, Lonsdale DM (1982) Nature 299:698–702
Stern DB, Palmer JD (1984a) Proc Natl Acad Sci USA 81:1946–1950
Stern DB, Palmer JD (1984b) Nucleic Acids Res 12:6141–6157
Wolfe KH, Li W-H, Sharp PM (1987) Proc Natl Acad Sci USA 84:9054–9058
Wolfe KH, Gouy M, Yang Y-W, Sharp PM, Li W-H (1989a) Proc Natl Acad Sci USA 86:6201–6205
Wolfe KH, Sharp PM, Li W-H (1989b) J Mol Evol 29:208–211
Yamato K, Ogura Y, Kanegae T, Yamada Y, Ohyama K (1992) Theor Appl Genet 83:279–288
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Communicated by C. W. Birky, Jr.
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Coulthart, M.B., Spencer, D.F. & Gray, M.W. Comparative analysis of a recombining-repeat-sequence family in the mitochondrial genomes of wheat (Triticum aestivum L.) and rye (Secale cereale L.). Curr Genet 23, 255–264 (1993). https://doi.org/10.1007/BF00351504
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DOI: https://doi.org/10.1007/BF00351504