Abstract
Mitochondria from the green alga Bryopsis sp. very often contained a 4.5 kb double-stranded RNA (dsRNA) at a defined level. Complementary DNA probes derived from the mitochondrial dsRNA hybridized with none of the algal chloroplast dsRNAs of 1.7 to 2.2 kb, but did hybridize with a similar-sized dsRNA among several dsRNAs from the mitochondria of B. maxima. Sequence analysis of the mitochondrial dsRNA from Bryopsis sp. revealed only two large, overlapping, open reading frames (ORFs) on one strand if UGA was taken as a non-termination codon, suggesting the independent phylogenetic evolution of the mitochondrial dsRNA. Consensus sequence for RNA-dependent RNA polymerase was found within the longer ORF (2472 bp) of the dsRNA. The overlapping 52 bp of the ORFs in different reading frames is suggestive of the occurrence of a -1 ribosomal frameshift in the mitochondrial translation system. The observed simple genetic structures suggest that the algal mitochondrial dsRNA might be deficient in a gene for movement from cell to cell in host plants and, hence, has a plasmid-like nature that is distinct from that of infectious plant viruses. The nature and origin of the endogenous dsRNAs of various sizes and their relationships are discussed.
Similar content being viewed by others
References
Antoniw JF, White RF, Xie W: Cryptic viruses of beet and other plants. In: Fraser RSS (ed) Recognition and Response in Plant Virus Interactions, pp. 273–286. SpringerVerlag, Berlin/ Heidelberg (1990).
Ashihara H: Presence of phosphoribosylpyrophosphate synthetase in chloroplasts from fronds of Bryopsis. Curr Sci 59: 939–941 (1991).
Boccardo G, Accotto GP: RNAdependent RNA polymerase activity in two morphologically different white clover cryptic viruses. Virology 163: 413–419 (1988).
Boccardo G, Lisa V, Luisoni E, Milne RG: Cryptic plant viruses. Adv Virus Res 32: 171–214 (1987).
Boyen C, Leblanc C, Bonnard G, Grienenberger JM, Kloareg B: Nucleotide sequence of the cox3 gene from Chondrus crispus: evidence that UGA encodes tryptophan and evolutionary implications. Nucl Acids Res. 22: 1400–1403 (1994).
Brierley I: Ribosomal frameshifting viral RNAs. J Gen Virol 76: 1885–1892 (1995).
Brown GG, Finnegan PM: RNA plasmids. Int Rev Cytol 117: 1–56 (1989).
Chomeczynski P, Sacchi N: Singlestep method of RNA isolation by acid guanidinium thiocyanatephenolchloroform extraction. Anal Biochem 162: 156–159 (1987).
Chung IK, Armstrong TC, Patterson JL: Identification of a short viral transcript in Leishmania RNA virusinfected cells. Virology 198: 552–556 (1994).
Citovsky V: Probing plasmodesmal transport with plant viruses. Plant Physiol 102: 1071–1076 (1993).
Dinman JD, Icho T, Wickner RB: A–1 ribosomal frameshift in a doublestranded RNA virus of yeast forms a gagpol fusion protein. Proc Natl Acad Sci USA 88: 174–178 (1991).
Dodds JA, Morris TJ, Jordan RL: Plant viral doublestranded RNA. Annu Rev Phytopath 22: 151–168 (1984).
Fairbanks DJ, Smith SE, Brown JK: Inheritance of large mitochondrial RNA's in alfalfa. Theor Appl Biol 76: 619–622 (1988).
Fukuhara T, Moriyama H, Nitta T: The unusual structure of a novel RNA replicon in rice. J Biol Chem 270: 18147–18149 (1995).
Fukuhara T, Moriyama H, Pak JY, Hyakutake H, Nitta T: Enigmatic doublestranded RNA in Japonica rice. Plant Mol Biol 21: 1121–1130 (1993).
Ghabrial SA, Bozarth RF, Buck KW, Yamashita S, Martelli GP, Milne RG: Partitiviridae. In: Murphy FA (ed) Sixth Report of the International Committee for the Taxonomy of Viruses, pp. 253–260, SpringerVerlag, New York (1994).
Ghabrial SA, Bruenn JA, Buck KW, Wickner PB, Patterson JL, Stuart KD, Wang AL, Wang CC: Totiviridae. In: Murphy FA (ed) Sixth Report of the International Committee for the Taxonomy of Viruses, pp. 245–252, SpringerVerlag, New York (1994).
Grill LK, Garger SJ: Identification and characterization of doublestranded RNA associated with cytoplasmic male sterility in Vicia faba. Proc Natl Acad Sci USA 78: 7043–7046 (1981).
Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM: RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341: 660–662 (1989).
HayashiIshimaru Y, Ohama T, Kawatsu Y, Nakamura K, Osawa S: UAG is a sense codon in several chlorophycean mitochondria. Curr Genet 30: 29–33 (1996).
Higgins DG, Bleasby AJ, Fuchs R: CLUSTAL V: improved software formultiple sequence alignment. Comput Appl Biosci 8: 189–191 (1992).
Hillman BL, Fulbright DW, Nuss DL, van Alfen NK: Hypoviridae. In: Murphy FA (ed) Sixth Report of the International Committee for the Taxonomy of Viruses, pp. 261–264. Springer-Verlag, New York (1994).
Icho T, Wickner RB: The doublestranded RNA genome of yeast virus LA encodes its own putative RNA polymerase by fusing two open reading frames. J Biol Chem 264: 6716–6723 (1989).
Ishihara J, Pak JY, Fukuhara T, Nitta T: Association of particles that contain doublestranded RNAs with algal chloroplasts and mitochondria. Planta 187: 475–482 (1992).
Kim KH, Lommel SA: Identification and analysis of the site of —1 ribosomal frameshifting in red clover necrotic mosaic virus. Virology 200: 574–582 (1994).
Koonin EV, Mushegian AR, Ryabov EV, Dolja VV: Diverse groups of plant RNAand DNAviruses share related movement proteins that may possess chaperonelike activity. J Gen Virol 72: 2895–2903 (1991).
Koonin EV: The phylogeny of RNAdependent RNA polymerases of positivestrand RNA viruses. J Gen virol 72: 2197–2206 (1991).
Kück U, Neuhaus H: Universal genetic code evidenced inmitochondria of chlamydomonas reinhardii. Appl Microbiol Biotechnol 23: 462–469 (1986).
Lefebvre A, Scalla R, Pfeiffer P: The doublestranded RNA associated with the ‘447’ cytoplasmic male sterility in Vicia faba is packaged together with its replicase in cytoplasmic membranous vesicles. Plant Mol Biol 14: 477–490 (1990).
Lonsdale DH: Viral RNA in mitochondria? Nature 323: 299 (1986).
MacBeth KJ, Patterson JL: The short transcript of Leishmania RNA virus is generated by RNA cleavage. J Virol 69: 3458–3464 (1995).
Matzura O, Wennborg A: RNAdraw: an integrated program for RNA secondary structure calculation and analysis under 32bit Microsoft Windows Computer Applications. CABIOS 12: 247–249 (1996).
Melcher U: Similarities between putative transport proteins of plant viruses. J Gen Virol 71: 1009–1018 (1990).
Milne RG, Natsuaki T: Cryptoviruses. In: Singh RP, Singh U, Kohmoto K (eds) Pathogenesis and Host Specificity in Plant Disease, vol. 3, pp. 239–247. Pergamon, Oxford (1994).
Misonou T, Ishihara J, Pak JY, Nitta T: Restriction endonuclease analysis of chloroplast and mitochondrial DNAs from Bryopsis (Derbesiales, Chlorophyta). Phycologia 28: 422–428 (1989).
Miyazaki S, Iwabuchi K, Pak JY, Fukuhara T, Nitta T: Selective occurrence of endogenous doublestranded RNAs in insects. Insect Biochem Mol Biol 26: 955–961 (1996).
Moriyama H, Kanaya K, Wang JZ, Nitta T, Fukuhara T: Stringently and developmentally regulated levels of a cytoplasmic doublestranded RNA and its highefficiency transmission via egg and pollen in rice. Plant Mol Biol 31: 713–719 (1996).
Moriyama H, Nitta T, Fukuhara T: Doublestranded RNA in rice: a novel RNA replicon in plants. Mol Gen Genet 248: 364–369 (1995).
Morris TJ, Dodds JA: Isolation and analysis of doublestranded RNA from virusinfected plant and fungal tissue. Phytopathology 69: 854–858 (1979).
Newhouse JR, MacDonald WL, Hoch HC: Viruslike particles in hyphae and conidia of European hypovirulent (dsRNAcontaining) strains of Cryphonectria parasitica. Can J Bot 68: 90–101 (1990).
Pak JY, Solorzano C, Arai M, Nitta T: Two distinct steps for spontaneous generation of subprotoplasts from a disintegrated Bryopsis cell. Plant Physiol 96: 819–826 (1991).
Pfeiffer P, Jung JL, Heitzler J, Keith G: Unusual structure of the doublestranded RNA associated with the ‘447’ cytoplasmic male sterility in Vicia faba. J Gen Virol 74: 1167–1173 (1993).
Polashock JJ, Hillman BI: A small mitochondrial doublestranded (ds) RNA element associated with a hypovirulent strain of the chestnut blight fungus and ancestrally related to yeast cytoplasmic T and WdsRNAs. Proc Natl Acad Sci USA 91: 8680–8684 (1994).
Rodoriguez-Cousino N, Esteban LM, Esteban R: Molecular cloning and characterization of W doublestranded RNA, a linear molecule present in Saccharomyces cerevisiae. J Biol Chem 266: 12772–12778 (1991).
Rogers HJ, Buck KW, Braiser CM: A mitochondrial target for doublestranded RNA in diseased isolates of the fungus that cause Dutch elm disease. Nature 329: 558–560 (1987).
Schuster DM, Buchman GW, Rashtchian A: A simple and efficient method for amplification cDNA ends using 5′ RACE. Focus 14: 46–52 (1992).
Stuart KD, Weeks R, Guilbride L, Myler PJ: Molecular organization of Leishmania RNA virus 1. Proc Natl Acad Sci USA 89: 8596–8600 (1992).
Wang AL, Wang CC: Viruses of the protozoa. Annu Rev Microbiol 45: 251–263 (1991).
Wolff G, Plante I, Lang BF, Kück U, Burger G: Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. Gene content and genome organization. J Mol Biol 237: 75–86 (1994).
Xie WS, Antoniw JF, White RF: Nucleotide sequence of beet cryptic virus 3 dsRNA2 which encodes a putative RNAdependent RNA polymerase. J Gen Virol 74: 2303 (1993).
Zabalgogeazcoca IA, Cox-Fostre DC, Gildow FE: Pedigree analysis of the transmission of a double-stranded-RNA in barley cultivars. Plant Sci 91: 45–53 (1993).
Zhang M, Brown GG: Structure of maize mitochondrial replicon RNA b and its relationship with other autonomously replicationg RNA species. J Mol Biol 230: 757–765 (1993).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Koga, R., Fukuhara, T. & Nitta, T. Molecular characterization of a single mitochondria-associated double-stranded RNA in the green alga Bryopsis. Plant Mol Biol 36, 717–724 (1998). https://doi.org/10.1023/A:1005907310553
Issue Date:
DOI: https://doi.org/10.1023/A:1005907310553