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Transduction of a cellular gene by a plant retroelement
Cell, Vol. 77, 479-490,
May 20, 1994, Copyright
0 1994 by Cell Press
Letter to the Editor
Transduction of a Cellular Gene by a Plant Retroelement Ftetroviral transduction of cellular genes is believed to involve transcription initiation at a retroviral promoter and readthrough into adjacent host gene sequences (Weiss et al., 1984). The chimeric transcript is processed and packaged into a viral particle along with a normal viral transcript. Recombination between these two transcripts during reverse transcription results in a defective retrovirus in which part of the coding sequences of the normal virus is replaced with a spliced and often truncated version of the cellular gene. Transduced cellular genes have been found in the oncoviruses of mammals and birds, but have not been described in other retroelements or in other organisms. The Bsl retroelement of maize was originally isolated as a recent insertion in a mutant Ad717 allele (Acfh745446, Johns et al., 1985). Although Bsl has many of the features of retrotransposons, including identical long terminal repeats (LTRs) and typical primer binding sites, it is unusual in structure because of its small size and the absence of a pal gene (Johns et al., 1989; Jin and Bennetzen, 1989). Searches of the Get-Bank (version 81 .O) and EMBL (version 37.0) data bases using Bs7 as a query reveal that one-fifth of the Bs7 sequence has significant similarity to plant plasma membrane proton-translocating ATPase @ma) cDNAs. This 854 bp region has highest similarity (88% nucleotide and 83% amino acid sequence identity) to a recently sequenced maize pma cDNA (Zrnpfna7) extending from the last codon of exon 4 through the first 72 bp of exon 10 (Figure 1). We have called this region of 8~7 retroelement pma (rpma). Comparison of r-pma to the Zmpmal genomic sequence
reveals that rpma lacks introns and has sustained an internal deletion including most of exon 8. The structure of Bs7 is very reminiscent of oncogenecontaining retroviruses (Figure 2). Like Bs7 , oncoviruses harbor processed, altered versions of cellular genes (v-ones). Since v-ones have replaced internal coding domains, gene products required for viral replication must be provided in trans by a helper virus. Similarly, f3s7 lacks the coding capacity required for autonomous retrotransposition; pal gene se quences appear to have been replaced by r-pme. The recent insertion of Es7 into the maize A&7 gene must therefore have been facilitated by pal function supplied in trans. Despite these structural defects, the Bs7 element is found in l-5 copies in all maize lines analyzed as well as in the genome of its closest relative, teosinte (Johns et al., 1985; Bennetzen et al., 1988). The presence of r-pma in Bs7 provides an example of the transduction of a cellular gene by a retroelement other than the vertebrate oncoviruses. Although Bsl is referred to as an LTR retrotransposon, there is a possibility that it is a retrovirus since most of the distinguishing internal domains have been replaced by r-pma. However, if 6~7 is deriied from a retrotransposon, its existence provides evidence that retrotransposons can transduce cellular sequences. The ability of retrotransposons to transduce cellular sequences is a key feature in the theory that retroviruses evolved following the transduction of an env-like cellular gene by an ancestral retrotransposon (Doolittle et al., 1989; Xiong and Eickbush, 1990). Other aspects of structural similarity between Bs7 and oncoviruses are intriguing but only speculative at this time. Like many oncoviruses, Bs7 has an open reading frame (ORFl; Johns et al., 1989; Jin and Bennetzen, 1989) that, if translated, would form a fusion protein including gag and
Figure 1. Part of Maize Ssl r-pma Has Significant Sequence identity with Zmpmal Partial Zmpmal cDNA and genomic sequences have been deposited in the GenSank data base with the accession numbers UO9994 and UO8985, respectively.
Figure 2. The Maize 13~7 Retroelement turally Reminiscent of Oncoviruses
Is Struc-
Cdl 480
the cellularly derived gene fragment (Weiss et al., 1984). Like the proteins encoded by some proto-oncogenes, PMA is a phosphoprotein localized to the plasma membrane, has protein kinase activity, is regulated by autophosphorylation, and is involved in the regulation of growth (Serrano, 1989). PMA proteins are responsible for generating a membrane potential across the plasma membrane by active transport of protons and facilitate the symport of other ions and nutrients. Plant PMA proteins in particular play a critical role during cell elongation by the acidification of the cell wall in response to the hormone auxin. The putative gag-pma gene product would contain the second of four PMA transmembrane loops and a highly conserved domain involved in the coupling of ATP hydrolysis and proton transport. This domain also contains an aspartate residue involved in PMA regulation by autophosphorylation. r-pma, however, does not encode the PMA protein kinase or phosphatase domains. The presence of 8~7 in normal maize and teosinte strains indicates that 6.~1 sequences do not condition a diseased phenotype. While this defective element may simply be maintained in the plant genome, the presence and conservation of ORFl suggests the intriguing possibility that a GAGPMA fusion protein may facilitate Bsl retrotransposition or contribute to normal plant development.
Thomas E. Bureau,‘t Shawn E. White,t and Susan R. Wessler*t *Department of Genetics, tDepartment of Botany University of Georgia Athens, Georgia 30602 References Bennetzen, J. L., Brown, W. E., and Springer, P. S. (1988). In Plant Transposable Elements, 0. Nelson, ed. (New York: Plenum Press), pp. 237-250. Doolittle, R. F., Feng, D.-F., Johnson, Quart. Rev. Biol. 64, l-30. Jin, Y.-K., and Bennetzen, 8235-6239.
M. S., and McClure,
J. L. (1989).
Proc. Natl. Acad.
M. A. (1989). Sci. USA 86,
Johns, M. A., Barbock, M. S., Fuerstenberg, S. M., Fuerstenberg, S. I., Freeling, M., and Simpson, R. 8. (1989). Plant Mol. Biol. 12, 633-642. Johns, 1102. Serrano, 61-94. Weiss, Viruses Press).
M. A., Mottinger, R. (1989).
J., and Freeling,
Annu.
Rev.
Plant
M. (1985). EMBO Physiol.
J. 4, 1093-
Plant Mol.
Biol. 40,
R., Teich, N., Varmus, l-t., and Coffin, J. (1984). RNA Tumor (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory
Xiong, Y., and Eickbush,
T. H. (1990). EMBO
J. 9, 3363-3362.
May 20, 1994, Copyright
0 1994 by Cell Press
Letter to the Editor
Transduction of a Cellular Gene by a Plant Retroelement Ftetroviral transduction of cellular genes is believed to involve transcription initiation at a retroviral promoter and readthrough into adjacent host gene sequences (Weiss et al., 1984). The chimeric transcript is processed and packaged into a viral particle along with a normal viral transcript. Recombination between these two transcripts during reverse transcription results in a defective retrovirus in which part of the coding sequences of the normal virus is replaced with a spliced and often truncated version of the cellular gene. Transduced cellular genes have been found in the oncoviruses of mammals and birds, but have not been described in other retroelements or in other organisms. The Bsl retroelement of maize was originally isolated as a recent insertion in a mutant Ad717 allele (Acfh745446, Johns et al., 1985). Although Bsl has many of the features of retrotransposons, including identical long terminal repeats (LTRs) and typical primer binding sites, it is unusual in structure because of its small size and the absence of a pal gene (Johns et al., 1989; Jin and Bennetzen, 1989). Searches of the Get-Bank (version 81 .O) and EMBL (version 37.0) data bases using Bs7 as a query reveal that one-fifth of the Bs7 sequence has significant similarity to plant plasma membrane proton-translocating ATPase @ma) cDNAs. This 854 bp region has highest similarity (88% nucleotide and 83% amino acid sequence identity) to a recently sequenced maize pma cDNA (Zrnpfna7) extending from the last codon of exon 4 through the first 72 bp of exon 10 (Figure 1). We have called this region of 8~7 retroelement pma (rpma). Comparison of r-pma to the Zmpmal genomic sequence
reveals that rpma lacks introns and has sustained an internal deletion including most of exon 8. The structure of Bs7 is very reminiscent of oncogenecontaining retroviruses (Figure 2). Like Bs7 , oncoviruses harbor processed, altered versions of cellular genes (v-ones). Since v-ones have replaced internal coding domains, gene products required for viral replication must be provided in trans by a helper virus. Similarly, f3s7 lacks the coding capacity required for autonomous retrotransposition; pal gene se quences appear to have been replaced by r-pme. The recent insertion of Es7 into the maize A&7 gene must therefore have been facilitated by pal function supplied in trans. Despite these structural defects, the Bs7 element is found in l-5 copies in all maize lines analyzed as well as in the genome of its closest relative, teosinte (Johns et al., 1985; Bennetzen et al., 1988). The presence of r-pma in Bs7 provides an example of the transduction of a cellular gene by a retroelement other than the vertebrate oncoviruses. Although Bsl is referred to as an LTR retrotransposon, there is a possibility that it is a retrovirus since most of the distinguishing internal domains have been replaced by r-pma. However, if 6~7 is deriied from a retrotransposon, its existence provides evidence that retrotransposons can transduce cellular sequences. The ability of retrotransposons to transduce cellular sequences is a key feature in the theory that retroviruses evolved following the transduction of an env-like cellular gene by an ancestral retrotransposon (Doolittle et al., 1989; Xiong and Eickbush, 1990). Other aspects of structural similarity between Bs7 and oncoviruses are intriguing but only speculative at this time. Like many oncoviruses, Bs7 has an open reading frame (ORFl; Johns et al., 1989; Jin and Bennetzen, 1989) that, if translated, would form a fusion protein including gag and
Figure 1. Part of Maize Ssl r-pma Has Significant Sequence identity with Zmpmal Partial Zmpmal cDNA and genomic sequences have been deposited in the GenSank data base with the accession numbers UO9994 and UO8985, respectively.
Figure 2. The Maize 13~7 Retroelement turally Reminiscent of Oncoviruses
Is Struc-
Cdl 480
the cellularly derived gene fragment (Weiss et al., 1984). Like the proteins encoded by some proto-oncogenes, PMA is a phosphoprotein localized to the plasma membrane, has protein kinase activity, is regulated by autophosphorylation, and is involved in the regulation of growth (Serrano, 1989). PMA proteins are responsible for generating a membrane potential across the plasma membrane by active transport of protons and facilitate the symport of other ions and nutrients. Plant PMA proteins in particular play a critical role during cell elongation by the acidification of the cell wall in response to the hormone auxin. The putative gag-pma gene product would contain the second of four PMA transmembrane loops and a highly conserved domain involved in the coupling of ATP hydrolysis and proton transport. This domain also contains an aspartate residue involved in PMA regulation by autophosphorylation. r-pma, however, does not encode the PMA protein kinase or phosphatase domains. The presence of 8~7 in normal maize and teosinte strains indicates that 6.~1 sequences do not condition a diseased phenotype. While this defective element may simply be maintained in the plant genome, the presence and conservation of ORFl suggests the intriguing possibility that a GAGPMA fusion protein may facilitate Bsl retrotransposition or contribute to normal plant development.
Thomas E. Bureau,‘t Shawn E. White,t and Susan R. Wessler*t *Department of Genetics, tDepartment of Botany University of Georgia Athens, Georgia 30602 References Bennetzen, J. L., Brown, W. E., and Springer, P. S. (1988). In Plant Transposable Elements, 0. Nelson, ed. (New York: Plenum Press), pp. 237-250. Doolittle, R. F., Feng, D.-F., Johnson, Quart. Rev. Biol. 64, l-30. Jin, Y.-K., and Bennetzen, 8235-6239.
M. S., and McClure,
J. L. (1989).
Proc. Natl. Acad.
M. A. (1989). Sci. USA 86,
Johns, M. A., Barbock, M. S., Fuerstenberg, S. M., Fuerstenberg, S. I., Freeling, M., and Simpson, R. 8. (1989). Plant Mol. Biol. 12, 633-642. Johns, 1102. Serrano, 61-94. Weiss, Viruses Press).
M. A., Mottinger, R. (1989).
J., and Freeling,
Annu.
Rev.
Plant
M. (1985). EMBO Physiol.
J. 4, 1093-
Plant Mol.
Biol. 40,
R., Teich, N., Varmus, l-t., and Coffin, J. (1984). RNA Tumor (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory
Xiong, Y., and Eickbush,
T. H. (1990). EMBO
J. 9, 3363-3362.