An RNA Activator of Subgenomic mRNA1 Transcription in Tomato Bushy Stunt Virus

Many (+)-strand RNA viruses transcribe small subgenomic (sg) mRNAs that allow for regulated expression of a subset of their genes. Tomato bushy stunt virus (TBSV) transcribes two such messages and here we report the identification of a long-distance RNA·RNA interaction that is essential for the efficient accumulation of capsid protein-encoding sg mRNA1. The relevant base pairing interaction occurs within the TBSV RNA genome between a 7-nucleotide (nt) long sequence, separated by just 3 nt from the downstream sg mRNA1 initiation site, and a complementary sequence positioned some ∼1000 nt further upstream. Analyses of this interaction indicate that it (i) functions in the (+)-strand, (ii) modulates both (+)- and (−)-strand sg mRNA1 accumulation, (iii) specifically regulates the accumulation of sg mRNA1 (−)-strands, (iv) controls sg mRNA1 expression from an ectopic transcriptional initiation site, (v) may occur in cis and, and (vi) could nucleate the formation of a more complex RNA structure. These data are most consistent with a role for this interaction in regulating sg mRNA1 accumulation at the level of transcription. Many (+)-strand RNA viruses transcribe small subgenomic (sg) mRNAs that allow for regulated expression of a subset of their genes. Tomato bushy stunt virus (TBSV) transcribes two such messages and here we report the identification of a long-distance RNA·RNA interaction that is essential for the efficient accumulation of capsid protein-encoding sg mRNA1. The relevant base pairing interaction occurs within the TBSV RNA genome between a 7-nucleotide (nt) long sequence, separated by just 3 nt from the downstream sg mRNA1 initiation site, and a complementary sequence positioned some ∼1000 nt further upstream. Analyses of this interaction indicate that it (i) functions in the (+)-strand, (ii) modulates both (+)- and (−)-strand sg mRNA1 accumulation, (iii) specifically regulates the accumulation of sg mRNA1 (−)-strands, (iv) controls sg mRNA1 expression from an ectopic transcriptional initiation site, (v) may occur in cis and, and (vi) could nucleate the formation of a more complex RNA structure. These data are most consistent with a role for this interaction in regulating sg mRNA1 accumulation at the level of transcription. subgenomic activator sequence 1 core element cucumber necrosis virus coat protein distal element open reading frame potato virus X receptor sequence 1 red clover necrotic mosaic virus stem-loop tomato bushy stunt virus wild type Viral infections of eukaryotic cells are complex processes that require regulated expression of a variety of viral genes. Depending on the virus, this expression can be regulated at different levels, including transcriptional, post-transcriptional, translational, and post-translational (1Maia I.G. Seron K. Haenni A. Bernardi F. Plant Mol. Biol. 1996; (+)-strand RNA of subgenomic mRNAs allow for regulated expression of viral The by sg mRNAs are can the messages the of open reading that are in the viral such are within the of sg a for their efficient a the and of viral protein for sg are (i) of sg mRNAs from a (−)-strand initiation A. and (ii) of a RNA (−)-strand is a for of sg mRNAs A. that (−)-strand of the genome by of the a transcribe sg mRNAs this is consistent with data from on an of (+)-strand RNA viruses Biol. for this is bushy stunt virus (TBSV) is the of both the and the (+)-strand RNA genome of The viral RNA and RNA protein are both from the the of the of the the more coat protein and the the and are from two sg mRNAs that are TBSV infections A. The transcriptional of the of the two sg sg and RNA for efficient of this both and distal initiation RNA accumulation of this sg a long-distance base pairing interaction between a sequence within the core element just the sg initiation site, and a complementary sequence within the distal element some (nt) RNA interaction functions in the (+)-strand of the viral genome and is the of within the and Biol. the of (−)-strand sg occurs of (+)-strand sg accumulation Biol. with the (+)-strand of the is consistent with a for sg is the RNA in the of sg mRNA1. is for a viral it for the efficient expression of of are in that is sg mRNA1 is that it can be by the of at and of initiation RNA the we RNA and within the TBSV genome that are for sg mRNA1 transcription. for a long-distance RNA·RNA interaction that the accumulation of sg mRNA1. The data indicate that this interaction occurs in the (+)-strand, in specifically the accumulation of (−)-strand sg and is for regulating expression from an ectopic transcriptional initiation The of this long-distance RNA·RNA interaction are and with of the interaction in regulating sg data sg mRNAs are in of the TBSV genome and that are for sg mRNA1 two and be essential for efficient sg mRNA1 accumulation, and the data a for their base pairing in the the interaction be specifically for (−)-strand sg mRNA1 accumulation and sg mRNA1 from an ectopic initiation These data a role for this long-distance RNA·RNA interaction in regulating transcriptional and of the and small of and the (i) in the of the and (ii) could this interaction be by RNA of that the of the genome in the formation of this base in cis the could be in this we and sequence by for that could the of a on the for the a in the of most of within a in a could the of for base pairing with of the at is in the activator of sg in the (+)-strand virus red clover necrotic mosaic virus the in the of the activator in with a sequence just the sg transcriptional initiation in sg with the base pairing of be by of and occur in the is the at is from the sg is in for of RNA The sg mRNA1 of TBSV a for of of in the are could with this are the accumulation of sg mRNA1 and sg for TBSV and infections RNA A. A. A. sg is in the accumulation at sg mRNA1 accumulation is in the at The of in with and that the two could different within the of in of and the formation of stem-loop of and by stem-loop in most of the in the and are at at and the are structure. The sequence is in for an by an that is a in and the of the is of the is essential for efficient sg mRNA1 accumulation, the of this interaction is is that the base pairing interaction between and the formation of a more complex structure. the the of an is by and sequence The formation of such a could further the of RNA by of is and may be in RNA within the TBSV genome Mol. Biol. the of could the sequence just is complementary the sequence just base pairing of could further the The the for this RNA interaction be more complex and are for the in sg mRNA1 and sg in The are on a of sequence RNA for sg mRNA1 The is in and the is by a by base pairing of and is by a with The initiation for sg mRNA1 is by a RNA for sg The of the and are by and The base pairing in and of both and are The initiation for sg is by a The of the RNA complex is by a that the sequence the two of the with the and interaction is the long-distance interaction be in sg in The is for efficient sg both and with the interaction with between the (i) the base pairing just the of (ii) the long-distance (iii) the occur in the (+)-strand (iv) the some (i) the RNA (ii) the base pairing interaction is the base pairing interaction (iii) the of the base pairing interaction the initiation are different is that this that for RNA of sg the for sg may be and could be for an base pairing interaction the sequence that the potato virus X long-distance base pairing the of the genome and just the initiation of two sg mRNAs sg accumulation RNA The between the of the and the in both of is the in is that is and that the for sg mRNA1 in TBSV is 3 the of the two more and is two RNA for RNA in regulating sg accumulation in TBSV data indicate that in the (+)-strand of the genome and in the transcriptional is both long-distance occur the RNA be in an may be relevant their and could a type of both are by in sequence is by the of both sg mRNA1 and sg on sg is on the sequence of it on the of sg this it is that the the of in is for the of viral RNA specifically sg A. the on sg RNA in TBSV are consistent with their in transcriptional a Biol. RNA (i) of sg occurs of complementary (+)-strand accumulation, be are and for (+)-strand (ii) The in the (+)-strand of the be for in (−)-strand (iii) The interaction is specifically for (−)-strand sg mRNA1 accumulation, in with a role for this element in of (−)-strand data are consistent with a transcriptional further be the by TBSV for sg transcription. Viral infections of eukaryotic cells are complex processes that require regulated expression of a variety of viral genes. Depending on the virus, this expression can be regulated at different levels, including transcriptional, post-transcriptional, translational, and post-translational (1Maia I.G. Seron K. Haenni A. Bernardi F. Plant Mol. Biol. 1996; (+)-strand RNA of subgenomic mRNAs allow for regulated expression of viral The by sg mRNAs are can the messages the of open reading that are in the viral such are within the of sg a for their efficient a the and of viral protein for sg are (i) of sg mRNAs from a (−)-strand initiation A. and (ii) of a RNA (−)-strand is a for of sg mRNAs A. that (−)-strand of the genome by of the a transcribe sg mRNAs this is consistent with data from on an of (+)-strand RNA viruses Biol. for this is Tomato bushy stunt virus (TBSV) is the of both the and the (+)-strand RNA genome of The viral RNA and RNA protein are both from the the of the of the the more coat protein and the the and are from two sg mRNAs that are TBSV infections A. The transcriptional of the of the two sg sg and RNA for efficient of this both and distal initiation RNA accumulation of this sg a long-distance base pairing interaction between a sequence within the core element just the sg initiation site, and a complementary sequence within the distal element some (nt) RNA interaction functions in the (+)-strand of the viral genome and is the of within the and Biol. the of (−)-strand sg occurs of (+)-strand sg accumulation Biol. with the (+)-strand of the is consistent with a for sg transcription. is the RNA in the of sg mRNA1. is for a viral it for the efficient expression of of are in that is sg mRNA1 is that it can be by the of at and of initiation RNA the we RNA and within the TBSV genome that are for sg mRNA1 transcription. for a long-distance RNA·RNA interaction that the accumulation of sg mRNA1. The data indicate that this interaction occurs in the (+)-strand, in specifically the accumulation of (−)-strand sg and is for regulating expression from an ectopic transcriptional initiation The of this long-distance RNA·RNA interaction are and with of the interaction in regulating sg data sg mRNAs are in of the TBSV genome and that are for sg mRNA1 two and be essential for efficient sg mRNA1 accumulation, and the data a for their base pairing in the the interaction be specifically for (−)-strand sg mRNA1 accumulation and sg mRNA1 from an ectopic initiation These data a role for this long-distance RNA·RNA interaction in regulating transcriptional and of the and small of and the (i) in the of the and (ii) could this interaction be by RNA of that the of the genome in the formation of this base in cis the could be in this we and sequence by for that could the of a on the for the a in the of most of within a in a could the of for base pairing with of the at is in the activator of sg in the (+)-strand virus red clover necrotic mosaic virus the in the of the activator in with a sequence just the sg transcriptional initiation in sg with the base pairing of be by of and occur in the is the at is from the sg is in for of RNA The sg mRNA1 of TBSV a for of of in the are could with this are the accumulation of sg mRNA1 and sg for TBSV and infections RNA A. A. A. sg is in the accumulation at sg mRNA1 accumulation is in the at The of in with and that the two could different within the of in of the is essential for efficient sg mRNA1 accumulation, the of this interaction is is that the base pairing interaction between and the formation of a more complex structure. the the of an is by and sequence The formation of such a could further the of RNA by of is and may be in RNA within the TBSV genome Mol. Biol. the of could the sequence just is complementary the sequence just base pairing of could further the The the for this RNA interaction be more complex and are for the in sg mRNA1 and sg in The are on a of sequence RNA for sg mRNA1 The is in and the is by a by base pairing of and is by a with The initiation for sg mRNA1 is by a RNA for sg The of the and are by and The base pairing in and of both and are The initiation for sg is by a The of the RNA complex is by a that the sequence the two of the with the and interaction is the long-distance interaction be in sg in The is for efficient sg both and with the interaction with between the (i) the base pairing just the of (ii) the long-distance (iii) the occur in the (+)-strand (iv) the some (i) the RNA (ii) the base pairing interaction is the base pairing interaction (iii) the of the base pairing interaction the initiation are different is that this that for RNA of sg the for sg may be and could be for an base pairing interaction the sequence that the potato virus X long-distance base pairing the of the genome and just the initiation of two sg mRNAs sg accumulation RNA The between the of the and the in both of is the in is that is and that the for sg mRNA1 in TBSV is 3 the of the two more and is two RNA for RNA in regulating sg accumulation in TBSV data indicate that in the (+)-strand of the genome and in the transcriptional is both long-distance occur the RNA be in an may be relevant their and could a type of both are by in sequence is by the of both sg mRNA1 and sg on sg is on the sequence of it on the of sg this it is that the the of in is for the of viral RNA specifically sg A. the on sg RNA in TBSV are consistent with their in transcriptional a Biol. RNA (i) of sg occurs of complementary (+)-strand accumulation, be are and for (+)-strand (ii) The in the (+)-strand of the be for in (−)-strand (iii) The interaction is specifically for (−)-strand sg mRNA1 accumulation, in with a role for this element in of (−)-strand data are consistent with a transcriptional further be the by TBSV for sg transcription. of the TBSV genome and that are for sg mRNA1 two and be essential for efficient sg mRNA1 accumulation, and the data a for their base pairing in the the interaction be specifically for (−)-strand sg mRNA1 accumulation and sg mRNA1 from an ectopic initiation These data a role for this long-distance RNA·RNA interaction in regulating transcriptional and of the and small of and the (i) in the of the and (ii) could this interaction be by RNA of that the of the genome in the formation of this base in cis the could be in this we and sequence by for that could the of a on the for the a in the of most of within a in a could the of for base pairing with of the at is in the activator of sg in the (+)-strand virus red clover necrotic mosaic virus the in the of the activator in with a sequence just the sg transcriptional initiation in sg with the base pairing of be by of and occur in the is the at is from the sg is in for of RNA The sg mRNA1 of TBSV a for of of in the are could with this are the accumulation of sg mRNA1 and sg for TBSV and infections RNA A. A. A. sg is in the accumulation at sg mRNA1 accumulation is in the at The of in with and that the two could different within the of in of the is essential for efficient sg mRNA1 accumulation, the of this interaction is is that the base pairing interaction between and the formation of a more complex structure. the the of an is by and sequence The formation of such a could further the of RNA by of is and may be in RNA within the TBSV genome Mol. Biol. the of could the sequence just is complementary the sequence just base pairing of could further the The the for this RNA interaction be more complex and are of the with the and interaction is the long-distance interaction be in sg in The is for efficient sg both and with the interaction with between the (i) the base pairing just the of (ii) the long-distance (iii) the occur in the (+)-strand (iv) the some (i) the RNA (ii) the base pairing interaction is the base pairing interaction (iii) the of the base pairing interaction the initiation are different is that this that for RNA of sg the for sg may be and could be for an base pairing interaction the sequence that the potato virus X long-distance base pairing the of the genome and just the initiation of two sg mRNAs sg accumulation RNA The between the of the and the in both of is the in is that is and that the for sg mRNA1 in TBSV is 3 the of the two more and is two RNA for RNA in regulating sg accumulation in TBSV data indicate that in the (+)-strand of the genome and in the transcriptional is both long-distance occur the RNA be in an may be relevant their and could a type of both are by in sequence is by the of both sg mRNA1 and sg on sg is on the sequence of it on the of sg this it is that the the of in is for the of viral RNA specifically sg A. the on sg RNA in TBSV are consistent with their in transcriptional a Biol. RNA (i) of sg occurs of complementary (+)-strand accumulation, be are and for (+)-strand (ii) The in the (+)-strand of the be for in (−)-strand (iii) The interaction is specifically for (−)-strand sg mRNA1 accumulation, in with a role for this element in of (−)-strand data are consistent with a transcriptional further be the by TBSV for sg transcription. and of the and small of and the (i) in the of the and (ii) could this interaction be by RNA of that the of the genome in the formation of this base in cis the could be in this we and sequence by for that could the of a on the for the a in the of most of within a in a could the of for base pairing with of the at is in the activator of sg in the (+)-strand virus red clover necrotic mosaic virus the in the of the activator in with a sequence just the sg transcriptional initiation in sg with the base pairing of be by of and occur in the is the at is from the sg is in for of RNA The sg mRNA1 of TBSV a for of of in the are could with this are the accumulation of sg mRNA1 and sg for TBSV and infections RNA A. A. A. sg is in the accumulation at sg mRNA1 accumulation is in the at The of in with and that the two could different within the of in of the is essential for efficient sg mRNA1 accumulation, the of this interaction is is that the base pairing interaction between and the formation of a more complex structure. the the of an is by and sequence The formation of such a could further the of RNA by of is and may be in RNA within the TBSV genome Mol. Biol. the of could the sequence just is complementary the sequence just base pairing of could further the The the for this RNA interaction be more complex and are of the with the and interaction is the long-distance interaction be in sg in The is for efficient sg both and with the interaction with between the (i) the base pairing just the of (ii) the long-distance (iii) the occur in the (+)-strand (iv) the some (i) the RNA (ii) the base pairing interaction is the base pairing interaction (iii) the of the base pairing interaction the initiation are different is that this that for RNA of sg the for sg may be and could be for an base pairing interaction the sequence that the potato virus X long-distance base pairing the of the genome and just the initiation of two sg mRNAs sg accumulation RNA The between the of the and the in both of is the in is that is and that the for sg mRNA1 in TBSV is 3 the of the two more and is two RNA for RNA in regulating sg accumulation in TBSV data indicate that in the (+)-strand of the genome and in the transcriptional is both long-distance occur the RNA be in an may be relevant their and could a type of both are by in sequence is by the of both sg mRNA1 and sg on sg is on the sequence of it on the of sg this it is that the the of in is for the of viral RNA specifically sg A. the on sg RNA in TBSV are consistent with their in transcriptional a Biol. RNA (i) of sg occurs of complementary (+)-strand accumulation, be are and for (+)-strand (ii) The in the (+)-strand of the be for in (−)-strand (iii) The interaction is specifically for (−)-strand sg mRNA1 accumulation, in with a role for this element in of (−)-strand data are consistent with a transcriptional further be the by TBSV for sg transcription. and of the and small of and the (i) in the of the and (ii) could this interaction be by RNA of that the of the genome in the formation of this base in cis the could be in this we and sequence by for that could the of a on the for the a in the of most of within a in a could the of for base pairing with of the at is in the activator of sg in the (+)-strand virus red clover necrotic mosaic virus the in the of the activator in with a sequence just the sg transcriptional initiation in sg with the base pairing of be by of and occur in the is the at is from the sg is in for of RNA The sg mRNA1 of TBSV a for of of in the are could with this are the accumulation of sg mRNA1 and sg for TBSV and infections RNA A. A. A. sg is in the accumulation at sg mRNA1 accumulation is in the at The of in with and that the two could different within the of in of the is essential for efficient sg mRNA1 accumulation, the of this interaction is is that the base pairing interaction between and the formation of a more complex structure. the the of an is by and sequence The formation of such a could further the of RNA by of is and may be in RNA within the TBSV genome Mol. Biol. the of could the sequence just is complementary the sequence just base pairing of could further the The the for this RNA interaction be more complex and are The and small of and the (i) in the of the and (ii) could this interaction be by RNA of that the of the genome in the formation of this base in cis the could be in this we and sequence by for that could the of a on the for the a in the of most of within a in a could the of for base pairing with of the at is in the activator of sg in the (+)-strand virus red clover necrotic mosaic virus the in the of the activator in with a sequence just the sg transcriptional initiation in sg with the base pairing of be by of and occur in the is the at is from the sg is in for of RNA The sg mRNA1 of TBSV a for of of in the are could with this are the accumulation of sg mRNA1 and sg for TBSV and infections RNA A. A. A. sg is in the accumulation at sg mRNA1 accumulation is in the at The of in with and that the two could different within the of in of the is essential for efficient sg mRNA1 accumulation, the of this interaction is is that the base pairing interaction between and the formation of a more complex structure. the the of an is by and sequence The formation of such a could further the of RNA by of is and may be in RNA within the TBSV genome Mol. Biol. the of could the sequence just is complementary the sequence just base pairing of could further the The the for this RNA interaction be more complex and are of the with the and interaction is the long-distance interaction be in sg in The is for efficient sg both and with the interaction with between the (i) the base pairing just the of (ii) the long-distance (iii) the occur in the (+)-strand (iv) the some (i) the RNA (ii) the base pairing interaction is the base pairing interaction (iii) the of the base pairing interaction the initiation are different is that this that for RNA of sg the for sg may be and could be for an base pairing interaction the sequence that the potato virus X long-distance base pairing the of the genome and just the initiation of two sg mRNAs sg accumulation RNA The between the of the and the in both of is the in is that is and that the for sg mRNA1 in TBSV is 3 the of the two more and is two RNA for RNA in regulating sg accumulation in TBSV data indicate that in the (+)-strand of the genome and in the transcriptional is both long-distance occur the RNA be in an may be relevant their and could a type of both are by in sequence is by the of both sg mRNA1 and sg on sg is on the sequence of it on the of sg this it is that the the of in is for the of viral RNA specifically sg A. the on sg RNA in TBSV are consistent with their in transcriptional a Biol. RNA (i) of sg occurs of complementary (+)-strand accumulation, be are and for (+)-strand (ii) The in the (+)-strand of the be for in (−)-strand (iii) The interaction is specifically for (−)-strand sg mRNA1 accumulation, in with a role for this element in of (−)-strand data are consistent with a transcriptional further be the by TBSV for sg transcription. The interaction is the long-distance interaction be in sg in The is for efficient sg both and with the interaction with between the (i) the base pairing just the of (ii) the long-distance (iii) the occur in the (+)-strand (iv) the some (i) the RNA (ii) the base pairing interaction is the base pairing interaction (iii) the of the base pairing interaction the initiation are different is that this that for RNA of sg the for sg may be and could be for an base pairing interaction the sequence that the potato virus X long-distance base pairing the of the genome and just the initiation of two sg mRNAs sg accumulation RNA The between the of the and the in both of is the in is that is and that the for sg mRNA1 in TBSV is 3 the of the two more and is two RNA for RNA in regulating sg accumulation in TBSV data indicate that in the (+)-strand of the genome and in the transcriptional is both long-distance occur the RNA be in an may be relevant their and could a type of both are by in sequence is by the of both sg mRNA1 and sg on sg is on the sequence of it on the of sg this it is that the the of in is for the of viral RNA specifically sg A. the on sg RNA in TBSV are consistent with their in transcriptional a Biol. RNA (i) of sg occurs of complementary (+)-strand accumulation, be are and for (+)-strand (ii) The in the (+)-strand of the be for in (−)-strand (iii) The interaction is specifically for (−)-strand sg mRNA1 accumulation, in with a role for this element in of (−)-strand data are consistent with a transcriptional further be the by TBSV for sg transcription.

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