Cloning of the
            <i>Arabidopsis RTM1</i>
            gene, which controls restriction of long-distance movement of tobacco etch virus

Chisholm, Stephen T.; Mahajan, Sunita K.; Whitham, Steven A.; Yamamoto, Miki; Carrington, James C.

doi:10.1073/pnas.97.1.489

Cited by 189 publications

(106 citation statements)

References 44 publications

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“…Research on plant viruses has also benefited from the use of such a versatile system. In particular, studies with viruses that naturally or experimentally infect Arabidopsis have led to the identification of host factors involved in their amplification (3,4) and movement (5,6) and in posttranscriptional gene silencing-mediated phenomena that include disease induction (7) and plant defense responses (8,9). However, no viroid has been reported to infect Arabidopsis so far.…”

mentioning

confidence: 99%

Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae

Daròs

Flores

2004

Proc. Natl. Acad. Sci. U.S.A.

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Viroids, subviral noncoding RNAs, replicate, move, and incite diseases in plants. Viroids replicate through a rolling-circle mechanism in which oligomeric RNAs of one or both polarities are cleaved and ligated into the circular monomers. Attempts to transmit viroids to Arabidopsis have failed for unknown reasons. To tackle this question, Arabidopsis was transformed with cDNAs expressing dimeric (؉) transcripts of representative species of the families Pospiviroidae and Avsunviroidae, which replicate in the nucleus and the chloroplast, respectively. Correct processing to the circular (؉) monomers was always observed, demonstrating that Arabidopsis has the appropriate RNase and RNA ligase. Northern blot hybridization also revealed the multimeric (؊) RNAs of Citrus exocortis viroid and Hop stunt viroid (HSVd) of the family Pospiviroidae, but not of Avocado sunblotch viroid of the family Avsunviroidae, showing that the first RNA-RNA transcription of the rolling-circle mechanism occurs in Arabidopsis for the two nuclear viroids and that their multimeric (؊) RNAs remain unprocessed as in typical hosts. Moreover, transgenic Arabidopsis expressing HSVd dimeric (؊) transcripts accumulated the circular (؉) monomers, although at low levels, together with the unprocessed primary transcript that served as the template for the second RNA-RNA transcription. Agroinoculation of Arabidopsis with the dimeric (؉) Citrus exocortis viroid, HSVd, and Coleus blumei viroid 1 cDNAs showed that these viroids could not move to distal plant parts, in contrast with the situation observed in their experimental hosts. Therefore, deficiencies in movement or low replication appear to be the factors limiting infectivity of some viroids in Arabidopsis.S ince Arabidopsis thaliana was adopted as the model organism for higher plants, multiple tools, resources, and experimental approaches have been developed that facilitate research with this system (1). Principal among them is the availability of the complete sequence of the Arabidopsis genome (2). Research on plant viruses has also benefited from the use of such a versatile system. In particular, studies with viruses that naturally or experimentally infect Arabidopsis have led to the identification of host factors involved in their amplification (3, 4) and movement (5, 6) and in posttranscriptional gene silencing-mediated phenomena that include disease induction (7) and plant defense responses (8, 9). However, no viroid has been reported to infect Arabidopsis so far.Viroids are small, noncoding circular RNAs of 246-401 nucleotides able to replicate autonomously in certain plants (see refs. 10-12 for reviews). Despite this minimal genome, viroids, in addition to their replication, are able to direct their intracellular, intercellular, and long-distance movement (13-15) and to activate host defense mechanisms (16-18) that in some cases are insufficient to block the induction of pathogenic effects. For these functions, viroids need to interact with multiple host factors, the identification of which wou...

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mentioning

confidence: 99%

Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae

Daròs

Flores

2004

Proc. Natl. Acad. Sci. U.S.A.

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“…The similarities of RTM1 and RTM2 to lectin-like (Chisholm et al, 2000) and small HSP-like proteins, respectively, suggest that these proteins provide structural rather than catalytic roles. Several models that incorporate structural roles for RTM1 and RTM2 in TEV-specific restriction are currently viable.…”

Section: Rtm2mentioning

confidence: 99%

“…Taken together, these data suggest either that a heat-inducible chaperone role for RTM2 was lost through evolutionary processes or that RTM2 is derived from a small HSP-like progenitor that lacked such temperature-related functions. By analogy with other HSP-related proteins that are expressed at normal temperatures, perhaps RTM2 is most appropriately referred to as a small heat shock cognate protein.The similarities of RTM1 and RTM2 to lectin-like (Chisholm et al, 2000) and small HSP-like proteins, respectively, suggest that these proteins provide structural rather than catalytic roles. Several models that incorporate structural roles for RTM1 and RTM2 in TEV-specific restriction are currently viable.…”

mentioning

confidence: 99%

“…The restriction could also be the result of recognition of TEV, followed by signaling to induce a TEV-restrictive state in phloem or in systemic tissue. Recently, the RTM1 gene was isolated and shown to encode a lectin-like protein with similarity to several proteins that have diverse roles in insect and pathogen defense (Chisholm et al, 2000). In this article, the specificity of the restriction system was investigated through a series of coinoculation experiments, and the RTM2 gene was isolated by a map-based cloning strategy.…”

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confidence: 99%

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Arabidopsis RTM2 Gene Is Necessary for Specific Restriction of Tobacco Etch Virus and Encodes an Unusual Small Heat Shock-Like Protein

Whitham¹,

Anderberg²,

Chisholm³

et al. 2000

The Plant Cell

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Arabidopsis plants have a system to specifically restrict the long-distance movement of tobacco etch potyvirus (TEV) without involving either hypersensitive cell death or systemic acquired resistance. At least two dominant genes, RTM1 and RTM2 , are necessary for this restriction. Through a series of coinfection experiments with heterologous viruses, the RTM1/RTM2-mediated restriction was shown to be highly specific for TEV. The RTM2 gene was isolated by a mapbased cloning strategy. Isolation of RTM2 was confirmed by transgenic complementation and sequence analysis of wild-type and mutant alleles. The RTM2 gene product is a multidomain protein containing an N-terminal region with high similarity to plant small heat shock proteins (HSPs). Phylogenetic analysis revealed that the RTM2 small HSP-like domain is evolutionarily distinct from each of the five known classes of plant small HSPs. Unlike most other plant genes encoding small HSPs, expression of the RTM2 gene was not induced by high temperature and did not contribute to thermotolerance of seedlings. The RTM2 gene product was also shown to contain a large C-terminal region with multiple repeating sequences. INTRODUCTIONSystemic infection of plants by viruses generally requires genome replication in individual cells, cell-to-cell movement through plasmodesmata, and long-distance movement through the phloem Baker et al., 1997). A block at any of these steps, either by active defense responses or by incompatible combinations of viral and host factors, can lead to resistance. Several types of active resistance responses to viruses are known (Baker et al., 1997;Carrington and Whitham, 1998). Dominant or semidominant resistance ( R ) genes that trigger hypersensitive cell death or extreme resistance at initial infection sites, occurring most often in a strain-specific or "gene-for-gene" manner, are well known. The tobacco N gene and the potato Rx gene, which condition resistance against tobacco mosaic virus and potato virus X strains, respectively, belong to the nucleotide binding site, leucine-rich repeat (NBS-LRR) class of R genes (Whitham et al., 1994;Bendahmane et al., 1999). Whereas N confers a hypersensitive response concomitant with localized cell-to-cell movement in inoculated leaves, Rx confers an extreme resistance in initially infected cells (Bendahmane et al., 1995).A second type of active resistance involves gene-silencing-like mechanisms. Virus-induced silencing is adaptive, meaning that a naive host can recognize viral nucleic acids and customize a sequence-specific response (Baulcombe, 1999;Grant, 1999). Thus, virus-induced silencing can limit virus accumulation, promote recovery (in some cases) from a systemic infection, and confer resistance to secondary infections with the same or homologous viruses (Ratcliff et al., 1997;Al-Kaff et al., 1998;Ratcliff et al., 1999). In contrast to resistance triggered by NBS-LRR-type R genes, resistance through silencing appears not to depend on a gene-for-gene recognition event. Passive resistance has been sugge...

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“…The systemic spread of tobacco etch virus is inhibited in some ecotypes of Arabidopsis thaliana without elicitation of an HR (24); the RTM1 and RTM2 genes are required for this resistance. Positional cloning revealed that these genes encode a lectin-like protein (25) and a small heat-shock-like protein (26), respectively. Although the mechanisms of resistance are not well understood, one possibility is that the RTM system inhibits viral movement functions.…”

Section: Tm-1 Binds To Tomv Replication Proteins To Inhibit Their Funmentioning

confidence: 99%

An inhibitor of viral RNA replication is encoded by a plant resistance gene

Ishibashi

Masuda

Naito

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

130

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The tomato Tm-1 gene confers resistance to tomato mosaic virus (ToMV). Here, we report that the extracts of Tm-1 tomato cells (GCR237) have properties that inhibit the in vitro RNA replication of WT ToMV more strongly than that of the Tm-1-resistancebreaking mutant of ToMV, LT1. We purified this inhibitory activity and identified a polypeptide of Ϸ80 kDa (p80 GCR237 ) using LCtandem MS. The amino acid sequence of p80 GCR237 had no similarity to any characterized proteins. The p80 GCR237 gene cosegregated with Tm-1; transgenic expression of p80 GCR237 conferred resistance to ToMV within tomato plants; and the knockdown of p80 GCR237 sensitized Tm-1 tomato plants to ToMV, indicating that Tm-1 encodes p80 GCR237 itself. We further show that in vitro-synthesized Tm-1 (p80 GCR237 ) protein binds to the replication proteins of WT ToMV and inhibits their function at a step before, but not after, the viral replication complex is formed on the membrane surfaces. Such binding was not observed for the replication proteins of LT1. These results suggest that Tm-1 (p80 GCR237 ) inhibits the replication of WT ToMV RNA through binding to the replication proteins.Tm-1 ͉ Tomato mosaic virus ͉ inhibitory interaction

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Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus

Cited by 189 publications

References 44 publications

Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae

Arabidopsis thaliana has the enzymatic machinery for replicating representative viroid species of the family Pospiviroidae

Arabidopsis RTM2 Gene Is Necessary for Specific Restriction of Tobacco Etch Virus and Encodes an Unusual Small Heat Shock-Like Protein

An inhibitor of viral RNA replication is encoded by a plant resistance gene

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