Replicase proteins as determinants of phloem-dependent long-distance movement of tobamoviruses in tobacco

Transgenic tobacco plants expressing a gene encoding the tobacco mosaic virus (TMV) movement protein (30K) were studied using immunocytochemical techniques. The movement protein was shown to be localized within or on most of the plasmodesmata observed in the transformed plant. These results are consistent with the idea that the movement protein interacts with the plasmodesmata to facilitate the cell-to-cell spread of TMV.

Plasmodesma

Movement protein

Tobamovirus

10.1099/0022-1317-72-1-209

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Citations (145)

Replicase proteins as determinants of phloem-dependent long-distance movement of tobamoviruses in tobacco

PROTOPLASMA (1997)

C. M. Deom Shigang Quan Xian Zhi He

Movement protein

Tobamovirus

Tobacco etch virus

10.1007/bf02539800

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Citations (24)

Activation of Tm‐2² resistance is mediated by a conserved cysteine essential for tobacco mosaic virus movement

Molecular Plant Pathology (2023)

Hagit Hak Hagai Raanan Shahar Schwarz Yifat Sherman Savithramma P. Dinesh‐Kumar

Abstract The tomato Tm‐2 2 gene was considered to be one of the most durable resistance genes in agriculture, protecting against viruses of the Tobamovirus genus, such as tomato mosaic virus (ToMV) and tobacco mosaic virus (TMV). However, an emerging tobamovirus, tomato brown rugose fruit virus (ToBRFV), has overcome Tm‐2 2 , damaging tomato production worldwide. Tm‐2 2 encodes a nucleotide‐binding leucine‐rich repeat (NLR) class immune receptor that recognizes its effector, the tobamovirus movement protein (MP). Previously, we found that ToBRFV MP (MP ToBRFV ) enabled the virus to overcome Tm‐2 2 ‐mediated resistance. Yet, it was unknown how Tm‐2 2 remained durable against other tobamoviruses, such as TMV and ToMV, for over 60 years. Here, we show that a conserved cysteine (C68) in the MP of TMV (MP TMV ) plays a dual role in Tm‐2 2 activation and viral movement. Substitution of MP ToBRFV amino acid H67 with the corresponding amino acid in MP TMV (C68) activated Tm‐2 2 ‐mediated resistance. However, replacement of C68 in TMV and ToMV disabled the infectivity of both viruses. Phylogenetic and structural prediction analysis revealed that C68 is conserved among all Solanaceae‐infecting tobamoviruses except ToBRFV and localizes to a predicted jelly‐roll fold common to various MPs. Cell‐to‐cell and subcellular movement analysis showed that C68 is required for the movement of TMV by regulating the MP interaction with the endoplasmic reticulum and targeting it to plasmodesmata. The dual role of C68 in viral movement and Tm‐2 2 immune activation could explain how TMV was unable to overcome this resistance for such a long period.

Tobamovirus

Movement protein

Plasmodesma

10.1111/mpp.13318

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Citations (15)

Tm-2² resistance targets a conserved cysteine essential for tobacco mosaic virus (TMV) movement

bioRxiv (Cold Spring Harbor Laboratory) (2022)

Hagit Hak Hagai Raanan Shahar Schwarz Yifat Sherman Savithramma P. Dinesh‐Kumar

ABSTRACT The tomato Tm-2 2 gene was considered one of the most durable resistance genes in agriculture, protecting against viruses of the Tobamovirus genus, such as Tomato mosaic virus (ToMV) and Tobacco mosaic virus (TMV). However, an emerging tobamovirus, Tomato brown rugose fruit virus (ToBRFV), has overcome Tm-2 2 , damaging tomato production worldwide. Tm-2 2 encodes a nucleotide-binding leucine-rich repeat (NLR) class immune receptor that recognizes its effector, the tobamovirus movement protein (MP). Previously, we found that ToBRFV MP (MP ToBRFV ) enabled the virus to overcome Tm-2 2 - mediated resistance. Yet, it was unknown how Tm-2 2 remained durable against other tobamoviruses, such as TMV and ToMV, for over 60 years. Here, we show that the presence of a conserved cysteine (C68) in the MP of TMV (MP TMV ) is both sufficient to trigger Tm-2 2 resistance and essential for viral movement. Substitution of MP ToBRFV amino acid H67 with the corresponding amino acid in MP TMV (C68) activated Tm-2 2 -medited resistance. However, replacement of C68 in TMV and ToMV disabled the infectivity of both viruses. Phylogenetic and structural prediction analysis revealed that C68 is conserved among all Solanaceae -infecting tobamoviruses except ToBRFV, and localizes to a predicted jelly-roll fold common to various MPs. Cell-to-cell, and subcellular movement analysis showed that C68 is required for the movement of TMV, by regulating the MP interaction with the endoplasmic reticulum and targeting it to plasmodesmata. The dual role of C68 in viral movement and Tm-2 2 immune activation could explain how TMV was unable to overcome this resistance for such a long period.

Tobamovirus

Movement protein

Plasmodesma

Mosaic virus

10.1101/2022.10.06.510505

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Citations (1)

Direct functional assay for tobacco mosaic viruscell-to-cell movement protein and identification of a domain involved inincreasing plasmodesmal permeability.

Proceedings of the National Academy of Sciences (1994)

Elisabeth Waigmann William J. Lucas Vitaly Citovsky Patricia Zambryski

Plasmodesmata are cytoplasmic bridges between plant cells thought to generally allow only the passage of small molecules and metabolites. However, large structures such as plant viruses also move from cell to cell via plasmodesmata. In tobacco mosaic virus (TMV) infection a viral movement protein (TMV-MP) mediates viral spread. Here, a microinjection assay is used to monitor the dynamics of TMV-MP function directly in wild-type plants. The results indicate that TMV-MP interacts with an endogenous plant pathway increasing plasmodesmal size exclusion limit to permit passage of 20-kDa dextrans. Furthermore, TMV-MP influences plasmodesmal size exclusion limit several cells distant from the injection site, indicating either that TMV-MP itself crosses plasmodesmata or that TMV-MP induces a diffusable signal capable of dilating microchannels of plasmodesmata. The region of TMV-MP responsible for increasing plasmodesmal size exclusion limit was mapped to the carboxyl-terminal part of the 268-amino acid residue protein between amino acid residues 126 and 224.

Plasmodesma

Movement protein

Tobamovirus

Plant cell

Cowpea mosaic virus

10.1073/pnas.91.4.1433

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Citations (265)

Comparison of the Oilseed rape mosaic virus and Tobacco mosaic virus movement proteins (MP) reveals common and dissimilar MP functions for tobamovirus spread

Virology (2014)

Annette Niehl Adrien Pasquier Inmaculada Ferriol Yves Mély Manfred Heinlein

Movement protein

Plasmodesma

Tobamovirus

Mosaic virus

10.1016/j.virol.2014.03.007

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Citations (17)

Invasion of minor veins of tobacco leaves inoculated with tobacco mosaic virus mutants defective in phloem-dependent movement.

Proceedings of the National Academy of Sciences (1996)

Xin Shun Ding M. H. Shintaku S A Carter Richard S. Nelson

To fully understand vascular transport of plant viruses, the viral and host proteins, their structures and functions, and the specific vascular cells in which these factors function must be determined. We report here on the ability of various cDNA-derived coat protein (CP) mutants of tobacco mosaic virus (TMV) to invade vascular cells in minor veins of Nicotiana tabacum L. cv. Xanthi nn. The mutant viruses we studied, TMV CP-O, U1mCP15-17, and SNC015, respectively, encode a CP from a different tobamovirus (i.e., from odontoglossum ringspot virus) resulting in the formation of non-native capsids, a mutant CP that accumulates in aggregates but does not encapsidate the viral RNA, or no CP. TMV CP-O is impaired in phloem-dependent movement, whereas U1mCP15-17 and SNC015 do not accumulate by phloem-dependent movement. In developmentally-defined studies using immunocytochemical analyses we determined that all of these mutants invaded vascular parenchyma cells within minor veins in inoculated leaves. In addition, we determined that the CPs of TMV CP-O and U1mCP15-17 were present in companion (C) cells of minor veins in inoculated leaves, although more rarely than CP of wild-type virus. These results indicate that the movement of TMV into minor veins does not require the CP, and an encapsidation-competent CP is not required for, but may increase the efficiency of, movement into the conducting complex of the phloem (i.e., the C cell/sieve element complex). Also, a host factor(s) functions at or beyond the C cell/sieve element interface with other cells to allow efficient phloem-dependent accumulation of TMV CP-O.

Tobamovirus

Movement protein

Plasmodesma

Tobacco etch virus

10.1073/pnas.93.20.11155

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Citations (86)

Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability (microinjection/plasmodesmata/size exclusion limit)

Elisabeth Waigmann William J. LUCASt Vitaly Citovsky Patricia Zambryski

Plasmodesmata are cytoplasmic bridges be- tween plant cells thought to generally allow only the passage of small molecules and metabolites. However, large structures such as plant viruses also move from cell to cell via plasmodes- mata. In tobacco mosaic virus (TMV) infection a viral move- ment protein (TMV-MP) mediates viral spread. Here, a mi- croinjection assay is used to monitor the dynamics of TMV-MP function directly in wild-type plants. The results indicate that TMV-MP interacts with an endogenous plant pathway increas- ing plasmodesmal size exclusion limit to permit passage of 20-kDa dextrans. Furthermore, TMV-MP influences plas- modesmal size exclusion limit several cells distant from the inuection site, indicating either that TMV-MP itself crosses plasmodesmata or that TMV-MP induces a diffusable signal capable of dilating microchannels of plasmodesmata. The region of TMV-MP responsible for increasing plasmodesmal size exclusion limit was mapped to the carboxyl-terminal part of the 268-amino acid residue protein between amino acid residues 126 and 224.

Plasmodesma

Movement protein

Tobamovirus

Cowpea mosaic virus

Plant cell

Source

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