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The Arabidopsis synaptotagmin SYTA regulates the cell-to-cell movement of diverse plant viruses.

Uchiyama A, Shimada-Beltran H, Levy A, Zheng JY, Javia PA, Lazarowitz SG - Front Plant Sci (2014)

Bottom Line: Thought to be exclusive to animals, synaptotagmins have recently been characterized in Arabidopsis thaliana, in which they comprise a five gene family.We found that both TuMV and TVCV systemic infection, and the cell-to-cell trafficking of the their movement proteins, were delayed in the Arabidopsis Col-0 syta-1 knockdown mutant.In contrast, CaMV systemic infection was not inhibited in syta-1.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology and Plant-Microbe Biology, Cornell University Ithaca, NY, USA.

ABSTRACT
Synaptotagmins are a large gene family in animals that have been extensively characterized due to their role as calcium sensors to regulate synaptic vesicle exocytosis and endocytosis in neurons, and dense core vesicle exocytosis for hormone secretion from neuroendocrine cells. Thought to be exclusive to animals, synaptotagmins have recently been characterized in Arabidopsis thaliana, in which they comprise a five gene family. Using infectivity and leaf-based functional assays, we have shown that Arabidopsis SYTA regulates endocytosis and marks an endosomal vesicle recycling pathway to regulate movement protein-mediated trafficking of the Begomovirus Cabbage leaf curl virus (CaLCuV) and the Tobamovirus Tobacco mosaic virus (TMV) through plasmodesmata (Lewis and Lazarowitz, 2010). To determine whether SYTA has a central role in regulating the cell-to-cell trafficking of a wider range of diverse plant viruses, we extended our studies here to examine the role of SYTA in the cell-to-cell movement of additional plant viruses that employ different modes of movement, namely the Potyvirus Turnip mosaic virus (TuMV), the Caulimovirus Cauliflower mosaic virus (CaMV) and the Tobamovirus Turnip vein clearing virus (TVCV), which in contrast to TMV does efficiently infect Arabidopsis. We found that both TuMV and TVCV systemic infection, and the cell-to-cell trafficking of the their movement proteins, were delayed in the Arabidopsis Col-0 syta-1 knockdown mutant. In contrast, CaMV systemic infection was not inhibited in syta-1. Our studies show that SYTA is a key regulator of plant virus intercellular movement, being necessary for the ability of diverse cell-to-cell movement proteins encoded by Begomoviruses (CaLCuV MP), Tobamoviruses (TVCV and TMV 30K protein) and Potyviruses (TuMV P3N-PIPO) to alter PD and thereby mediate virus cell-to-cell spread.

No MeSH data available.


Related in: MedlinePlus

CaMV produces typical disease symptoms in syta-1 plants. CaMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation. Two typical examples of CaMV-infected plants are shown for wt Col-0 and syta-1 plants.
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Figure 4: CaMV produces typical disease symptoms in syta-1 plants. CaMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation. Two typical examples of CaMV-infected plants are shown for wt Col-0 and syta-1 plants.

Mentions: We tested CaMV infectivity on our syta-1 knockdown lines compared to wild type Col-0 plants. Based on the appearance of typical viral systemic disease symptoms and quantifying CaMV DNA levels in systemically infected leaves, CaMV infectivity levels and systemic spread on syta-1 compared to wild type Col-0 plants were not statistically different (Figures 2B, 4, Table 4). In contrast to TuMV and TVCV (Figure 1, Tables 1, 2), and to CaLCuV (Lewis and Lazarowitz, 2010), CaMV systemic disease symptoms first appeared at the same time on both syta-1 and wild type plants, and CaMV infection progressed at the same rate, attaining levels up to 100% infectivity in both syta-1 and wt Col-0 plants. Fitting with this, CaMV DNA accumulated to the same levels in systemically infected leaves from both syta-1 and wt Col-0 plants.


The Arabidopsis synaptotagmin SYTA regulates the cell-to-cell movement of diverse plant viruses.

Uchiyama A, Shimada-Beltran H, Levy A, Zheng JY, Javia PA, Lazarowitz SG - Front Plant Sci (2014)

CaMV produces typical disease symptoms in syta-1 plants. CaMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation. Two typical examples of CaMV-infected plants are shown for wt Col-0 and syta-1 plants.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4222171&req=5

Figure 4: CaMV produces typical disease symptoms in syta-1 plants. CaMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation. Two typical examples of CaMV-infected plants are shown for wt Col-0 and syta-1 plants.
Mentions: We tested CaMV infectivity on our syta-1 knockdown lines compared to wild type Col-0 plants. Based on the appearance of typical viral systemic disease symptoms and quantifying CaMV DNA levels in systemically infected leaves, CaMV infectivity levels and systemic spread on syta-1 compared to wild type Col-0 plants were not statistically different (Figures 2B, 4, Table 4). In contrast to TuMV and TVCV (Figure 1, Tables 1, 2), and to CaLCuV (Lewis and Lazarowitz, 2010), CaMV systemic disease symptoms first appeared at the same time on both syta-1 and wild type plants, and CaMV infection progressed at the same rate, attaining levels up to 100% infectivity in both syta-1 and wt Col-0 plants. Fitting with this, CaMV DNA accumulated to the same levels in systemically infected leaves from both syta-1 and wt Col-0 plants.

Bottom Line: Thought to be exclusive to animals, synaptotagmins have recently been characterized in Arabidopsis thaliana, in which they comprise a five gene family.We found that both TuMV and TVCV systemic infection, and the cell-to-cell trafficking of the their movement proteins, were delayed in the Arabidopsis Col-0 syta-1 knockdown mutant.In contrast, CaMV systemic infection was not inhibited in syta-1.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology and Plant-Microbe Biology, Cornell University Ithaca, NY, USA.

ABSTRACT
Synaptotagmins are a large gene family in animals that have been extensively characterized due to their role as calcium sensors to regulate synaptic vesicle exocytosis and endocytosis in neurons, and dense core vesicle exocytosis for hormone secretion from neuroendocrine cells. Thought to be exclusive to animals, synaptotagmins have recently been characterized in Arabidopsis thaliana, in which they comprise a five gene family. Using infectivity and leaf-based functional assays, we have shown that Arabidopsis SYTA regulates endocytosis and marks an endosomal vesicle recycling pathway to regulate movement protein-mediated trafficking of the Begomovirus Cabbage leaf curl virus (CaLCuV) and the Tobamovirus Tobacco mosaic virus (TMV) through plasmodesmata (Lewis and Lazarowitz, 2010). To determine whether SYTA has a central role in regulating the cell-to-cell trafficking of a wider range of diverse plant viruses, we extended our studies here to examine the role of SYTA in the cell-to-cell movement of additional plant viruses that employ different modes of movement, namely the Potyvirus Turnip mosaic virus (TuMV), the Caulimovirus Cauliflower mosaic virus (CaMV) and the Tobamovirus Turnip vein clearing virus (TVCV), which in contrast to TMV does efficiently infect Arabidopsis. We found that both TuMV and TVCV systemic infection, and the cell-to-cell trafficking of the their movement proteins, were delayed in the Arabidopsis Col-0 syta-1 knockdown mutant. In contrast, CaMV systemic infection was not inhibited in syta-1. Our studies show that SYTA is a key regulator of plant virus intercellular movement, being necessary for the ability of diverse cell-to-cell movement proteins encoded by Begomoviruses (CaLCuV MP), Tobamoviruses (TVCV and TMV 30K protein) and Potyviruses (TuMV P3N-PIPO) to alter PD and thereby mediate virus cell-to-cell spread.

No MeSH data available.


Related in: MedlinePlus