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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

TuMV and TVCV infections are delayed in syta-1. (A) Time course of appearance of disease symptoms on wild type (wt) Arabidopsis Col-0 plants (blue), and syta-1 mutant lines 1 (red) and 16 (green) inoculated with equal amounts of TuMV (Table 1, Trial 2). (B) Development of systemic disease as assessed by viral CP accumulation in Col-0 plants (blue) and syta-1 mutant line 1 (red) inoculated with equal amounts of TVCV (Table 2, Trial 3). (C) TuMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation (pi). (D) TVCV or mock inoculated wild type Col-0 plants at 30 da post inoculation or syta-1 plants at 14 da post inoculation (pi).
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Figure 1: TuMV and TVCV infections are delayed in syta-1. (A) Time course of appearance of disease symptoms on wild type (wt) Arabidopsis Col-0 plants (blue), and syta-1 mutant lines 1 (red) and 16 (green) inoculated with equal amounts of TuMV (Table 1, Trial 2). (B) Development of systemic disease as assessed by viral CP accumulation in Col-0 plants (blue) and syta-1 mutant line 1 (red) inoculated with equal amounts of TVCV (Table 2, Trial 3). (C) TuMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation (pi). (D) TVCV or mock inoculated wild type Col-0 plants at 30 da post inoculation or syta-1 plants at 14 da post inoculation (pi).

Mentions: As we found for CaLCuV, infection by both TuMV and TVCV progressed more slowly in syta-1 when compared to wild type Col-0 plants: the onset of systemic infection was delayed, and infectivity levels were lower in syta-1 lines (Figure 1A; Tables 1, 2). TuMV systemic disease symptoms in wild type Col-0 were first evident at 5–6 da post inoculation, and 75–100% of inoculated wild type plants became infected. In contrast, the onset of TuMV disease symptoms was delayed from 1 to 3 da in our syta-1 knockdown lines, and infectivity was decreased to ~60–85% of the levels in wild type Col-0 (50–85% of the inoculated plants became infected), although there was no apparent attenuation of viral disease symptoms (Figures 1A,C; Table 1). TVCV systemic infection, based on the accumulation of viral CP, was also first evident at 5–6 da post inoculation in wild type Col-0, with ~30–45% of inoculated wild type plants being systemically infected by 16 da post-inoculation. In contrast, the onset of TVCV systemic infection was delayed from 1 to 4 da in syta-1 plants and infectivity was decreased to only ~30–50% of the levels in wild type Col-0, based again on the accumulated levels of TVCV CP in systemic leaf extracts (11–20% of inoculated plants became systemically infected) (Figures 1B,D, 2A; Table 2). Furthermore, the levels of TVCV CP in systemic leaf extracts were, on average, lower in syta-1 vs. wt Col-0 plants on the same days post-inoculation (Figure 2A, and data not shown). As with TuMV, TVCV disease symptoms appeared to be the same in wild type Col-0 and syta-1 plants at all stages of infection (Figure 1D and data not shown). Thus, as we had found for CaLCuV, SYTA was necessary for TuMV and TVCV systemic spread and infection in Arabidopsis, consistent with SYTA being important for the cell-to-cell movement of these two +RNA viruses.


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)

TuMV and TVCV infections are delayed in syta-1. (A) Time course of appearance of disease symptoms on wild type (wt) Arabidopsis Col-0 plants (blue), and syta-1 mutant lines 1 (red) and 16 (green) inoculated with equal amounts of TuMV (Table 1, Trial 2). (B) Development of systemic disease as assessed by viral CP accumulation in Col-0 plants (blue) and syta-1 mutant line 1 (red) inoculated with equal amounts of TVCV (Table 2, Trial 3). (C) TuMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation (pi). (D) TVCV or mock inoculated wild type Col-0 plants at 30 da post inoculation or syta-1 plants at 14 da post inoculation (pi).
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Related In: Results  -  Collection

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Figure 1: TuMV and TVCV infections are delayed in syta-1. (A) Time course of appearance of disease symptoms on wild type (wt) Arabidopsis Col-0 plants (blue), and syta-1 mutant lines 1 (red) and 16 (green) inoculated with equal amounts of TuMV (Table 1, Trial 2). (B) Development of systemic disease as assessed by viral CP accumulation in Col-0 plants (blue) and syta-1 mutant line 1 (red) inoculated with equal amounts of TVCV (Table 2, Trial 3). (C) TuMV or mock inoculated wild type Col-0 or syta-1 plants at 16 da post inoculation (pi). (D) TVCV or mock inoculated wild type Col-0 plants at 30 da post inoculation or syta-1 plants at 14 da post inoculation (pi).
Mentions: As we found for CaLCuV, infection by both TuMV and TVCV progressed more slowly in syta-1 when compared to wild type Col-0 plants: the onset of systemic infection was delayed, and infectivity levels were lower in syta-1 lines (Figure 1A; Tables 1, 2). TuMV systemic disease symptoms in wild type Col-0 were first evident at 5–6 da post inoculation, and 75–100% of inoculated wild type plants became infected. In contrast, the onset of TuMV disease symptoms was delayed from 1 to 3 da in our syta-1 knockdown lines, and infectivity was decreased to ~60–85% of the levels in wild type Col-0 (50–85% of the inoculated plants became infected), although there was no apparent attenuation of viral disease symptoms (Figures 1A,C; Table 1). TVCV systemic infection, based on the accumulation of viral CP, was also first evident at 5–6 da post inoculation in wild type Col-0, with ~30–45% of inoculated wild type plants being systemically infected by 16 da post-inoculation. In contrast, the onset of TVCV systemic infection was delayed from 1 to 4 da in syta-1 plants and infectivity was decreased to only ~30–50% of the levels in wild type Col-0, based again on the accumulated levels of TVCV CP in systemic leaf extracts (11–20% of inoculated plants became systemically infected) (Figures 1B,D, 2A; Table 2). Furthermore, the levels of TVCV CP in systemic leaf extracts were, on average, lower in syta-1 vs. wt Col-0 plants on the same days post-inoculation (Figure 2A, and data not shown). As with TuMV, TVCV disease symptoms appeared to be the same in wild type Col-0 and syta-1 plants at all stages of infection (Figure 1D and data not shown). Thus, as we had found for CaLCuV, SYTA was necessary for TuMV and TVCV systemic spread and infection in Arabidopsis, consistent with SYTA being important for the cell-to-cell movement of these two +RNA viruses.

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