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The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure.

Zhang H, Dong S, Wang M, Wang W, Song W, Dou X, Zheng X, Zhang Z - J. Exp. Bot. (2010)

Bottom Line: Although NbVPE silencing does not affect H(2)O(2) accumulation triggered by boehmerin, harpin, or Nep1, the HR is absent in NbVPE1a- and NbVPE1a/1b-silenced plants treated with harpin alone.These results suggest that harpin-triggered HR is VPE-dependent.The accumulation of transcripts associated with defence and cell redox is modified by VPE silencing in elicitor signalling.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture, Nanjing, 210095, China.

ABSTRACT
Elicitors/pathogen-associated molecular patterns (PAMPs) trigger the plant immune system, leading to rapid programmed cell death (hypersensitive response, HR) and stomatal closure. Previous reports have shown that the vacuolar processing enzyme (VPE), a cysteine proteinase responsible for the maturation of vacuolar proteins, has caspase-1-like activity and mediates TMV- and mycotoxin-induced cell death. The role of VPE from Nicotiana benthamiana in the response to three elicitors: bacterial harpin, fungal Nep1, and oomycete boehmerin, is described here. Single-silenced (NbVPE1a or NbVPE1b) and dual-silenced (NbVPE1a/1b) N. benthamiana plants were produced by virus-induced gene silencing. Although NbVPE silencing does not affect H(2)O(2) accumulation triggered by boehmerin, harpin, or Nep1, the HR is absent in NbVPE1a- and NbVPE1a/1b-silenced plants treated with harpin alone. However, NbVPE-silenced plants develop a normal HR after boehmerin and Nep1 treatment. These results suggest that harpin-triggered HR is VPE-dependent. Surprisingly, all gene-silenced plants show significantly impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production in guard cells. Dual-silenced plants show increased elicitor-triggered AOS production in guard cells. The accumulation of transcripts associated with defence and cell redox is modified by VPE silencing in elicitor signalling. Overall, these results indicate that VPE from N. benthamiana functions not only in elicitor-induced HR, but also in elicitor-induced stomatal closure, suggesting that VPE may be involved in elicitor-triggered immunity.

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NbVPE silencing shows insensitivity to elicitor-induced promotion of stomatal closure. Photograph of leaf epidermal peels from control and NbVPE-silenced plants were taken after 3 h of incubation in PBS (10 mM), boehmerin (50 nM), harpin (50 nM), and Nep1 (50 nM).
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fig4: NbVPE silencing shows insensitivity to elicitor-induced promotion of stomatal closure. Photograph of leaf epidermal peels from control and NbVPE-silenced plants were taken after 3 h of incubation in PBS (10 mM), boehmerin (50 nM), harpin (50 nM), and Nep1 (50 nM).

Mentions: VPE is localized in the vacuole and is involved in provoking the disintegration of vacuolar membranes, leading to hypersensitive cell death after exposure to TMV or mycotoxins (Hatsugai et al., 2006). Stomatal closure is driven by the reduction of intracellular solutes, and large amounts of cell solutes are stored in the vacuole. It has previously been reported that elicitors including boehmerin, harpin, and Nep1 can induce stomatal closure (Zhang et al., 2009), but it remains unclear whether NbVPE1a and NbVPE1b contribute to elicitor-induced stomatal closure. Stomatal responses to boehmerin, harpin, and Nep1 were observed in NbVPE-silenced leaves. Elicitors induced stomatal closure in control leaves, but closure was clearly impaired in NbVPE-silenced leaves (Fig. 4). Consequently, elicitor-induced stomatal aperture analyses were performed with NbVPE-silenced plants, and it was found that boehmerin-induced stomatal closure was significantly inhibited compared with control plants (Fig. 5A). Similarly, silenced plants showed a markedly reduced response to harpin and Nep1 (Fig. 5B, C). Compared with control PVX-infected plants, neither single- nor dual-silenced plants showed any alteration in stomata after treatment with PBS. These results suggest that NbVPE silencing compromises elicitor-induced stomatal closure.


The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure.

Zhang H, Dong S, Wang M, Wang W, Song W, Dou X, Zheng X, Zhang Z - J. Exp. Bot. (2010)

NbVPE silencing shows insensitivity to elicitor-induced promotion of stomatal closure. Photograph of leaf epidermal peels from control and NbVPE-silenced plants were taken after 3 h of incubation in PBS (10 mM), boehmerin (50 nM), harpin (50 nM), and Nep1 (50 nM).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2921209&req=5

fig4: NbVPE silencing shows insensitivity to elicitor-induced promotion of stomatal closure. Photograph of leaf epidermal peels from control and NbVPE-silenced plants were taken after 3 h of incubation in PBS (10 mM), boehmerin (50 nM), harpin (50 nM), and Nep1 (50 nM).
Mentions: VPE is localized in the vacuole and is involved in provoking the disintegration of vacuolar membranes, leading to hypersensitive cell death after exposure to TMV or mycotoxins (Hatsugai et al., 2006). Stomatal closure is driven by the reduction of intracellular solutes, and large amounts of cell solutes are stored in the vacuole. It has previously been reported that elicitors including boehmerin, harpin, and Nep1 can induce stomatal closure (Zhang et al., 2009), but it remains unclear whether NbVPE1a and NbVPE1b contribute to elicitor-induced stomatal closure. Stomatal responses to boehmerin, harpin, and Nep1 were observed in NbVPE-silenced leaves. Elicitors induced stomatal closure in control leaves, but closure was clearly impaired in NbVPE-silenced leaves (Fig. 4). Consequently, elicitor-induced stomatal aperture analyses were performed with NbVPE-silenced plants, and it was found that boehmerin-induced stomatal closure was significantly inhibited compared with control plants (Fig. 5A). Similarly, silenced plants showed a markedly reduced response to harpin and Nep1 (Fig. 5B, C). Compared with control PVX-infected plants, neither single- nor dual-silenced plants showed any alteration in stomata after treatment with PBS. These results suggest that NbVPE silencing compromises elicitor-induced stomatal closure.

Bottom Line: Although NbVPE silencing does not affect H(2)O(2) accumulation triggered by boehmerin, harpin, or Nep1, the HR is absent in NbVPE1a- and NbVPE1a/1b-silenced plants treated with harpin alone.These results suggest that harpin-triggered HR is VPE-dependent.The accumulation of transcripts associated with defence and cell redox is modified by VPE silencing in elicitor signalling.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Agriculture, Nanjing, 210095, China.

ABSTRACT
Elicitors/pathogen-associated molecular patterns (PAMPs) trigger the plant immune system, leading to rapid programmed cell death (hypersensitive response, HR) and stomatal closure. Previous reports have shown that the vacuolar processing enzyme (VPE), a cysteine proteinase responsible for the maturation of vacuolar proteins, has caspase-1-like activity and mediates TMV- and mycotoxin-induced cell death. The role of VPE from Nicotiana benthamiana in the response to three elicitors: bacterial harpin, fungal Nep1, and oomycete boehmerin, is described here. Single-silenced (NbVPE1a or NbVPE1b) and dual-silenced (NbVPE1a/1b) N. benthamiana plants were produced by virus-induced gene silencing. Although NbVPE silencing does not affect H(2)O(2) accumulation triggered by boehmerin, harpin, or Nep1, the HR is absent in NbVPE1a- and NbVPE1a/1b-silenced plants treated with harpin alone. However, NbVPE-silenced plants develop a normal HR after boehmerin and Nep1 treatment. These results suggest that harpin-triggered HR is VPE-dependent. Surprisingly, all gene-silenced plants show significantly impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production in guard cells. Dual-silenced plants show increased elicitor-triggered AOS production in guard cells. The accumulation of transcripts associated with defence and cell redox is modified by VPE silencing in elicitor signalling. Overall, these results indicate that VPE from N. benthamiana functions not only in elicitor-induced HR, but also in elicitor-induced stomatal closure, suggesting that VPE may be involved in elicitor-triggered immunity.

Show MeSH