Abstract
BACKGROUND: The mitogen-activated protein kinase (MAPK) cascade is an evolutionarily ancient mechanism of signal transduction found in eukaryotic cells. In plants, MAPK cascades are associated with responses to various abiotic and biotic stresses such as plant pathogens. MAPK cascades function through sequential phosphorylation: MAPK kinase kinases (MAPKKKs) phosphorylate MAPK kinases (MAPKKs), and phosphorylated MAPKKs phosphorylate MAPKs. Of these three types of kinase, the MAPKKKs exhibit the most divergence in the plant genome. Their great diversity is assumed to allow MAPKKKs to regulate many specific signaling pathways in plants despite the relatively limited number of MAPKKs and MAPKs. Although some plant MAPKKKs, including the MAPKKKα of Nicotiana benthamiana (NbMAPKKKα), are known to play crucial roles in plant defense responses, the functional relationship among MAPKKK genes is poorly understood. Here, we performed a comparative functional analysis of MAPKKKs to investigate the signaling pathway leading to the defense response. RESULTS: We cloned three novel MAPKKK genes from N. benthamiana: NbMAPKKKβ, NbMAPKKKγ, and NbMAPKKKε2. Transient overexpression of full-length NbMAPKKKβ or NbMAPKKKγ or their kinase domains in N. benthamiana leaves induced hypersensitive response (HR)-like cell death associated with hydrogen peroxide production. This activity was dependent on the kinase activity of the overexpressed MAPKKK. In addition, virus-induced silencing of NbMAPKKKβ or NbMAPKKKγ expression significantly suppressed the induction of programmed cell death (PCD) by viral infection. Furthermore, in epistasis analysis of the functional relationships among NbMAPKKKβ, NbMAPKKKγ, and NbMAPKKKα (previously shown to be involved in plant defense responses) conducted by combining transient overexpression analysis and virus-induced gene silencing, silencing of NbMAPKKKα suppressed cell death induced by the overexpression of the NbMAPKKKβ kinase domain or of NbMAPKKKγ, but silencing of NbMAPKKKβ failed to suppress cell death induced by the overexpression of NbMAPKKKα or NbMAPKKKγ. Silencing of NbMAPKKKγ suppressed cell death induced by the NbMAPKKKβ kinase domain but not that induced by NbMAPKKKα. CONCLUSIONS: These results demonstrate that in addition to NbMAPKKKα, NbMAPKKKβ and NbMAPKKKγ also function as positive regulators of PCD. Furthermore, these three MAPKKKs form a linear signaling pathway leading to PCD; this pathway proceeds from NbMAPKKKβ to NbMAPKKKγ to NbMAPKKKα.
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Claims 11
Claim · model-written summary
Three new MAPKKK genes were cloned from N. benthamiana.
- Taxon
- N. benthamiana
Nicotiana benthamianae0 - Gene
- NbMAPKKKβ, NbMAPKKKγ, and NbMAPKKKε2e0
- Outcome
- three novel MAPKKK genese0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“We cloned three novel MAPKKK genes from N. benthamiana: NbMAPKKKβ, NbMAPKKKγ, and NbMAPKKKε2.”
Claim · model-written summary
Overexpressing NbMAPKKKβ induced HR-like cell death with hydrogen peroxide production.
- Taxon
- N. benthamianaNicotiana benthamianae0
- Organ / stage
- leavese0
- Treatment
- Transient overexpression of full-length NbMAPKKKβe0
- Gene
- NbMAPKKKβe0
- Outcome
- hypersensitive response (HR)-like cell death associated with hydrogen peroxide productione0
Not reportedComparatorDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Transient overexpression of full-length NbMAPKKKβ or NbMAPKKKγ or their kinase domains in N. benthamiana leaves induced hypersensitive response (HR)-like cell death associated with hydrogen peroxide production.”
Claim · model-written summary
Overexpressing NbMAPKKKγ induced HR-like cell death with hydrogen peroxide production.
- Taxon
- N. benthamianaNicotiana benthamianae0
- Organ / stage
- leavese0
- Treatment
- NbMAPKKKγe0
- Gene
- NbMAPKKKγe0
- Outcome
- hypersensitive response (HR)-like cell death associated with hydrogen peroxide productione0
Not reportedComparatorDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Transient overexpression of full-length NbMAPKKKβ or NbMAPKKKγ or their kinase domains in N. benthamiana leaves induced hypersensitive response (HR)-like cell death associated with hydrogen peroxide production.”
Claim · model-written summary
Kinase activity was required for the cell death activity of overexpressed MAPKKKs.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Outcome
- This activitye0
- Qualifier
- kinase activity of the overexpressed MAPKKKe0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“This activity was dependent on the kinase activity of the overexpressed MAPKKK.”
t0“Nicotiana benthamiana”
Claim · model-written summary
Silencing NbMAPKKKβ significantly suppressed virus-induced programmed cell death.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Treatment
- virus-induced silencing of NbMAPKKKβe0
- Gene
- NbMAPKKKβe0
- Outcome
- programmed cell death (PCD) by viral infectione0
- Direction
- suppressede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“virus-induced silencing of NbMAPKKKβ or NbMAPKKKγ expression significantly suppressed the induction of programmed cell death (PCD) by viral infection.”
t0“Nicotiana benthamiana”
Claim · model-written summary
Silencing NbMAPKKKγ significantly suppressed virus-induced programmed cell death.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Treatment
- NbMAPKKKγ expressione0
- Gene
- NbMAPKKKγe0
- Outcome
- programmed cell death (PCD) by viral infectione0
- Direction
- suppressede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“virus-induced silencing of NbMAPKKKβ or NbMAPKKKγ expression significantly suppressed the induction of programmed cell death (PCD) by viral infection.”
t0“Nicotiana benthamiana”
Claim · model-written summary
Silencing NbMAPKKKα suppressed death induced by the NbMAPKKKβ kinase domain or NbMAPKKKγ.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Treatment
- silencing of NbMAPKKKαe0
- Gene
- NbMAPKKKαe0
- Outcome
- cell death induced by the overexpression of the NbMAPKKKβ kinase domain or of NbMAPKKKγe0
- Direction
- suppressede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“silencing of NbMAPKKKα suppressed cell death induced by the overexpression of the NbMAPKKKβ kinase domain or of NbMAPKKKγ”
t0“Nicotiana benthamiana”
Claim · model-written summary
Silencing NbMAPKKKβ failed to suppress death induced by NbMAPKKKα or NbMAPKKKγ.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Treatment
- silencing of NbMAPKKKβe0
- Gene
- NbMAPKKKβe0
- Outcome
- cell death induced by the overexpression of NbMAPKKKα or NbMAPKKKγe0
- Direction
- failed to suppresse0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“silencing of NbMAPKKKβ failed to suppress cell death induced by the overexpression of NbMAPKKKα or NbMAPKKKγ.”
t0“Nicotiana benthamiana”
Claim · model-written summary
Silencing NbMAPKKKγ suppressed death induced by the NbMAPKKKβ kinase domain.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Treatment
- Silencing of NbMAPKKKγe0
- Gene
- NbMAPKKKγe0
- Outcome
- cell death induced by the NbMAPKKKβ kinase domaine0
- Direction
- suppressede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Silencing of NbMAPKKKγ suppressed cell death induced by the NbMAPKKKβ kinase domain but not that induced by NbMAPKKKα.”
t0“Nicotiana benthamiana”
Claim · model-written summary
Silencing NbMAPKKKγ did not suppress death induced by NbMAPKKKα.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Treatment
- Silencing of NbMAPKKKγe0
- Gene
- NbMAPKKKγe0
- Outcome
- that induced by NbMAPKKKαe0
- Direction
- not that inducede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Silencing of NbMAPKKKγ suppressed cell death induced by the NbMAPKKKβ kinase domain but not that induced by NbMAPKKKα.”
t0“Nicotiana benthamiana”
Claim · model-written summary
The three MAPKKKs form a linear PCD pathway ordered β, γ, α.
- Taxon
- Nicotiana benthamianaNicotiana benthamianat0
- Gene
- NbMAPKKKβ to NbMAPKKKγ to NbMAPKKKαe0
- Outcome
- linear signaling pathway leading to PCDe0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“these three MAPKKKs form a linear signaling pathway leading to PCD; this pathway proceeds from NbMAPKKKβ to NbMAPKKKγ to NbMAPKKKα.”
t0“Nicotiana benthamiana”
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