Temperature Modulates Plant Defense Responses through NB-LRR Proteins
An elevated growth temperature often inhibits plant defense responses and renders plants more susceptible to pathogens. However, the molecular mechanisms underlying this modulation are unknown. To genetically dissect this regulation, we isolated mutants that retain disease resistance at a higher growth temperature in Arabidopsis. One such heat-stable mutant results from a point mutation in SNC1, a NB-LRR encoding gene similar to disease resistance (R) genes. Similar mutations introduced into a tobacco R gene, N, confer defense responses at elevated temperature. Thus R genes or R-like genes involved in recognition of pathogen effectors are likely the causal temperature-sensitive component in defense responses. This is further supported by snc1 intragenic suppressors that regained temperature sensitivity in defense responses. In addition, the SNC1 and N proteins had a reduction of nuclear accumulation at elevated temperature, which likely contributes to the inhibition of defense responses. These findings identify a plant temperature sensitive component in disease resistance and provide a potential means to generate plants adapting to a broader temperature range.
Vyšlo v časopise:
Temperature Modulates Plant Defense Responses through NB-LRR Proteins. PLoS Pathog 6(4): e32767. doi:10.1371/journal.ppat.1000844
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000844
Souhrn
An elevated growth temperature often inhibits plant defense responses and renders plants more susceptible to pathogens. However, the molecular mechanisms underlying this modulation are unknown. To genetically dissect this regulation, we isolated mutants that retain disease resistance at a higher growth temperature in Arabidopsis. One such heat-stable mutant results from a point mutation in SNC1, a NB-LRR encoding gene similar to disease resistance (R) genes. Similar mutations introduced into a tobacco R gene, N, confer defense responses at elevated temperature. Thus R genes or R-like genes involved in recognition of pathogen effectors are likely the causal temperature-sensitive component in defense responses. This is further supported by snc1 intragenic suppressors that regained temperature sensitivity in defense responses. In addition, the SNC1 and N proteins had a reduction of nuclear accumulation at elevated temperature, which likely contributes to the inhibition of defense responses. These findings identify a plant temperature sensitive component in disease resistance and provide a potential means to generate plants adapting to a broader temperature range.
Zdroje
1. LongSP
WoodwardFI
1988 Plants and temperature; Long SP, Woodward FI, editors. Cambridge, England Society for Experimental Biology
2. PenfieldS
2008 Temperature perception and signal transduction in plants. New Phytol 179 615 628
3. GarrettKA
DendySP
FrankEE
RouseMN
TraversSE
2006 Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44 489 509
4. DropkinV
1969 The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59 1632 1637
5. SzittyaG
SilhavyD
MolnarA
HaveldaZ
LovasA
2003 Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. Embo J 22 633 640
6. WangY
BaoZ
ZhuY
HuaJ
2009 Analysis of temperature modulation of plant defense against biotrophic microbes. Mol Plant Microbe Interact 22 498 506
7. WhithamS
McCormickS
BakerB
1996 The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc Natl Acad Sci U S A 93 8776 8781
8. HwangCF
BhaktaAV
TruesdellGM
PudloWM
WilliamsonVM
2000 Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12 1319 1329
9. XiaoS
BrownS
PatrickE
BrearleyC
TurnerJG
2003 Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15 33 45
10. de JongCF
TakkenFL
CaiX
de WitPJ
JoostenMH
2002 Attenuation of Cf-mediated defense responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Mol Plant Microbe Interact 15 1040 1049
11. YangS
HuaJ
2004 A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 16 1060 1071
12. ZhangY
GoritschnigS
DongX
LiX
2003 A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15 2636 2646
13. BombliesK
LempeJ
EppleP
WarthmannN
LanzC
2007 Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol 5 e236 doi:10.1371/journal.pbio.0050236
14. LarkindaleJ
HallJD
KnightMR
VierlingE
2005 Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138 882 897
15. ClarkeSM
MurLA
WoodJE
ScottIM
2004 Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38 432 447
16. UknesS
Mauch-ManiB
MoyerM
PotterS
WilliamsS
1992 Acquired resistance in Arabidopsis. Plant Cell 4 645 656
17. LawtonK
WeymannK
FriedrichL
VernooijB
UknesS
1995 Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 8 863 870
18. JirageD
TootleTL
ReuberTL
FrostLN
FeysBJ
1999 Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci U S A 96 13583 13588
19. LiY
YangS
YangH
HuaJ
2007 The TIR-NB-LRR gene SNC1 is regulated at the transcript level by multiple factors. Mol Plant Microbe Interact 20 1449 1456
20. RairdanGJ
MoffettP
2006 Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18 2082 2093
21. BieriS
MauchS
ShenQH
PeartJ
DevotoA
2004 RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance. Plant Cell 16 3480 3495
22. WenW
MeinkothJL
TsienRY
TaylorSS
1995 Identification of a signal for rapid export of proteins from the nucleus. Cell 82 463 473
23. ZhangY
LiX
2005 A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1. Plant Cell 17 1306 1316
24. PalmaK
ZhangY
LiX
2005 An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Curr Biol 15 1129 1135
25. WhithamS
Dinesh-KumarSP
ChoiD
HehlR
CorrC
1994 The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78 1101 1115
26. MestreP
BaulcombeDC
2006 Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18 491 501
27. Burch-SmithTM
SchiffM
CaplanJL
TsaoJ
CzymmekK
2007 A Novel Role for the TIR Domain in Association with Pathogen-Derived Elicitors. PLoS Biol 5 e68 doi:10.1371/journal.pbio.0050068
28. YangM
WardzalaE
JohalGS
GrayJ
2004 The wound-inducible Lls1 gene from maize is an orthologue of the Arabidopsis Acd1 gene, and the LLS1 protein is present in non-photosynthetic tissues. Plant Mol Biol 54 175 191
29. LiY
PenningtonBO
HuaJ
2009 Multiple R-like genes are negatively regulated by BON1 and BON3 in arabidopsis. Mol Plant Microbe Interact 22 840 848
30. JablonskaB
AmmirajuJS
BhattaraiKK
MantelinS
Martinez de IlarduyaO
2007 The Mi-9 gene from Solanum arcanum conferring heat-stable resistance to root-knot nematodes is a homolog of Mi-1. Plant Physiol 143 1044 1054
31. RathjenJP
MoffettP
2003 Early signal transduction events in specific plant disease resistance. Curr Opin Plant Biol 6 300 306
32. TakkenFL
AlbrechtM
TamelingWI
2006 Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9 383 390
33. MerkleT
2003 Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling. Curr Genet 44 231 260
34. MeierI
2005 Nucleocytoplasmic trafficking in plant cells. Int Rev Cytol 244 95 135
35. XuXM
MeierI
2008 The nuclear pore comes to the fore. Trends Plant Sci 13 20 27
36. ChengYT
GermainH
WiermerM
BiD
XuF
2009 Nuclear Pore Complex Component MOS7/Nup88 Is Required for Innate Immunity and Nuclear Accumulation of Defense Regulators in Arabidopsis. Plant Cell
37. ScharfKD
HeiderH
HohfeldI
LyckR
SchmidtE
1998 The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol Cell Biol 18 2240 2251
38. IshitaniM
XiongL
LeeH
StevensonB
ZhuJK
1998 HOS1, a genetic locus involved in cold-responsive gene expression in arabidopsis. Plant Cell 10 1151 1161
39. EvansN
BaierlA
SemenovMA
GladdersP
FittBD
2008 Range and severity of a plant disease increased by global warming. J R Soc Interface 5 525 531
40. LukowitzW
GillmorCS
ScheibleWR
2000 Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol 123 795 805
41. TzfiraT
TianGW
LacroixB
VyasS
LiJ
2005 pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol Biol 57 503 516
42. CloughSJ
BentAF
1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743
43. ZhaiZ
Sooksa-nguanT
VatamaniukOK
2009 Establishing RNA interference as a reverse-genetic approach for gene functional analysis in protoplasts. Plant Physiol 149 642 652
44. SambrookJ
FritschEF
ManiatisT
1989 Molecular Cloning, a Laboratory Manual. Cold Spring Harbor Cold Spring Harbor Laboratory Press
45. YangH
YangS
LiY
HuaJ
2007 The Arabidopsis BAP1 and BAP2 genes are general inhibitors of programmed cell death. Plant Physiol 145 135 146
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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