Phosphorylation-Dependent Differential Regulation of Plant Growth,
Cell Death, and Innate Immunity by the Regulatory Receptor-Like Kinase
BAK1
Plants rely heavily on receptor-like kinases (RLKs) for perception and
integration of external and internal stimuli. The Arabidopsis regulatory
leucine-rich repeat RLK (LRR-RLK) BAK1 is involved in steroid hormone responses,
innate immunity, and cell death control. Here, we describe the differential
regulation of three different BAK1-dependent signaling pathways by a novel
allele of BAK1, bak1-5. Innate immune signaling mediated by the
BAK1-dependent RKs FLS2 and EFR is severely compromised in
bak1-5 mutant plants. However, bak1-5
mutants are not impaired in BR signaling or cell death control. We also show
that, in contrast to the RD kinase BRI1, the non-RD kinases FLS2 and EFR have
very low kinase activity, and we show that neither was able to
trans-phosphorylate BAK1 in vitro. Furthermore, kinase activity
for all partners is completely dispensable for the ligand-induced
heteromerization of FLS2 or EFR with BAK1 in planta, revealing
another pathway specific mechanistic difference. The specific suppression of
FLS2- and EFR-dependent signaling in bak1-5 is not due to a
differential interaction of BAK1-5 with the respective ligand-binding RK but
requires BAK1-5 kinase activity. Overall our results demonstrate a
phosphorylation-dependent differential control of plant growth, innate immunity,
and cell death by the regulatory RLK BAK1, which may reveal key differences in
the molecular mechanisms underlying the regulation of ligand-binding RD and
non-RD RKs.
Vyšlo v časopise:
Phosphorylation-Dependent Differential Regulation of Plant Growth,
Cell Death, and Innate Immunity by the Regulatory Receptor-Like Kinase
BAK1. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1002046
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002046
Souhrn
Plants rely heavily on receptor-like kinases (RLKs) for perception and
integration of external and internal stimuli. The Arabidopsis regulatory
leucine-rich repeat RLK (LRR-RLK) BAK1 is involved in steroid hormone responses,
innate immunity, and cell death control. Here, we describe the differential
regulation of three different BAK1-dependent signaling pathways by a novel
allele of BAK1, bak1-5. Innate immune signaling mediated by the
BAK1-dependent RKs FLS2 and EFR is severely compromised in
bak1-5 mutant plants. However, bak1-5
mutants are not impaired in BR signaling or cell death control. We also show
that, in contrast to the RD kinase BRI1, the non-RD kinases FLS2 and EFR have
very low kinase activity, and we show that neither was able to
trans-phosphorylate BAK1 in vitro. Furthermore, kinase activity
for all partners is completely dispensable for the ligand-induced
heteromerization of FLS2 or EFR with BAK1 in planta, revealing
another pathway specific mechanistic difference. The specific suppression of
FLS2- and EFR-dependent signaling in bak1-5 is not due to a
differential interaction of BAK1-5 with the respective ligand-binding RK but
requires BAK1-5 kinase activity. Overall our results demonstrate a
phosphorylation-dependent differential control of plant growth, innate immunity,
and cell death by the regulatory RLK BAK1, which may reveal key differences in
the molecular mechanisms underlying the regulation of ligand-binding RD and
non-RD RKs.
Zdroje
1. ShiuSHKarlowskiWMPanRTzengYHMayerKF
2004
Comparative analysis of the receptor-like kinase family in
Arabidopsis and rice.
Plant Cell
16
1220
1234
2. OuyangSQLiuYFLiuPLeiGHeSJ
2010
Receptor-like kinase OsSIK1 improves drought and salt stress
tolerance in rice (Oryza sativa) plants.
Plant J
3. De SmetIVossUJurgensGBeeckmanT
2009
Receptor-like kinases shape the plant.
Nat Cell Biol
11
1166
1173
4. BollerTFelixG
2009
A renaissance of elicitors: perception of microbe-associated
molecular patterns and danger signals by pattern-recognition
receptors.
Annu Rev Plant Biol
60
379
406
5. CitriAYardenY
2006
EGF-ERBB signalling: towards the systems level.
Nat Rev Mol Cell Biol
7
505
516
6. JorissenRNWalkerFPouliotNGarrettTPWardCW
2003
Epidermal growth factor receptor: mechanisms of activation and
signalling.
Exp Cell Res
284
31
53
7. WardCWLawrenceMCStreltsovVAAdamsTEMcKernNM
2007
The insulin and EGF receptor structures: new insights into
ligand-induced receptor activation.
Trends Biochem Sci
32
129
137
8. BoseRZhangX
2009
The ErbB kinase domain: structural perspectives into kinase
activation and inhibition.
Exp Cell Res
315
649
658
9. JuraNEndresNFEngelKDeindlSDasR
2009
Mechanism for activation of the EGF receptor catalytic domain by
the juxtamembrane segment.
Cell
137
1293
1307
10. Red BrewerMChoiSHAlvaradoDMoravcevicKPozziA
2009
The juxtamembrane region of the EGF receptor functions as an
activation domain.
Mol Cell
34
641
651
11. MorandellSStasykTSkvortsovSAscherSHuberLA
2008
Quantitative proteomics and phosphoproteomics reveal novel
insights into complexity and dynamics of the EGFR signaling
network.
Proteomics
8
4383
4401
12. JohnsonLNNobleMEOwenDJ
1996
Active and inactive protein kinases: structural basis for
regulation.
Cell
85
149
158
13. NolenBTaylorSGhoshG
2004
Regulation of protein kinases; controlling activity through
activation segment conformation.
Mol Cell
15
661
675
14. ChinchillaDShanLHePde VriesSKemmerlingB
2009
One for all: the receptor-associated kinase BAK1.
Trends Plant Sci
14
535
541
15. PostelSKufnerIBeuterCMazzottaSSchwedtA
2009
The multifunctional leucine-rich repeat receptor kinase BAK1 is
implicated in Arabidopsis development and immunity.
Eur J Cell Biol
16. HechtVVielle-CalzadaJ-PHartogMVSchmidtEDLBoutilierK
2001
The Arabidopsis Somatic Embryogenesis Receptor Kinase 1 Gene Is
Expressed in Developing Ovules and Embryos and Enhances Embryogenic
Competence in Culture.
Plant Physiol
127
803
816
17. AlbrechtCRussinovaEKemmerlingBKwaaitaalMde VriesSC
2008
Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve
brassinosteroid-dependent and -independent signaling
pathways.
Plant Physiol
148
611
619
18. NamKHLiJ
2002
BRI1/BAK1, a receptor kinase pair mediating brassinosteroid
signaling.
Cell
110
203
212
19. LiJWenJLeaseKADokeJTTaxFE
2002
BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts
with BRI1 and modulates brassinosteroid signaling.
Cell
110
213
222
20. WangXGosheMBSoderblomEJPhinneyBSKucharJA
2005
Identification and functional analysis of in vivo phosphorylation
sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor
kinase.
Plant Cell
17
1685
1703
21. WangXKotaUHeKBlackburnKLiJ
2008
Sequential transphosphorylation of the BRI1/BAK1 receptor kinase
complex impacts early events in brassinosteroid signaling.
Dev Cell
15
220
235
22. JeongYJShangYKimBHKimSYSongJH
2010
BAK7 displays unequal genetic redundancy with BAK1 in
brassinosteroid signaling and early senescence in
arabidopsis.
Mol Cells
29
259
266
23. KemmerlingBSchwedtARodriguezPMazzottaSFrankM
2007
The BRI1-associated kinase 1, BAK1, has a
brassinolide-independent role in plant cell-death control.
Curr Biol
17
1116
1122
24. HeKGouXYuanTLinHAsamiT
2007
BAK1 and BKK1 regulate brassinosteroid-dependent growth and
brassinosteroid-independent cell-death pathways.
Curr Biol
17
1109
1115
25. GaoMWangXWangDXuFDingX
2009
Regulation of cell death and innate immunity by two receptor-like
kinases in Arabidopsis.
Cell Host Microbe
6
34
44
26. HeeseAHannDRGimenez-IbanezSJonesAMHeK
2007
The receptor-like kinase SERK3/BAK1 is a central regulator of
innate immunity in plants.
Proc Natl Acad Sci U S A
104
12217
12222
27. ChinchillaDZipfelCRobatzekSKemmerlingBNurnbergerT
2007
A flagellin-induced complex of the receptor FLS2 and BAK1
initiates plant defence.
Nature
448
497
500
28. KrolEMentzelTChinchillaDBollerTFelixG
2010
Perception of the Arabidopsis danger signal peptide 1 involves
the pattern recognition receptor AtPEPR1 and its close homologue
AtPEPR2.
J Biol Chem
285
13471
13479
29. ShanLHePLiJHeeseAPeckSC
2008
Bacterial effectors target the common signaling partner BAK1 to
disrupt multiple MAMP receptor-signaling complexes and impede plant
immunity.
Cell Host Microbe
4
17
27
30. SchulzeBMentzelTJehleAKMuellerKBeelerS
2010
Rapid heteromerization and phosphorylation of ligand-activated
plant transmembrane receptors and their associated kinase
BAK1.
J Biol Chem
285
9444
9451
31. XiangTZongNZouYWuYZhangJ
2008
Pseudomonas syringae effector AvrPto blocks innate immunity by
targeting receptor kinases.
Curr Biol
18
74
80
32. XiangTZongNZhangJChenJChenM
2011
BAK1 is not a target of the Pseudomonas syringae effector
AvrPto.
Mol Plant Microbe Interact
24
100
107
33. KinoshitaTCano-DelgadoASetoHHiranumaSFujiokaS
2005
Binding of brassinosteroids to the extracellular domain of plant
receptor kinase BRI1.
Nature
433
167
171
34. OhMHWangXWuXZhaoYClouseSD
2010
Autophosphorylation of Tyr-610 in the receptor kinase BAK1 plays
a role in brassinosteroid signaling and basal defense gene
expression.
Proc Natl Acad Sci U S A
107
17827
17832
35. DardickCRonaldP
2006
Plant and animal pathogen recognition receptors signal through
non-RD kinases.
PLoS Pathog
2
e2
doi:10.1371/journal.ppat.0020002
36. NekrasovVLiJBatouxMRouxMChuZH
2009
Control of the pattern-recognition receptor EFR by an ER protein
complex in plant immunity.
Embo J
28
3428
3438
37. BoudsocqMWillmannMRMcCormackMLeeHShanL
2010
Differential innate immune signalling via Ca(2+) sensor
protein kinases.
Nature
464
418
422
38. FiilBKPetersenKPetersenMMundyJ
2009
Gene regulation by MAP kinase cascades.
Curr Opin Plant Biol
12
615
621
39. HePShanLLinNCMartinGBKemmerlingB
2006
Specific bacterial suppressors of MAMP signaling upstream of
MAPKKK in Arabidopsis innate immunity.
Cell
125
563
575
40. MelottoMUnderwoodWKoczanJNomuraKHeSY
2006
Plant stomata function in innate immunity against bacterial
invasion.
Cell
126
969
980
41. ThompsonMJMeudtWJMandavaNBDutkySRLusbyWR
1982
Synthesis of brassinosteroids and relationship of structure to
plant growth-promoting effects.
Steroids
39
89
105
42. NagataNAsamiTYoshidaS
2001
Brassinazole, an inhibitor of brassinosteroid biosynthesis,
inhibits development of secondary xylem in cress plants (Lepidium
sativum).
Plant Cell Physiol
42
1006
1011
43. MussigCLissoJColl-GarciaDAltmannT
2006
Molecular analysis of brassinosteroid action.
Plant Biol (Stuttg)
8
291
296
44. GodaHSawaSAsamiTFujiokaSShimadaY
2004
Comprehensive comparison of auxin-regulated and
brassinosteroid-regulated genes in Arabidopsis.
Plant Physiol
134
1555
1573
45. WangZYNakanoTGendronJHeJChenM
2002
Nuclear-localized BZR1 mediates brassinosteroid-induced growth
and feedback suppression of brassinosteroid biosynthesis.
Dev Cell
2
505
513
46. KimTWWangZY
2010
Brassinosteroid signal transduction from receptor kinases to
transcription factors.
Annu Rev Plant Biol
61
681
704
47. XuWHuangJLiBLiJWangY
2008
Is kinase activity essential for biological functions of
BRI1?
Cell Res
18
472
478
48. MiyaAAlbertPShinyaTDesakiYIchimuraK
2007
CERK1, a LysM receptor kinase, is essential for chitin elicitor
signaling in Arabidopsis.
Proc Natl Acad Sci U S A
104
19613
19618
49. WanJZhangXCNeeceDRamonellKMCloughS
2008
A LysM receptor-like kinase plays a critical role in chitin
signaling and fungal resistance in Arabidopsis.
Plant Cell
20
471
481
50. LuDWuSGaoXZhangYShanL
2010
A receptor-like cytoplasmic kinase, BIK1, associates with a
flagellin receptor complex to initiate plant innate
immunity.
Proc Natl Acad Sci U S A
107
496
501
51. Gomez-GomezLBauerZBollerT
2001
Both the extracellular leucine-rich repeat domain and the kinase
activity of FSL2 are required for flagellin binding and signaling in
Arabidopsis.
Plant Cell
13
1155
1163
52. ZhangJLiWXiangTLiuZLalukK
2010
Receptor-like cytoplasmic kinases integrate signaling from
multiple plant immune receptors and are targeted by a Pseudomonas syringae
effector.
Cell Host Microbe
7
290
301
53. LemmonMASchlessingerJ
2010
Cell signaling by receptor tyrosine kinases.
Cell
141
1117
1134
54. BirchmeierCBirchmeierWGherardiEVande WoudeGF
2003
Met, metastasis, motility and more.
Nat Rev Mol Cell Biol
4
915
925
55. ChenXChernMCanlasPERuanDJiangC
2010
An ATPase promotes autophosphorylation of the pattern recognition
receptor XA21 and inhibits XA21-mediated immunity.
Proc Natl Acad Sci U S A
107
8029
8034
56. HeKGouXPowellRAYangHYuanT
2008
Receptor-like protein kinases, BAK1 and BKK1, regulate a
light-dependent cell-death control pathway.
Plant Signal Behav
3
813
815
57. DoddsPNRathjenJP
2010
Plant immunity: towards an integrated view of plant-pathogen
interactions.
Nat Rev Genet
11
539
548
58. KobeBHeierhorstJFeilSCParkerMWBenianGM
1996
Giant protein kinases: domain interactions and structural basis
of autoregulation.
Embo J
15
6810
6821
59. MayansOvan der VenPFWilmMMuesAYoungP
1998
Structural basis for activation of the titin kinase domain during
myofibrillogenesis.
Nature
395
863
869
60. NolenBYunCYWongCFMcCammonJAFuXD
2001
The structure of Sky1p reveals a novel mechanism for constitutive
activity.
Nat Struct Biol
8
176
183
61. MeylanETschoppJ
2005
The RIP kinases: crucial integrators of cellular
stress.
Trends Biochem Sci
30
151
159
62. BossemeyerD
1994
The glycine-rich sequence of protein kinases: a multifunctional
element.
Trends Biochem Sci
19
201
205
63. TaylorSSRadzio-AndzelmEMadhusudanChengXTen EyckL
1999
Catalytic subunit of cyclic AMP-dependent protein kinase:
structure and dynamics of the active site cleft.
Pharmacol Ther
82
133
141
64. XuWHWangYSLiuGZChenXTinjuangjunP
2006
The autophosphorylated Ser686, Thr688, and Ser689 residues in the
intracellular juxtamembrane domain of XA21 are implicated in stability
control of rice receptor-like kinase.
Plant J
45
740
751
65. ChenXChernMCanlasPEJiangCRuanD
2010
A conserved threonine residue in the juxtamembrane domain of the
XA21 pattern recognition receptor is critical for kinase autophosphorylation
and XA21-mediated immunity.
J Biol Chem
66. AsaiTTenaGPlotnikovaJWillmannMRChiuWL
2002
MAP kinase signalling cascade in Arabidopsis innate
immunity.
Nature
415
977
983
67. RobatzekSChinchillaDBollerT
2006
Ligand-induced endocytosis of the pattern recognition receptor
FLS2 in Arabidopsis.
Genes Dev
20
537
542
68. NeffMMTurkEKalishmanM
2002
Web-based primer design for single nucleotide polymorphism
analysis.
Trends Genet
18
613
615
69. NakagawaTKuroseTHinoTTanakaKKawamukaiM
2007
Development of series of gateway binary vectors, pGWBs, for
realizing efficient construction of fusion genes for plant
transformation.
J Biosci Bioeng
104
34
41
70. CloughSJBentAF
1998
Floral dip: a simplified method for Agrobacterium-mediated
transformation of Arabidopsis thaliana.
Plant J
16
735
743
71. KarlovaRBoerenSvan DongenWKwaaitaalMAkerJ
2009
Identification of in vitro phosphorylation sites in the
Arabidopsis thaliana somatic embryogenesis receptor-like
kinases.
Proteomics
9
368
379
72. BerrowNSAldertonDSainsburySNettleshipJAssenbergR
2007
A versatile ligation-independent cloning method suitable for
high-throughput expression screening applications.
Nucleic Acids Res
35
e45
73. NtoukakisVMucynTSGimenez-IbanezSChapmanHCGutierrezJR
2009
Host inhibition of a bacterial virulence effector triggers
immunity to infection.
Science 2009
324
784
787
74. EarleyKWHaagJRPontesOOpperKJuehneT
2006
Gateway-compatible vectors for plant functional genomics and
proteomics.
Plant J
45
616
629
75. Gimenez-IbanezSHannDRNtoukakisVPetutschnigELipkaV
2009
AvrPtoB targets the LysM receptor kinase CERK1 to promote
bacterial virulence on plants.
Curr Biol
19
423
429
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