|
|
|
Regulation of NLR stability in plant immunity |
Tao WANG1, Jiaxin LI2, Qian-Hua SHEN1() |
1. State Key Laboratory of Plant Cell and Chromosome Engineering/Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China 2. Eberly College of Science, The Pennsylvania State University, University Park, PA 16802, USA |
|
|
|
Abstract: Plant nucleotide binding domain and leucine-rich repeat (NLR) receptors recognize pathogen effectors directly or indirectly and mediate innate immune responses. NLR-mediated immunity also has direct impacts on plant growth and development, as well as yield and survival. The levels of NLR proteins are therefore intricately controlled in plants to balance defense responses and other processes. In recent years, the ubiquitination-26S proteasome system and the HSP90 chaperones have emerged as having key functions in the regulation of NLR stability. The N-end rule pathway of protein degradation is also directly linked to NLR stability. Recent progress in the regulation of NLR stability and turnover is summarized here, focusing on the key components and pathways. |
Keywords
E3 ubiquitin ligase
degradation
nucleotide-binding leucine-rich repeat receptor
plant immunity
proteasome
protein stability
ubiquitination
|
最新录用日期:
在线预览日期:
发布日期: 2019-05-22
|
|
|
1 |
J LDangl, D M Horvath, B JStaskawicz. Pivoting the plant immune system from dissection to deployment. Science, 2013, 341(6147): 746–751
https://doi.org/10.1126/science.1236011
pmid: 23950531
|
2 |
CZipfel. Plant pattern-recognition receptors. Trends in Immunology, 2014, 35(7): 345–351
https://doi.org/10.1016/j.it.2014.05.004
pmid: 24946686
|
3 |
P NDodds, J P Rathjen. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews: Genetics, 2010, 11(8): 539–548
https://doi.org/10.1038/nrg2812
pmid: 20585331
|
4 |
J DJones, R EVance, J LDangl. Intracellular innate immune surveillance devices in plants and animals. Science, 2016, 354(6316): aaf6395
https://doi.org/10.1126/science.aaf6395
pmid: 27934708
|
5 |
D ECook, C H Mesarich, B PThomma. Understanding plant immunity as a surveillance system to detect invasion. Annual Review of Phytopathology, 2015, 53(1): 541–563
https://doi.org/10.1146/annurev-phyto-080614-120114
pmid: 26047564
|
6 |
KTsuda, F Katagiri. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Current Opinion in Plant Biology, 2010, 13(4): 459–465
https://doi.org/10.1016/j.pbi.2010.04.006
pmid: 20471306
|
7 |
KTsuda, AMine, GBethke, D Igarashi, C JBotanga, YTsuda, J Glazebrook, MSato, FKatagiri. Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLOS Genetics, 2013, 9(12): e1004015
https://doi.org/10.1371/journal.pgen.1004015
pmid: 24348271
|
8 |
FJacob, S Vernaldi, TMaekawa. Evolution and conservation of plant NLR functions. Frontiers in Immunology, 2013, 4: e297
https://doi.org/10.3389/fimmu.2013.00297
pmid: 24093022
|
9 |
HCui, KTsuda, J EParker. Effector-triggered immunity: from pathogen perception to robust defense. Annual Review of Phytopathology, 2015, 66(1): 487–511
https://doi.org/10.1146/annurev-arplant-050213-040012
pmid: 25494461
|
10 |
EChae, K Bomblies, S TKim, DKarelina, MZaidem, SOssowski, C Martín-Pizarro, R A ELaitinen, B ARowan, H Tenenboim, SLechner, MDemar, A Habring-Müller, CLanz, GRätsch, DWeigel. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell, 2014, 159(6): 1341–1351
https://doi.org/10.1016/j.cell.2014.10.049
pmid: 25467443
|
11 |
Y TCheng, YLi, SHuang, Y Huang, XDong, YZhang, XLi. Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(35): 14694–14699
https://doi.org/10.1073/pnas.1105685108
pmid: 21873230
|
12 |
ERodriguez, H El Ghoul, JMundy, MPetersen. Making sense of plant autoimmunity and ‘negative regulators’. FEBS Journal, 2016, 283(8): 1385–1391
https://doi.org/10.1111/febs.13613
pmid: 26640229
|
13 |
Y TCheng, XLi. Ubiquitination in NB-LRR-mediated immunity. Current Opinion in Plant Biology, 2012, 15(4): 392–399
https://doi.org/10.1016/j.pbi.2012.03.014
pmid: 22503756
|
14 |
XLi, PKapos, YZhang. NLRs in plants. Current Opinion in Immunology, 2015, 32: 114–121
https://doi.org/10.1016/j.coi.2015.01.014
pmid: 25667191
|
15 |
KShirasu. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annual Review of Plant Biology, 2009, 60(1): 139–164
https://doi.org/10.1146/annurev.arplant.59.032607.092906
pmid: 19014346
|
16 |
C MPickart, M JEddins. Ubiquitin: structures, functions, mechanisms. Biochimica et Biophysica Acta, 2004, 1695(1–3): 55–72
https://doi.org/10.1016/j.bbamcr.2004.09.019
pmid: 15571809
|
17 |
JSmalle, R D Vierstra. The ubiquitin 26S proteasome proteolytic pathway. Annual Review of Plant Biology, 2004, 55(1): 555–590
https://doi.org/10.1146/annurev.arplant.55.031903.141801
pmid: 15377232
|
18 |
R DVierstra. The ubiquitin-26S proteasome system at the nexus of plant biology. Nature Reviews: Molecular Cell Biology, 2009, 10(6): 385–397
https://doi.org/10.1038/nrm2688
pmid: 19424292
|
19 |
THoppe. Multiubiquitylation by E4 enzymes: ‘one size’ doesn’t fit all. Trends in Biochemical Sciences, 2005, 30(4): 183–187
https://doi.org/10.1016/j.tibs.2005.02.004
pmid: 15817394
|
20 |
MTrujillo. News from the PUB: plant U-box type E3 ubiquitin ligases. Journal of Experimental Botany, 2018, 69(3): 371–384
https://doi.org/10.1093/jxb/erx411
pmid: 29237060
|
21 |
EIsono, A Katsiarimpa, I KMüller, FAnzenberger, Y D Stierhof, NGeldner, JChory, C Schwechheimer. The deubiquitinating enzyme AMSH3 is required for intracellular trafficking and vacuole biogenesis in Arabidopsis thaliana. Plant Cell, 2010, 22(6): 1826–1837
https://doi.org/10.1105/tpc.110.075952
pmid: 20543027
|
22 |
AVarshavsky. The N-end rule pathway and regulation by proteolysis. Protein Science, 2011, 20(8): 1298–1345
https://doi.org/10.1002/pro.666
pmid: 21633985
|
23 |
AMogk, R Schmidt, BBukau. The N-end rule pathway for regulated proteolysis: prokaryotic and eukaryotic strategies. Trends in Cell Biology, 2007, 17(4): 165–172
https://doi.org/10.1016/j.tcb.2007.02.001
pmid: 17306546
|
24 |
D JGibbs, S CLee, NMd Isa, S Gramuglia, TFukao, G WBassel, C S Correia, FCorbineau, F LTheodoulou, J Bailey-Serres, M JHoldsworth. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 2011, 479(7373): 415–418
https://doi.org/10.1038/nature10534
pmid: 22020279
|
25 |
D JGibbs, MBailey, H MTedds, M J Holdsworth. From start to finish: amino-terminal protein modifications as degradation signals in plants. New Phytologist, 2016, 211(4): 1188–1194
https://doi.org/10.1111/nph.14105
pmid: 27439310
|
26 |
ABachmair, DFinley, AVarshavsky. In vivo half-life of a protein is a function of its amino-terminal residue. Science, 1986, 234(4773): 179–186
https://doi.org/10.1126/science.3018930
pmid: 3018930
|
27 |
MGou, ZShi, YZhu, Z Bao, GWang, JHua. The F-box protein CPR1/CPR30 negatively regulates R protein SNC1 accumulation. Plant Journal, 2012, 69(3): 411–420
https://doi.org/10.1111/j.1365-313X.2011.04799.x
pmid: 21967323
|
28 |
XLi, J DClarke, YZhang, X Dong. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Molecular Plant-Microbe Interactions, 2001, 14(10): 1131–1139
https://doi.org/10.1094/MPMI.2001.14.10.1131
pmid: 11605952
|
29 |
TKroj, E Chanclud, CMichel-Romiti, XGrand, J BMorel. Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytologist, 2016, 210(2): 618–626
https://doi.org/10.1111/nph.13869
pmid: 26848538
|
30 |
O XDong, KAo, FXu, K C M Johnson, YWu, LLi, SXia, YLiu, Y Huang, ERodriguez, XChen, SChen, YZhang, M Petersen, XLi. Individual components of paired typical NLR immune receptors are regulated by distinct E3 ligases. Nature Plants, 2018, 4(9): 699–710
https://doi.org/10.1038/s41477-018-0216-8
pmid: 30082764
|
31 |
WLi, BWang, JWu, GLu, YHu, XZhang, ZZhang, Q Zhao, QFeng, HZhang, ZWang, GWang, B Han, ZWang, BZhou. The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Molecular Plant-Microbe Interactions, 2009, 22(4): 411–420
https://doi.org/10.1094/MPMI-22-4-0411
pmid: 19271956
|
32 |
BZhou, SQu, GLiu, M Dolan, HSakai, GLu, M Bellizzi, G LWang. The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Molecular Plant-Microbe Interactions, 2006, 19(11): 1216–1228
https://doi.org/10.1094/MPMI-19-1216
pmid: 17073304
|
33 |
C HPark, G Shirsekar, MBellizzi, SChen, P Songkumarn, XXie, XShi, YNing, BZhou, P Suttiviriya, MWang, KUmemura, G LWang. The E3 ligase APIP10 connects the effector AvrPiz-t to the NLR receptor piz-t in rice. PLOS Pathogens, 2016, 12(3): e1005529
https://doi.org/10.1371/journal.ppat.1005529
pmid: 27031246
|
34 |
C HPark, SChen, GShirsekar, B Zhou, C HKhang, PSongkumarn, A JAfzal, YNing, R Wang, MBellizzi, BValent, G LWang. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell, 2012, 24(11): 4748–4762
https://doi.org/10.1105/tpc.112.105429
pmid: 23204406
|
35 |
SSeeholzer, T Tsuchimatsu, TJordan, SBieri, SPajonk, WYang, A Jahoor, K KShimizu, BKeller, P Schulze-Lefert. Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Molecular Plant-Microbe Interactions, 2010, 23(4): 497–509
https://doi.org/10.1094/MPMI-23-4-0497
pmid: 20192836
|
36 |
TWang, CChang, CGu, STang, QXie, Q H Shen. An E3 ligase affects the NLR receptor stability and immunity to Powdery Mildew. Plant Physiology, 2016, 172(4): 2504–2515
https://doi.org/10.1104/pp.16.01520
pmid: 27780896
|
37 |
Rvan Wersch, XLi, YZhang. Mighty Dwarfs: Arabidopsis autoimmune mutants and their usages in genetic dissection of plant immunity. Frontiers of Plant Science, 2016, 7: 1717
https://doi.org/10.3389/fpls.2016.01717
pmid: 27909443
|
38 |
YHuang, S Minaker, CRoth, SHuang, PHieter, VLipka, M Wiermer, XLi. An E4 ligase facilitates polyubiquitination of plant immune receptor resistance proteins in Arabidopsis. Plant Cell, 2014, 26(1): 485–496
https://doi.org/10.1105/tpc.113.119057
pmid: 24449689
|
39 |
CCopeland, V Woloshen, YHuang, XLi. AtCDC48A is involved in the turnover of an NLR immune receptor. Plant Journal, 2016, 88(2): 294–305
https://doi.org/10.1111/tpj.13251
pmid: 27340941
|
40 |
G HBaek, IKim, HRao. The Cdc48 ATPase modulates the interaction between two proteolytic factors Ufd2 and Rad23. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(33): 13558–13563
https://doi.org/10.1073/pnas.1104051108
pmid: 21807993
|
41 |
DBarthelme, J ZChen, JGrabenstatter, T ABaker, R TSauer. Architecture and assembly of the archaeal Cdc48·20S proteasome. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(17): E1687–E1694
https://doi.org/10.1073/pnas.1404823111
pmid: 24711419
|
42 |
J YChung, Y CPark, HYe, HWu. All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction. Journal of Cell Science, 2002, 115(4): 679–688
pmid: 11865024
|
43 |
PXie. TRAF molecules in cell signaling and in human diseases. Journal of Molecular Signaling, 2013, 8(1): 7
https://doi.org/10.1186/1750-2187-8-7
pmid: 23758787
|
44 |
ROelmüller, T Peškan-Berghöfer, BShahollari, ATrebicka, I Sherameti, AVarma. MATH domain proteins represent a novel protein family in Arabidopsis thaliana, and at least one member is modified in roots during the course of a plant-microbe interaction. Physiologia Plantarum, 2005, 124(2): 152–166
https://doi.org/10.1111/j.1399-3054.2005.00505.x
|
45 |
SHuang, XChen, XZhong, M Li, KAo, JHuang, XLi. Plant TRAF proteins regulate NLR immune receptor turnover. Cell Host & Microbe, 2016, 19(2): 204–215
https://doi.org/10.1016/j.chom.2016.01.005
pmid: 26867179
|
46 |
JHuang, CZhu, XLi. SCFSNIPER4 controls the turnover of two redundant TRAF proteins in plant immunity. Plant Journal, 2018, 95(3): 504–515
https://doi.org/10.1111/tpj.13965
pmid: 29770510
|
47 |
C SHwang, A Shemorry, DAuerbach, AVarshavsky. The N-end rule pathway is mediated by a complex of the RING-type Ubr1 and HECT-type Ufd4 ubiquitin ligases. Nature Cell Biology, 2010, 12(12): 1177–1185
https://doi.org/10.1038/ncb2121
pmid: 21076411
|
48 |
C SHwang, A Shemorry, AVarshavsky. N-terminal acetylation of cellular proteins creates specific degradation signals. Science, 2010, 327(5968): 973–977
https://doi.org/10.1126/science.1183147
pmid: 20110468
|
49 |
K ELee, J EHeo, J MKim, C S Hwang. N-terminal acetylation-targeted N-end rule proteolytic system: the Ac/N-end rule pathway. Molecules and Cells, 2016, 39(3): 169–178
https://doi.org/10.14348/molcells.2016.2329
pmid: 26883906
|
50 |
TArnesen, P Van Damme, BPolevoda, KHelsens, R Evjenth, NColaert, J EVarhaug, J Vandekerckhove, J RLillehaug, FSherman, K Gevaert. Proteomics analyses reveal the evolutionary conservation and divergence of N-terminal acetyltransferases from yeast and humans. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(20): 8157–8162
https://doi.org/10.1073/pnas.0901931106
pmid: 19420222
|
51 |
K KStarheim, K Gevaert, TArnesen. Protein N-terminal acetyltransferases: when the start matters. Trends in Biochemical Sciences, 2012, 37(4): 152–161
https://doi.org/10.1016/j.tibs.2012.02.003
pmid: 22405572
|
52 |
FXu, YHuang, LLi, PGannon, ELinster, M Huber, PKapos, WBienvenut, B Polevoda, TMeinnel, RHell, C Giglione, YZhang, MWirtz, SChen, XLi. Two N-terminal acetyltransferases antagonistically regulate the stability of a nod-like receptor in Arabidopsis. Plant Cell, 2015, 27(5): 1547–1562
https://doi.org/10.1105/tpc.15.00173
pmid: 25966763
|
53 |
L HPearl, C Prodromou. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annual Review of Biochemistry, 2006, 75(1): 271–294
https://doi.org/10.1146/annurev.biochem.75.103004.142738
pmid: 16756493
|
54 |
YKadota, K Shirasu. The HSP90 complex of plants. Biochimica et Biophysica Acta, 2012, 1823(3): 689–697
https://doi.org/10.1016/j.bbamcr.2011.09.016
pmid: 22001401
|
55 |
Gvan Ooijen, GMayr, M MKasiem, M Albrecht, B JCornelissen, F LTakken. Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. Journal of Experimental Botany, 2008, 59(6): 1383–1397
https://doi.org/10.1093/jxb/ern045
pmid: 18390848
|
56 |
RLu, I Malcuit, PMoffett, M TRuiz, JPeart, A JWu, J P Rathjen, ABendahmane, LDay, D C Baulcombe. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO Journal, 2003, 22(21): 5690–5699
https://doi.org/10.1093/emboj/cdg546
pmid: 14592968
|
57 |
D AHubert, P Tornero, YBelkhadir, PKrishna, A Takahashi, KShirasu, J LDangl. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO Journal, 2003, 22(21): 5679–5689
https://doi.org/10.1093/emboj/cdg547
pmid: 14592967
|
58 |
B FHolt 3rd, Y Belkhadir, J LDangl. Antagonistic control of disease resistance protein stability in the plant immune system. Science, 2005, 309(5736): 929–932
https://doi.org/10.1126/science.1109977
pmid: 15976272
|
59 |
MBotër, B Amigues, JPeart, CBreuer, YKadota, CCasais, G Moore, CKleanthous, FOchsenbein, K Shirasu, RGuerois. Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity. Plant Cell, 2007, 19(11): 3791–3804
https://doi.org/10.1105/tpc.107.050427
pmid: 18032631
|
60 |
SBieri, SMauch, Q HShen, J Peart, ADevoto, CCasais, FCeron, SSchulze, H H Steinbiss, KShirasu, PSchulze-Lefert. RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance. Plant Cell, 2004, 16(12): 3480–3495
https://doi.org/10.1105/tpc.104.026682
pmid: 15548741
|
61 |
PMestre, D C Baulcombe. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell, 2006, 18(2): 491–501
https://doi.org/10.1105/tpc.105.037234
pmid: 16387833
|
62 |
CAzevedo, A Sadanandom, KKitagawa, AFreialdenhoven, K Shirasu, PSchulze-Lefert. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science, 2002, 295(5562): 2073–2076
https://doi.org/10.1126/science.1067554
pmid: 11847307
|
63 |
YLi, SLi, DBi, Y TCheng, XLi, YZhang. SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLOS Pathogens, 2010, 6(9): e1001111
https://doi.org/10.1371/journal.ppat.1001111
pmid: 20862316
|
64 |
KKitagawa, D Skowyra, S JElledge, J WHarper, PHieter. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Molecular Cell, 1999, 4(1): 21–33
https://doi.org/10.1016/S1097-2765(00)80184-7
pmid: 10445024
|
65 |
MZhang, M Botër, KLi, YKadota, B Panaretou, CProdromou, KShirasu, L HPearl. Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes. EMBO Journal, 2008, 27(20): 2789–2798
https://doi.org/10.1038/emboj.2008.190
pmid: 18818696
|
66 |
M GCatlett, K BKaplan. Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p. Journal of Biological Chemistry, 2006, 281(44): 33739–33748
https://doi.org/10.1074/jbc.M603847200
pmid: 16945921
|
67 |
SHuang, J Monaghan, XZhong, LLin, TSun, O XDong, X Li. HSP90s are required for NLR immune receptor accumulation in Arabidopsis. Plant Journal, 2014, 79(3): 427–439
https://doi.org/10.1111/tpj.12573
pmid: 24889324
|
68 |
Sde la Fuente van Bentem, J HVossen, K J de Vries, Svan Wees, W ITameling, H LDekker, C Gde Koster, M AHaring, F LTakken, B JCornelissen. Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein. Plant Journal, 2005, 43(2): 284–298
https://doi.org/10.1111/j.1365-313X.2005.02450.x
pmid: 15998314
|
69 |
DBi, K C Johnson, ZZhu, YHuang, FChen, YZhang, X Li. Mutations in an Atypical TIR-NB-LRR-LIM resistance protein confer autoimmunity. Frontiers of Plant Science, 2011, 2: e71
https://doi.org/10.3389/fpls.2011.00071
pmid: 22639607
|
70 |
JLiu, HYang, FBao, K Ao, XZhang, YZhang, SYang. IBR5 Modulates temperature-dependent, R protein CHS3-mediated defense responses in Arabidopsis. PLOS Genetics, 2015, 11(10): e1005584
https://doi.org/10.1371/journal.pgen.1005584
pmid: 26451844
|
71 |
HYang, YShi, JLiu, L Guo, XZhang, SYang. A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant Journal, 2010, 63(2): 283–296
https://doi.org/10.1111/j.1365-313X.2010.04241.x
pmid: 20444230
|
72 |
JLee, JNam, H CPark, G Na, KMiura, J BJin, C YYoo, DBaek, D H Kim, J CJeong, DKim, S YLee, D ESalt, T Mengiste, QGong, SMa, H J Bohnert, S SKwak, R ABressan, P M Hasegawa, D JYun. Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant Journal, 2007, 49(1): 79–90
https://doi.org/10.1111/j.1365-313X.2006.02947.x
pmid: 17163880
|
73 |
MGou, QHuang, WQian, Z Zhang, ZJia, JHua. Sumoylation E3 ligase SIZ1 modulates plant immunity partly through the immune receptor gene SNC1 in Arabidopsis. Molecular Plant-Microbe Interactions, 2017, 30(4): 334–342
https://doi.org/10.1094/MPMI-02-17-0041-R
pmid: 28409535
|
74 |
S HKim, FGao, SBhattacharjee, J AAdiasor, J CNam, WGassmann. The Arabidopsis resistance-like gene SNC1 is activated by mutations in SRFR1 and contributes to resistance to the bacterial effector AvrRps4. PLOS Pathogens, 2010, 6(11): e1001172
https://doi.org/10.1371/journal.ppat.1001172
pmid: 21079790
|
75 |
K C MJohnson, JZhao, ZWu, CRoth, VLipka, MWiermer, X Li. The putative kinase substrate MUSE7 negatively impacts the accumulation of NLR proteins. Plant Journal, 2017, 89(6): 1174–1183
https://doi.org/10.1111/tpj.13454
pmid: 28004865
|
76 |
RWang, YNing, XShi, F He, CZhang, JFan, NJiang, YZhang, T Zhang, YHu, MBellizzi, G LWang. Immunity to rice blast disease by suppression of effector-triggered necrosis. Current Biology, 2016, 26(18): 2399–2411
https://doi.org/10.1016/j.cub.2016.06.072
pmid: 27641772
|
77 |
YNing, RWang, XShi, X Zhou, G LWang. A layered defense strategy mediated by rice E3 ubiquitin ligases against diverse pathogens. Molecular Plant, 2016, 9(8): 1096–1098
https://doi.org/10.1016/j.molp.2016.06.015
pmid: 27381441
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|