The RhoGAP SPIN6 Associates with SPL11 and OsRac1 and Negatively Regulates Programmed Cell Death and Innate Immunity in Rice
Rice diseases are the major threat for stable rice production and food security worldwide. Deep understanding of the disease resistance pathway in rice is essential for effective control of the diseases. Although rice contains many E3 ubiquitin ligases, the function of their substrates in immune responses is still not fully understood. We previously characterized U-box E3 ligase SPL11 in rice that is involved in the regulation of cell death, immune responses, and flowering. However, how SPL11 interacts with its substrates to control cell death and immunity is not clear. In this study, we found that the SPL11 interacts with SPIN6, ubiquitinates, and degrades the protein via the 26S proteasome pathway. Both the Spin6 RNAi and mutant plants show enhanced resistance to rice pathogens and activate defense gene expression and ROS generation. Importantly, we found that SPIN6 is the RhoGAP of the small GTPase OsRac1, which is a key component in rice immunity. Our study provides further insights into the relationship between SPIN6 and its interacting proteins SPL11 and OsRac1, and its function in the control of cell death and immunity in rice.
Vyšlo v časopise:
The RhoGAP SPIN6 Associates with SPL11 and OsRac1 and Negatively Regulates Programmed Cell Death and Innate Immunity in Rice. PLoS Pathog 11(2): e32767. doi:10.1371/journal.ppat.1004629
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004629
Souhrn
Rice diseases are the major threat for stable rice production and food security worldwide. Deep understanding of the disease resistance pathway in rice is essential for effective control of the diseases. Although rice contains many E3 ubiquitin ligases, the function of their substrates in immune responses is still not fully understood. We previously characterized U-box E3 ligase SPL11 in rice that is involved in the regulation of cell death, immune responses, and flowering. However, how SPL11 interacts with its substrates to control cell death and immunity is not clear. In this study, we found that the SPL11 interacts with SPIN6, ubiquitinates, and degrades the protein via the 26S proteasome pathway. Both the Spin6 RNAi and mutant plants show enhanced resistance to rice pathogens and activate defense gene expression and ROS generation. Importantly, we found that SPIN6 is the RhoGAP of the small GTPase OsRac1, which is a key component in rice immunity. Our study provides further insights into the relationship between SPIN6 and its interacting proteins SPL11 and OsRac1, and its function in the control of cell death and immunity in rice.
Zdroje
1. Jones JD, and Dangl J. L. (2006) The plant immune system. Nature 444: 323–329. 17108957
2. McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25: 79–82. 10664588
3. Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141: 384–390. 16760492
4. Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, et al. (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141: 404–411. 16603664
5. Marino D, Peeters N, Rivas S (2012) Ubiquitination during plant immune signaling. Plant Physiol 160: 15–27. doi: 10.1104/pp.112.199281 22689893
6. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10: 385–397. doi: 10.1038/nrm2688 19424292
7. Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, et al. (2004) Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16: 2795–2808. 15377756
8. Yin Z, Chen J, Zeng L, Goh M, Leung H, et al. (2000) Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13: 869–876. 10939258
9. Kojo K, Yaeno T, Kusumi K, Matsumura H, Fujisawa S, et al. (2006) Regulatory mechanisms of ROI generation are affected by rice spl mutations. Plant Cell Physiol 47: 1035–1044. 16816407
10. Li W, Ahn IP, Ning Y, Park CH, Zeng L, et al. (2012) The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol 159: 239–250. doi: 10.1104/pp.111.192617 22383540
11. Liu J, Li W, Ning Y, Shirsekar G, Cai Y, et al. (2012) The U-Box E3 ligase SPL11/PUB13 is a convergence point of defense and flowering signaling in plants. Plant Physiol 160: 28–37. doi: 10.1104/pp.112.199430 22659522
12. Lu D, Lin W, Gao X, Wu S, Cheng C, et al. (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332: 1439–1442. doi: 10.1126/science.1204903 21680842
13. Tcherkezian J, Lamarche-Vane N (2007) Current knowledge of the large RhoGAP family of proteins. Biol Cell 99: 67–86. 17222083
14. Jiang SY, Ramachandran S (2006) Comparative and evolutionary analysis of genes encoding small GTPases and their activating proteins in eukaryotic genomes. Physiol Genomics 24: 235–251. 16332933
15. Tameling WI, Baulcombe DC (2007) Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19: 1682–1694. 17526750
16. Tameling WI, Nooijen C, Ludwig N, Boter M, Slootweg E, et al. (2010) RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell 22: 4176–4194. doi: 10.1105/tpc.110.077461 21169509
17. Hoefle C, Huesmann C, Schultheiss H, Bornke F, Hensel G, et al. (2011) A barley ROP GTPase ACTIVATING PROTEIN associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 23: 2422–2439. doi: 10.1105/tpc.110.082131 21685259
18. Cheung MY, Zeng NY, Tong SW, Li WY, Xue Y, et al. (2008) Constitutive expression of a rice GTPase-activating protein induces defense responses. New Phytol 179: 530–545. 19086295
19. Cheung MY, Xue Y, Zhou L, Li MW, Sun SS, et al. (2010) An ancient P-loop GTPase in rice is regulated by a higher plant-specific regulatory protein. J Biol Chem 285: 37359–37369. doi: 10.1074/jbc.M110.172080 20876569
20. Kawano Y, Shimamoto K (2013) Early signaling network in rice PRR-mediated and R-mediated immunity. Curr Opin Plant Biol 16: 496–504. doi: 10.1016/j.pbi.2013.07.004 23927868
21. Kawano Y, Akamatsu A, Hayashi K, Housen Y, Okuda J, et al. (2010) Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity. Cell Host & Microbe 7: 362–375. doi: 10.1016/j.chom.2010.04.010 20478538
22. Chen LT, Hamada S, Fujiwara M, Zhu TH, Thao NP, et al. (2010) The Hop/Sti1-Hsp90 Chaperone Complex Facilitates the Maturation and Transport of a PAMP Receptor in Rice Innate Immunity. Cell Host & Microbe 7: 185–196. 25566513
23. Akamatsu A, Wong HL, Fujiwara M, Okuda J, Nishide K, et al. (2013) An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host & Microbe 13: 465–476. 25566513
24. Vega-Sanchez ME, Zeng L, Chen S, Leung H, Wang GL (2008) SPIN1, a K homology domain protein negatively regulated and ubiquitinated by the E3 ubiquitin ligase SPL11, is involved in flowering time control in rice. Plant Cell 20: 1456–1469. doi: 10.1105/tpc.108.058610 18586868
25. Park CH, Chen S, Shirsekar G, Zhou B, Khang CH, et al. (2012) 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 24: 4748–4762. doi: 10.1105/tpc.112.105429 23204406
26. Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, et al. (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22: 561–570. 10886776
27. Ding B, Bellizzi Mdel R, Ning Y, Meyers BC, Wang GL (2012) HDT701, a Histone H4 Deacetylase, Negatively Regulates Plant Innate Immunity by Modulating Histone H4 Acetylation of Defense-Related Genes in Rice. Plant Cell 24: 3783–3794. doi: 10.1105/tpc.112.101972 22968716
28. Ning Y, Jantasuriyarat C, Zhao Q, Zhang H, Chen S, et al. (2011) The SINA E3 Ligase OsDIS1 Negatively Regulates Drought Response in Rice. Plant Physiol 157: 242–255. doi: 10.1104/pp.111.180893 21719639
29. Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45: 490–495. 15111724
30. Qu S, Liu G, Zhou B, Bellizzi M, Zeng L, et al. (2006) The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics 172: 1901–1914. 16387888
31. Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, et al. (2001) Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 98: 759–764. 11149940
32. Ning Y, Xie Q, Wang GL (2011) OsDIS1-mediated stress response pathway in rice. Plant Signal Behav 6. doi: 10.4161/psb.6.12.18192 22231201
33. Waadt R, Schmidt LK, Lohse M, Hashimoto K, Bock R, et al. (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56: 505–516. doi: 10.1111/j.1365-313X.2008.03612.x 18643980
34. Liu L, Zhang Y, Tang S, Zhao Q, Zhang Z, et al. (2010) An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana. Plant J 61: 893–903. doi: 10.1111/j.1365-313X.2009.04109.x 20015064
35. Sorkin A, McClure M, Huang F, Carter R (2000) Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr Biol 10: 1395–1398. 11084343
36. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948. 17846036
37. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150–163. 15260895
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 2
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Control of Murine Cytomegalovirus Infection by γδ T Cells
- ATPaseTb2, a Unique Membrane-bound FoF1-ATPase Component, Is Essential in Bloodstream and Dyskinetoplastic Trypanosomes
- Rational Development of an Attenuated Recombinant Cyprinid Herpesvirus 3 Vaccine Using Prokaryotic Mutagenesis and In Vivo Bioluminescent Imaging
- Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection