ESCRT-I Mediates FLS2 Endosomal Sorting and Plant Immunity


The plant immune receptor FLAGELLIN SENSING 2 (FLS2) is present at the plasma membrane and is internalized following activation of its ligand flagellin (flg22). We show that ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT (ESCRT)-I subunits play roles in FLS2 endocytosis in Arabidopsis. VPS37-1 co-localizes with FLS2 at endosomes and immunoprecipitates with the receptor upon flg22 elicitation. Vps37-1 mutants are reduced in flg22-induced FLS2 endosomes but not in endosomes labeled by Rab5 GTPases suggesting a defect in FLS2 trafficking rather than formation of endosomes. FLS2 localizes to the lumen of multivesicular bodies, but this is altered in vps37-1 mutants indicating compromised endosomal sorting of FLS2 by ESCRT-I loss-of-function. VPS37-1 and VPS28-2 are critical for immunity against bacterial infection through a role in stomatal closure. Our findings identify that VPS37-1, and likewise VPS28-2, regulate late FLS2 endosomal sorting and reveals that ESCRT-I is critical for flg22-activated stomatal defenses involved in plant immunity.


Vyšlo v časopise: ESCRT-I Mediates FLS2 Endosomal Sorting and Plant Immunity. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004035
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004035

Souhrn

The plant immune receptor FLAGELLIN SENSING 2 (FLS2) is present at the plasma membrane and is internalized following activation of its ligand flagellin (flg22). We show that ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT (ESCRT)-I subunits play roles in FLS2 endocytosis in Arabidopsis. VPS37-1 co-localizes with FLS2 at endosomes and immunoprecipitates with the receptor upon flg22 elicitation. Vps37-1 mutants are reduced in flg22-induced FLS2 endosomes but not in endosomes labeled by Rab5 GTPases suggesting a defect in FLS2 trafficking rather than formation of endosomes. FLS2 localizes to the lumen of multivesicular bodies, but this is altered in vps37-1 mutants indicating compromised endosomal sorting of FLS2 by ESCRT-I loss-of-function. VPS37-1 and VPS28-2 are critical for immunity against bacterial infection through a role in stomatal closure. Our findings identify that VPS37-1, and likewise VPS28-2, regulate late FLS2 endosomal sorting and reveals that ESCRT-I is critical for flg22-activated stomatal defenses involved in plant immunity.


Zdroje

1. BollerT, FelixG (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.

2. ChinchillaD, ZipfelC, RobatzekS, KemmerlingB, NurnbergerT, et al. (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497–500.

3. BeckM, ZhouJ, FaulknerC, MacLeanD, RobatzekS (2012) Spatio-Temporal Cellular Dynamics of the Arabidopsis Flagellin Receptor Reveal Activation Status-Dependent Endosomal Sorting. Plant Cell 24: 4205–4219.

4. ChoiS, TamakiT, EbineK, UemuraT, UedaT, et al. (2013) RABA Members Act in Distinct Steps of Subcellular Trafficking of the FLAGELLIN SENSING2 Receptor. Plant Cell 25: 1174–1187.

5. BarberonM, ZelaznyE, RobertS, ConejeroG, CurieC, et al. (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108: E450–458.

6. KasaiK, TakanoJ, MiwaK, ToyodaA, FujiwaraT (2011) High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J Biol Chem 286: 6175–6183.

7. MukhopadhyayD, RiezmanH (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315: 201–205.

8. ScheuringD, ViottiC, KrugerF, KunzlF, SturmS, et al. (2011) Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23: 3463–3481.

9. SpitzerC, ReyesFC, BuonoR, SliwinskiMK, HaasTJ, et al. (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21: 749–766.

10. ViottiC, BubeckJ, StierhofYD, KrebsM, LanghansM, et al. (2010) Endocytic and Secretory Traffic in Arabidopsis Merge in the Trans-Golgi Network/Early Endosome, an Independent and Highly Dynamic Organelle. Plant Cell 22: 1344–1357.

11. LuD, LinW, GaoX, WuS, ChengC, et al. (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332: 1439–1442.

12. RobatzekS, ChinchillaD, BollerT (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20: 537–542.

13. RaiborgC, StenmarkH (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458: 445–452.

14. LeungKF, DacksJB, FieldMC (2008) Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9: 1698–1716.

15. ReyesFC, BuonoR, OteguiMS (2011) Plant endosomal trafficking pathways. Curr Opin Plant Biol 14: 666–673.

16. RichardsonLGL, MullenRT (2011) Meta-analysis of the expression profiles of the Arabidopsis ESCRT machinery. Plant Signal Behav 6: 1897–1903.

17. RichardsonLG, HowardAS, KhuuN, GiddaSK, McCartneyA, et al. (2011) Protein-Protein Interaction Network and Subcellular Localization of the Arabidopsis Thaliana ESCRT Machinery. Front Plant Sci 2: 20.

18. ShahriariM, RichterK, KeshavaiahC, SabovljevicA, HuelskampM, et al. (2011) The Arabidopsis ESCRT protein-protein interaction network. Plant Mol Biol 76: 85–96.

19. SpitzerC, SchellmannS, SabovljevicA, ShahriariM, KeshavaiahC, et al. (2006) The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133: 4679–4689.

20. WinterV, HauserMT (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci 11: 115–123.

21. HaasTJ, SliwinskiMK, MartinezDE, PreussM, EbineK, et al. (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19: 1295–1312.

22. HerberthS, ShahriariM, BruderekM, HessnerF, MullerB, et al. (2012) Artificial ubiquitylation is sufficient for sorting of a plasma membrane ATPase to the vacuolar lumen of Arabidopsis cells. Planta 236: 63–77.

23. BottanelliF, GershlickDC, DeneckeJ (2012) Evidence for sequential action of Rab5 and Rab7 GTPases in prevacuolar organelle partitioning. Traffic 13: 338–354.

24. CaiY, ZhuangX, WangJ, WangH, LamSK, et al. (2012) Vacuolar Degradation of Two Integral Plasma Membrane Proteins, AtLRR84A and OsSCAMP1, Is Cargo Ubiquitination-Independent and Prevacuolar Compartment-Mediated in Plant Cells. Traffic 13: 1023–1040.

25. JiaT, GaoC, CuiY, WangJ, DingY, et al. (2013) ARA7(Q69L) expression in transgenic Arabidopsis cells induces the formation of enlarged multivesicular bodies. J Exp Bot 64: 2817–2829.

26. WangJ, CaiY, MiaoY, LamSK, JiangL (2009) Wortmannin induces homotypic fusion of plant prevacuolar compartments. J Exp Bot 60: 3075–3083.

27. ZipfelC, RobatzekS, NavarroL, OakeleyEJ, JonesJD, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767.

28. MelottoM, UnderwoodW, KoczanJ, NomuraK, HeSY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969–980.

29. KimTH, BohmerM, HuH, NishimuraN, SchroederJI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61: 561–591.

30. SchroederJI, HagiwaraS (1990) Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci USA 87: 9305–9309.

31. MersmannS, BourdaisG, RietzS, RobatzekS (2010) Ethylene Signaling Regulates Accumulation of the FLS2 Receptor and Is Required for the Oxidative Burst Contributing to Plant Immunity. Plant Physiol 154: 391–400.

32. MontilletJL, LeonhardtN, MondyS, TranchimandS, RumeauD, et al. (2013) An Abscisic Acid-Independent Oxylipin Pathway Controls Stomatal Closure and Immune Defense in Arabidopsis. PLoS Biol 11: e1001513.

33. ApostolakosP, LivanosP, NikolakopoulouTL, GalatisB (2010) Callose implication in stomatal opening and closure in the fern Asplenium nidus. New Phytol 186: 623–635.

34. DjeddiA, MicheletX, CulettoE, AlbertiA, BaroisN, et al. (2012) Induction of autophagy in ESCRT mutants is an adaptive response for cell survival in C. elegans. J Cell Sci 125: 685–694.

35. HuangHR, J ChenZ, KunesS, ChangGD, ManiatisT (2010) Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc Natl Acad Sci USA 107(18): 8322–8327.

36. McGettrickAF, O'NeillLAJ (2010) Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr Opin Immunol 22: 20–27.

37. HusebyeH, HalaasO, StenmarkH, TunheimG, SandangerO, et al. (2006) Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J 25: 683–692.

38. KatsiarimpaA, AnzenbergerF, SchlagerN, NeubertS, HauserMT, et al. (2011) The Arabidopsis Deubiquitinating Enzyme AMSH3 Interacts with ESCRT-III Subunits and Regulates Their Localization. Plant Cell 23: 3026–3040.

39. LeitnerJ, RetzerK, KorbeiB, LuschnigC (2012) Dynamics in PIN2 auxin carrier ubiquitylation in gravity-responding Arabidopsis roots. Plant Signal Behav 7: 1271–1273.

40. SalomonS, RobatzekS (2006) Induced Endocytosis of the Receptor Kinase FLS2. Plant Signal Behav 1: 293–295.

41. GeldnerN, HymanDL, WangX, SchumacherK, ChoryJ (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21: 1598–1602.

42. IraniNG, Di RubboS, MylleE, Van den BeginJ, Schneider-PizonJ, et al. (2012) Fluorescent castasterone reveals BRI1 signaling from the plasma membrane. Nat Chem Biol 8: 583–589.

43. BrankatschkB, WichertSP, JohnsonSD, SchaadO, RossnerMJ, et al. (2012) Regulation of the EGF transcriptional response by endocytic sorting. Sci Signal 5: ra21.

44. SousaLP, LaxI, ShenHY, FergusonSM, De CamilliP, et al. (2012) Suppression of EGFR endocytosis by dynamin depletion reveals that EGFR signaling occurs primarily at the plasma membrane. Proc Natl Acad Sci USA 109: 4419–4424.

45. BacheKG, SlagsvoldT, CabezasA, RosendalKR, RaiborgC, et al. (2004) The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol Biol Cell 15: 4337–4346.

46. ShiH, ShenQJ, QiYP, YanHJ, NieHZ, et al. (2013) BR-SIGNALING KINASE1 Physically Associates with FLAGELLIN SENSING2 and Regulates Plant Innate Immunity in Arabidopsis. Plant Cell 25: 1143–1157.

47. SegonzacC, FeikeD, Gimenez-IbanezS, HannDR, ZipfelC, et al. (2011) Hierarchy and roles of PAMP-induced responses in Nicotiana benthamiana. Plant Physiol 156 (2) 687–99.

48. SawinskiK, MersmannS, RobatzekS, BöhmerM (2013) Guarding the Green: Pathways to Stomatal Immunity. Mol Plant Microbe Interact 26: 626–632.

49. SutterJU, SiebenC, HartelA, EisenachC, ThielG, et al. (2007) Abscisic Acid Triggers the Endocytosis of the Arabidopsis KAT1 K+ Channel and Its Recycling to the Plasma Membrane. Curr Biol 17: 1396–1402.

50. LuY-J, SchornackS, SpallekT, GeldnerN, ChoryJ, et al. (2012) Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell Microbiol 14: 682–697.

51. NakagawaT, KuroseT, HinoT, TanakaK, KawamukaiM, et al. (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.

52. SalomonS, GrunewaldD, StüberK, SchaafS, MacLeanD, et al. (2010) High-Throughput Confocal Imaging of Intact Live Tissue Enables Quantification of Membrane Trafficking in Arabidopsis. Plant Physiol 154: 1096–1104.

53. GöhreV, SpallekT, HäwekerH, MersmannS, MentzelT, et al. (2008) Plant Pattern-Recognition Receptor FLS2 Is Directed for Degradation by the Bacterial Ubiquitin Ligase AvrPtoB. Curr Biol 18: 1824–1832.

54. RouxM, SchwessingerB, AlbrechtC, ChinchillaD, JonesA, et al. (2011) The Arabidopsis Leucine-Rich Repeat Receptor–Like Kinases BAK1/SERK3 and BKK1/SERK4 Are Required for Innate Immunity to Hemibiotrophic and Biotrophic Pathogens. Plant Cell 23: 2440–2455.

55. LuX, TintorN, MentzelT, KombrinkE, BollerT, et al. (2009) Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc Natl Acad Sci USA 106: 22522–22527.

56. ZhouJ, SpallekT, FaulknerC, RobatzekS (2012) CalloseMeasurer: a novel software solution to measure callose deposition and recognise spreading callose patterns. Plant Methods 8: 49.

57. AlbrechtC, BoutrotF, SegonzacC, SchwessingerB, Gimenez-IbanezS, et al. (2012) Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci USA 109: 303–308.

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Genetika Reprodukčná medicína

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