Dynamic changes in the subcellular distribution of the tobacco ROS-producing enzyme RBOHD in response to the oomycete elicitor cryptogein
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
24987013
PubMed Central
PMC4144778
DOI
10.1093/jxb/eru265
PII: eru265
Knihovny.cz E-zdroje
- Klíčová slova
- BY-2 cells, Nicotiana tabacum, cryptogein, protein trafficking, protein trafficking., reactive oxygen species, respiratory burst oxidase homolog D (RBOHD),
- MeSH
- buněčná membrána metabolismus MeSH
- fungální proteiny metabolismus MeSH
- konfokální mikroskopie MeSH
- kvantitativní polymerázová řetězová reakce MeSH
- NADPH-oxidasy genetika metabolismus MeSH
- Phytophthora fyziologie MeSH
- reaktivní formy kyslíku metabolismus MeSH
- rostlinné proteiny genetika metabolismus MeSH
- tabák genetika metabolismus mikrobiologie MeSH
- transmisní elektronová mikroskopie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- fungální proteiny MeSH
- NADPH-oxidasy MeSH
- reaktivní formy kyslíku MeSH
- rostlinné proteiny MeSH
Plant NADPH oxidases, also known as respiratory burst oxidase homologues (RBOHs), have been identified as a major source of reactive oxygen species (ROS) during plant-microbe interactions. The subcellular localization of the tobacco (Nicotiana tabacum) ROS-producing enzyme RBOHD was examined in Bright Yellow-2 cells before and after elicitation with the oomycete protein cryptogein using electron and confocal microscopy. The plasma membrane (PM) localization of RBOHD was confirmed and immuno-electron microscopy on purified PM vesicles revealed its distribution in clusters. The presence of the protein fused to GFP was also seen in intracellular compartments, mainly Golgi cisternae. Cryptogein induced, within 1h, a 1.5-fold increase in RBOHD abundance at the PM and a concomitant decrease in the internal compartments. Use of cycloheximide revealed that most of the proteins targeted to the PM upon elicitation were not newly synthesized but may originate from the Golgi pool. ROS accumulation preceded RBOHD transcript- and protein-upregulation, indicating that ROS resulted from the activation of a PM-resident pool of enzymes, and that enzymes newly addressed to the PM were inactive. Taken together, the results indicate that control of RBOH abundance and subcellular localization may play a fundamental role in the mechanism of ROS production.
INRA UMR1347 Agroécologie ERL CNRS 6300 BP 86510 F 21065 Dijon Cedex France
INRA UR341 Mathématiques et Informatique Appliquées F 78352 Jouy en Josas Cedex France
Université de Bourgogne UMR1347 Agroécologie ERL CNRS 6300 BP 86510 F 21065 Dijon Cedex France
Zobrazit více v PubMed
Asai S, Ohta K, Yoshioka H. 2008. MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana . The Plant Cell 20, 1390–1406 PubMed PMC
Asai S, Yoshioka H. 2009. Nitric oxide as a partner of reactive oxygen species participates in disease resistance to nectrotophic pathogen Botryis cinerea in Nicotiana benthamiana . Molecular Plant-Microbe Interactions 22, 619–629 PubMed
Baddeley AJ, Moyeed RA, Howard CV, Boyde A. 1993. Analysis of a three-dimensional point pattern with replication. Journal of the Royal Statistical Society Series C (Applied Statistics) 42, 641–668
Bindschedler LV, Dewdney J, Blee KA, et al. 2006. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. The Plant Journal 47, 851–863 PubMed PMC
Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B. 2004. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. Journal of Microscopy 214, 159–173 PubMed
Boulaflous A, Saint-Jore-Dupas C, Herranz-Gordo M-C, Pagny-Salehabadi S, Plasson C, Garidou F, Kiefer-Meyer M-C, Ritzenthaler C, Faye L, Gomord V. 2009. Cytosolic N-terminal arginine-based signals together with a luminal signal target a type II membrane protein to the plant ER. BMC Plant Biology 9, 144. PubMed PMC
Bradford MM. 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254 PubMed
Bradley DJ, Kjellbom P, Lamb CJ. 1992. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70, 21–30 PubMed
Brandizzi F, Irons S, Kearns A, Hawes C. 2003. BY-2 cells: culture and transformation for live cell imaging. In: Bonifacino JS. et al., eds. Current protocols in cell biology, Ch. 1, Unit 1.7. Wiley; PubMed
Brown DA, London E. 1998. Structure and origin of ordered lipid domains in biological membranes. Journal of Membrane Biology 164, 103–114 PubMed
Casbon A-J, Allen L-AH, Dunn KW, Dinauer MC. 2009. Macrophage NADPH oxidase flavocytochrome B localizes to the plasma membrane and Rab11-positive recycling endosomes. Journal of Immunology 182, 2325–2339 PubMed PMC
Chen SX, Schopfer P. 1999. Hydroxyl-radical production in physiological reactions. A novel function of peroxidase. European Journal of Biochemistry 260, 726–735 PubMed
Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof Y-D, Schumacher K, Gonneau M, Hofte H, Vernhettes S. 2009. Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis . The Plant Cell 21, 1141–1154 PubMed PMC
Curtis MD, Grossniklaus U. 2003. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiology 133, 462–469 PubMed PMC
Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP. 2012. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. The Plant Cell 24, 275–287 PubMed PMC
Delledonne M, Zeier J, Marocco A, Lamb C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences, USA 98, 13454–13459 PubMed PMC
Ejlerskov P, Christensen DP, Beyaie D, Burritt JB, Paclet M-H, Gorlach A, van Deurs B, Vilhardt F. 2012. NADPH oxidase is internalized by clathrin-coated pits and localizes to a Rab27A/B GTPase-regulated secretory compartment in activated macrophages. Journal of Biological Chemistry 287, 4835–4852 PubMed PMC
Fujita A, Cheng J, Hirakawa M, Furukawa K, Kusunoki S, Fujimoto T. 2007. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Molecular Biology of the Cell 18, 2112–2122 PubMed PMC
Fujiwara M, Hamada S, Hiratsuka M, Fukao Y, Kawasaki T, Shimamoto K. 2009. Proteome analysis of detergent-resistant membranes (DRMs) associated with OsRac1-mediated innate immunity in rice. Plant and Cell Physiology 50, 1191–1200 PubMed PMC
Furt F, Konig S, Bessoule JJ, et al. 2010. Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane. Plant Physiology 152, 2173–2187 PubMed PMC
Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, De Lorenzo G, Ferrari S. 2008. The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea . Plant Physiology 148, 1695–1706 PubMed PMC
Halliwell B. 2006. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology 141, 312–322 PubMed PMC
Heino S, Lusa S, Somerharju P, Ehnholm C, Olkkonen VM, Ikonen E. 2000. Dissecting the role of the Golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface. Proceedings of the National Academy of Sciences, USA 97, 8375–8380 PubMed PMC
Jin S, Zhou F, Katirai F, Li P-L. 2011. Lipid raft redox signaling: molecular mechanisms in health and disease. Antioxidants and Redox Signaling 15, 1043–1083 PubMed PMC
Kawahara T, Jackson HM, Smith SME, Simpson PD, Lambeth JD. 2011. Nox5 forms a functional oligomer mediated by self-association of its dehydrogenase domain. Biochemistry 50, 2013–2025 PubMed PMC
Keller H, Blein J, Bonnet P, Ricci P. 1996. Physiological and molecular characteristics of elicitin-induced systemic acquired resistance in tobacco. Plant Physiology 110, 365–376 PubMed PMC
Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C. 1998. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. The Plant Cell 10, 255–266 PubMed PMC
Kim SI, Yi JS, Ko YG. 2006. Amyloid β oligomerization is induced by brain lipid rafts. Journal of Cellular Biochemistry 99, 878–889 PubMed
Kobayashi M, Kawakita K, Maeshima M, Doke N, Yoshioka H. 2006. Subcellular localization of Strboh proteins and NADPH-dependent O2 –-generating activity in potato tuber tissues. Journal of Experimental Botany 57, 1373–1379 PubMed
Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L. 2007. Rice SCAMP1 defines clathrin-coated, trans-Golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. The Plant Cell 19, 296–319 PubMed PMC
Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251–275 PubMed
Larsson C, Sommarin M, Widell S. 1994. Isolation of highly purified plasma membranes and the separation of inside-out and right-side-out vesicles. Methods in Enzymology 228, 451–469
Le PU, Nabi IR. 2003. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. Journal of Cell Science 116, 1059–1071 PubMed
Lee Y, Rubio MC, Alassimone J, Geldner N. 2013. A mechanism for localized lignin deposition in the endodermis. Cell 153, 402–412 PubMed
Leitch IJ, Hanson L, Lim KY, Kovarik A, Chase MW, Clarkson JJ, Leitch AR. 2008. The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Annals of Botany 101, 805–814 PubMed PMC
Lherminier J, Elmayan T, Fromentin J, Elaraqui KT, Vesa S, Morel J, Verrier J-L, Cailleteau B, Blein J-P, Simon-Plas F. 2009. NADPH oxidase-mediated reactive oxygen species production: subcellular localization and reassessment of its role in plant defense. Molecular Plant-Microbe Interactions 22, 868–881 PubMed
Li R, Liu P, Wan Y, Chen T, et al. 2012. A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. The Plant Cell 24, 2105–2122 PubMed PMC
Lillemeier BF, Pfeiffer JR, Surviladze Z, Wilson BS, Davis MM. 2006. Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proceedings of the National Academy of Sciences, USA 103, 18992–18997 PubMed PMC
Liu P, Li R-L, Zhang L, Wang Q-L, Niehaus K, Baluska F, Samaj J, Lin J-X. 2009. Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. The Plant Journal 60, 303–313 PubMed
Marino D, Dunand C, Puppo A, Pauly N. 2011. A burst of plant NADPH oxidases. Trends in Plant Science 17, 9–15 PubMed
Milhas D, Clarke CJ, Idkowiak-Baldys J, Canals D, Hannun YA. 2010. Anterograde and retrograde transport of neutral sphingomyelinase-2 between the Golgi and the plasma membrane. Biochimica et Biophysica Acta 1801, 1361–1374 PubMed PMC
Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R. 2009. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45. PubMed
Mongrand S, Morel J, Laroche J, Claverol S, Carde J-P, Hartmann M-A, Bonneu M, Simon-Plas F, Lessire R, Bessoule J-J. 2004. Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. Journal of Biological Chemistry 279, 36277–36286 PubMed
Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule J-J, Blein J-P, Simon-Plas F. 2006. Proteomics of plant detergent-resistant membranes. Molecular and Cellular Proteomics 5, 1396–1411 PubMed
Mori IC, Schroeder JI. 2004. Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiology 135, 702–708 PubMed PMC
Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497
Neumann-Giesen C, Falkenbach B, Beicht P, Claasen S, Luers G, Stuermer CA, Herzog V, Tikkanen R. 2004. Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochemical Journal 378, 509–518 PubMed PMC
Nichols BJ, Kenworthy AK, Polishchuk RS, Lodge R, Roberts TH, Hirschberg K, Phair RD, Lippincott-Schwartz J. 2001. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. Journal of Cell Biology 153, 529–541 PubMed PMC
O’Brien JA, Daudi A, Butt VS, Bolwell GP. 2012. Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236, 765–779 PubMed
Oda T, Hashimoto H, Kuwabara N, et al. 2010. Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. Journal of Biological Chemistry 285, 1435–1445 PubMed PMC
Ohser J. 1983. On estimators for the reduced second moment measure of point processes. Mathematische Operationsforschung und Statistik, Series Statistics 14, 63–71
Paladino S, Sarnataro D, Pillich R, Tivodar S, Nitsch L, Zurzolo C. 2004. Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins. Journal of Cell Biology 167, 699–709 PubMed PMC
Panchal RG, Ruthel G, Kenny TA, Kallstrom GH, Lane D, Badie SS, Li L, Bavari S, Aman MJ. 2003. In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding. Proceedings of the National Academy of Sciences, USA 100, 15936–15941 PubMed PMC
Pogany M, von Rad U, Grun S, Dongo A, Pintye A, Simoneau P, Bahnweg G, Kiss L, Barna B, Durner J. 2009. Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiology 151, 1459–1475 PubMed PMC
Prior IA, Muncke C, Parton RG, Hancock JF. 2003. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. Journal of Cell Biology 160, 165–170 PubMed PMC
R Development Core Team. 2009. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing
Raffaele S, Bayer E, Lafarge D, et al. 2009. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. The Plant Cell 21, 1541–1555 PubMed PMC
Ricci P, Bonnet P, Huet JC, Sallantin M, Beauvais-Cante F, Bruneteau M, Billard V, Michel G, Pernollet JC. 1989. Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. European Journal of Biochemistry 183, 555–563 PubMed
Ripley BD. 1976. The second order analysis of stationary point process. Journal of Applied Probability 13, 255–266
Ritzenthaler C, Nebenfuhr A, Movafeghi A, Stussi-Garaud C, Behnia L, Pimpl P, Staehelin LA, Robinson DG. 2002. Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. The Plant Cell 14, 237–261 PubMed PMC
Robinson DG, Jiang L, Schumacher K. 2008. The endosomal system of plants: charting new and familiar territories. Plant Physiology 147, 1482–1492 PubMed PMC
Romero-Puertas MC, Perazzolli M, Zago ED, Delledonne M. 2004. Nitric oxide signalling functions in plant-pathogen interactions. Cellular Microbiology 6, 795–803 PubMed
Sagi M, Fluhr R. 2001. Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiology 126, 1281–1290 PubMed PMC
Sagi M, Fluhr R. 2006. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiology 141, 336–340 PubMed PMC
Schmidt GW, Delaney SK. 2010. Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Molecular Genetics and Genomics 283, 233–241 PubMed
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675 PubMed PMC
Simon-Plas F, Elmayan T, Blein J-P. 2002. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. The Plant Journal 31, 137–147 PubMed
Simons K, Gerl MJ. 2010. Revitalizing membrane rafts: new tools and insights. Nature Reviews Molecular Cell Biology 11, 688–699 PubMed
Stanislas T, Bouyssie D, Rossignol M, Vesa S, Fromentin J, Morel J, Pichereaux C, Monsarrat B, Simon-Plas F. 2009. Quantitative proteomics reveals a dynamic association of proteins to detergent-resistant membranes upon elicitor signaling in tobacco. Molecular and Cellular Proteomics 8, 2186–2198 PubMed PMC
Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R. 2011. Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14, 691–699 PubMed
Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. 2008. Local positive feedback regulation determines cell shape in root hair cells. Science 319, 1241–1244 PubMed
Torres MA. 2010. ROS in biotic interactions. Physiologia Plantarum 138, 414–429 PubMed
Torres MA, Dangl JL, Jones JDG. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences, USA 99, 517–522 PubMed PMC
Torres MA, Jones JDG, Dangl JL. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana . Nature Genetics 37, 1130–1134 PubMed
Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD. 1998. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). The Plant Journal 14, 365–370 PubMed
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3-new capabilities and interfaces. Nucleic Acids Research 40, e115. PubMed PMC
Ushio-Fukai M. 2009. Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxidants and Redox Signaling 11, 1289–1299 PubMed PMC
Viard M, Martin F, Pugin A, Ricci P, Blein J. 1994. Protein phosphorylation is induced in tobacco cells by the elicitor cryptogein. Plant Physiology 104, 1245–1249 PubMed PMC
Wientjes FB, Segal AW, Hartwig JH. 1997. Immunoelectron microscopy shows a clustered distribution of NADPH oxidase components in the human neutrophil plasma membrane. Journal of Leukocyte Biology 61, 303–312 PubMed
Yoda H, Hiroi Y, Sano H. 2006. Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiology 142, 193–206 PubMed PMC
Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JDG, Doke N. 2003. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans . The Plant Cell 15, 706–718 PubMed PMC
Yun B-W, Feechan A, Yin M, et al. 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264–268 PubMed
Zhang H, Fang Q, Zhang Z, Wang Y, Zheng X. 2009. The role of respiratory burst oxidase homologues in elicitor-induced stomatal closure and hypersensitive response in Nicotiana benthamiana . Journal of Experimental Botany 60, 3109–3122 PubMed PMC
Zhang J, Shao F, Li Y, et al. 2007. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host and Microbe 1, 175–185 PubMed
On the Origin and Fate of Reactive Oxygen Species in Plant Cell Compartments
Plasma membrane order and fluidity are diversely triggered by elicitors of plant defence