Plasma membrane order and fluidity are diversely triggered by elicitors of plant defence
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
27604805
PubMed Central
PMC5014163
DOI
10.1093/jxb/erw284
PII: erw284
Knihovny.cz E-zdroje
- Klíčová slova
- Cryptogein mutants, elicitors, fluidity, membrane order, plant defence, plasma membrane, reactive oxygen species, signalling.,
- MeSH
- Arabidopsis fyziologie MeSH
- buněčná membrána metabolismus fyziologie MeSH
- fluidita membrány fyziologie MeSH
- fluorescenční mikroskopie MeSH
- fluorescenční spektrometrie MeSH
- konfokální mikroskopie MeSH
- nemoci rostlin MeSH
- odolnost vůči nemocem fyziologie MeSH
- reaktivní formy kyslíku metabolismus MeSH
- signální transdukce fyziologie MeSH
- tabák fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- reaktivní formy kyslíku MeSH
Although plants are exposed to a great number of pathogens, they usually defend themselves by triggering mechanisms able to limit disease development. Alongside signalling events common to most such incompatible interactions, modifications of plasma membrane (PM) physical properties could be new players in the cell transduction cascade. Different pairs of elicitors (cryptogein, oligogalacturonides, and flagellin) and plant cells (tobacco and Arabidopsis) were used to address the issue of possible modifications of plant PM biophysical properties induced by elicitors and their links to other events of the defence signalling cascade. We observed an increase of PM order whatever the elicitor/plant cell pair used, provided that a signalling cascade was induced. Such membrane modification is dependent on the NADPH oxidase-mediated reactive oxygen species production. Moreover, cryptogein, which is the sole elicitor able to trap sterols, is also the only one able to trigger an increase in PM fluidity. The use of cryptogein variants with altered sterol-binding properties confirms the strong correlation between sterol removal from the PM and PM fluidity enhancement. These results propose PM dynamics as a player in early signalling processes triggered by elicitors of plant defence.
Zobrazit více v PubMed
Almagro L, Bru R, Pugin A, Pedreno MA. 2012. Early signaling network in tobacco cells elicited with methyl jasmonate and cyclodextrins. Plant Physiology and Biochemistry 51, 1–9. PubMed
Amari K, Diaz-Vivancos P, Pallas V, Sanchez-Pina MA, Hernandez JA. 2007. Oxidative stress induction by Prunus necrotic ringspot virus infection in apricot seeds. Physiologia Plantarum 131, 302–310. PubMed
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
Barna B, Fodor J, Harrach BD, Pogany M, Kiraly Z. 2012. The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiology and Biochemistry 59, 37–43. PubMed
Bartels S, Boller T. 2015. Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. Journal of Experimental Botany 66, 5183–5193. PubMed
Batz O, Logemann E, Reinold S, Hahlbrock K. 1998. Extensive reprogramming of primary and secondary metabolism by fungal elicitor or infection in parsley cells. Biological Chemistry 379, 1127–1135. PubMed
Berzosa C, Gomez-Trullen EM, Piedrafita E, Cebrian I, Martinez-Ballarin E, Miana-Mena FJ, Fuentes-Broto L, Garcia JJ. 2011. Erythrocyte membrane fluidity and indices of plasmatic oxidative damage after acute physical exercise in humans. European Journal of Applied Physiology 111, 1127–1133. PubMed
Bigeard J, Colcombet J, Hirt H. 2015. Signaling mechanisms in pattern-triggered immunity (PTI). Molecular Plant 8, 521–539. PubMed
Blixt Y, Varga MJ, Everitt E. 1993. Enhancement of intracellular uncoating of adenovirus in HeLa cells in the presence of benzyl alcohol as a membrane fluidizer. Archives of Virology 129, 265–277. PubMed
Bloom M, Evans E, Mouritsen OG. 1991. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. Quarterly Reviews of Biophysics 24, 293–397. PubMed
Boissy G, O’Donohue M, Gaudemer O, Perez V, Pernollet JC, Brunie S. 1999. The 2.1 A structure of an elicitin–ergosterol complex: a recent addition to the Sterol Carrier Protein family. Protein Science 8, 1191–1199. PubMed PMC
Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60, 379–406. PubMed
Bonneau L, Gerbeau-Pissot P, Thomas D, Der C, Lherminier J, Bourque S, Roche Y, Simon-Plas F. 2010. Plasma membrane sterol complexation, generated by filipin, triggers signaling responses in tobacco cells. Biochimica et Biophysica Acta 1798, 2150–2159. PubMed
Borchman D, Lamba OP, Salmassi S, Lou M, Yappert MC. 1992. The dual effect of oxidation on lipid bilayer structure. Lipids 27, 261–265. PubMed
Bourque S, Binet MN, Ponchet M, Pugin A, Lebrun-Garcia A. 1999. Characterization of the cryptogein binding sites on plant plasma membranes. Journal of Biological Chemistry 274, 34699–34705. PubMed
Bru R, Selles S, Casado-Vela J, Belchi-Navarro S, Pedreno MA. 2006. Modified cyclodextrins are chemically defined glucan inducers of defense responses in grapevine cell cultures. Journal of Agricultural and Food Chemistry 54, 65–71. PubMed
Bruch RC, Thayer WS. 1983. Differential effect of lipid peroxidation on membrane fluidity as determined by electron spin resonance probes. Biochimica et Biophysica Acta 733, 216–222. PubMed
Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. 2010. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proceedings of the National Academy of Sciences, USA 107, 9452–9457. PubMed PMC
Chan EC, Liu GS, Dusting GJ. 2015. Redox mechanisms in pathological angiogenesis in the retina: roles for NADPH oxidase. Current Pharmaceutical Design 21, 5988–5998. PubMed
Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. 2006. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. The Plant Cell 18, 465–476. PubMed PMC
Choudhury S, Panda P, Sahoo L, Panda SK. 2013. Reactive oxygen species signaling in plants under abiotic stress. Plant Signaling and Behavior 8, e23681. PubMed PMC
Christian AE, Byun HS, Zhong N, Wanunu M, Marti T, Furer A, Diederich F, Bittman R, Rothblat GH. 1999. Comparison of the capacity of beta-cyclodextrin derivatives and cyclophanes to shuttle cholesterol between cells and serum lipoproteins. Journal of Lipid Research 40, 1475–1482. PubMed
Davey AM, Walvick RP, Liu Y, Heikal AA, Sheets ED. 2007. Membrane order and molecular dynamics associated with IgE receptor cross-linking in mast cells. Biophysical Journal 92, 343–355. PubMed PMC
Dinic J, Biverstahl H, Maler L, Parmryd I. 2011. Laurdan and di-4-ANEPPDHQ do not respond to membrane-inserted peptides and are good probes for lipid packing. Biochimica et Biophysica Acta 1808, 298–306. PubMed
Dokladal L, Oboril M, Stejskal K, et al. 2012. Physiological and proteomic approaches to evaluate the role of sterol binding in elicitin-induced resistance. Journal of Experimental Botany 63, 2203–2215. PubMed PMC
Du J, Verzaux E, Chaparro-Garcia A, et al. 2015. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants 1, 15034. PubMed
Eichenberger K, Bohni P, Winterhalter KH, Kawato S, Richter C. 1982. Microsomal lipid peroxidation causes an increase in the order of the membrane lipid domain. FEBS Letters 142, 59–62. PubMed
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
Gaus K, Chklovskaia E, Fazekas de St Groth B, Jessup W, Harder T. 2005. Condensation of the plasma membrane at the site of T lymphocyte activation. Journal of Cell Biology 171, 121–131. PubMed PMC
Gaus K, Zech T, Harder T. 2006. Visualizing membrane microdomains by Laurdan 2-photon microscopy. Molecular Membrane Biology 23, 41–48. PubMed
Gerbeau-Pissot P, Der C, Thomas D, Anca IA, Grosjean K, Roche Y, Perrier-Cornet JM, Mongrand S, Simon-Plas F. 2014. Modification of plasma membrane organization in tobacco cells elicited by cryptogein. Plant Physiology 164, 273–286. PubMed PMC
Gomez-Gomez L, Boller T. 2002. Flagellin perception: a paradigm for innate immunity. Trends in Plant Science 7, 251–256. PubMed
Grosjean K, Mongrand S, Beney L, Simon-Plas F, Gerbeau-Pissot P. 2015. Differential effect of plant lipids on membrane organization: specificities of phytosphingolipids and phytosterols. Journal of Biological Chemistry 290, 5810–5825. PubMed PMC
Halling KK, Slotte JP. 2004. Membrane properties of plant sterols in phospholipid bilayers as determined by differential scanning calorimetry, resonance energy transfer and detergent-induced solubilization. Biochimica et Biophysica Acta 1664, 161–171. PubMed
Heberle FA, Wu J, Goh SL, Petruzielo RS, Feigenson GW. 2011. Comparison of three ternary lipid bilayer mixtures: FRET and ESR reveal nanodomains. Biophysical Journal 99, 3309–3318. PubMed PMC
Hirasawa KI, Amano T, Shioi Y. 2004. Lipid-binding form is a key conformation to induce a programmed cell death initiated in tobacco BY-2 cells by a proteinaceous elicitor of cryptogein. Physiologia Plantarum 121, 196–203. PubMed
Howland MC, Parikh AN. 2010. Model studies of membrane disruption by photogenerated oxidative assault. Journal of Physical Chemistry B 114, 6377–6385. PubMed
Jin L, Millard AC, Wuskell JP, Clark HA, Loew LM. 2005. Cholesterol-enriched lipid domains can be visualized by di-4-ANEPPDHQ with linear and nonlinear optics. Biophysical Journal 89, L04–06. PubMed PMC
Jin L, Millard AC, Wuskell JP, Dong X, Wu D, Clark HA, Loew LM. 2006. Characterization and application of a new optical probe for membrane lipid domains. Biophysical Journal 90, 2563–2575. PubMed PMC
Kadota Y, Goh T, Tomatsu H, Tamauchi R, Higashi K, Muto S, Kuchitsu K. 2004. Cryptogein-induced initial events in tobacco BY-2 cells: pharmacological characterization of molecular relationship among cytosolic Ca(2+) transients, anion efflux and production of reactive oxygen species. Plant and Cell Physiology 45, 160–170. PubMed
Keinath NF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA, Shimosato-Asano H, Grossniklaus U, Schulze WX, Robatzek S, Panstruga R. 2011. PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. Journal of Biological Chemistry 285, 39140–39149. PubMed PMC
Klymchenko AS, Oncul S, Didier P, Schaub E, Bagatolli L, Duportail G, Mely Y. 2009. Visualization of lipid domains in giant unilamellar vesicles using an environment-sensitive membrane probe based on 3-hydroxyflavone. Biochimica et Biophysica Acta 1788, 495–499. PubMed
Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H. 2007. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. The Plant Cell 19, 1065–1080. PubMed PMC
Konigshofer H, Tromballa HW, Loppert HG. 2008. Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant, Cell and Environment 31, 1771–1780. PubMed
Kulik A, Noirot E, Grandperret V, Bourque S, Fromentin J, Salloignon P, Truntzer C, Dobrowolska G, Simon-Plas F, Wendehenne D. 2015. Interplays between nitric oxide and reactive oxygen species in cryptogein signalling. Plant, Cell and Environment 38, 331–348. PubMed
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
Leborgne-Castel N, Lherminier J, Der C, Fromentin J, Houot V, Simon-Plas F. 2008. The plant defense elicitor cryptogein stimulates clathrin-mediated endocytosis correlated with reactive oxygen species production in bright yellow-2 tobacco cells. Plant Physiology 146, 1255–1266. PubMed PMC
Lebrun-Garcia A, Bourque S, Binet MN, Ouaked F, Wendehenne D, Chiltz A, Schaffner A, Pugin A. 1999. Involvement of plasma membrane proteins in plant defense responses. Analysis of the cryptogein signal transduction in tobacco. Biochimie 81, 663–668. PubMed
Lecourieux D, Lamotte O, Bourque S, Wendehenne D, Mazars C, Ranjeva R, Pugin A. 2005. Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38, 527–538. PubMed
Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A. 2002. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. The Plant Cell 14, 2627–2641. PubMed PMC
Lherminier J, Elmayan T, Fromentin J, Elaraqui KT, Vesa S, Morel J, Verrier JL, Cailleteau B, Blein JP, 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
Lijavetzky D, Almagro L, Belchi-Navarro S, Martinez-Zapater JM, Bru R, Pedreno MA. 2008. Synergistic effect of methyljasmonate and cyclodextrin on stilbene biosynthesis pathway gene expression and resveratrol production in Monastrell grapevine cell cultures. BMC Res Notes 1, 132. PubMed PMC
Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327, 46–50. PubMed
Lopez CA, de Vries AH, Marrink SJ. 2013. Computational microscopy of cyclodextrin mediated cholesterol extraction from lipid model membranes. Scientific Reports 3, 2071. PubMed PMC
Macho AP, Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Molecular Cell 54, 263–272. PubMed
Marino D, Dunand C, Puppo A, Pauly N. 2011. A burst of plant NADPH oxidases. Trends in Plant Science 17, 9–15. PubMed
Maruta N, Trusov Y, Brenya E, Parekh U, Botella JR. 2015. Membrane-localized extra-large G proteins and Gbg of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiology 167, 1004–1016. PubMed PMC
Matsui H, Fujiwara M, Hamada S, Shimamoto K, Nomura Y, Nakagami H, Takahashi A, Gomez-Gomez L, Felix G, Boller T. 1999. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. The Plant Journal 18, 277–284. PubMed
Mikes V, Milat ML, Ponchet M, Ricci P, Blein JP. 1997. The fungal elicitor cryptogein is a sterol carrier protein. FEBS Letters 416, 190–192. PubMed
Mikes V, Milat ML, Ponchet M, Panabieres F, Ricci P, Blein JP. 1998. Elicitins, proteinaceous elicitors of plant defense, are a new class of sterol carrier proteins. Biochemical and Biophysical Research Communications 245, 133–139. PubMed
Morales M, Bru R, Garcia-Carmona F, Ros Barcelo A, Pedreno MA. 1998. Effect of dimethyl-β-cyclodextrins on resveratrol metabolism in Gamay grapevine cell cultures before and after inoculation with Xylophilus ampelinus. Plant Cell, Tissue and Organ Culture 53, 179–187.
Morales J, Kadota Y, Zipfel C, Molina A, Torres MA. 2016. The Arabidopsis NADPH oxidases RbohD and RbohF display differential expression patterns and contributions during plant immunity. Journal of Experimental Botany 67, 1663–1676. PubMed
Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule JJ, Blein JP, Simon-Plas F. 2006. Proteomics of plant detergent-resistant membranes. Molecular and Cellular Proteomics 5, 1396–1411. PubMed
Mrak RE. 1992. Opposite effects of dimethyl sulfoxide and ethanol on synaptic membrane fluidity. Alcohol 9, 513–517. PubMed
Nanda AK, Andrio E, Marino D, Pauly N, Dunand C. 2010. Reactive oxygen species during plant–microorganism early interactions. Journal of Integrative Plant Biology 52, 195–204. PubMed
Nathan C, Cunningham-Bussel A. 2013. Beyond oxidative stress: an immunologist’s guide to reactive oxygen species. Nature Reviews Immunology 13, 349–361. PubMed PMC
Noirot E, Der C, Lherminier J, Robert F, Moricova P, Kieu K, Leborgne-Castel N, Simon-Plas F, Bouhidel K. 2014. Dynamic changes in the subcellular distribution of the tobacco ROS-producing enzyme RBOHD in response to the oomycete elicitor cryptogein. Journal of Experimental Botany 65, 5011–5022. PubMed PMC
Ogasawara Y, Kaya H, Hiraoka G, et al. 2008. Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. Journal of Biological Chemistry 283, 8885–8892. PubMed
Osman H, Vauthrin S, Mikes V, Milat ML, Panabieres F, Marais A, Brunie S, Maume B, Ponchet M, Blein JP. 2001. Mediation of elicitin activity on tobacco is assumed by elicitin–sterol complexes. Molecular Biology of the Cell 12, 2825–2834. PubMed PMC
Owen DM, Oddos S, Kumar S, Davis DM, Neil MA, French PM, Dustin ML, Magee AI, Cebecauer M. 2010. High plasma membrane lipid order imaged at the immunological synapse periphery in live T cells. Molecular Membrane Biology 27, 178–189. 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
Polkowska-Kowalczyk L, Maciejewska U. 2001. The oxidative processes induced in cell suspensions of Solanum species by culture filtrate of Phytophthora infestans. Zeitschrift für Naturforschung C 56, 235–244. PubMed
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
Rilfors L, Lindblom G, Wieslander A, Christiansson A. 1984. Lipid bilayer stability in biological membranes. In: Kates M, Manson LA, eds. Biomembranes, Vol. 12 New York: Plenum Press, 205–245.
Roche Y, Gerbeau-Pissot P, Buhot B, Thomas D, Bonneau L, Gresti J, Mongrand S, Perrier-Cornet JM, Simon-Plas F. 2008. Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts. FASEB Journal 22, 3980–3991. PubMed
Roche Y, Klymchenko AS, Gerbeau-Pissot P, Gervais P, Mely Y, Simon-Plas F, Perrier-Cornet JM. 2010. Behavior of plant plasma membranes under hydrostatic pressure as monitored by fluorescent environment-sensitive probes. Biochimica et Biophysica Acta 1798, 1601–1607. PubMed
Sasabe M, Takeuchi K, Kamoun S, Ichinose Y, Govers F, Toyoda K, Shiraishi T, Yamada T. 2000. Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. European Journal of Biochemistry 267, 5005–5013. PubMed
Schroeder F. 1984. Role of membrane lipid asymmetry in aging. Neurobiology of Aging 5, 323–333. PubMed
Simon-Plas F, Elmayan T, Blein JP. 2002. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. The Plant Journal 31, 137–147. PubMed
Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387, 569–572. PubMed
Simons K, Sampaio JL. 2011. Membrane organization and lipid rafts. Cold Spring Harbor Perspectives in Biology 3, a004697. PubMed PMC
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, Koussevitzky S, Mittler R, Miller G. 2011. ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell and Environment 35, 259–270. PubMed
Torres MA. 2010. ROS in biotic interactions. Physiologia Plantarum 138, 414–429. PubMed
Torres MA, Dangl JL, Jones JD. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of National Academy of Sciences, USA 99, 517–522. PubMed PMC
Valitova J, Sulkarnayeva A, Kotlova E, Ponomareva A, Mukhitova FK, Murtazina L, Ryzhkina I, Beckett R, Minibayeva F. 2014. Sterol binding by methyl-beta-cyclodextrin and nystatin—comparative analysis of biochemical and physiological consequences for plants. FEBS Journal 281, 2051–2060. PubMed
van der Meer W, Pottel H, Herreman W, Ameloot M, Hendrickx H. 1984. Effect of orientational order on the decay of the fluorescence anisotropy in membrane suspensions. Biophysical Journal 46, 515–523. PubMed PMC
Vaultier MN, Cantrel C, Vergnolle C, Justin AM, Demandre C, Benhassaine-Kesri G, Cicek D, Zachowski A, Ruelland E. 2006. Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells. FEBS Letters 580, 4218–4223. PubMed
Vauthrin S, Mikes V, Milat ML, Ponchet M, Maume B, Osman H, Blein JP. 1999. Elicitins trap and transfer sterols from micelles, liposomes and plant plasma membranes. Biochimica et Biophysica Acta 1419, 335–342. PubMed
Veatch SL, Keller SL. 2005. Seeing spots: complex phase behavior in simple membranes. Biochimica et Biophysica Acta 1746, 172–185. PubMed
Viard MP, Martin F, Pugin A, Ricci P, Blein JP. 1994. Protein phosphorylation is induced in tobacco cells by the elicitor cryptogein. Plant Physiology 104, 1245–1249. PubMed PMC
Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A. 1999. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283, 680–682. PubMed
Wang J, Megha, London E. 2004. Relationship between sterol/steroid structure and participation in ordered lipid domains (lipid rafts): implications for lipid raft structure and function. Biochemistry 43, 1010–1018. PubMed
Wang Y, Lin A, Loake GJ, Chu C. 2013. H2O2-induced leaf cell death and the crosstalk of reactive nitric/oxygen species. Journal of Integrative Plant Biology 55, 202–208. PubMed
Wendehenne D, Binet MN, Blein JP, Ricci P, Pugin A. 1995. Evidence for specific, high-affinity binding sites for a proteinaceous elicitor in tobacco plasma membrane. FEBS Letters 374, 203–207. PubMed
Wood MJ, Komives EA. 1999. Production of large quantities of isotopically labeled protein in Pichia pastoris by fermentation. Journal of Biomolecular NMR 13, 149–159. PubMed
Wudick MM, Li X, Valentini V, Geldner N, Chory J, Lin J, Maurel C, Luu DT. 2015. Subcellular redistribution of root aquaporins induced by hydrogen peroxide. Molecular Plant 8, 1103–1114. PubMed
Yan Z, Wang J, Li J, Jiang N, Zhang R, Yang W, Yao W, Wu W. 2015. Oxidative stress and endocytosis are involved in upregulation of interleukin-8 expression in airway cells exposed to PM2.5. Environmental Toxicology (in press). PubMed
Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JD, 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
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
Zipfel C. 2014. Plant pattern-recognition receptors. Trends in Immunology 35, 345–351. PubMed