Abstract
Ca2+ as in other cellular signaling pathways plays a key signal-mediating function in plant immune responses. However, a negative immune activity of some Ca2+-binding calmodulins implicates a rather confusing function of Ca2+ despite its importance in plant immunity. We therefore studied here an effect of Ca2+ on Arabidopsis disease resistance to an adapted Golovinomyces orontii powdery mildew fungus. Pre-treatment with Ca2+ enhanced plant defense against G. orontii especially during late pathogenesis. A similar inhibition of G. orontii growth by Ca2+ was also observed in the salicylic acid-depleted nahG plants. Golovinomyces orontii-dependent induction of defense genes by Ca2+ suggests that it acts as a defense-priming factor in plant post-invasive resistance to adapted powdery mildew fungal pathogens.
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Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A et al (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106
Blume B, Nurnberger T, Nass N, Scheel D (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12:1425–1440
Boller T, Felix G (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
Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464:418–422
Brown GD, Gordon S (2001) Immune recognition. A new receptor for beta-glucans. Nature 413:36–37
Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J et al (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705
Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC et al (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977
Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, Schulze-Lefert P et al (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38:716–720
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548
Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy AS, Poovaiah BW (2009) Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158
Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, Manisseri C, Somerville SC, Voigt CA (2013) Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol 161:1433–1444
Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Gotz F, Glawischnig E, Lee J, Felix G et al (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282:32338–32348
Heo WD, Lee SH, Kim MC, Kim JC, Chung WS, Chun HJ, Lee KJ, Park CY, Park HC, Choi JY et al (1999) Involvement of specific calmodulin isoforms in salicylic acid-independent activation of plant disease resistance responses. Proc Natl Acad Sci USA 96:766–771
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Kim MC, Panstruga R, Elliott C, Muller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P (2002) Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416:447–451
Kwon C (2010) Plant defense responses coming to shape. Plant Pathol J 26:115–120
Kwon C, Bednarek P, Schulze-Lefert P (2008a) Secretory pathways in plant immune responses. Plant Physiol 147:1575–1583
Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H et al (2008b) Co-option of a default secretory pathway for plant immune responses. Nature 451:835–840
Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J (1995) Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 8:863–870
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. Plant Cell 14:2627–2641
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
Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D et al (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183
Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14(Suppl):S389–S400
Ma W, Qi Z, Smigel A, Walker RK, Verma R, Berkowitz GA (2009) Ca2+, cAMP, and transduction of non-self perception during plant immune responses. Proc Natl Acad Sci USA 106:20995–21000
McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389
Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032
Saijo S, Fujikado N, Furuta T, Chung SH, Kotaki H, Seki K, Sudo K, Akira S, Adachi Y, Ohno N et al (2007) Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat Immunol 8:39–46
Schmidt SM, Panstruga R (2011) Pathogenomics of fungal plant parasites: what have we learnt about pathogenesis? Curr Opin Plant Biol 14:392–399
Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746
Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, Findon H, Haynes K, Steele C, Botto M, Gordon S et al (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 8:31–38
Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481
Wessling R, Panstruga R (2012) Rapid quantification of plant-powdery mildew interactions by qPCR and conidiospore counts. Plant Methods 8:35
Wheeler RT, Kombe D, Agarwala SD, Fink GR (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 4:e1000227
Yi C, Park S, Yun HS, Kwon C (2013) Vesicle-associated membrane proteins 721 and 722 are required for unimpeded growth of Arabidopsis under ABA application. J Plant Physiol 170:529–533
Yun HS, Kwon C (2012) Trafficking at the host cell surface during plant immune responses. J Plant Biol 55:185–190
Zimmermann S, Nurnberger T, Frachisse JM, Wirtz W, Guern J, Hedrich R, Scheel D (1997) Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94:2751–2755
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767
Acknowledgments
This work was supported by Grants from the Rural Development Administration (PJ009763), the Next-Generation BioGreen 21 Program (PJ009516 supported by Rural Development Administration) and the National Research Foundation (2013R1A1A2058295 and 2014R1A1A2A16050549).
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The authors declare that they have no conflict of interest.
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Gayoung Lee, Chian Kwon, and Soohong Kim have contributed equally to this work.
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Lee, G., Kwon, C., Kim, S. et al. Calcium potentiates post-invasive resistance to Golovinomyces orontii fungus in Arabidopsis. Genes Genom 37, 545–550 (2015). https://doi.org/10.1007/s13258-015-0283-4
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DOI: https://doi.org/10.1007/s13258-015-0283-4