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Inhibition of prepenetration processes of the powdery mildew Golovinomyces orontii on host inflorescence stems is reduced in the Arabidopsis cuticular mutant cer3 but not in cer1

  • Fungal Diseases
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Abstract

The obligate biotrophic fungus Golovinomyces orontii causes powdery mildew (PM) disease on its host Arabidopsis thaliana. Most research on the G. orontiiArabidopsis pathosystem uses rosette leaves as experimental materials, so little is known about the behavior of G. orontii on other Arabidopsis organs. We thus conducted microscopic analyses of the PM infection process on leaves, stems, fruits and roots of Arabidopsis. Adaxial and abaxial surfaces of mature rosette leaves supported G. orontii infection, but growth was somewhat suppressed on cauline leaves. Prepenetration processes (germination and appressorium formation) were strongly inhibited on stems, fruits and roots. To test the effect of alterations in the Arabidopsis cuticle on the inhibition of prepenetration processes on stems, we used cuticle mutants of Arabidopsis eceriferum (cer) cer1 and cer3. Both mutants had been characterized for reduction in cuticular wax, but our chlorophyll leaching assay revealed increased cuticle permeability only in cer3. Mature rosette leaves and stems of cer1 and cer3 were inoculated, and prepenetration inhibition on stems was found to be significantly reduced in cer3 but not in cer1. We discuss the function of the cuticle in prepenetration inhibition, as well as our finding on suppression of G. orontii growth and reproduction on cer3 rosette leaves.

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Abbreviations

cer :

eceriferum

dpi:

Days post inoculation

ECM:

Extracellular matrix

JA:

Jasmonic acid

PM:

Powdery mildew

SA:

Salicylic acid

References

  • Bessire M, Chassot C, Jacquat A-C, Humphry M, Borel S, Petétot JM-C, Métraux J-P, Nawrath C (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J 26:2158–2168

    Article  PubMed  CAS  Google Scholar 

  • Bourdenx B, Bernard A, Domergue F, Pascal S, Leger A, Roby D, Pervent M, Vile D, Haslam RP, Napier JA, Lessire R, Joubes J (2011) Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol 156:29–45

    Google Scholar 

  • Carver TLW, Thomas BJ (1990) Normal germling development by Erysiphe graminis on cereal leaves freed of epicuticular wax. Plant Pathol 39:367–375

    Article  Google Scholar 

  • Carver TLW, Thomas BJ, Ingerson-Morris SM, Roderick HW (1990) The role of the abaxial leaf surface waxes of Lolium spp. in resistance to Erysiphe graminis. Plant Pathol 39:573–583

    Article  Google Scholar 

  • Carver TLW, Kunoh H, Thomas BJ, Nicholson RL (1999) Release and visualization of the extracellular matrix of conidia of Blumeria graminis. Mycol Res 103:547–560

    Article  Google Scholar 

  • Chandran D, Tai YC, Hather G, Dewdney J, Denoux C, Burgess DG, Ausubel FM, Speed TP, Wildermuth MC (2009) Temporal global expression data reveal known and novel salicylate-impacted processes and regulators mediating powdery mildew growth and reproduction on Arabidopsis. Plant Physiol 149:1435–1451

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Goodwin SM, Boroff VL, Liu X, Jenks MA (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15:1170–1185

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Goodwin SM, Liu X, Chen X, Bressan RA, Jenks MA (2005) Mutation of the RESURRECTION1 locus of Arabidopsis reveals an association of cuticular wax with embryo development. Plant Physiol 139:909–919

    Article  PubMed  CAS  Google Scholar 

  • Garbay B, Tautu MT, Costaglioli P (2007) Low level of pathogenesis-related protein 1 mRNA expression in 15-day-old Arabidopsis cer6-2 and cer2 eceriferum mutants. Plant Sci 172:299–305

    Article  CAS  Google Scholar 

  • Hansjakob A, Bischof S, Bringmann G, Riederer M, Hildebrandt U (2010) Very-long-chain aldehydes promote in vitro prepenetration processes of Blumeria graminis in a dose- and chain length-dependent manner. New Phytol 188:1039–1054

    Article  PubMed  CAS  Google Scholar 

  • Iwamoto M, Takeuchi Y, Takada Y, Yamaoka N (2002) Coleoptile surface cuticle of barley is involved in survival and penetration of Blumeria graminis. Physiol Mol Plant Pathol 60:31–38

    Article  Google Scholar 

  • Jenks MA, Tuttle HA, Eigenbrode SD, Feldmann KA (1995) Leaf epicuticular waxes of the eceriferum mutants in Arabidopsis. Plant Physiol 108:369–377

    PubMed  CAS  Google Scholar 

  • Jenks MA, Eigenbrode SD, Lemieux B (2002) Cuticular waxes of Arabidopsis. The Arabidopsis book 1:e0016. doi:10.1199/tab.0016

  • Kunoh H (2002) Localized induction of accessibility and inaccessibility by powdery mildew. In: Belanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews: a comprehensive treatise. APS Press, St. Paul, pp 126–133

    Google Scholar 

  • Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12:721–727

    Article  PubMed  CAS  Google Scholar 

  • Kurata T, Kawabata-Awai C, Sakuradani E, Shimizu S, Okada K, Wada T (2003) The YORE-YORE gene regulates multiple aspects of epidermal cell differentiation in Arabidopsis. Plant J 36:55–66

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Beisson F, Ohlrogge J, Pollard M (2007) Monoacylglycerols are components of root waxes and can be produced in the aerial cuticle by ectopic expression of a suberin-associated acyltransferase. Plant Physiol 144:1267–1277

    Article  PubMed  CAS  Google Scholar 

  • Micali C, Göllner K, Humphry M, Consonni C, Panstruga R (2008) The powdery mildew disease of Arabidopsis: a paradigm for the interaction between plants and biotrophic fungi. The Arabidopsis book 6:e0115. doi:10.1199/tab.0115

    Google Scholar 

  • Plotnikova JM, Reuber TL, Ausubel FM, Pfister DH (1998) Powdery mildew pathogenesis of Arabidopsis thaliana. Mycologia 90:1009–1016

    Article  Google Scholar 

  • Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Ringelmann A, Riedel M, Riederer M, Hildebrandt U (2009) Two sides of a leaf blade: Blumeria graminis needs chemical cues in cuticular waxes of Lolium perenne for germination and differentiation. Planta 230:95–105

    Article  PubMed  CAS  Google Scholar 

  • Rowland O, Lee R, Franke R, Schreiber L, Kunst L (2007) The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Lett 581:3538–3544

    Article  PubMed  CAS  Google Scholar 

  • Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23:1138–1152

    Article  PubMed  CAS  Google Scholar 

  • Sesma A, Osbourn AE (2004) The rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi. Nature 431:582–586

    Article  PubMed  CAS  Google Scholar 

  • Shah J (2005) Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annu Rev Phytopathol 43:229–260

    Article  PubMed  CAS  Google Scholar 

  • Sosnowski M, Ramsey M, Murray G, Scott E, Wilmshurst C (2001) Symptoms of blackleg (Leptosphaeria maculans) on the roots of canola in Australia. Plant Pathol 50:808

    Google Scholar 

  • Sukno SA, García VM, Shaw BD, Thon MR (2008) Root infection and systemic colonization of maize by Colletotrichum graminicola. Appl Environ Microbiol 74:823–832

    Article  PubMed  CAS  Google Scholar 

  • Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-northerns, expression angling, and promoter analyses. Plant J 43:153–163

    Article  PubMed  CAS  Google Scholar 

  • Tsuba M, Katagiri C, Takeuchi Y, Takada Y, Yamaoka N (2002) Chemical factors of the leaf surface involved in the morphogenesis of Blumeria graminis. Physiol Mol Plant Pathol 60:51–57

    Article  CAS  Google Scholar 

  • Vereijssen J, Schneider HJHM, Termorshuizen AAJ (2004) Possible root infection of Cercospora beticola in sugar beet. Eur J Plant Pathol 110:103–106

    Article  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  PubMed  CAS  Google Scholar 

  • Vogel J, Somerville S (2000) Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc Natl Acad Sci USA 97:1897–1902

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Chin C-K, Gianfagna T (2000) Relationship between cutin monomers and tomato resistance to powdery mildew infection. Physiol Mol Plant Pathol 57:55–61

    Article  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  PubMed  CAS  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2:e718

    Article  PubMed  Google Scholar 

  • Zabka V, Stangl M, Bringmann G, Vogg G, Riederer M, Hildebrandt U (2008) Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol 177:251–263

    PubMed  Google Scholar 

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Acknowledgments

We thank Drs. Takuji Wada and Tetsuya Kurata for technical advice and the kind gift of cer1-1, cer3-6 (yre-1), and cer3-8 (yre-2) lines; Profs. Ko Shimamoto and Masao Tasaka at NAIST, Prof. Hideyoshi Toyoda and Dr. Teruo Nonomura at Kinki University for helpful discussions; and Ms. Shitomi Nakagawa for experimental support. N.I. was supported by a Scientific Research for Plant Graduate Student from NAIST, supported by The Ministry of Education, Culture, Sports, Science and Technology, JAPAN. E.A.S was supported by National Science Foundation, East Asia and Pacific Summer Institutes #0812887.

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Correspondence to Noriko Inada.

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Inada, N., Savory, E.A. Inhibition of prepenetration processes of the powdery mildew Golovinomyces orontii on host inflorescence stems is reduced in the Arabidopsis cuticular mutant cer3 but not in cer1 . J Gen Plant Pathol 77, 273–281 (2011). https://doi.org/10.1007/s10327-011-0331-0

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