Skip to main content

Biological Host Response: A Paradigm and Strategy to Overcome Biotic Stress Caused by Powdery Mildew Causal Agents in Plants

  • Chapter
  • First Online:
New Frontiers in Stress Management for Durable Agriculture

Abstract

Powdery mildew disease is one of the most important diseases of agriculturally and economically important crop plants and tree species. Powdery mildew causing fungi are a complex group of fungi which can infect a broad range of host species which include agricultural crops, fruit trees, and ornamental plants. The biological hosts for powdery mildew infection are important sources for food including cereals, millets, legumes, pulses, vegetables, fruits, beverages, and ornamentals with esthetic value. Considering the importance of powdery mildew disease and its impact on crop productivity and quality of the produce, it necessitates to understand the mode of infection, molecular mechanism underlying its pathogenicity, and also how plants respond to the infection to devise strategies to curb the pathogens. An attempt is made to appraise previous studies reported on powdery mildew causing fungi and elucidate mechanisms to target the pathogens effectively.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adam L, Somerville SC (1996) Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J 9(3):341–356

    Article  CAS  PubMed  Google Scholar 

  • Adam L, Ellwood S, Wilson I, Saenz G, Xiao S, Oliver RP, Turner JG, Somerville S (1999) Comparison of Erysiphe cichoracearum and E. cruciferarum and a survey of 360 Arabidopsis thaliana accessions for resistance to these two powdery mildew pathogens. Mol Plant Microbe Interact 12:1031–1043

    Article  CAS  PubMed  Google Scholar 

  • Ahmed AA, Pedersen C, Schultz-Larsen T, Kwaaitaal M, Jørgensen HJL, Thordal-Christensen H (2015) The barley powdery mildew candidate secreted effector protein CSEP0105 inhibits the chaperone activity of a small heat shock protein. Plant Physiol 168(1):321–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmed AA, McLellan H, Aguilar GB, Hein I, Thordal-Christensen H, Birch PR (2016a) Engineering barriers to infection by undermining pathogen effector function or by gaining effector recognition. In: Collinge DB (ed) Biotechnology for plant disease control. Wiley, New York, pp 23–50

    Google Scholar 

  • Ahmed AA, Pedersen C, Thordal-Christensen H (2016b) The barley powdery mildew effector candidates CSEP0081 and CSEP0254 promote fungal infection success. PLoS one 11(6):e0157586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Appiano M, Pavan S, Catalano D, Zheng Z, Bracuto V, Lotti C, Visser RG, Ricciardi L, Bai Y (2015) Identification of candidate MLO powdery mildew susceptibility genes in cultivated Solanaceae and functional characterization of tobacco NtMLO1. Transgenic Res 24(5):847–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnaud G (1921) Study on parasite fungi (Parodiellinaceae), including Erysiphacea (in French). Ann Epiphyt 7:1–115

    Google Scholar 

  • Arthur JC, Lich JD, Aziz RK, Kotb M, Ting JPY (2007) Heat shock protein 90 associates with monarch-1 and regulates its ability to promote degradation of NF-κB-inducing kinase. J Immunol 17(9):6291–6296

    Article  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in chloroplasts. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photo inhibition. Elsevier, Amsterdam, pp 227–287

    Google Scholar 

  • Aust HJ, Hoyningen-Huene J (1986) Microclimate in relation to powdery mildew epidemics. Annu Rev Phytopathol 24:491–510

    Article  Google Scholar 

  • Bai Y, Pavan S, Zheng Z, Zappel NF, Reinstädler A, Lotti C, De Giovanni C, Ricciardi L, Lindhout P, Visser R, Theres K (2008) Naturally occurring broad-spectrum powdery mildew resistance in a Central American tomato accession is caused by loss of Mlo function. Mol Plant Microbe Interact 2(1):30–39

    Article  CAS  Google Scholar 

  • Bari R, Jones JDG (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  Google Scholar 

  • Belanger RR, Labbé C (2002) Control of powdery mildews without chemicals: prophylactic and biological alternatives for horticultural crops. In: Bélanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews: a comprehensive treatise. CABI, Wallingford, pp 256–267

    Google Scholar 

  • Bencina M, Panneman H, Ruijter GJ, LegiÅ¡a M, Visser J (1997) Characterization and overexpression of the Aspergillus niger gene encoding the cAMP-dependent protein kinase catalytic subunit. Microbiology 143(4):1211–1220

    Article  CAS  PubMed  Google Scholar 

  • Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci U S A 102:3135–3140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bheri M, Fareeda G, Makandar R (2016) Assessing host specialization of Erysiphe pisi on garden pea germplasm through genotypic and phenotypic characterization. Euphytica 212:1–14

    Article  CAS  Google Scholar 

  • Bheri M, Bhosle SM, Makandar R (2019) Shotgun proteomics provides an insight into pathogenesis-related proteins using anamorphic stage of the biotroph, Erysiphe pisi pathogen of garden pea. Microbiol Res 222:25–34

    Article  CAS  PubMed  Google Scholar 

  • Bhosle SM, Marathe N, Makandar R (2019) The er2 gene resistance against powdery mildew infection is associated with enhanced antioxidative protection and defense gene expression. Physiol Mol Plant Pathol 106(2019):253–262

    Article  CAS  Google Scholar 

  • Bindslev L (2001) Signal transduction in the establishment of Blumeri agraminis infection structures. PhD thesis, Institute of Molecular Biology, Copenhagen University, Denmark

    Google Scholar 

  • Böhlenius H, Mørch SM, Godfrey D, Nielsen ME, Thordal-Christensen H (2010) The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley. Plant Cell 22(11):3831–3844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Both M, Eckert SE, Csukai M, MuÈller E, Dimopoulos G, Spanu PD (2005) Transcript profiles of Blumeria graminis development during infection reveal a cluster of genes that are potential virulence determinants. Mol Plant Microbe Interact 18:125–133

    Article  CAS  PubMed  Google Scholar 

  • 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(7287):418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inze D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10(7):1723–1732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43(1):83–116

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Braun U (1987) A monograph of the erysiphales (powdery mildews), vol 89. E. Schweizerbart: Beiheftzur Nova Hedwigia, Stuttgart

    Google Scholar 

  • Braun U (1995) The powdery mildews (Erysiphales) of Europe. Gustav Fischer, Stuttgart

    Google Scholar 

  • Braun U, Cook RTA, Inman AJ, Shin HD (2002a) The taxonomy of the powdery mildew fungi. In: Bélanger RR, Bushnell WR, Dik AJ, TLW C (eds) The powdery mildews: a comprehensive treatise. APS Press, St. Paul, pp 13–55

    Google Scholar 

  • Braun U, Cook RTA, Inman AJ, Shin HD (2002b) The taxonomy of the powdery mildews. In: Belanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews, a comprehensive treatise. The American Phytopathological Society Press, St. Paul, pp 56–65

    Google Scholar 

  • Bruce TJA, Pickett JA (2007) Plant defense signaling induced by biotic attacks. Curr Opin Plant Biol 10:387–392

    Article  CAS  PubMed  Google Scholar 

  • Bruno KS, Aramayo R, Minke PF, Metzenberg RL, Plamann M (1996) Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP-dependent protein kinase. EMBO J 15:5772–5782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Proc Natl Acad Sci USA 107:9452–9457

    Article  PubMed  PubMed Central  Google Scholar 

  • Buschges R, Hollricher K, Panstruga R, Simmons G, Wolter M, Frijters A, Van Daelen R, Van der Lee T, Diergaarde P, Groenedijk J (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705

    Article  CAS  PubMed  Google Scholar 

  • Caldo RA, Nettleton D, Wise RP (2004) Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16(9):2514–2528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Candresse T, Le Gall O, Maisonneuve B, German-Retana S, Redondo E (2002) The use of green fluorescent protein tagged recombinant viruses to test lettuce mosaic virus resistance in lettuce. Phytopathology 92:169–176

    Article  CAS  PubMed  Google Scholar 

  • Carver TLW, Ingerson SM (1987) Responses of Erysiphe graminis germlings to contact with artificial and host surfaces. Physiol Mol Plant Pathol 30:359–372

    Article  Google Scholar 

  • Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant acquired resistance by salicylic acid. Science 262:1883–1885

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Shiotani K, Togashi T, Miki D, Aoyama M, Wong HL, Kawasaki T, Shimamoto K (2010) Analysis of the Rac/Rop small GTPase family in rice: expression, subcellular localization and role in disease resistance. Plant Cell Physiol 51(4):585–595

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  PubMed  Google Scholar 

  • Choi W, Dean RA (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9(11):1973–1983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coghlan SE, Walters DR (1990) Polyamine metabolism in ‘green islands’ on powdery mildew infected barley leaves: possible interactions with senescence. New Phytol 116(3):417–424

    Article  CAS  PubMed  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977

    Article  CAS  PubMed  Google Scholar 

  • Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, Schulze-Lefert P, Somerville SC (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat Genet 38(6):716

    Article  CAS  PubMed  Google Scholar 

  • D’Maris Amick Dempsey AC, Vlot MC, Daniel FK (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156

    Article  PubMed  PubMed Central  Google Scholar 

  • David D, Nair SA, Pillai MR (2013) Smurf E3 ubiquitin ligases at the cross roads of oncogenesis and tumor suppression. Biochim Biophys Acta 1835(1):119–128

    CAS  PubMed  Google Scholar 

  • De Waard MA (1997) Significance of ABC transporters in fungicide sensitivity and resistance. Pectic Sci 51:271–275

    Google Scholar 

  • De Wit PJGM, Mehrabi R, Van Den Brug HA, Stergiopoulos I (2009) Fungal effector proteins: past, present and future. Mol Plant Pathol 10:735–747

    Article  PubMed  Google Scholar 

  • Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46:268–278

    Article  CAS  PubMed  Google Scholar 

  • Deslandes L, Rivas S (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 17:644–655

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Pendon JA, Truniger V, Nieto C, Garcia-Mas J, Bendahmane A, Aranda MA (2004) Advances in understanding recessive resistance to plant viruses. Mol Plant Pathol 5:223–233

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11(8):539

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG (2004) The Melampsoralini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16(3):755–768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Donald T, Pellerone F, Adam-Blondon AF, Bouquet A, Thomas M, Dry I (2002) Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine. Theor Appl Genet 104:610–618

    Article  CAS  PubMed  Google Scholar 

  • Doster M, Schnathorst W (1985) Effects of leaf maturity and cultivar resistance on development of the powdery mildew fungus on grapevines. Phytopathology 75:318–321

    Article  Google Scholar 

  • Douchkov D, Lück S, Johrde A, Nowara D, Himmelbach A, Rajaraman J, Schweizer P (2014) Discovery of genes affecting resistance of barley to adapted and non-adapted powdery mildew fungi. Genome Biol 15(12):518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dumas B, Freyssinet G, Pallett KE (1995) Tissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiol 107:1091–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eckey C, Korell M, Leib K, Biedenkopf D, Jansen C, Langen G, Kogel KH (2004) Identification of powderymildew-induced barley genes by cDNA-AFLP: functional assessment of an early expressed map kinase. Plant Mol Biol 55:1–15

    Article  CAS  PubMed  Google Scholar 

  • Elliott C, Müller J, Miklis M, Bhat RA, Schulze-Lefert P, Panstruga R (2005) Conserved extracellular cysteine residues and cytoplasmic loop-loop interplay are required for functionality of the heptahelical MLO protein. Biochem J 385(1):243–254

    Article  CAS  PubMed  Google Scholar 

  • Ellis J (2006) Insights into nonhost disease resistance: can they assist disease control in agriculture? Plant Cell 18:523–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis J, Jones D (1998) Structure and function of proteins controlling strain-specific pathogen resistance in plants. Curr Opin Plant Biol 1:288–293

    Article  CAS  PubMed  Google Scholar 

  • Ellis C, Turner JG (2002) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13(5):1025–1033

    Article  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  CAS  PubMed  Google Scholar 

  • Fang EG, Dean RA (2000) Site-directed mutagenesis of the magB gene affects growth and development in Magnaporthe grisea. Mol Plant Microbe Interact 13(11):1214–1227

    Article  CAS  PubMed  Google Scholar 

  • Feechan A, Jermakow AM, Torregrosa L, Panstruga R, Dry IB (2008) Identification of grapevine MLO gene candidates involved in susceptibility to powdery mildew. Funct Plant Biol 35:1255–1266

    Article  PubMed  Google Scholar 

  • Feechan A, Kocsis M, Riaz S, Zhang W, Gadoury DM, Walker MA, Cadle-Davidson L (2015) Strategies for RUN1 deployment using RUN2 and REN2 to manage grapevine powdery mildew informed by studies of race specificity. Phytopathology 105(8):1104–1113

    Article  CAS  PubMed  Google Scholar 

  • Fekete C, Fung RW, Szabó Z, Qiu W, Chang L, Schachtman DP, Kovács LG (2009) Up-regulated transcripts in a compatible powdery mildew–grapevine interaction. Plant Physiol Biochem 47(8):732–738

    Article  CAS  PubMed  Google Scholar 

  • Fischer G, Wittman-Liebold B, Lang K, Kiefhaber T, Schmid FX (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337:476–478

    Article  CAS  PubMed  Google Scholar 

  • Flor HH (1954) Identification of races of flax rust by lines with single rust-conditioning genes (no. 1087). US Dept. of Agriculture

    Google Scholar 

  • Flor HH (1956) The complementary genic systems in flax and flax rust. Adv Genet 8:29–54

    Article  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9(1):275–296

    Article  Google Scholar 

  • Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 13(2):821–829

    Article  CAS  Google Scholar 

  • Foyer CH, Theodoulou FL, Delrot S (2001) The functions of inter-and intracellular glutathione transport systems in plants. Trends Plant Sci 6(10):486–492

    Article  CAS  PubMed  Google Scholar 

  • Francis SA, Dewey FM, Gurr SJ (1996) The role of cutinase in germling development and infection by Erysiphe graminis f.sp. hordei. Physiol Mol Plant Pathol 49(3):201–211

    Article  CAS  Google Scholar 

  • Freskgard PO, Bergenhem N, Jonsson BH, Svensson M, Carlsson U (1992) Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258(5081):466–468

    Article  CAS  PubMed  Google Scholar 

  • Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci U S A 98:373–378

    Article  CAS  PubMed  Google Scholar 

  • Fung RW, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, McIntyre LM, Schachtman DP, Qiu W (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 46(1):236–249

    Article  CAS  Google Scholar 

  • Gabriel DW, Rolfe BG (1990) Working models of specific recognition in plant–microbe interactions. Annu Rev Phytopathol 28:365–391

    Article  CAS  Google Scholar 

  • Gao Z, Eyers S, Thomas C, Ellis N, Maule A (2004a) Identification of markers tightly linked to sbm recessive genes for resistance to Pea seed-borne mosaic virus. Theor Appl Genet 109:488–494

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, Maule AJ (2004b) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40:376–385

    Article  CAS  PubMed  Google Scholar 

  • Giraldo MC, Valent B (2013) Filamentous plant pathogen effectors in action. Nat Rev Microbiol 11(11):800

    Article  CAS  PubMed  Google Scholar 

  • Gjetting T, Carver TL, Skot L, Lyngkjaer MF (2004) Differential gene expression in individual papilla-resistant and powdery mildew-infected barley epidermal cells. Mol Plant Microbe Interact 17:729–738

    Article  CAS  PubMed  Google Scholar 

  • Godfrey D, Böhlenius H, Pedersen C, Zhang Z, Emmersen J, Thordal-Christensen H (2010) Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 11(1):317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gold S, Duncan G, Barrett K, Kronstad J (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev 8(23):2805–2816

    Article  CAS  PubMed  Google Scholar 

  • Göllner K, Schweizer P, Bai Y, Panstruga R (2008) Natural genetic resources of Arabidopsis thaliana reveal a high prevalence and unexpected phenotypic plasticity of RPW8-mediated powdery mildew resistance. New Phytol 177:725–742

    Article  CAS  PubMed  Google Scholar 

  • Gopalan S, Bauer DW, Alfano JR, Loniello AO, He SY, Collmer A (1996) Expression of the Pseudomonas syringaea virulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8:1095–1105

    CAS  PubMed  PubMed Central  Google Scholar 

  • Green JR, Carver TLW, Gurr SJ (2002) The formation and function of infection and feeding structures. In: Belanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews, a comprehensive treatise. APS Press, St Paul, pp 66–82

    Google Scholar 

  • Gronover CS, Kasulke D, Tudzynski P, Tudzynski B (2001) The role of G protein alpha subunits in the infection process of the gray mold fungus Botrytis cinerea. Mol Plant Microbe Interact 14(11):1293–1302

    Article  CAS  PubMed  Google Scholar 

  • Guan X, Zhao H, Xu Y, Wang Y (2011) Transient expression of glyoxal oxidase from the Chinese wild grape Vitispseudoreticulata can suppress powdery mildew in a susceptible genotype. Protoplasma 248:415–423

    Article  CAS  PubMed  Google Scholar 

  • Hacquard S, Kracher B, Maekawa T, Vernaldi S, Schulze-Lefert P, Ver Loren van Themaat E (2013) Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. Proc Natl Acad Sci U S A 110:E2219–E2228

    Article  PubMed  PubMed Central  Google Scholar 

  • Hall AA, Gurr SJ (2000) Initiation of appressorial germ tube differentiation and appressorial hooking: distinct morphological events regulated by cAMP signalling in Blumeria graminis f. sp. hordei. Physiol Mol Plant Pathol 56:39–46

    Article  CAS  Google Scholar 

  • Hall AA, Bindslev L, Rouster J, Rasmussen SW, Oliver RP, Gurr SJ (1999) Involvement of cAMP and protein kinase A in conidial differentiation by Erysiphe graminis f. sp. hordei. Mol Plant Microbe Interact 12(11):960–968

    Article  CAS  PubMed  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(4):1039–1054

    Article  CAS  PubMed  Google Scholar 

  • Hansjakob A, Riederer M, Hildebrandt U (2011) Wax matters: absence of very-long-chain aldehydes from the leaf cuticular wax of the glossy11 mutant of maize compromises the prepenetration processes of Blumeria graminis. Plant Pathol 60(6):1151–1161

    Article  CAS  Google Scholar 

  • Hardham AR, Jones DA, Takemoto D (2007) Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10:342–348

    Article  CAS  PubMed  Google Scholar 

  • Hemetsberger C, Mueller AN, Matei A, Herrberger C, Hensel G, Kumlehn J, Doehlemann G (2015) The fungal core effector Pep1 is conserved across smuts of dicots and monocots. New Phytol 206(3):1116–1126

    Article  CAS  PubMed  Google Scholar 

  • Heringa RJ, Norei AV, Tazelaar MF (1969) Resistance to powdery mildew (Erysiphe polygoni D.C.) in peas (Pisum sativum L.). Euphytica 18:163–169

    Article  Google Scholar 

  • Hirata T, Takamatsu S (1996) Nucleotide sequence diversity of rDNA internal transcribed spacers extracted from conidia and cleistothecia from several powdery mildew fungi. Mycoscience 37:283–288

    Article  Google Scholar 

  • Hoefle C, Huckelhoven R (2008) Enemy at the gates: traffic at the plant cell pathogen interface. Cell Microbiol 10:2400–2407

    Article  CAS  PubMed  Google Scholar 

  • Hoefle C, Huesmann C, Schultheiss H, Börnke F, Hensel G, Kumlehn J, Hückelhoven R (2011) A barley ROP GTPase ACTIVATING PROTEIN associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 23(6):2422–2439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu G, Kamp A, Linning R, Naik S, Bakkeren G (2007) Complementation of Ustilagomaydis MAPK mutants by a wheat leaf rust, Puccinia triticina homolog: potential for functional analyses of rust genes. Mol Plant Microbe Interact 20(6):637–647

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Liang Y, Zhang M, Tan F, Zhong S, Li X, Gong G, Chang X, Shang J, Tang S, Li T, Luo P (2018) Comparative transcriptome profiling of Blumeria graminis f. sp. tritici during compatible and incompatible interactions with sister wheat lines carrying and lacking Pm40. PLoS One 13(7):e0198891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huckelhoven R (2005) Powdery mildew susceptibility and biotrophic infection strategies. FEMS Microbiol Lett 245:9–17

    Article  CAS  PubMed  Google Scholar 

  • Hückelhoven R, Kogel K-H (1998) Tissue-specific superoxide generation at interaction sites in resistant and susceptible near-isogenic barley lines attacked by the powdery mildew fungus (Erysiphe graminis f. sp. hordei). Mol Plant Microbe Interact 11:292–300

    Article  Google Scholar 

  • Huckelhoven R, Fodor J, Preis C, Kogel KH (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with H2O2 but not with salicylic acid accumulation. Plant Physiol 119:1251–1260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huckelhoven R, Dechert C, Kogel K-H (2003) Overexpression of barley BAX inhibitor 1 induces breakdown of mlo mediated penetration resistance to Blumeria graminis. Proc Natl Acad Sci U S A 100:5555–5560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Humphry M, Consonni C, Panstruga R (2006) mlo-based powdery mildew immunity: silver bullet or simply nonhost resistance? Mol Plant Pathol 7:605–610

    Article  PubMed  Google Scholar 

  • Humphry M, Reinstadler A, Ivanov S, Bisseling T, Panstruga R (2011) Durable broad-spectrum powdery mildew resistance in pea er1 plants is conferred by natural loss-of-function mutations in PsMLO1. Mol Plant Pathol 12(9):866–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurkman WJ, Tanaka CK (1996) Germin gene expression is induced in wheat leaves by powdery mildew infection. Plant Physiol 111:735–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang I, Robinson DG (2009) Transport vesicle formation in plant cells. Curr Opin Plant Biol 12(6):660–669

    Article  CAS  PubMed  Google Scholar 

  • Hyde KD (1988) Studies on the tropical marine fungi of Brunei. Bot J Linnean Soc 98(2):135–151

    Article  Google Scholar 

  • Idnurm A, Howlett BJ (2001) Pathogenicity genes of phytopathogenic fungi. Mol Plant Pathol 2(4):241–255

    Article  CAS  PubMed  Google Scholar 

  • Iyer-Pascuzzi AS, McCouch SR (2007) Recessive resistance genes and the Oryza sativa-Xanthomonas oryzae pv. oryzae pathosystem. Mol Plant Microbe Interact 20:731–739

    Article  CAS  PubMed  Google Scholar 

  • Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853–1856

    Article  CAS  PubMed  Google Scholar 

  • Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:2503–2513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19(15):4004–4014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jones L, Riaz S, Morales-Cruz A, Amrine KC, McGuire B, Gubler WD, Walker MA, Cantu D (2014) Adaptive genomic structural variation in the grape powdery mildew pathogen, Erysiphe necator. BMC Genomics 15(1):1081

    Article  PubMed  PubMed Central  Google Scholar 

  • Jørgensen JH (1994) Genetics of powdery mildew resistance in barley. Crit Rev Plant Sci 13:97–119

    Article  Google Scholar 

  • Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42:392–405

    Article  CAS  PubMed  Google Scholar 

  • Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330(6006):968–971

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kinane J, Oliver RP (2003) Evidence that the appressorial development in barley powdery mildew is controlled by MAP kinase activity in conjunction with the cAMP pathway. Fungal Genet Biol 39(1):94–102

    Article  CAS  PubMed  Google Scholar 

  • Kinane J, Dalvin S, Bindslev L, Hall A, Gurr S, Oliver R (2000) Evidence that the cAMP pathway controls emergence of both primary and appressorial germ tubes of barley powdery mildew. Mol Plant Microbe Interact 13(5):494–502

    Article  CAS  PubMed  Google Scholar 

  • Kirik MM, Kitsno VO, Basyuk GF (1974) The role of redox enzymes in the resistance of pea to Erysiphe polygoni DC. Nauk Pr Ukr Sils KogospodAkad 84:198–201

    CAS  Google Scholar 

  • Kiyosawa S, Mackill DS, Bonman JM, Tanak Y, Ling ZZ (1986) An attempt of classification of world’s rice varieties based on reaction pattern to blast fungus strains. Bull Natl Inst Agrobiol Resour 2:13–39

    Google Scholar 

  • Kobayshi I, Tanaka C, Yamoka N, Kunoh H (1991) Morphogenesis of Erysiphe graminis conidia on artificial membranes. Trans Mycol Soc Jpn 32:187–198

    Google Scholar 

  • Koch E, Slusarenko A (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2(5):437–445

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kohorn BD, Kohorn SL (2012) The cell wall associated kinases, WAKs, as pectin receptors. Front Plant Sci 3:88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kooman-Gersmann M, Honée G, Bonnema G, De Wit PJGM (1996) A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants. Plant Cell 8:929–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulkarni RD, Thon MR, Pan H, Dean RA (2005) Novel G–protein–coupled receptor–like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol 6:R24

    Article  PubMed  PubMed Central  Google Scholar 

  • Kusch S, Ahmadinejad N, Panstruga R, Kuhn H (2014) In silico analysis of the core signaling proteome from the barley powdery mildew pathogen (Blumeria graminis f. sp. hordei). BMC Genomics 15(1):843

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Biol 48(1):251–275

    Article  CAS  Google Scholar 

  • Lawrence GJ, Mayo GME, Shepherd KW (1981) Interactions between genes controlling pathogenicity in the flax rust fungus. Phytopathology 71:12–19

    Article  Google Scholar 

  • Leister RT, Ausubel FM, Katagiri F (1996) Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc Natl Acad Sci U S A 93:15497–15502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Wright SJ, Krystofova S, Park G, Borkovich KA (2007) Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol 61:423–452

    Article  CAS  PubMed  Google Scholar 

  • Li W, Wang B, Wu J, Lu G, Hu Y, Zhang X, Wang Z (2009) The Magnaporthe oryzaea virulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol Plant Microbe Interact 22(4):411–420

    Article  CAS  PubMed  Google Scholar 

  • Liang S, Wang ZY, Liu PJ, Li DB (2006) A Gγ subunit promoter T-DNA insertion mutant A1-412 of Magnaporthe grisea is defective in appressorium formation, penetration and pathogenicity (Chinese). Chin Sci Bull 51:2037–2040

    Article  Google Scholar 

  • Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F (2005) Pre-and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310(5751):1180–1183

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Dean RA (1997) G protein α subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol Plant Microbe Interact 10(9):1075–1086

    Article  CAS  PubMed  Google Scholar 

  • Liu T, Liu Z, Song C, Hu Y, Han Z, She J, Zhou JM (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336(6085):1160–1164

    Article  CAS  PubMed  Google Scholar 

  • Lo SCC, Hipskind JD, Nicholson RL (1999) cDNA cloning of a sorghum pathogenesis-related protein (PR-10) and differential expression of defense-related genes following inoculation with Cochio bolus heterostrophus or Colletotrichum sublineolum. Mol Plant Microbe Interact 12:479–489

    Article  CAS  PubMed  Google Scholar 

  • Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54(2):263–272

    Article  CAS  PubMed  Google Scholar 

  • Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436

    Article  CAS  PubMed  Google Scholar 

  • Mehrabi R, Zhao X, Kim Y, Xu JR (2009) The cAMP signaling and MAP kinase pathways in plant pathogenic fungi. Plant Relationsh:157–172

    Google Scholar 

  • Mey G, Held K, Scheffer J, Tenberge KB, Tudzynski P (2002) CPMK2, an SLT2-homologous mitogen-activated protein (MAP) kinase, is essential for pathogenesis of Claviceps purpurea on rye: evidence for a second conserved pathogenesis-related MAP kinase cascade in phytopathogenic fungi. Mol Microbiol 46:305–318

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mohapatra C, Chand R, Navathe S, Sharma S (2016) Histo-chemical and biochemical analysis reveals association of er1 mediated powdery mildew resistance and redox balance in pea. Plant Physiol Biochem 106:54–63

    Article  CAS  PubMed  Google Scholar 

  • Monteiro S, Barakat M, Piçarra-Pereira MA, Teixeira AR, Ferreira RB (2003) Osmotin and thaumatin from grape: a putative general defense mechanism against pathogenic fungi. Phytopathology 93:1505–1512

    Article  CAS  PubMed  Google Scholar 

  • Morales M, Orjeda G, Nieto C, van Leeuwen H, Monfort A, Charpentier M, Caboche M, Arus P, Puigdomenech P, Aranda MA, Dogimont C, Bendahmane A, Garcia-Mas J (2005) A physical map covering the nsv locus that confers resistance to Melon necrotic spot virus in melon (Cucumis melo L.). Theor Appl Genet 111:914–922

    Article  CAS  PubMed  Google Scholar 

  • Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interaction transcriptome analysis identifies Magnaportheoryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21(4):1273–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, andPevzner SJ (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333(6042):596–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narsinghani VG (1979) Inheritance of powdery mildew in peas (Pisum sativum L.). Indian J Horticult 36(4):471–472

    Google Scholar 

  • Nathues E, Joshi S, Tenberge KB, von den Driesch M, Oeser B, Bäumer N, Tudzynski P (2004) CPTF1, a CREB-like transcription factor, is involved in the oxidative stress response in the phytopathogen, Claviceps purpurea and modulates ROS level in its host Secale cereale. Mol Plant Microbe Interact 17(4):383–393

    Article  CAS  PubMed  Google Scholar 

  • Nicaise V, German-Retana S, Sanjuán R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, LeGall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol 132(3):1272–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomenech P, Pitrat M, Caboche M, Dogimont C, Garcia Mas J (2006) An eIF4E allele confers resistance to an uncapped and non polyadenylated RNA virus in melon. Plant J 48(3):452–462

    Article  CAS  PubMed  Google Scholar 

  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972

    Article  CAS  PubMed  Google Scholar 

  • Nomura K, Melotto M, He SY (2005) Suppression of host defense in compatible plant–Pseudomonas syringae interactions. Curr Opin Plant Biol 8(4):361–368

    Article  CAS  PubMed  Google Scholar 

  • Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–3141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nurnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266

    Article  PubMed  Google Scholar 

  • Oliver R, Osbourn A (1995) Molecular dissection of fungal phytopathogenicity. Microbiology 141(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6(4):320–326

    Article  CAS  PubMed  Google Scholar 

  • Panstruga R (2005) Discovery of novel conserved peptide domains by ortholog comparison within plant multi-protein families. Plant Mol Biol 59(3):485–500

    Article  CAS  PubMed  Google Scholar 

  • Patykowski J, Urbanek H (2003) Activity of enzymes related to H2O2 generation and metabolism in leaf apoplastic fraction of tomato leaves infected with Botrytis cinerea. J Phytopathol 151:153–161

    Article  CAS  Google Scholar 

  • Pavan S, Schiavulli A, Appiano M, Marcotrigiano AR, Cillo F, Visser RG, Bai Y, Lotti C, Ricciardi L (2011) Pea powdery mildew er1 resistance is associated to loss-of-function mutations at a MLO homologous locus. Theor Appl Genet 123(8):1425–1431

    Article  PubMed  Google Scholar 

  • Pedersen C, van Themaat EVL, McGuffin LJ, Abbott JC, Burgis TA, Barton G, Cramer R (2012) Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13(1):694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pennington HG, Gheorghe DM, Damerum A, Pliego C, Spanu PD, Cramer R, Bindschedler LV (2016) Interactions between the powdery mildew effector BEC1054 and barley proteins identify candidate host targets. J Proteome Res 15(3):826–839

    Article  CAS  PubMed  Google Scholar 

  • Peterhansel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze-Lefert P (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9:1397–1409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CM, Leon-Reyes A, van der Ent S, van Wees SC (2009) Networking by small molecule hormones in plant immunity. Nat Chem Biol 5:3

    Article  CAS  Google Scholar 

  • Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129:1076–1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D’Hont A, Hollricher K, Jorgensen JH, Schulze-Lefert P, Panstruga R (2004) A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430:887–889

    Article  CAS  PubMed  Google Scholar 

  • Pliego C, Nowara D, Bonciani G, Gheorghe DM, Xu R, Surana P, Schweizer P (2013) Host-induced gene silencing in barley powdery mildew reveals a class of ribonuclease-like effectors. Mol Plant Microbe Interact 26(6):633–642

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Quentin M, Abad P, Favery B (2013) Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Front Plant Sci 4:53

    Article  PubMed  PubMed Central  Google Scholar 

  • Rakotomalala M, Pinel-Galzi A, Albar L, Ghesquiere A, Rabenantoandro Y, Ramavovololona P, Fargette D (2008) Resistance to rice yellow mottle virus in rice germplasm in Madagascar. Eur J Plant Pathol 122:277–286

    Article  Google Scholar 

  • Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JD, Brown JK (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18(9):2402–2414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rispail N, Di Pietro A (2009) Fusarium oxysporum Ste12 controls invasive growth and virulence downstream of the Fmk1 MAPK cascade. Mol Plant Microbe Interact 22:830–839

    Article  CAS  PubMed  Google Scholar 

  • Rivas S, Romeis T, Jones JDG (2002) The Cf-9 disease resistance protein is present in an similar to 420-kilodalton heteromultimeric membrane-associated complex at one molecule per complex. Plant Cell 14:689–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45

    Article  CAS  PubMed  Google Scholar 

  • Robatzek S (2007) Vesicle trafficking in plant immune responses. Cell Microbiol 9:1–8

    Article  CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379

    Article  CAS  PubMed  Google Scholar 

  • Rooney HCE (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance (vol 308, pg 1783, 2005). Science 310(5745):54

    Article  Google Scholar 

  • Sacristán S, Vigouroux M, Pedersen C, Skamnioti P, Thordal-Christensen H, Micali C et al (2009) Coevolution between a family of parasite virulence effectors and a class of LINE-1 retrotransposons. PLoS One 4(10):e7463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141(2):336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salmeron JM, Barker SJ, Carland FM, Mehta AY, Staskawicz BJ (1994) Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell 6:511–520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schaeffer HJ, Weber MJ (1999) Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol 19(4):2435–2444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheffer J, Chen C, Heidrich P, Dickman MB, Tudzynski P (2005) A CDC42 homologue in Claviceps purpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryotic Cell 4(7):1228–1238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schiff CL, Wilson IW, Somerville SC (2001) Polygenic powdery mildew disease resistance in Arabidopsis thaliana: quantitative trait analysis of the accession Warschau-1. Plant Pathol 50:690–701

    Article  CAS  Google Scholar 

  • Schultheiss H, Dechert C, Kogel KH, Hückelhoven R (2002) A small GTP-binding host protein is required for entry of powdery mildew fungus into epidermal cells of barley. Plant Physiol 128(4):1447–1454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schultheiss H, Dechert C, Kogel KH, Hückelhoven R (2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J 36(5):589–601

    Article  CAS  PubMed  Google Scholar 

  • Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41:641–667

    Article  CAS  PubMed  Google Scholar 

  • Schweizer P, Pokorny J, Schulze-Lefert P, Dudler R (2000) Double-stranded RNA interference with gene function at the single-cell level in cereals. Plant J 24:895–903

    Article  CAS  PubMed  Google Scholar 

  • Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, Michelmore RW, Staskawicz BJ (1996) Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274:2063–2065

    Article  CAS  PubMed  Google Scholar 

  • Seong K, Hou Z, Tracy M, Kistler HC, Xu JR (2005) Random insertional mutagenesis identifies genes associated with virulence in the wheat scab fungus Fusarium graminearum. Phytopathology 95(7):744–750

    Article  CAS  PubMed  Google Scholar 

  • Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4(1):17–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi A, Mmbaga MT (2006) Perpetuation of powdery mildew infection and identification of Erysiphe australiana as the crape myrtle pathogen in mid-Tennessee. Plant Dis 90(8):1098

    Article  PubMed  Google Scholar 

  • Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64(2):204–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva-Gomesa S, Decouta A, Nigoua J (2014) Pathogen-associated molecular patterns (PAMPs). In: Parnham M (ed) Encyclopedia of inflammatory diseases. Springer, Basel, pp 1–16

    Google Scholar 

  • Smart CD, Myers KL, Restrepo S, Martin GB, Fry WE (2003) Partial resistance of tomato to Phytophthora infestans is not dependent upon ethylene, jasmonic acid, or salicylic acid signaling pathways. Mol Plant Microbe Interact 16(2):141–148

    Article  CAS  PubMed  Google Scholar 

  • Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stüber K, Lebrun MH (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330(6010):1543–1546

    Article  CAS  PubMed  Google Scholar 

  • Speth EB, Lee YN, He SY (2007) Pathogen virulence factors as molecular probes of basic plant cellular functions. Curr Opin Plant Biol 10(6):580–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein M, Dittgen J, Sánchez-Rodríguez 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stergiopoulos I, de Wit PJ (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263

    Article  CAS  PubMed  Google Scholar 

  • Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, Valent B (1995) Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7:1221

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tak H, Mhatre M (2013) Molecular characterization of VvSDIR1 from Vitis vinifera and its functional analysis by heterologous expression in Nicotiana tabacum. Protoplasma 250(2):565–576

    Article  CAS  PubMed  Google Scholar 

  • Takamatsu S (2004) Phylogeny and evolution of the powdery mildew fungi (Erysiphales, Ascomycota) inferred from nuclear ribosomal DNA sequences. Mycoscience 45(2):147–157

    Article  CAS  Google Scholar 

  • Tang D, Innes RW (2002) Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J 32(6):975–983

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060–2063

    Article  CAS  PubMed  Google Scholar 

  • Thomma BP, Nürnberger T, Joosten MH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell Online 23(1):4–15

    Article  CAS  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11(6):1187–1194

    Article  CAS  Google Scholar 

  • Tiwari KR, Penner GA, Warkentin TD (1997) Inheritance of powdery mildew resistance in pea. Can J Plant Sci 77:307–310

    Article  Google Scholar 

  • Tiwari KR, Penner GA, Warkentin TD (1998) Identification of powdery mildew resistance in pea. Can J Plant Sci 77:307–310

    Article  Google Scholar 

  • Trujillo M, Troeger M, Niks RE, Kogel KH, Huckelhoven R (2004) Mechanistic and genetic overlap of barley host and non host resistance to Blumeria graminis. Mol Plant Pathol 5(5):389–396

    Article  CAS  PubMed  Google Scholar 

  • Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci U S A 104:1075–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyrka M, Perovic D, Wardynska A, Ordon F (2008) A new diagnostic SSR marker for selection of the Rym4/Rym5 locus in barley breeding. J Appl Genet 49:127–134

    Article  PubMed  Google Scholar 

  • Underwood W, Somerville SC (2008) Focal accumulation of defences at sites of fungal pathogen attack. J Exp Bot 59:3501–3508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urban M, Bhargava T, Hamer JE (1999) An ATP driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J 18(3):512–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaid A, Tyagi PD (1997) Genetics of powdery mildew resistance in pea. Euphytica 96(2):203–206

    Article  Google Scholar 

  • Van Den Burg HA, Westerink N, Francoijs KJ, Roth R, Woestenenk E (2003) Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability. J Biol Chem 278:27340

    Article  CAS  PubMed  Google Scholar 

  • Van der Hoorn RAL, Kamoun S (2008) From guardee to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Várallyay É, Giczey G, Burgyán J (2012) Virus-induced gene silencing of Mlo genes induces powdery mildew resistance in Triticum aestivum. Arch Virol 157(7):1345–1350

    Article  CAS  PubMed  Google Scholar 

  • Viaud MC, Balhadère PV, Talbot NJ (2002) A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell 14(4):917–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vivancos P, de Simone A, Kiddle G, Foyer CH (2015) Glutathione-linking cell proliferation to oxidative stress. Free Radic Biol Med 89:1154–1164

    Article  CAS  Google Scholar 

  • Vleeshouwers VG, Oliver RP (2014) Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens. Mol Plant Microbe Interact 27(3):196–206

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogel JP, Raab TK, Somerville CR, Somerville SC (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J. 40:968–978

    Article  CAS  PubMed  Google Scholar 

  • von Röpenack E, Parr A, Schulze-Lefert P (1998) Structural analyses and dynamics of soluble and cell wall-bound phenolics in a broad spectrum resistance to the powdery mildew fungus in barley. J Biol Chem 272:9013–9022

    Article  Google Scholar 

  • Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20(2):471–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang ZY, Thornton CR, Kershaw MJ, Debao L, Talbot NJ (2003) The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol 47(6):1601–1612

    Article  CAS  PubMed  Google Scholar 

  • Wei F, Gobelman-Werner K, Morroll SM, Kurth J, Mao L, Wing R, Leister D, Schulze-Lefert P, Wise RP (1999) The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. Genetics 153(4):1929–1948

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wen Y, Wang X, Xiao S, Wang Y (2012) Ectopic expression of VpALDH2B4, a novel aldehyde dehydrogenase gene from Chinese wild grapevine (Vitispseudoreticulata), enhances resistance to mildew pathogen sand salt stress in Arabidopsis. Planta 236:525–539

    Article  CAS  PubMed  Google Scholar 

  • Weng K, Li ZQ, Liu RQ, Wang L, Wang YJ, Xu Y (2014) Transcriptome of Erysiphe necator-infected Vitispseudoreticulata leaves provides insight into grapevine resistance to powdery mildew. Horticult Res 1:14049

    Article  CAS  Google Scholar 

  • Weßling R, Epple P, Altmann S, He Y, Yang L, Henz SR, Mukhtar MS (2014) Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16(3):364–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whipps JM, Budge SP, Fenlon JS (1998) Characteristics and host range of tomato powdery mildew. Plant Pathol 47(1):36–48

    Article  Google Scholar 

  • Wicker T, Oberhaensli S, Parlange F, Buchmann JP, Shatalina M, Roffler S, Spanu PD (2013) The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat Genet 45(9):1092–1096

    Article  CAS  PubMed  Google Scholar 

  • Wilson IW, Schiff CL, Hughes DE, Somerville SC (2001) Quantitative trait loci analysis of powdery mildew disease resistance in the Arabidopsis thaliana accession kashmir-1. Genetics 158:1301–1309

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wladimir I, Tameling L, Takken FLW (2008) Resistance proteins: scout of the plant innate immune system. Eur J Plant Pathol 121:243–255

    Article  Google Scholar 

  • Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40(1):251–285

    Article  CAS  PubMed  Google Scholar 

  • Wolter M, Hollricher K, Salamini F, Schulze-Lefert P (1993) The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol Gen Genet 239(1–2):122–128

    Article  CAS  PubMed  Google Scholar 

  • Xiao SY, Ellwood S, Findlay K, Oliver RP, Turner JG (1997) Characterization of three loci controlling resistance of Arabidopsis thaliana accession Ms-0 to two powdery mildew diseases. Plant J 12:757–768

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120

    Article  CAS  PubMed  Google Scholar 

  • Xu JR (2000) MAP kinases in fungal pathogens. Fungal Genet Biol 31(3):137–152

    Article  CAS  PubMed  Google Scholar 

  • Xu JR, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10:2696–2706

    Article  CAS  PubMed  Google Scholar 

  • Xu JR, Urban M, Sweigard JA, Hamer JE (1997) The CPKA gene of Magnaporthe grisea is essential for appressorial penetration. Mol Plant Microbe Interact 10(2):187–194

    Article  CAS  Google Scholar 

  • Xu W, Yu Y, Ding J, Hua Z, Wang Y (2010) Characterization of a novel stilbene synthase promoter involved in pathogen-and stress-inducible expression from Chinese wild Vitispseudoreticulata. Planta 231:475–487

    Article  CAS  PubMed  Google Scholar 

  • Xu TF, Zhao XC, Jiao YT, Wei JY, Wang L, Xu Y (2014) A pathogenesis related protein, VpPR-10.1, from Vitispseudoreticulata: an insight of its mode of antifungal activity. PLoS ONE 9:e95102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue CY, Park G, Choi WB, Zheng L, Dean RA, Xu JR (2002) Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14:2107–2119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue C, Hsueh YP, Heitman J (2008) Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32(6):1010–1032

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Wang W, Coleman M, Orgil U, Feng J, Ma X, Ferl R, Turner JG, Xiao S (2009) Arabidopsis 14-3-3 lambda is a positive regulator of RPW8-mediated disease resistance. Plant J 60(3):539–550

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Shi Y, Ma J, Correll J, Evans M, Motes D, Xiong H, Weng Y, Qin J (2018) Identification of the pathogen Podosphaeraerigerontis-canadensis causing powdery mildew disease on dandelion (Taraxacumofficinale) in US Arkansas state. Austral Plant Dis Notes 13:12

    Article  CAS  Google Scholar 

  • Yarwood CE (1957) Powdery mildews. Bot Rev 23:235–300

    Article  Google Scholar 

  • Yi HY, Wei Rong X, Shu Xiu L, Tao L, YueJin W (2011) Fusion expression and purificationof the transcription factor VpRFP1 gene resistance to Uncinulanecator from Chinese wild Vitispseudoreticulata and preparation of its polyclonal antibodies. J Agric Biotechnol 19:85–92

    Google Scholar 

  • Yu Y, Xu W, Wang S, Xu Y, Li HE, Wang Y, Li S (2011) VpRFP1, a novel C4C4-type RING finger protein gene from Chinese wild Vitispseudoreticulata, functions as a transcriptional activator in defence response of grapevine. J Exp Bot 62(15):5671–5682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Xu W, Wang J, Wang L, Yao W, Yang Y, Xu Y, Ma F, Du Y, Wang Y (2013) The Chinese wild grapevine (Vitispseudoreticulata) E3 ubiquitin ligase Erysiphe necator-induced RING finger protein 1 (EIRP1) activates plant defense responses by inducing proteolysis of the VpWRKY11 transcription factor. New Phytol 200(3):834–846

    Article  CAS  PubMed  Google Scholar 

  • Zeyen RJ, Carver TLW, Lyngkjaer MF (2002) Epidermal cell papillae. In: Bélanger RR, Bushnell WR, Dik AJ, Carver TLW (eds) The powdery mildews: a comprehensive treatise. APS, St. Paul, pp 107–124

    Google Scholar 

  • Zhai C, Lin F, Dong Z, He X, Yuan B, Zeng X, Wang L, Pan Q (2011) The isolation and characterization of Pik, a rice blast resistance gene which emerged after rice domestication. New Phytol 189:321–334

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Gurr SJ (2001) Expression and sequence analysis of the Blumeria graminis mitogen-activated protein kinase genes, mpk1 and mpk2. Gene 266:57–65

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Collinge DB, Thordal-Christensen H (1995) Germin like oxalate oxidase, a H2O2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J 8:139–145

    Article  CAS  Google Scholar 

  • Zhang Z, Priddey G, Gurr SJ (2001) The barley powdery mildew protein kinase C gene, pkc1 and pkc-like gene, are differentially expressed during morphogenesis. Mol Plant Pathol 2(6):327–337

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Henderson C, Gurr SJ (2004) Blumeria graminis secretes an extracellular catalase during infection of barley: potential role in suppression of host defence. Mol Plant Pathol 5(6):537–547

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Henderson C, Perfect E, Carver TLW, Thomas BJ, Skamnioti P, Gurr SJ (2005) Of genes and genomes, needles and haystacks: Blumeria graminis and functionality. Mol Plant Pathol 6(5):561–575

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Tang W, Liu K, Huang Q, Zhang X, Yan X, Chen Y, Wang J, Qi Z, Wang Z, Zheng X (2011) Eight RGS and RGS-like proteins orchestrate growth, differentiation, and pathogenicity of Magnaportheoryzae. PLoS Pathogens 7(12):e1002450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang WJ, Pedersen C, Kwaaitaal M, Gregersen PL, Mørch SM, Hanisch S, Kristensen A, Fuglsang AT, Collinge DB, Thordal-Christensen H (2012a) Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Mol Plant Pathol 13(9):1110–1119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Wu Y, Gao M, Zhang J, Kong Q, Liu Y, Zhang Y (2012b) Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11(3):253–263

    Article  CAS  PubMed  Google Scholar 

  • Zheng Z, Nonomura T, Appiano M, Pavan S, Matsuda Y, Toyoda H, Wolters AMA, Visser RG, Bai Y (2013) Loss of function in Mlo orthologs reduces susceptibility of pepper and tomato to powdery mildew disease caused by Leveillulataurica. PloS One 8(7):e70723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou JM, Chai J (2008a) Plant pathogenic bacterial type III effectors subdue host responses. Curr Opin Microbiol 11(2):179–185

    Article  CAS  PubMed  Google Scholar 

  • Zhou JM, Chai J (2008b) Plant pathogen bacterial type III effectors sub due host responses. Curr Opin Microbiol 11:179–185

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Shi J, Cao J, He M, Wang Y (2012) VpWRKY3, a biotic and abiotic stress-related transcription factor from the Chinese wild Vitispseudoreticulata. Plant Cell Rep 31(11):2109–2120

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Shi J, Xu W, Li H, He M, Xu Y, Xu T, Yang Y, Cao J, Wang Y (2013) Three ERF transcription factors from Chinese wild grapevine Vitispseudoreticulata participate in different biotic and abiotic stress-responsive pathways. J Plant Physiol 170(10):923–933

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q, Gao P, Wan Y, Cui H, Fan C, Liu S, Luan F (2018) Comparative transcriptome profiling of genes and pathways related to resistance against powdery mildew in two contrasting melon genotypes. Sci Horticult 227:169–180

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by Department of Science and Technology (DST; SR/SO/BB02/2010), Department of Biotechnology (DBT; BT/PR1264/PBD/16/848/2009), Universities with Potential for Excellence (UPE Phase II; UH/UGC/UPE Phase-2/Interface Studies/research projects/R-29). Facilities at UoH which include DBT-CREBB, DST-FIST, UGC-SAP, CIL, and Plant Culture Facility, Plant Sciences Facility at School of Life sciences are also acknowledged. Also, the authors acknowledge the financial support in the form of fellowship to SMB (DST-INSPIRE).

Conflict of interest: There is no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ragiba Makandar .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bhosle, S.M., Marathe, N., Makandar, R. (2020). Biological Host Response: A Paradigm and Strategy to Overcome Biotic Stress Caused by Powdery Mildew Causal Agents in Plants. In: Rakshit, A., Singh, H., Singh, A., Singh, U., Fraceto, L. (eds) New Frontiers in Stress Management for Durable Agriculture. Springer, Singapore. https://doi.org/10.1007/978-981-15-1322-0_22

Download citation

Publish with us

Policies and ethics