Identification and utilization of a sow thistle powdery mildew as a poorly adapted pathogen to dissect post-invasion non-host resistance mechanisms in Arabidopsis

To better dissect non-host resistance against haustorium-forming powdery mildew pathogens, a sow thistle powdery mildew isolate designated Golovinomyces cichoracearum UMSG1 that has largely overcome penetration resistance but is invariably stopped by post-invasion non-host resistance of Arabidopsis thaliana was identified. The post-invasion non-host resistance is mainly manifested as the formation of a callosic encasement of the haustorial complex (EHC) and hypersensitive response (HR), which appears to be controlled by both salicylic acid (SA)-dependent and SA-independent defence pathways, as supported by the susceptibility of the pad4/sid2 double mutant to the pathogen. While the broad-spectrum resistance protein RPW8.2 enhances post-penetration resistance against G. cichoracearum UCSC1, a well-adapted powdery mildew pathogen, RPW8.2, is dispensable for post-penetration resistance against G. cichoracearum UMSG1, and its specific targeting to the extrahaustorial membrane is physically blocked by the EHC, resulting in HR cell death. Taken together, the present work suggests an evolutionary scenario for the Arabidopsis–powdery mildew interaction: EHC formation is a conserved subcellular defence evolved in plants against haustorial invasion; well-adapted powdery mildew has evolved the ability to suppress EHC formation for parasitic growth and reproduction; RPW8.2 has evolved to enhance EHC formation, thereby conferring haustorium-targeted, broad-spectrum resistance at the post-invasion stage.

[1]  M. Gullino,et al.  First Report of Powdery Mildew Caused by Golovinomyces cichoracearum on Gerbera (Gerbera jamesonii) in Italy. , 2010, Plant disease.

[2]  Z.-P. Zhang,et al.  First Report of Grapevine leafroll-associated virus 4 and 5 in Grapevines in China. , 2010, Plant disease.

[3]  J. Glazebrook,et al.  Network Properties of Robust Immunity in Plants , 2009, PLoS genetics.

[4]  Yingqiang Wen,et al.  Specific Targeting of the Arabidopsis Resistance Protein RPW8.2 to the Interfacial Membrane Encasing the Fungal Haustorium Renders Broad-Spectrum Resistance to Powdery Mildew[W][OA] , 2009, The Plant Cell Online.

[5]  Pradeep Kachroo,et al.  Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. , 2009, PLoS genetics.

[6]  A. Gevens,et al.  First Report of Powdery Mildew Caused by Golovinomyces cichoracearum on Crotalaria juncea ('Tropic Sun' Sunn hemp). , 2009, Plant disease.

[7]  P. Schulze-Lefert,et al.  Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. , 2009, The Plant journal : for cell and molecular biology.

[8]  P. Schulze-Lefert,et al.  A Glucosinolate Metabolism Pathway in Living Plant Cells Mediates Broad-Spectrum Antifungal Defense , 2009, Science.

[9]  Frederick M. Ausubel,et al.  Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response , 2009, Science.

[10]  M. Gullino,et al.  Powdery Mildew Caused by Golovinomyces cichoracearum on Paris Daisy (Argyranthemum frutescens) in Italy. , 2008, Plant disease.

[11]  G. Jürgens,et al.  Co-option of a default secretory pathway for plant immune responses , 2008, Nature.

[12]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[13]  H. Araki,et al.  Intraspecific Genetic Variations, Fitness Cost and Benefit of RPW8, A Disease Resistance Locus in Arabidopsis thaliana , 2007, Genetics.

[14]  M. Newman,et al.  A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. , 2007, The Plant journal : for cell and molecular biology.

[15]  J. Botto,et al.  The plant cell , 2007, Plant Molecular Biology Reporter.

[16]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[17]  Joachim L Schultze,et al.  Salicylic Acid–Independent ENHANCED DISEASE SUSCEPTIBILITY1 Signaling in Arabidopsis Immunity and Cell Death Is Regulated by the Monooxygenase FMO1 and the Nudix Hydrolase NUDT7[W] , 2006, The Plant Cell Online.

[18]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[19]  Paul Schulze-Lefert,et al.  Arabidopsis PEN3/PDR8, an ATP Binding Cassette Transporter, Contributes to Nonhost Resistance to Inappropriate Pathogens That Enter by Direct Penetration[W][OA] , 2006, The Plant Cell Online.

[20]  Riyaz Bhat,et al.  Pre- and Postinvasion Defenses Both Contribute to Nonhost Resistance in Arabidopsis , 2005, Science.

[21]  J. Parker,et al.  The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[22]  K. Mendgen,et al.  Sequential deposition of plant glycoproteins and polysaccharides at the host-parasite interface ofUromyces vignae andVigna sinensis , 1995, Protoplasma.

[23]  P. Schulze-Lefert,et al.  Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[24]  Heather Youngs,et al.  The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. , 2004, Molecular biology of the cell.

[25]  J. Mansfield,et al.  Ultrastructural characterisation of pathogen development and host responses during compatible and incompatible interactions between Arabidopsis thaliana and Peronospora parasitica , 2004 .

[26]  L. Piater,et al.  Innate immunity in plants and animals: striking similarities and obvious differences , 2004, Immunological reviews.

[27]  Nicolai Strizhov,et al.  An Arabidopsis Callose Synthase, GSL5, Is Required for Wound and Papillary Callose Formation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016097. , 2003, The Plant Cell Online.

[28]  Erich Kombrink,et al.  SNARE-protein-mediated disease resistance at the plant cell wall , 2003, Nature.

[29]  Monica Stein,et al.  Loss of a Callose Synthase Results in Salicylic Acid-Dependent Disease Resistance , 2003, Science.

[30]  H. Thordal-Christensen.  Fresh insights into processes of nonhost resistance. , 2003, Current opinion in plant biology.

[31]  E. M. Soylu,et al.  Light and Electron Microscopy of the Compatible Interaction Between Arabidopsis and the Downy Mildew Pathogen Peronospora parasitica , 2003 .

[32]  G. Loake,et al.  Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. , 2003, The Plant journal : for cell and molecular biology.

[33]  M. C. Heath,et al.  An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. , 2003, Molecular plant-microbe interactions : MPMI.

[34]  James K. M. Brown,et al.  Genetic and forma specialis diversity in Blumeria graminis of cereals and its implications for host-pathogen co-evolution. , 2003, Molecular plant pathology.

[35]  C. Brearley,et al.  Enhanced Transcription of the Arabidopsis Disease Resistance Genes RPW8.1 and RPW8.2 via a Salicylic Acid–Dependent Amplification Circuit Is Required for Hypersensitive Cell Death Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006940. , 2003, The Plant Cell Online.

[36]  Beat Keller,et al.  The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway , 2002, Planta.

[37]  Frederick M. Ausubel,et al.  Isochorismate synthase is required to synthesize salicylic acid for plant defence , 2001, Nature.

[38]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[39]  N. Donofrio,et al.  Abnormal callose response phenotype and hypersusceptibility to Peronospoara parasitica in defence-compromised arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. , 2001, Molecular plant-microbe interactions : MPMI.

[40]  P. Schulze-Lefert,et al.  The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. , 2001, The Plant journal : for cell and molecular biology.

[41]  M. Coleman,et al.  Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. , 2001, Science.

[42]  S. Somerville,et al.  Comparison of Erysiphe cichoracearum and E. cruciferarum and a survey of 360 Arabidopsis thaliana accessions for resistance to these two powdery mildew pathogens. , 1999, Molecular plant-microbe interactions : MPMI.

[43]  F. Ausubel,et al.  Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. Ecker,et al.  EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. , 1999, Science.

[45]  Jonathan D. G. Jones,et al.  EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. Nicole,et al.  Cytochemical Aspects of the Plant–Rust Fungus Interface during the Compatible Interaction Coffea arabica (cv. Caturra)–Hemileiavastatrix (race III) , 1999, International Journal of Plant Sciences.

[47]  F. Ausubel,et al.  Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. , 1998, The Plant journal : for cell and molecular biology.

[48]  J. Parker,et al.  Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. Xie,et al.  COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. , 1998, Science.

[50]  David B. Collinge,et al.  Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction , 1997 .

[51]  J. Parker,et al.  Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. , 1996, The Plant cell.

[52]  S. Somerville,et al.  Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. , 1996, The Plant journal : for cell and molecular biology.

[53]  M. C. Heath,et al.  Nuclear behavior of the cowpea rust fungus during the early stages of basidiospore- or urediospore-derived growth in resistant or susceptible cowpea cultivars , 1996 .

[54]  M. C. Heath,et al.  Changes in the plant endomembrane system associated with callose synthesis during the interaction between cowpea (Vigna unguiculata) and the cowpea rust fungus (Uromyces vignae) , 1995 .

[55]  L. Hadwiger,et al.  Nonhost resistance genes and race-specific resistance. , 1993, Trends in microbiology.

[56]  C. Perumalla.  Effect of callose inhibition on haustorium formation by the cowpea rust fungus in the non-host, bean plant , 1989 .

[57]  J. Aist,et al.  Cell wall appositions and plant disease resistance: Acoustic microscopy of papillae that block fungal ingress. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Aist,et al.  Papillae and Related Wound Plugs of Plant Cells , 1976 .