Identification of loci controlling non-host disease resistance in Arabidopsis against the leaf rust pathogen Puccinia triticina.

SUMMARY Plant immunity against the majority of microbial pathogens is conveyed by a phenomenon termed non-host resistance (NHR). This multifactorial trait provides durable protection against a given pathogen species. We investigated the molecular basis of NHR in Arabidopsis against the wheat leaf rust pathogen, Puccinia triticina (Ptr). Urediospores germinated with high efficiency and grew randomly over the Arabidopsis leaf surface. However, only 12% of urediospores produced a germ tube that successfully located a stoma and just 0.2% of urediospores went on to produce a haustorium within a penetrated mesophyll cell. Attempted Ptr infection induced the production of reactive oxygen intermediates (ROIs), nitric oxide (NO), salicylic acid (SA) and camalexin. The expression of SA, jasmonic acid (JA) and ROI-dependent genes was also detected. A series of well-characterized defence-related mutants were challenged with Ptr, but none of these lines exhibited significantly increased susceptibility to this fungus. Our findings also suggest that attempted Ptr infection triggers transient stomatal closure in Arabidopsis. We assessed the response of a collection of 79 geographically diverse Arabidopsis accessions to Ptr. Wa-1 plants supported a striking increase in Ptr substomatal vesicle frequency relative to all other tested accessions. Furthermore, SA and camalexin levels became elevated in Wa-1 plants relative to the Col reference line, in response to attempted Ptr infection. Additionally, the kinetics of SA-dependent gene expression was expedited in this accession relative to Col plants. To uncover the genetic architecture of NHR against Ptr, we assayed the response of the Arabidopsis Landsberg erecta (Ler) x Columbia (Col) recombinant inbred population to this fungus. Multiple small-to-medium effect quantitative trait loci were identified that govern the expression of NHR in Arabidopsis against Ptr.

[1]  M. Grant,et al.  Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates , 2007, Proceedings of the National Academy of Sciences.

[2]  Sheng Yang He,et al.  Plant Stomata Function in Innate Immunity against Bacterial Invasion , 2006, Cell.

[3]  Jörg Durner,et al.  Conserved requirement for a plant host cell protein in powdery mildew pathogenesis , 2006, Nature Genetics.

[4]  T. Boller,et al.  Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation , 2006, Cell.

[5]  G. Loake,et al.  S-nitrosylation: an emerging redox-based post-translational modification in plants. , 2006, Journal of experimental botany.

[6]  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.

[7]  C. Chevalier,et al.  Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. , 2006, Journal of experimental botany.

[8]  C. Wasternack,et al.  The Outcomes of Concentration-Specific Interactions between Salicylate and Jasmonate Signaling Include Synergy, Antagonism, and Oxidative Stress Leading to Cell Death , 2005, Plant Physiology.

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

[10]  Luca Comai,et al.  The advantages and disadvantages of being polyploid , 2005, Nature Reviews Genetics.

[11]  G. Loake,et al.  Cauliflower mosaic virus, a Compatible Pathogen of Arabidopsis, Engages Three Distinct Defense-Signaling Pathways and Activates Rapid Systemic Generation of Reactive Oxygen Species1 , 2005, Plant Physiology.

[12]  G. Loake,et al.  A central role for S-nitrosothiols in plant disease resistance , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  P. Schulze-Lefert,et al.  Recognition at a Distance , 2005, Science.

[14]  T. Hartung,et al.  Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Chen-Hung Kao,et al.  Multiple-Interval Mapping for Quantitative Trait Loci Controlling Endosperm Traits , 2004, Genetics.

[16]  S. Akira,et al.  Functions of toll-like receptors: lessons from KO mice. , 2004, Comptes rendus biologies.

[17]  Jonathan D. G. Jones,et al.  Bacterial disease resistance in Arabidopsis through flagellin perception , 2004, Nature.

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

[19]  J. Chory,et al.  Genomics tools for QTL analysis and gene discovery. , 2004, Current opinion in plant biology.

[20]  M. Aboul-Soud,et al.  Measurement of Salicylic Acid by a High-Performance Liquid Chromatography Procedure Based on Ion-Exchange , 2004, Chromatographia.

[21]  Lin Zhang,et al.  Isolation of genes expressed during compatible interactions between leaf rust (Puccinia triticina) and wheat using cDNA-AFLP. , 2003, Molecular plant pathology.

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

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

[24]  J. J. Grant,et al.  Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. , 2003, Molecular plant-microbe interactions : MPMI.

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

[26]  Frederick M Ausubel,et al.  Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. , 2003, The Plant journal : for cell and molecular biology.

[27]  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.

[28]  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.

[29]  J. Maloof QTL for plant growth and morphology. , 2003, Current opinion in plant biology.

[30]  Jonathan D. G. Jones,et al.  Arabidopsis RAR1 Exerts Rate-Limiting Control of R Gene–Mediated Defenses against Multiple Pathogens Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001040. , 2002, The Plant Cell Online.

[31]  Ken Shirasu,et al.  RAR1 and NDR1 Contribute Quantitatively to Disease Resistance in Arabidopsis, and Their Relative Contributions Are Dependent on the R Gene Assayed Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001032. , 2002, The Plant Cell Online.

[32]  M. Geisler,et al.  Variable timing of developmental progression in the stomatal pathway in Arabidopsis cotyledons. , 2002, The New phytologist.

[33]  Ken Shirasu,et al.  The RAR1 Interactor SGT1, an Essential Component of R Gene-Triggered Disease Resistance , 2002, Science.

[34]  M. C. Heath,et al.  H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. , 2002, The Plant journal : for cell and molecular biology.

[35]  Jonathan D. G. Jones,et al.  Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[37]  N. Read,et al.  Synergistic induction of wheat stem rust appressoria by chemical and topographical signals , 2001 .

[38]  J. J. Grant,et al.  Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. , 2000, The Plant journal : for cell and molecular biology.

[39]  S. Somerville,et al.  Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. J. Grant,et al.  Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. , 2000, Plant physiology.

[41]  M. C. Heath Nonhost resistance and nonspecific plant defenses. , 2000, Current opinion in plant biology.

[42]  T. Boller,et al.  FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. , 2000, Molecular cell.

[43]  J. Glazebrook,et al.  Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. , 2000, Molecular plant-microbe interactions : MPMI.

[44]  J. Glazebrook,et al.  Arabidopsis PAD3, a Gene Required for Camalexin Biosynthesis, Encodes a Putative Cytochrome P450 Monooxygenase , 1999, Plant Cell.

[45]  A. Osbourn,et al.  Compromised disease resistance in saponin-deficient plants. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Low,et al.  Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. , 1999, Plant physiology.

[47]  Z. Pretorius,et al.  Intercellular proteins and β‐1,3‐glucanase activity associated with leaf rust resistance in wheat , 1999 .

[48]  Jean-Pierre Métraux,et al.  Salicylic Acid Induction–Deficient Mutants of Arabidopsis Express PR-2 and PR-5 and Accumulate High Levels of Camalexin after Pathogen Inoculation , 1999, Plant Cell.

[49]  B. Thomma,et al.  Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. , 1999, The Plant journal : for cell and molecular biology.

[50]  Z. Zeng,et al.  Multiple interval mapping for quantitative trait loci. , 1999, Genetics.

[51]  R. Dixon,et al.  Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory , 1999, Current Biology.

[52]  Jonathan D. G. Jones,et al.  Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). , 1998, The Plant journal : for cell and molecular biology.

[53]  G. Hu,et al.  Scanning electron microscopy of early infection structure formation by Puccinia recondita f. sp. tritici on and in susceptible and resistant wheat lines , 1998 .

[54]  R. Dixon,et al.  A Plant Homolog of the Neutrophil NADPH Oxidase gp91phox Subunit Gene Encodes a Plasma Membrane Protein with Ca2+ Binding Motifs , 1998, Plant Cell.

[55]  T. Makishima,et al.  An Arabidopsis thaliana cDNA complementing a hamster apoptosis suppressor mutant. , 1997, The Plant journal : for cell and molecular biology.

[56]  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 .

[57]  D F Klessig,et al.  The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. , 1997, The Plant cell.

[58]  R. Dixon,et al.  THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE. , 1997, Annual review of plant physiology and plant molecular biology.

[59]  Jane Glazebrook,et al.  The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats , 1997, Cell.

[60]  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.

[61]  F. Ausubel,et al.  Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. , 1996, Genetics.

[62]  E. Ward,et al.  A Central Role of Salicylic Acid in Plant Disease Resistance , 1994, Science.

[63]  F. Ausubel,et al.  Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[64]  B. Feys,et al.  Arabidopsis Mutants Selected for Resistance to the Phytotoxin Coronatine Are Male Sterile, Insensitive to Methyl Jasmonate, and Resistant to a Bacterial Pathogen. , 1994, The Plant cell.

[65]  Z B Zeng,et al.  Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[66]  C. Lister,et al.  Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana , 1993 .

[67]  J. Ecker,et al.  Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. , 1992, Molecular plant-microbe interactions : MPMI.

[68]  S. Potter,et al.  Acquired resistance in Arabidopsis. , 1992, The Plant cell.

[69]  H. Grambow,et al.  The effect of morphogenically active factors from host and nonhost plants on the in vitro differentiation of infection structures of Puccinia graminis f. sp. tritici , 1977 .

[70]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[71]  D. Brown,et al.  The isolation of genes. , 1973, Scientific American.

[72]  P. Schulze-Lefert,et al.  Plant sciences. Recognition at a distance. , 2005, Science.

[73]  J. Glazebrook,et al.  Arabidopsis PAD 3 , a Gene Required for Camalexin Biosynthesis , Encodes a Putative Cytochrome P 450 Monooxygenase , 1999 .

[74]  M. Hahn,et al.  Morphogenesis and mechanisms of penetration by plant pathogenic fungi. , 1996, Annual review of phytopathology.

[75]  M. Gibson,et al.  Beyond ANOVA: Basics of Applied Statistics. , 1986 .