A Post-Haustorial Defense Mechanism is Mediated by the Powdery Mildew Resistance Gene, PmG3M, Derived from Wild Emmer Wheat

The destructive wheat powdery mildew disease is caused by the fungal pathogen Blumeria graminis f. sp. tritici (Bgt). PmG3M, derived from wild emmer wheat Triticum dicoccoides accession G305-3M, is a major gene providing a wide-spectrum resistance against Bgt. PmG3M was previously mapped to wheat chromosome 6B using an F6 recombinant inbred line (RIL) mapping population generated by crossing G305-3M with the susceptible T. durum wheat cultivar Langdon (LDN). In the current study, we aimed to explore the defense mechanisms conferred by PmG3M against Bgt. Histopathology of fungal development was characterized in artificially inoculated leaves of G305-3M, LDN, and homozygous RILs using fluorescence and light microscopy. G305-3M exhibited H2O2 accumulation typical of a hypersensitive response, which resulted in programmed cell death (PCD) in Bgt-penetrated epidermal cells, while LDN showed well-developed colonies without PCD. In addition, we observed a post-haustorial resistance mechanism that arrested the development of fungal feeding structures and pathogen growth in both G305-3M and resistant RIL, while LDN and a susceptible RIL displayed fully developed digitated haustoria and massive accumulation of fungal biomass. In contrast, both G305-3M and LDN exhibited callose deposition in attempt to prevent fungal invasion, supporting this as a mechanism of a basal defense response not associated with PmG3M resistance mechanism per se. The presented results shed light on the resistance mechanisms conferred by PmG3M against wheat powdery mildew.

[1]  G. Coaker,et al.  Plant NLR-triggered immunity: from receptor activation to downstream signaling. , 2020, Current opinion in immunology.

[2]  C. Pozniak,et al.  Three previously characterized resistances to yellow rust are encoded by a single locus Wtk1 , 2020, bioRxiv.

[3]  A. Feechan,et al.  A Microbial Fermentation Mixture Primes for Resistance Against Powdery Mildew in Wheat , 2019, Front. Plant Sci..

[4]  T. Wicker,et al.  The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat , 2019, Nature Communications.

[5]  P. Schulze-Lefert,et al.  Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism , 2019, eLife.

[6]  B. Poinssot,et al.  The Cell Wall-Derived Xyloglucan Is a New DAMP Triggering Plant Immunity in Vitis vinifera and Arabidopsis thaliana , 2018, Front. Plant Sci..

[7]  L. Paulin,et al.  Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family , 2018, Nature Communications.

[8]  S. Whisson,et al.  The Phytophthora infestans Haustorium Is a Site for Secretion of Diverse Classes of Infection-Associated Proteins , 2018, mBio.

[9]  D. Tang,et al.  The NB-LRR gene Pm60 confers powdery mildew resistance in wheat. , 2018, The New phytologist.

[10]  A. Dinoor,et al.  Reciprocal Hosts' Responses to Powdery Mildew Isolates Originating from Domesticated Wheats and Their Wild Progenitor , 2018, Front. Plant Sci..

[11]  Cristiana T Argueso,et al.  Evolution of Hormone Signaling Networks in Plant Defense. , 2017, Annual review of phytopathology.

[12]  R. Panstruga,et al.  mlo-Based Resistance: An Apparently Universal "Weapon" to Defeat Powdery Mildew Disease. , 2017, Molecular plant-microbe interactions : MPMI.

[13]  D. Douchkov,et al.  Down-regulation of the glucan synthase-like 6 gene (HvGsl6) in barley leads to decreased callose accumulation and increased cell wall penetration by Blumeria graminis f. sp. hordei. , 2016, The New phytologist.

[14]  B. Keller,et al.  Molecular genetics and evolution of disease resistance in cereals. , 2016, The New phytologist.

[15]  M. Moscou,et al.  The development of quick, robust, quantitative phenotypic assays for describing the host–nonhost landscape to stripe rust , 2015, Front. Plant Sci..

[16]  T. Wicker,et al.  Multiple Avirulence Loci and Allele-Specific Effector Recognition Control the Pm3 Race-Specific Resistance of Wheat to Powdery Mildew[OPEN] , 2015, Plant Cell.

[17]  L. Kiss,et al.  New Insights into the Life Cycle of the Wheat Powdery Mildew: Direct Observation of Ascosporic Infection in Blumeria graminis f. sp. tritici. , 2015, Phytopathology.

[18]  Ying-ying Wang,et al.  Molecular characterization of a new powdery mildew resistance gene Pm54 in soft red winter wheat , 2015, Theoretical and Applied Genetics.

[19]  A. Korol,et al.  Genetic dissection of quantitative powdery mildew resistance loci in tetraploid wheat , 2014, Molecular Breeding.

[20]  Patrick Schweizer,et al.  Differential accumulation of callose, arabinoxylan and cellulose in nonpenetrated versus penetrated papillae on leaves of barley infected with Blumeria graminis f. sp. hordei. , 2014, The New phytologist.

[21]  Ming-Bo Wang,et al.  A simple method for comparing fungal biomass in infected plant tissues. , 2013, Molecular plant-microbe interactions : MPMI.

[22]  S. Somerville,et al.  Elevated Early Callose Deposition Results in Complete Penetration Resistance to Powdery Mildew in Arabidopsis1[C][W][OA] , 2013, Plant Physiology.

[23]  Liam J McGuffin,et al.  Structure and evolution of barley powdery mildew effector candidates , 2012, BMC Genomics.

[24]  A. Dinoor,et al.  Identification and characterization of a novel powdery mildew resistance gene PmG3M derived from wild emmer wheat, Triticum dicoccoides , 2012, Theoretical and Applied Genetics.

[25]  Pari Skamnioti,et al.  Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism , 2010, Science.

[26]  E. Ver Loren van Themaat,et al.  Tryptophan-Derived Metabolites Are Required for Antifungal Defense in the Arabidopsis mlo2 Mutant1[C][W][OA] , 2009, Plant Physiology.

[27]  Ming-shun Chen,et al.  Reactive Oxygen Species Are Involved in Plant Defense against a Gall Midge[C][W][OA] , 2009, Plant Physiology.

[28]  A. de Vicente,et al.  Comparative histochemical analyses of oxidative burst and cell wall reinforcement in compatible and incompatible melon-powdery mildew (Podosphaera fusca) interactions. , 2008, Journal of plant physiology.

[29]  D. Glawe,et al.  The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens. , 2008, Annual review of phytopathology.

[30]  S. V. Wees.  Phenotypic Analysis of Arabidopsis Mutants: Trypan Blue Stain for Fungi, Oomycetes, and Dead Plant Cells , 2008 .

[31]  R. Hückelhoven.  Cell wall-associated mechanisms of disease resistance and susceptibility. , 2007, Annual review of phytopathology.

[32]  S. Takamatsu,et al.  Multilocus phylogenetic analyses within Blumeria graminis, a powdery mildew fungus of cereals. , 2007, Molecular phylogenetics and evolution.

[33]  I. Somssich,et al.  Nuclear Activity of MLA Immune Receptors Links Isolate-Specific and Basal Disease-Resistance Responses , 2007, Science.

[34]  E. Prats,et al.  Stomatal lock-open, a consequence of epidermal cell death, follows transient suppression of stomatal opening in barley attacked by Blumeria graminis. , 2006, Journal of experimental botany.

[35]  P. Dodds,et al.  Haustorially Expressed Secreted Proteins from Flax Rust Are Highly Enriched for Avirulence Elicitors[W] , 2005, The Plant Cell Online.

[36]  M. Stumpf,et al.  Gene Expression Profiles of Blumeria graminis Indicate Dynamic Changes to Primary Metabolism during Development of an Obligate Biotrophic Pathogenw⃞ , 2005, The Plant Cell Online.

[37]  N. Huo,et al.  Comparative analysis of early H2O2 accumulation in compatible and incompatible wheat–powdery mildew interactions , 2005 .

[38]  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.

[39]  R. Mittler.  Oxidative stress, antioxidants and stress tolerance. , 2002, Trends in plant science.

[40]  A. Newton,et al.  The Barley mlo-gene: an important powdery mildew resistance source , 2000 .

[41]  M. Lyngkjær,et al.  Induced accessibility and inaccessibility to Blumeria graminis f.sp. hordei in barley epidermal cells attacked by a compatible isolate , 1999 .

[42]  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 .

[43]  F. Zeller,et al.  Evidence of allelism between genes Pm8 and Pm17 and chromosomal location of powdery mildew and leaf rust resistance genes in the common wheat cultivar‘Amigo' , 1997 .

[44]  Uwe Braun,et al.  The taxonomy of the powdery mildew fungi. , 2002 .

[45]  C. Campbell.  Disease progress in time: modelling and data analysis , 1998 .