Biphasic Gene Expression Changes Elicited by Phakopsora pachyrhizi in Soybean Correlate with Fungal Penetration and Haustoria Formation1[W][OA]

Inoculation of soybean (Glycine max) plants with Phakopsora pachyrhizi, the causal organism of Asian soybean rust, elicits a biphasic response characterized by a burst of differential gene expression in the first 12 h. A quiescent period occurs from 24 to 48 h after inoculation, in which P. pachyrhizi continues to develop but does not elicit strong host responses, followed by a second phase of intense gene expression. To correlate soybean responses with P. pachyrhizi growth and development, we inoculated the soybean cultivar Ankur (accession PI462312), which carries the Rpp3 resistance gene, with avirulent and virulent isolates of P. pachyrhizi. The avirulent isolate Hawaii 94-1 elicits hypersensitive cell death that limits fungal growth on Ankur and results in an incompatible response, while the virulent isolate Taiwan 80-2 grows extensively, sporulates profusely, and produces a compatible reaction. Inoculated leaves were collected over a 288-h time course for microarray analysis of soybean gene expression and microscopic analysis of P. pachyrhizi growth and development. The first burst in gene expression correlated with appressorium formation and penetration of epidermal cells, while the second burst of gene expression changes followed the onset of haustoria formation in both compatible and incompatible interactions. The proliferation of haustoria coincided with the inhibition of P. pachyrhizi growth in the incompatible interaction or the beginning of accelerated growth in the compatible interaction. The temporal relationships between P. pachyrhizi growth and host responses provide an important context in which to view interacting gene networks that mediate the outcomes of their interactions.

[1]  P. Keane,et al.  A modified method for clearing and staining leaf-infecting fungi in whole leaves , 1988, Australasian Plant Pathology.

[2]  P. Dodds,et al.  Co-evolutionary interactions between host resistance and pathogen effector genes in flax rust disease. , 2011, Molecular plant pathology.

[3]  D. Ort,et al.  Biotic stress globally downregulates photosynthesis genes. , 2010, Plant, cell & environment.

[4]  B. Matthews,et al.  Transcriptome analysis of a compatible response by Glycine max to Phakopsora pachyrhizi infection , 2010 .

[5]  G. Hartman,et al.  Identifying differentially expressed genes in leaves of Glycine tomentella in the presence of the fungal pathogen Phakopsora pachyrhizi , 2010, Planta.

[6]  David A Jones,et al.  Internalization of Flax Rust Avirulence Proteins into Flax and Tobacco Cells Can Occur in the Absence of the Pathogen[W] , 2010, Plant Cell.

[7]  K. Goellner,et al.  Phakopsora pachyrhizi, the causal agent of Asian soybean rust. , 2010, Molecular plant pathology.

[8]  T. Sakurai,et al.  Genome sequence of the palaeopolyploid soybean , 2010, Nature.

[9]  He Zhang,et al.  Computational identification of plant transcription factors and the construction of the PlantTFDB database. , 2010, Methods in molecular biology.

[10]  C. Gatz,et al.  Transcriptional Regulation of Plant Defense Responses , 2010 .

[11]  Jianlin Cheng,et al.  SoyDB: a knowledge database of soybean transcription factors , 2010, BMC Plant Biology.

[12]  G. Hartman,et al.  Transcriptome analysis of resistant and susceptible genotypes of Glycine tomentella during Phakopsora pachyrhizi infection reveals novel rust resistance genes , 2010, Theoretical and Applied Genetics.

[13]  Hao Wang,et al.  Antagonistic HLH/bHLH Transcription Factors Mediate Brassinosteroid Regulation of Cell Elongation and Plant Development in Rice and Arabidopsis[C][W][OA] , 2009, The Plant Cell Online.

[14]  P. D. de Wit,et al.  Fungal effector proteins. , 2009, Annual review of phytopathology.

[15]  M. Bolton.  Primary metabolism and plant defense--fuel for the fire. , 2009, Molecular plant-microbe interactions : MPMI.

[16]  M. Frank,et al.  Transgenic suppression of cell death limits penetration success of the soybean rust fungus Phakopsora pachyrhizi into epidermal cells of barley. , 2009, Phytopathology.

[17]  C. Gatz,et al.  Chapter 10 Transcriptional Regulation of Plant Defense Responses , 2009 .

[18]  P. Cregan,et al.  Bulked Segregant Analysis Using the GoldenGate Assay to Locate the Rpp3 Locus that Confers Resistance to Soybean Rust in Soybean , 2009 .

[19]  Jonathan D. G. Jones,et al.  Role of plant hormones in plant defence responses , 2009, Plant Molecular Biology.

[20]  M. Tollenaar,et al.  Mechanisms Involved in Soybean Rust-Induced Yield Reduction , 2008 .

[21]  M. Tollenaar,et al.  Impact of Phakopsora pachyrhizi Infection on Soybean Leaf Photosynthesis and Radiation Absorption , 2008 .

[22]  K. Goellner,et al.  Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. , 2008, Molecular plant-microbe interactions : MPMI.

[23]  G. Stacey,et al.  Chitin signaling and plant disease resistance , 2008, Plant signaling & behavior.

[24]  Matthew L Settles,et al.  Transcriptome analysis of high-temperature adult-plant resistance conditioned by Yr39 during the wheat-Puccinia striiformis f. sp. tritici interaction. , 2008, Molecular plant pathology.

[25]  L. Vieira,et al.  Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles , 2008, Theoretical and Applied Genetics.

[26]  B. Matthews,et al.  Expression patterns in soybean resistant to Phakopsora pachyrhizi reveal the importance of peroxidases and lipoxygenases , 2008, Functional & Integrative Genomics.

[27]  G. Stacey,et al.  A LysM Receptor-Like Kinase Plays a Critical Role in Chitin Signaling and Fungal Resistance in Arabidopsis[W][OA] , 2008, The Plant Cell Online.

[28]  Joshua S. Yuan,et al.  Differential expression of genes in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) is soybean growth stage-specific , 2008, Theoretical and Applied Genetics.

[29]  David Mackey,et al.  Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. , 2007, Annual review of phytopathology.

[30]  P. Dodds,et al.  Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. , 2007, Annual review of phytopathology.

[31]  P. Dodds,et al.  The role of secreted proteins in diseases of plants caused by rust, powdery mildew and smut fungi. , 2007, Current opinion in microbiology.

[32]  D. Nettleton,et al.  Distinct biphasic mRNA changes in response to Asian soybean rust infection. , 2007, Molecular plant-microbe interactions : MPMI.

[33]  P. Wincker,et al.  Transcript Profiling of Poplar Leaves upon Infection with Compatible and Incompatible Strains of the Foliar Rust Melampsora larici-populina1[W] , 2007, Plant Physiology.

[34]  D. V. Phillips,et al.  Mapping and Confirmation of the ‘Hyuuga’ Red-Brown Lesion Resistance Gene for Asian Soybean Rust , 2007 .

[35]  C. N. Stewart,et al.  Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage , 2007, Functional & Integrative Genomics.

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

[37]  David Mackey,et al.  MAMPs and MIMPs: proposed classifications for inducers of innate immunity , 2006, Molecular microbiology.

[38]  Dan Nettleton,et al.  A Discussion of Statistical Methods for Design and Analysis of Microarray Experiments for Plant Scientists , 2006, The Plant Cell Online.

[39]  B. Kobe,et al.  Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[40]  G. Hartman,et al.  Evaluation of Virulence of Phakopsora pachyrhizi and P. meibomiae Isolates. , 2006, Plant Disease.

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

[42]  G. Hartman,et al.  Breeding for Resistance to Soybean Rust. , 2005, Plant disease.

[43]  Alok J. Saldanha,et al.  Java Treeview - extensible visualization of microarray data , 2004, Bioinform..

[44]  S Miyano,et al.  Open source clustering software. , 2004, Bioinformatics.

[45]  S. Rhee,et al.  Functional Annotation of the Arabidopsis Genome Using Controlled Vocabularies1 , 2004, Plant Physiology.

[46]  T. Heitz,et al.  Metabolic reprogramming in plant innate immunity: the contributions of phenylpropanoid and oxylipin pathways , 2004, Immunological reviews.

[47]  Cathy H. Wu,et al.  UniProt: the Universal Protein knowledgebase , 2004, Nucleic Acids Res..

[48]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  K. Mendgen,et al.  Rust haustoria: nutrient uptake and beyond. , 2003, The New phytologist.

[50]  P. Khatri,et al.  Global functional profiling of gene expression ? ? This work was funded in part by a Sun Microsystem , 2003 .

[51]  W. Boerjan,et al.  Lignin biosynthesis. , 2003, Annual review of plant biology.

[52]  P. Khatri,et al.  Global functional profiling of gene expression. , 2003, Genomics.

[53]  B. Trevaskis,et al.  The soybean GmN6L gene encodes a late nodulin expressed in the infected zone of nitrogen-fixing nodules. , 2002, Molecular plant-microbe interactions : MPMI.

[54]  Alex E. Lash,et al.  Gene Expression Omnibus: NCBI gene expression and hybridization array data repository , 2002, Nucleic Acids Res..

[55]  R. Staples.  Nutrients for a rust fungus: the role of haustoria. , 2001, Trends in plant science.

[56]  R. Staples.  Research on the Rust Fungi During the Twentieth Century. , 2000, Annual review of phytopathology.

[57]  T. Meindl,et al.  The Bacterial Elicitor Flagellin Activates Its Receptor in Tomato Cells According to the Address–Message Concept , 2000, Plant Cell.

[58]  P. Schulze-Lefert,et al.  Closing the ranks to attack by powdery mildew. , 2000, Trends in plant science.

[59]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[60]  T. Boller,et al.  Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. , 1999, The Plant journal : for cell and molecular biology.

[61]  T. Boller,et al.  A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. , 1999, The Plant journal : for cell and molecular biology.

[62]  Gapped BLAST and PSI-BLAST: A new , 1997 .

[63]  V. Patil,et al.  VIABILITY OF UREDOSPORES OF PHAKOPSORA PACHYRHIZI SYD. AT DIFFERENT STORAGE CONDITIONS , 1997 .

[64]  P. J. Davies.  The Plant Hormones: Their Nature, Occurrence, and Functions , 1987 .

[65]  E. E. Hartwig.  Identification of a Fourth Major Gene Conferring Resistance to Soybean Rust1 , 1986 .

[66]  M. C. Heath.  Relationship Between Heat-Induced Fungal Death and Plant Necrosis in Compatible and Incompatible Interactions Involving the Bean and Cowpea Rust Fungi , 1984 .

[67]  F. Ebrahim-Nesbat,et al.  Light and Electron Microscopic Studies on the Development of Soybean Rust (Phakopsora pachyrhizi Syd.) in Susceptible Soybean Leaves , 1983 .

[68]  E. E. Hartwig,et al.  Relationships Among Three Genes Conferring Specific Resistance to Rust in Soybeans1 , 1983 .

[69]  J. Melching.  The Plant Pathogen Containment Facility at Frederick, Maryland , 1983 .

[70]  B. J. Deverall,et al.  Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean , 1980 .

[71]  R. Wyse.  Partitioning within the Taproot Sink of Sugarbeet: Effect of Photosynthate Supply 1 , 1980 .

[72]  D. Byth,et al.  Inheritance of resistance to rust (Phakopsora pachyrhizi) in soybeans. , 1980 .

[73]  E. E. Hartwig,et al.  Resistance to soybean rust and mode of inheritance. , 1980 .

[74]  L. Ilag,et al.  Ingress and pathogenic development of Phakopsora pachyrhizi Syd. in soybean. , 1980 .

[75]  D. Byth,et al.  Effect of rust (Phakopsora pachyrhizi) on soybean yield and quality in south-eastern Queensland , 1979 .

[76]  R. McLean.  Histological studies of resistance to soybean rust, Phakopsora pachyrhizi Syd , 1979 .

[77]  B. J. Deverall,et al.  Responses of soybean to infection by, and to germination fluids from, urediniospores of Phakopsora pachyrhizi , 1977 .

[78]  W. Fehr,et al.  Stages of soybean development , 1977 .

[79]  M. Bonde.  Histology of the Suscept-Pathogen Relationship Between Glycine max and Phakopsora pachyrhizi, the Cause of Soybean Rust , 1976 .

[80]  M. Marchetti.  Uredial Development of Phakopsora pachyrhizi in Soybeans , 1975 .

[81]  R Fisher,et al.  Design of Experiments , 1936 .

[82]  C. Bonferroni.  Il calcolo delle assicurazioni su gruppi di teste , 1935 .