Advances in proteomic technologies and their scope of application in understanding plant–pathogen interactions

Proteomics, one of the major tools of ‘omics’ is evolving phenomenally since the development and application of two-dimensional gel electrophoresis coupled with mass spectrometry at the end of twentieth century. However, the adoption and application of advanced proteomic technologies in understanding plant–pathogen interactions are far less, when compared to their application in other related fields of systems biology. Hence, this review is diligently focused on the advances in various proteomic approaches and their gamut of applications in different facets of phyto-pathoproteomics. Especially, the scope and application of proteomics in understanding fundamental concepts of plant–pathogen interactions such as identification of pathogenicity determinants (effector proteins), disease resistance proteins (resistance and pathogenesis-related proteins) and their regulation by post-translational modifications have been portrayed. This review, for the first time, presents a critical appraisal of various proteomic applications by assessing all phyto-pathoproteomics-related research publications that were published in peer-reviewed journals, during the period 2000–2016. This assessment has revealed the present status and contribution of proteomic applications in different categories of phyto-pathoproteomics, namely, cellular components, host–pathogen interactions, model and non-model plants, and utilization of different proteomic approaches. Comprehensively, the analysis highlights the burgeoning application of global proteome approaches in various crop diseases, and demand for acceleration in deploying advanced proteomic technologies to thoroughly comprehend the intricacies of complex and rapidly evolving plant–pathogen interactions.

[1]  S. Robatzek,et al.  Breaking the barriers: microbial effector molecules subvert plant immunity. , 2008, Annual review of phytopathology.

[2]  P. Brennan,et al.  Proteomics technologies for the global identification and quantification of proteins. , 2010, Advances in protein chemistry and structural biology.

[3]  Huanming Yang,et al.  A Draft Sequence of the Rice Genome (Oryza sativa L. ssp. japonica) , 2002, Science.

[4]  Ruedi Aebersold,et al.  Quantitative proteome analysis using isotope-coded affinity tags and mass spectrometry , 2006, Nature Protocols.

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

[6]  C. Lenz,et al.  Fourteen years of plant proteomics reflected in Proteomics: Moving from model species and 2DE‐based approaches to orphan species and gel‐free platforms , 2015, Proteomics.

[7]  Gilson Luiz Volpato,et al.  Aggressiveness Overcomes Body-Size Effects in Fights Staged between Invasive and Native Fish Species with Overlapping Niches , 2012, PloS one.

[8]  Ramesh Sundar Amalraj,et al.  Sugarcane proteomics: An update on current status, challenges, and future prospects , 2015, Proteomics.

[9]  T. Rabilloud.  When 2D is not enough, go for an extra dimension , 2013, Proteomics.

[10]  J. Weissenbach,et al.  Genome sequence of the plant pathogen Ralstonia solanacearum , 2002, Nature.

[11]  D. B. Kristensen,et al.  Mapping of phosphorylated proteins on two‐dimensional polyacrylamide gels using protein phosphatase , 2002, Proteomics.

[12]  G. Van den Ackerveken,et al.  Susceptibility to plant disease: more than a failure of host immunity. , 2013, Trends in plant science.

[13]  C. Zipfel,et al.  Effector biology of plant-associated organisms: concepts and perspectives. , 2012, Cold Spring Harbor symposia on quantitative biology.

[14]  J A Eisen,et al.  The Genome of the Natural Genetic Engineer Agrobacterium tumefaciens C58 , 2001, Science.

[15]  Barbara Kaboord,et al.  Isolation of proteins and protein complexes by immunoprecipitation. , 2008, Methods in molecular biology.

[16]  Brian D. Halligan,et al.  ProMoST (Protein Modification Screening Tool): a web-based tool for mapping protein modifications on two-dimensional gels , 2004, Nucleic Acids Res..

[17]  The Arabidopsis Genome Initiative.  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[18]  R. Aebersold,et al.  Proteomics: the first decade and beyond , 2003, Nature Genetics.

[19]  T. Nürnberger,et al.  Immune receptor complexes at the plant cell surface. , 2014, Current opinion in plant biology.

[20]  J. Dangl,et al.  NB-LRR proteins: pairs, pieces, perception, partners, and pathways. , 2010, Current opinion in plant biology.

[21]  Dieter Jahn,et al.  JVirGel: calculation of virtual two-dimensional protein gels , 2003, Nucleic Acids Res..

[22]  J. Klose.  Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues , 1975, Humangenetik.

[23]  M. Ünlü,et al.  Difference gel electrophoresis. A single gel method for detecting changes in protein extracts , 1997, Electrophoresis.

[24]  C. Clément,et al.  Uncovering plant-pathogen crosstalk through apoplastic proteomic studies , 2014, Front. Plant Sci..

[25]  A. T. Iavarone,et al.  Quantitative proteomic approach for cellulose degradation by Neurospora crassa. , 2011, Journal of proteome research.

[26]  C. Zipfel,et al.  Plant pattern recognition receptor complexes at the plasma membrane. , 2012, Current opinion in plant biology.

[27]  B. Chait,et al.  Improved beta-elimination-based affinity purification strategy for enrichment of phosphopeptides. , 2003, Analytical chemistry.

[28]  Christopher T. Walsh,et al.  Protein Posttranslational Modifications: The Chemistry of Proteome Diversifications , 2006 .

[29]  P. Righetti,et al.  Global proteome analysis in plants by means of peptide libraries and applications. , 2016, Journal of proteomics.

[30]  D. A. Palmieri,et al.  The genome sequence of the plant pathogen Xylella fastidiosa , 2000, Nature.

[31]  Steven P. Gygi,et al.  Large-scale phosphorylation analysis of mouse liver , 2007, Proceedings of the National Academy of Sciences.

[32]  R. González-Fernández,et al.  Proteomics of Plant Pathogenic Fungi , 2010, Journal of biomedicine & biotechnology.

[33]  Mariko Alexander,et al.  A molecular tug-of-war: Global plant proteome changes during viral infection , 2016 .

[34]  J. Renaut,et al.  An improved protocol to study the plant cell wall proteome , 2015, Front. Plant Sci..

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

[36]  Michael P Washburn,et al.  Proteomic analysis by multidimensional protein identification technology. , 2006, Methods in molecular biology.

[37]  E. Huitema,et al.  Effector-triggered post-translational modifications and their role in suppression of plant immunity , 2012, Front. Plant Sci..

[38]  D. Hochstrasser,et al.  Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. , 1996, Biotechnology & genetic engineering reviews.

[39]  Nicolás Guillén,et al.  Sugar Cane , 2019, Encyclopedic Dictionary of Archaeology.

[40]  J. Burgyán.  Role of silencing suppressor proteins. , 2008, Methods in molecular biology.

[41]  M. Mann,et al.  Global and site-specific quantitative phosphoproteomics: principles and applications. , 2009, Annual review of pharmacology and toxicology.

[42]  T. Boller,et al.  A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. , 2009, Annual review of plant biology.

[43]  J. Brownstein,et al.  Emerging fungal threats to animal, plant and ecosystem health , 2012, Nature.

[44]  J. Shabanowitz,et al.  Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae , 2002, Nature Biotechnology.

[45]  Marc Dieu,et al.  Evaluation of three‐dimensional gel electrophoresis to improve quantitative profiling of complex proteomes , 2013, Proteomics.

[46]  Ganesh Kumar Agrawal,et al.  Plant organelle proteomics: collaborating for optimal cell function. , 2011, Mass spectrometry reviews.

[47]  Jian-Min Zhou,et al.  Phytopathogen effectors subverting host immunity: different foes, similar battleground. , 2012, Cell host & microbe.

[48]  Z. Fu,et al.  Go in for the kill , 2014, Virulence.

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

[50]  An Improvement of Shotgun Proteomics Analysis by Adding Next-Generation Sequencing Transcriptome Data in Orange , 2012, PloS one.

[51]  G. Agrawal,et al.  Time to dig deep into the plant proteome: a hunt for low-abundance proteins , 2015, Front. Plant Sci..

[52]  P. D. de Wit,et al.  Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. , 2007, Molecular plant-microbe interactions : MPMI.

[53]  J. Garin,et al.  Isotope dilution strategies for absolute quantitative proteomics. , 2009, Journal of proteomics.

[54]  P. O’Farrell.  High resolution two-dimensional electrophoresis of proteins. , 1975, The Journal of biological chemistry.

[55]  B. Goldman,et al.  Genome Sequence of the Plant Pathogen and Biotechnology Agent Agrobacterium tumefaciens C58 , 2001, Science.

[56]  D. Liebler,et al.  Targeted Quantitation of Proteins by Mass Spectrometry , 2013, Biochemistry.

[57]  A. Oliphant,et al.  A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). , 2002, Science.

[58]  R. Pedreschi,et al.  A decade of plant proteomics and mass spectrometry: translation of technical advancements to food security and safety issues. , 2013, Mass spectrometry reviews.

[59]  Anna Bierczynska-Krzysik,et al.  Methods for samples preparation in proteomic research. , 2007, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[60]  M. Larsen,et al.  Analytical strategies for phosphoproteomics , 2009, Expert review of neurotherapeutics.

[61]  Henning Urlaub,et al.  Increased proteome coverage by combining PAGE and peptide isoelectric focusing: Comparative study of gel-based separation approaches , 2013, Proteomics.

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

[63]  M. Albrecht,et al.  Resistance proteins: molecular switches of plant defence. , 2006, Current opinion in plant biology.

[64]  F. Katagiri,et al.  Understanding the plant immune system. , 2010, Molecular plant-microbe interactions : MPMI.

[65]  Christian Panse,et al.  Targeted proteomics coming of age – SRM, PRM and DIA performance evaluated from a core facility perspective , 2016, Proteomics.

[66]  Ramesh Sundar Amalraj,et al.  Sugarcane proteomics: Establishment of a protein extraction method for 2‐DE in stalk tissues and initiation of sugarcane proteome reference map , 2010, Electrophoresis.

[67]  M. Mann,et al.  Proteomic analysis of post-translational modifications , 2003, Nature Biotechnology.

[68]  B. Valent,et al.  Filamentous plant pathogen effectors in action , 2013, Nature Reviews Microbiology.

[69]  G. Scheele.  Two-Dimensional Gel Analysis of Soluble Proteins , 1975 .

[70]  R. Terauchi,et al.  Emerging concepts in effector biology of plant-associated organisms. , 2009, Molecular plant-microbe interactions : MPMI.

[71]  E. C. Teixeira,et al.  Comparison of the genomes of two Xanthomonas pathogens with differing host specificities , 2002, Nature.

[72]  Matthias Mann,et al.  Use of stable isotope labeling by amino acids in cell culture as a spike-in standard in quantitative proteomics , 2011, Nature Protocols.

[73]  C. Faulkner,et al.  Plants and pathogens: putting infection strategies and defence mechanisms on the map. , 2012, Current opinion in plant biology.

[74]  S. Robatzek,et al.  Pattern recognition receptors: from the cell surface to intracellular dynamics. , 2007, Molecular plant-microbe interactions : MPMI.

[75]  S. Mohammed,et al.  Strong cation exchange (SCX) based analytical methods for the targeted analysis of protein post-translational modifications. , 2011, Current opinion in biotechnology.

[76]  N. Rauniyar,et al.  Parallel Reaction Monitoring: A Targeted Experiment Performed Using High Resolution and High Mass Accuracy Mass Spectrometry , 2015, International journal of molecular sciences.

[77]  C. Kole,et al.  Arabidopsis Genome Initiative , 2016 .

[78]  Adele Bourmaud,et al.  Technical considerations for large-scale parallel reaction monitoring analysis. , 2014, Journal of proteomics.

[79]  G. Agrawal,et al.  Proteomic analysis of a compatible interaction between sugarcane and Sporisorium scitamineum , 2016, Proteomics.

[80]  J. Yates,et al.  Large-scale analysis of the yeast proteome by multidimensional protein identification technology , 2001, Nature Biotechnology.

[81]  Jian-Min Zhou,et al.  Plant immunity triggered by microbial molecular signatures. , 2010, Molecular plant.

[82]  Z. Fu,et al.  Go in for the kill: How plants deploy effector- triggered immunity to combat pathogens , 2014 .

[83]  J. Renaut,et al.  Plant biotic stress and proteomics , 2010 .

[84]  K. V. van Wijk,et al.  The Arabidopsis Chloroplast Stromal N-Terminome: Complexities of Amino-Terminal Protein Maturation and Stability1[OPEN] , 2015, Plant Physiology.

[85]  C. Zipfel.  Early molecular events in PAMP-triggered immunity. , 2009, Current opinion in plant biology.

[86]  Phillip C. Wright,et al.  An insight into iTRAQ: where do we stand now? , 2012, Analytical and Bioanalytical Chemistry.

[87]  Akhilesh Pandey,et al.  Quantitative proteomics using stable isotope labeling with amino acids in cell culture , 2008, Nature Protocols.