An unspecific phytotoxin oxalic acid and its effect on sunflower proteome

Oxalic acid (OA) is found naturally in many plants and animals: it plays diverse roles in nature. It is an important pathogenicity determinant of many necrotrophic pathogens including Sclerotinia sclerotiorum (Lib.) de Bary. In order to understand the resistance mechanisms in Helianthus annuus L., a proteomic study was conducted on sunflower 12 h after inoculation by OA. A total of 17 differentially expressed proteins (either OA-induced or -suppressed proteins) were identified as a result of OA treatment. The candidate proteins were classified into two groups depending on their up/downregulation. The first group – upregulated proteins – included 13 proteins identified as being involved in the Calvin cycle, photosynthesis, programmed cell death (PCD) pathway, heat shock proteins, proteins with antioxidant activities and flavonol synthase (FLS). The second group – downregulated proteins – included those from the cupin family, ATP synthase subunit β, ketol-acid reducto-isomerase, and actin. Studying the biological significance of proteins responsive to OA might ultimately convey us to improve sunflower lines with higher levels of resistance to Sclerotinia and help to control this devastating necrotrophic plant pathogen.

[1]  Zishan Zhang,et al.  Mechanisms by which the infection of Sclerotinia sclerotiorum (Lib.) de Baryaffects the photosynthetic performance in tobacco leaves , 2014, BMC Plant Biology.

[2]  D. Jiāng,et al.  Novel secretory protein Ss-Caf1 of the plant-pathogenic fungus Sclerotinia sclerotiorum is required for host penetration and normal sclerotial development. , 2014, Molecular plant-microbe interactions : MPMI.

[3]  A. Heller,et al.  Oxalic Acid Has an Additional, Detoxifying Function in Sclerotinia sclerotiorum Pathogenesis , 2013, PloS one.

[4]  Hua Li,et al.  Differentially Expressed Proteins and Associated Histological and Disease Progression Changes in Cotyledon Tissue of a Resistant and Susceptible Genotype of Brassica napus Infected with Sclerotinia sclerotiorum , 2013, PloS one.

[5]  W. Ende,et al.  Sugars and plant innate immunity , 2012 .

[6]  R. Darvishzadeh,et al.  Sclerotinia-induced accumulation of protein in the basal stem of resistant and susceptible lines of sunflower. , 2012 .

[7]  I. Díaz,et al.  C1A cysteine-proteases and their inhibitors in plants. , 2012, Physiologia plantarum.

[8]  V. Orsat,et al.  Microwave-Assisted Extraction of Flavonoids: A Review , 2012, Food and Bioprocess Technology.

[9]  Royston Goodacre,et al.  Metabolomic approaches reveal that cell wall modifications play a major role in ethylene-mediated resistance against Botrytis cinerea. , 2011, The Plant journal : for cell and molecular biology.

[10]  Brett Williams,et al.  Tipping the Balance: Sclerotinia sclerotiorum Secreted Oxalic Acid Suppresses Host Defenses by Manipulating the Host Redox Environment , 2011, PLoS pathogens.

[11]  F. Ferrini,et al.  Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants , 2011, Plant signaling & behavior.

[12]  G. Vannozzi,et al.  Shikimate Dehydrogenase Expression and Activity in Sunflower Genotypes Susceptible and Resistant to Sclerotinia sclerotiorum (Lib.) de Bary , 2011 .

[13]  S. Chivasa,et al.  Proteomic Analysis of Extracellular ATP-Regulated Proteins Identifies ATP Synthase β-Subunit as a Novel Plant Cell Death Regulator* , 2010, Molecular & Cellular Proteomics.

[14]  G. Agati,et al.  Multiple functional roles of flavonoids in photoprotection. , 2010, The New phytologist.

[15]  R. Dixon,et al.  The 'ins' and 'outs' of flavonoid transport. , 2010, Trends in plant science.

[16]  S. Muthukrishnan,et al.  Oxalic acid-induced resistance to Rhizoctonia solani in rice is associated with induction of phenolics, peroxidase and pathogenesis-related proteins , 2010 .

[17]  S. Strelkov,et al.  Oxalic acid‐mediated stress responses in Brassica napus L. , 2009, Proteomics.

[18]  S. Munné-Bosch,et al.  How relevant are flavonoids as antioxidants in plants? , 2009, Trends in plant science.

[19]  G. Qin,et al.  Response of jujube fruits to exogenous oxalic acid treatment based on proteomic analysis. , 2009, Plant & cell physiology.

[20]  R. Errakhi,et al.  Anion channel activity is necessary to induce ethylene synthesis and programmed cell death in response to oxalic acid. , 2008, Journal of experimental botany.

[21]  M. Dickman,et al.  Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. , 2008, Molecular plant-microbe interactions : MPMI.

[22]  B. Freeman,et al.  An Overview of Plant Defenses against Pathogens and Herbivores , 2008 .

[23]  G. Tucker,et al.  Silencing of the Major Salt-Dependent Isoform of Pectinesterase in Tomato Alters Fruit Softening1 , 2007, Plant Physiology.

[24]  A. Weber,et al.  Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways , 2007, BMC Genomics.

[25]  Brody J Deyoung,et al.  Plant NBS-LRR proteins in pathogen sensing and host defense , 2006, Nature Immunology.

[26]  S. Pinson,et al.  Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia solani. , 2006, Molecular plant pathology.

[27]  A. Maldonado,et al.  A proteomic approach to study pea (Pisum sativum) responses to powdery mildew (Erysiphe pisi) , 2006, Proteomics.

[28]  E. Peterlunger,et al.  Colour variation in red grapevines (Vitis vinifera L.): genomic organisation, expression of flavonoid 3'-hydroxylase, flavonoid 3',5'-hydroxylase genes and related metabolite profiling of red cyanidin-/blue delphinidin-based anthocyanins in berry skin , 2006, BMC Genomics.

[29]  T. Hsiang,et al.  Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. , 2005, Journal of experimental botany.

[30]  F. Galeotti,et al.  A Phytoalexin‐Like Flavonol Involved in the Carnation (Dianthus caryophyllus)‐Fusarium oxysporum f. sp. dianthi Pathosystem , 2005 .

[31]  N. Kav,et al.  Proteome-level investigation of Brassica carinata-derived resistance to Leptosphaeria maculans. , 2005, Journal of agricultural and food chemistry.

[32]  H. Yamane,et al.  Digging deeper into the plant cell wall proteome. , 2004, Plant physiology and biochemistry : PPB.

[33]  R. D'Ovidio,et al.  Relationships among endo-polygalacturonase, oxalate, pH, and plant polygalacturonase-inhibiting protein (PGIP) in the interaction between Sclerotinia sclerotiorum and soybean. , 2004, Molecular plant-microbe interactions : MPMI.

[34]  G. Edwards,et al.  Malate metabolism by NADP-malic enzyme in plant defense , 1999, Photosynthesis Research.

[35]  D. Bidney,et al.  Regeneration of fertile plants from protoplasts of sunflower (Helianthus annuus L.) , 1991, Plant Cell Reports.

[36]  Wei Wang,et al.  Protein extraction for two‐dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds , 2003, Electrophoresis.

[37]  S. Abouna,et al.  Differential regulation by ambient pH of putative virulence factor secretion by the phytopathogenic fungus Botrytis cinerea. , 2003, FEMS microbiology ecology.

[38]  David A Jones,et al.  GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. , 2003, The Plant journal : for cell and molecular biology.

[39]  G. Martin,et al.  The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  B. Winkel-Shirley,et al.  Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. , 2001, Plant physiology.

[41]  P. Khurana,et al.  Germins and germin like proteins: an overview. , 2001, Indian journal of experimental biology.

[42]  M. Dickman,et al.  pH Signaling in Sclerotinia sclerotiorum: Identification of a pacC/RIM1 Homolog , 2001, Applied and Environmental Microbiology.

[43]  J. Hennig,et al.  Early defence responses in plants infected with pathogenic organisms. , 2001, Cellular & molecular biology letters.

[44]  M. Dickman,et al.  Oxalic Acid, a Pathogenicity Factor for Sclerotinia sclerotiorum, Suppresses the Oxidative Burst of the Host Plant , 2000, Plant Cell.

[45]  R. Strange,et al.  Phytotoxicity of solanapyrones A and B produced by the chickpea pathogen Ascochyta rabiei(Pass.) Labr. and the apparent metabolism of solanapyrone A by chickpea tissues , 2000 .

[46]  R Edwards,et al.  Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. , 2000, Trends in plant science.

[47]  A. Izzo,et al.  Flavonoids: old and new aspects of a class of natural therapeutic drugs. , 1999, Life sciences.

[48]  R. Bélanger,et al.  Silicon-mediated accumulation of flavonoid phytoalexins in cucumber. , 1998, Phytopathology.

[49]  J. Dunwell Cupins: a new superfamily of functionally diverse proteins that include germins and plant storage proteins. , 1998, Biotechnology & genetic engineering reviews.

[50]  A. R. Reddy,et al.  Differential sensitivity of rice pathogens to growth inhibition by flavonoids , 1997 .

[51]  C. Evans,et al.  Oxalate production by fungi : its role in pathogenicity and ecology in the soil environment , 1996 .

[52]  P. H. Ferrar,et al.  o-Diphenol oxidase inhibition—an additional role for oxalic acid in the phytopathogenic arsenal of Sclerotinia sclerotiorum and Sclerotium rolfsii , 1993 .

[53]  Y. Mo,et al.  Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[54]  M. Fěvre,et al.  Production of Cell Wall-Degrading Enzymes by the Phytopathogenic Fungus Sclerotinia sclerotiorum , 1991, Applied and environmental microbiology.

[55]  D. Rowe,et al.  Use of a host-pathogen interaction system to test whether oxalic acid is the sole pathogenic determinant in the exudate of Sclerotinia trifoliorum , 1991 .

[56]  M. Dickman,et al.  Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. , 1990 .

[57]  K. McCue,et al.  Induction of 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase activity by fungal elicitor in cultures of Petroselinum crispum. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[58]  K. Ono,et al.  Formation of Hydrogen Peroxide by NAD(P)H Oxidation with Isolated Cell Wall-Associated Peroxidase from Cultured Liverwort Cells, Marchantia polymorpha L. , 1987 .

[59]  P. Marcianò,et al.  Oxalic acid, cell wall-degrading enzymes and pH in pathogenesis and their significance in the virulence of two Sclerotinia sclerotiorum isolates on sunflower , 1983 .

[60]  J. G. Hancock,et al.  Role of oxalic acid in the Sclerotinia wilt of sunflower. , 1981 .

[61]  J. W. McClure The Physiology of Phenolic Compounds in Plants , 1979 .

[62]  D. Dorrell,et al.  Screening sunflower seedlings for resistance to toxic metabolites produced by Sclerotinia sclerotiorum. , 1978 .

[63]  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.

[64]  S. Beer,et al.  SIMULTANEOUS PRODUCTION AND SYNERGISTIC ACTION OF OXALIC ACID AND POLYGALACTURONASE DURING PATHOGENESIS BY SCLEROTIUM ROLFSII. , 1965, Phytopathology.

[65]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .