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Molecular characterization and genomic mapping of the pathogenesis-related protein 1 (PR-1) gene family in hexaploid wheat (Triticum aestivum L.)

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Abstract

The group 1 pathogenesis-related (PR-1) proteins, known as hallmarks of defense pathways, are encoded by multigene families in plants as evidenced by the presence of 22 and 32 PR-1 genes in the finished Arabidopsis and rice genomes, respectively. Here, we report the initial characterization and mapping of 23 PR-1-like (TaPr-1) genes in hexaploid wheat (Triticum aestivum L.), which possesses one of the largest (>16,000 megabases) genomes among monocot crop plants. Sequence analysis revealed that the 23 TaPr-1 genes all contain intron-free open reading frames that encode a signal peptide at the N-terminus and a conserved PR-1-like domain. Phylogenetic analysis indicated that TaPr-1 genes form three major monophyletic groups along with their counterparts in other monocots; each group consists of genes encoding basic, basic with a C-terminal extension, and acidic PR-1 proteins, respectively, suggesting diversity and conservation of PR-1 gene functions in monocot plants. Mapping analysis assisted by untranslated region-specified discrimination (USD) markers and various cytogenetic stocks located the 23 TaPr-1 genes to seven different chromosomes, with the majority mapping to chromosomes of homoeologous groups 5 and 7. Reverse transcriptase (RT)-PCR analysis revealed that 12 TaPr-1 genes were induced or up-regulated upon pathogen challenge. Together, this study provides insights to the origin, evolution, homoeologous relationships, and expression patterns of the TaPr-1 genes. The data presented provide critical information for further genome-wide characterization of the wheat PR-1 gene family and the USD markers developed will facilitate genetic and functional analysis of PR-1 genes associated with plant defense and/or other important traits.

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References

  • Abeysekara NS, Friesen TL, Keller B, Faris JD (2009) Identification and characterization of a novel host–toxin interaction in the wheat-Stagonospora nodorum pathosystem. Theor Appl Genet 120(1):117–126

    Article  PubMed  CAS  Google Scholar 

  • Alexander D, Goodman RM, Gut-Rella M, Glascock C, Weymann K, Friedrich L, Maddox D, Ahl-Goy P, Luntz T, Ward E et al (1993) Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc Natl Acad Sci USA 90(15):7327–7331

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:211–215

    Google Scholar 

  • Boguski MS, Lowe TM, Tolstoshev CM (1993) dbEST—database for “expressed sequence tags”. Nat Genet 4(4):332–333

    Article  PubMed  CAS  Google Scholar 

  • Bryngelsson T, Sommer-Knudsen J, Gregersen PL, Collinge DB, Ek B, Thordal-Christensen H (1994) Purification, characterization, and molecular cloning of basic PR-1-type pathogenesis-related proteins from barley. Mol Plant Microbe Interact 7(2):267–275

    Article  PubMed  CAS  Google Scholar 

  • Buchel AS, Linthorst HJM (1999) PR-1: a group of plant proteins induced upon pathogen infection. In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, FL

    Google Scholar 

  • Casacuberta JM, Puigdomenech P, San Segundo B (1991) A gene coding for a basic pathogenesis-related (PR-like) protein from Zea mays. Molecular cloning and induction by a fungus (Fusarium moniliforme) in germinating maize seeds. Plant Mol Biol 16(4):527–536

    Article  PubMed  CAS  Google Scholar 

  • Chalupska D, Lee HY, Faris JD, Evrard A, Chalhoub B, Haselkorn R, Gornicki P (2008) Acc homoeoloci and the evolution of wheat genomes. Proc Natl Acad Sci USA 105(28):9691–9696

    Article  PubMed  CAS  Google Scholar 

  • Cornelissen BJ, Horowitz J, van Kan JA, Goldberg RB, Bol JF (1987) Structure of tobacco genes encoding pathogenesis-related proteins from the PR-1 group. Nucleic Acids Res 15(17):6799–6811

    Article  PubMed  CAS  Google Scholar 

  • Dvorak J, Terlizzi P, Zhang HB, Resta P (1993) The evolution of polyploid wheats: identification of the A genome donor species. Genome 36(1):21–31

    Article  PubMed  CAS  Google Scholar 

  • Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307

    CAS  Google Scholar 

  • Erayman M, Sandhu D, Sidhu D, Dilbirligi M, Baenziger PS, Gill KS (2004) Demarcating the gene-rich regions of the wheat genome. Nucleic Acids Res 32(12):3546–3565

    Article  PubMed  CAS  Google Scholar 

  • Faris JD, Li WL, Liu DJ, Chen PD, Gill BS (1999) Candidate gene analysis of quantitative disease resistance in wheat. Theor Appl Genet 98:219–225

    Article  CAS  Google Scholar 

  • Faris JD, Haen KM, Gill BS (2000) Saturation mapping of a gene-rich recombination hot spot region in wheat. Genetics 154(2):823–835

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1989) Mathematics vs. evolution: mathematical evolutionary theory. Science 246(4932):941–942

    Article  PubMed  CAS  Google Scholar 

  • Fernandez C, Szyperski T, Bruyere T, Ramage P, Mosinger E, Wuthrich K (1997) NMR solution structure of the pathogenesis-related protein P14a. J Mol Biol 266(3):576–593

    Article  PubMed  CAS  Google Scholar 

  • Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38(8):953–956

    Article  PubMed  CAS  Google Scholar 

  • Friesen TL, Faris JD, Solomon PS, Oliver RP (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10(7):1421–1428

    Article  PubMed  CAS  Google Scholar 

  • Gaudet DA, Wang Y, Penniket C, Lu ZX, Bakkeren G, Laroche A (2010) Morphological and molecular analyses of host and nonhost interactions involving barley and wheat and the covered smut pathogen Ustilago hordei. Mol Plant Microbe Interact 23(12):1619–1634

    Article  PubMed  CAS  Google Scholar 

  • Gillikin JW, Burkhart W, Graham JS (1991) Complete amino acid sequence of a polypeptide from Zea mays similar to the pathogenesis-related-1 family. Plant Physiol 96(4):1372–1375

    Article  PubMed  CAS  Google Scholar 

  • Hillier LD, Lennon G et al (1996) Generation and analysis of 280,000 human expressed sequence tags. Genome Res 6(9):807–828

    Article  PubMed  CAS  Google Scholar 

  • Hoffman DR (1993) Allergens in Hymenoptera venom. XXV: the amino acid sequences of antigen 5 molecules and the structural basis of antigenic cross-reactivity. J Allergy Clin Immunol 92(5):707–716

    Article  PubMed  CAS  Google Scholar 

  • Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci USA 99(12):8133–8138

    Article  PubMed  CAS  Google Scholar 

  • Joosten MH, Bergmans CJ, Meulenhoff EJ, Cornelissen BJ, De Wit PJ (1990) Purification and serological characterization of three basic 15-kilodalton pathogenesis-related proteins from tomato. Plant Physiol 94(2):585–591

    Article  PubMed  CAS  Google Scholar 

  • Kiba A, Takata O, Ohnishi K, Hikichi Y (2006) Comparative analysis of induction pattern of programmed cell death and defense-related responses during hypersensitive cell death and development of bacterial necrotic leaf spots in eggplant. Planta 224(5):981–994

    Article  PubMed  CAS  Google Scholar 

  • Kiba A, Nishihara M, Nakatsuka T, Yamamura S (2007) Pathogenesis-related protein 1 homologue is an antifungal protein in Wasabia japonica leaves and confers resistance to Botrytis cinerea in transgenic tobacco. Plant Biotechnol 24:247–253

    Article  CAS  Google Scholar 

  • Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare. Agric Hortic 19:13–14

    Google Scholar 

  • Kirby TW, Mueller GA, DeRose EF, Lebetkin MS, Meiss G, Pingoud A, London RE (2002) The nuclease A inhibitor represents a new variation of the rare PR-1 fold. J Mol Biol 320(4):771–782

    Article  PubMed  CAS  Google Scholar 

  • Kratzschmar J, Haendler B, Eberspaecher U, Roosterman D, Donner P, Schleuning WD (1996) The human cysteine-rich secretory protein (CRISP) family. Primary structure and tissue distribution of CRISP-1, CRISP-2 and CRISP-3. Eur J Biochem 236(3):827–836

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1(2):174–181

    Article  PubMed  CAS  Google Scholar 

  • Lawton KA, Potter SL, Uknes S, Ryals J (1994) Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6(5):581–588

    Article  PubMed  CAS  Google Scholar 

  • Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E (1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J 16(2):223–233

    Article  PubMed  CAS  Google Scholar 

  • Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RA, Ritsema T, Pieterse CM (2009) Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 149(4):1797–1809

    Article  PubMed  CAS  Google Scholar 

  • Li WL, Faris JD, Chittoor JM, Leach JE, Hulbert SH, Liu DJ, Chen PD, Gill BS (1999) Genomic mapping of defense response genes in wheat. Theor Appl Genet 98:226–233

    Article  CAS  Google Scholar 

  • Liu Q, Xue Q (2006) Computational identification of novel PR-1-type genes in Oryza sativa. J Genet 85(3):193–198

    Article  PubMed  CAS  Google Scholar 

  • Liu ZH, Anderson JA, Hu J, Friesen TL, Rasmussen JB, Faris JD (2005) A wheat intervarietal genetic linkage map based on microsatellite and target region amplified polymorphism markers and its utility for detecting quantitative trait loci. Theor Appl Genet 111(4):782–794

    Article  PubMed  CAS  Google Scholar 

  • Liu G, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G, Wei Y (2007) Targeted alterations in iron homeostasis underlie plant defense responses. J Cell Sci 120(Pt 4):596–605

    Article  PubMed  CAS  Google Scholar 

  • Lu HJ, Fellers JP, Friesen TL, Meinhardt SW, Faris JD (2006) Genomic analysis and marker development for the Tsn1 locus in wheat using bin-mapped ESTs and flanking BAC contigs. Theor Appl Genet 112(6):1132–1142

    Article  PubMed  CAS  Google Scholar 

  • Matsuoka Y, Nasuda S (2004) Durum wheat as a candidate for the unknown female progenitor of bread wheat: an empirical study with a highly fertile F1 hybrid with Aegilops tauschii Coss. Theor Appl Genet 109(8):1710–1717

    Article  PubMed  Google Scholar 

  • McFadden ES, Sears ER (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J Hered 37:81–89

    PubMed  Google Scholar 

  • Meng L, Ruth KC, Fletcher JC, Feldman L (2010) The roles of different CLE domains in Arabidopsis CLE polypeptide activity and functional specificity. Mol Plant 3(4):760–772

    Article  PubMed  CAS  Google Scholar 

  • Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics 279(4):415–427

    Article  PubMed  CAS  Google Scholar 

  • Molina A, Gorlach J, Volrath S, Ryals J (1999) Wheat genes encoding two types of PR-1 proteins are pathogen inducible, but do not respond to activators of systemic acquired resistance. Mol Plant Microbe Interact 12(1):53–58

    Article  PubMed  CAS  Google Scholar 

  • Morris SW, Vernooij B, Titatarn S, Starrett M, Thomas S, Wiltse CC, Frederiksen RA, Bhandhufalck A, Hulbert S, Uknes S (1998) Induced resistance responses in maize. Mol Plant Microbe Interact 11(7):643–658

    Article  PubMed  CAS  Google Scholar 

  • Murphy EV, Zhang Y, Zhu W, Biggs J (1995) The human glioma pathogenesis-related protein is structurally related to plant pathogenesis-related proteins and its gene is expressed specifically in brain tumors. Gene 159(1):131–135

    Article  PubMed  CAS  Google Scholar 

  • Nelson JC, Van Deynze AE, Autrique E, Sorrells ME, Lu YH, Negre S, Bernard M, Leroy P (1995) Molecular mapping in wheat. Homoeologous group 3. Genome 38:525–533

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus JM, Sticher L, Meins F Jr, Boller T (1991) A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc Natl Acad Sci USA 88(22):10362–10366

    Article  PubMed  CAS  Google Scholar 

  • Niderman T, Genetet I, Bruyere T, Gees R, Stintzi A, Legrand M, Fritig B, Mosinger E (1995) Pathogenesis-related PR-1 proteins are antifungal. Isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol 108(1):17–27

    Article  PubMed  CAS  Google Scholar 

  • Pestsova EG, Goncharov NP, Salina EA (1998) Elimination of a tandem repeat of telomeric heterochromatin during the evolution of wheat. Theor Appl Genet 97:1380–1386

    Article  Google Scholar 

  • Pfitzner UM, Goodman HM (1987) Isolation and characterization of cDNA clones encoding pathogenesis-related proteins from tobacco mosaic virus infected tobacco plants. Nucleic Acids Res 15(11):4449–4465

    Article  PubMed  CAS  Google Scholar 

  • Pfitzner AJ, Pfitzner UM, Goodman HM (1990) Nucleotide sequences of two PR-1 pseudogenes from Nicotiana tabacum cv. Wisconsin 38. Nucleic Acids Res 18(11):3404

    Article  PubMed  CAS  Google Scholar 

  • Qi LL, Echalier B et al (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168(2):701–712

    Article  PubMed  CAS  Google Scholar 

  • Rauscher M, Adam AL, Wirtz S, Guggenheim R, Mendgen K, Deising HB (1999) PR-1 protein inhibits the differentiation of rust infection hyphae in leaves of acquired resistant broad bean. Plant J 19(6):625–633

    Article  PubMed  CAS  Google Scholar 

  • Schuren FH, Asgeirsdottir SA, Kothe EM, Scheer JM, Wessels JG (1993) The Sc7/Sc14 gene family of Schizophyllum commune codes for extracellular proteins specifically expressed during fruit-body formation. J Gen Microbiol 139(9):2083–2090

    PubMed  CAS  Google Scholar 

  • Sears ER (1954) The aneuploids of common wheat. Mo Agric Exp Stn Res Bull 572:1–59

    Google Scholar 

  • Sels J, Mathys J, De Coninck BM, Cammue BP, De Bolle MF (2008) Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem 46(11):941–950

    Article  PubMed  CAS  Google Scholar 

  • Senda K, Ogawa K (2004) Induction of PR-1 accumulation accompanied by runaway cell death in the lsd1 mutant of Arabidopsis is dependent on glutathione levels but independent of the redox state of glutathione. Plant Cell Physiol 45(11):1578–1585

    Article  PubMed  CAS  Google Scholar 

  • Smith DB, Flavell RB (1975) Characterization of the wheat genome by renaturation kinetics. Chromosoma 50:223–242

    Article  CAS  Google Scholar 

  • Sourdille P, Singh S, Cadalen T, Brown-Guedira GL, Gay G, Qi L, Gill BS, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion bin system for the establishment of genetic-physical map relationships in wheat (Triticum aestivum L.). Funct Integr Genomics 4(1):12–25

    Article  PubMed  CAS  Google Scholar 

  • Stevens C, Titarenko E, Hargreaves JA, Gurr SJ (1996) Defence-related gene activation during an incompatible interaction between Stagonospora (Septoria) nodorum and barley (Hordeum vulgare L.) coleoptile cells. Plant Mol Biol 31(4):741–749

    Article  PubMed  CAS  Google Scholar 

  • Szyperski T, Fernandez C, Mumenthaler C, Wuthrich K (1998) Structure comparison of human glioma pathogenesis-related protein GliPR and the plant pathogenesis-related protein P14a indicates a functional link between the human immune system and a plant defense system. Proc Natl Acad Sci USA 95(5):2262–2266

    Article  PubMed  CAS  Google Scholar 

  • Takumi S, Nasuda S, Liu YG, Tsunewaki K (1993) Wheat phylogeny determined by RFLP analysis of nuclear DNA. I. Einkorn wheat. Jpn J Genet 68:73–79

    Article  Google Scholar 

  • Talbert LE, Blake NK, Storlie EW, Lavin M (1995) Variability in wheat based on low-copy DNA sequence comparisons. Genome 38(5):951–957

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tornero P, Conejero V, Vera P (1994) A gene encoding a novel isoform of the PR-1 protein family from tomato is induced upon viroid infection. Mol Gen Genet 243(1):47–53

    Article  PubMed  CAS  Google Scholar 

  • Tornero P, Gadea J, Conejero V, Vera P (1997) Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Mol Plant Microbe Interact 10(5):624–634

    Article  PubMed  CAS  Google Scholar 

  • Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4(6):645–656

    Article  PubMed  CAS  Google Scholar 

  • van Loon LC, van Kammen A (1970) Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. “Samsun” and “Samsun NN”. II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 40(2):190–211

    PubMed  Google Scholar 

  • van Loon LC, van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  Google Scholar 

  • van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Vlasuk GP, Inouye S, Inouye M (1984) Effects of replacing serine and threonine residues within the signal peptide on the secretion of the major outer membrane lipoprotein of Escherichia coli. J Biol Chem 259(10):6195–6200

    PubMed  CAS  Google Scholar 

  • Werner JE, Endo TR, Gill BS (1992) Toward a cytogenetically based physical map of the wheat genome. Proc Natl Acad Sci USA 89(23):11307–11311

    Article  PubMed  CAS  Google Scholar 

  • Ying H, Liu H (2007) Identification of an alternative signal peptide cleavage site of mouse monoclonal antibodies by mass spectrometry. Immunol Lett 111(1):66–68

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Jamie Hauff, Kelsey Dunnell and Rachel Lindgren for technical assistance, and Michael Edwards for reviewing the manuscript. This research was supported by the USDA-Agricultural Research Service CRIS project 5442-22000-033-00D.

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Correspondence to Shunwen Lu.

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Communicated by K. Shirasu.

Nucleotide sequence data reported are available in the GenBank databases under the accession numbers HQ541961–HQ541981 (for TaPr-1-1 through -21), HQ700376 and HQ700377 (for TaPr-1-22 and -23, respectively).

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Lu, S., Friesen, T.L. & Faris, J.D. Molecular characterization and genomic mapping of the pathogenesis-related protein 1 (PR-1) gene family in hexaploid wheat (Triticum aestivum L.). Mol Genet Genomics 285, 485–503 (2011). https://doi.org/10.1007/s00438-011-0618-z

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