Skip to main content
SpringerLink
Log in

Organization of phenylalanine ammonia lyase (PAL), acidic PR-5 and osmotin-like (OSM) defence-response gene families in the potato genome

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Defence-response (DR) genes are candidates for the genetic functions underlying quantitative resistance to plant pathogens. The organization of three DR gene families encoding phenylalanine ammonia lyase (PAL), acidic PR-(pathogenesis-related) protein 5, and basic PR-5, or osmotin-like (OSM), proteins was studied in the potato genome. A bacterial artificial chromosome (BAC) library containing ~50,000 clones was constructed from high-molecular weight genomic DNA of the diploid potato clone PD59, a hybrid between Solanum tuberosum and S. phureja. BAC clones carrying one or more copies of the DR genes were identified and characterized by Southern hybridization, sequence analysis and genetic mapping. PAL, acidic PR-5 and OSM (basic PR-5) genes were all organized into gene families of varying complexity. The PAL gene family consisted of at least 16 members, several of which were physically linked. Four acidic PR-5 homologous were localized to a 45-kb segment on potato chromosome XII. One of these, PR-5/319, codes for the acidic thaumatin-like protein C found in intercellular fluids of potato. Nine OSM genes were organized at two loci: eight form a 90-kb cluster on chromosome VIII, and a single gene was found on chromosome XI. The topology of a phylogenetic tree based on PR-5 and OSM protein sequences from Solanaceae suggests a mode of evolution for these gene families. The results will form the basis for further studies on the potential role of these defence-related loci in quantitative resistance to pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allouis S, Qi X, Lindup S, Gale M, Devos K (2001) Construction of a BAC library of pearl millet Pennisetum glaucum. Theor Appl Genet 102:1200–1205

    Article  CAS  Google Scholar 

  • Arumuganathan K, Earle E (1991) Nuclear DNA content of some important plants species. Plant Mol Biol Rep 9:208–218

    CAS  Google Scholar 

  • Ballvora A, Ercolano M, Weiss J, Meksem K, Bormann C, Oberhagemann P, Salamini F, Gebhardt C (2002) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper /NBS/LRR class of plant resistance genes. Plant J 30:361–371

    Article  PubMed  CAS  Google Scholar 

  • Bonierbale M, Simon R, Zhang D, Ghislain M, Mba C, Qing Li X (2003) Genomics and molecular breeding for root and tuber crop improvement. In: Newbury J (ed) Plant molecular breeding. Blackwell, Oxford, pp 216–253

    Google Scholar 

  • Bonnema G, Hontelez J, Verkerk R, Zhang YQ, van Daelen R, van Kammen A, Zabel P (1996) An improved method of partially digesting plant megabase DNA suitable for YAC cloning: application to the construction of a 5.5 genome equivalent YAC library of tomato. Plant J 9:125–133

    Article  PubMed  CAS  Google Scholar 

  • Bormann CA, Rickert AM, Castillo Ruiz RA, Paal J, Lübeck J, Strahwald J, Buhr K, Gebhardt C (2004) Tagging QTL for maturity-corrected late blight resistance in tetraploid potato with PCR-based candidate gene markers. Mol Plant Microbe Interact 17:1126–1138

    Google Scholar 

  • Budiman MA, Mao L, Wood TC, Wing RA (2000) A deep-coverage tomato BAC library and prospects toward development of an STC framework for genome sequencing. Genome Res 10:129–136

    PubMed  CAS  Google Scholar 

  • Castillo-Ruiz RA (2002) A potato large insert library for isolation of candidate loci for late blight resistance and studies on their genome organziation. PhD Thesis, University of Cologne, Germany (available at http://kups.ub.uni-koeln.de/volltexte/2004/1067/)

  • Ercolano MR, Ballvora A, Paal J, Steinbiss H-H, Salamini F, Gebhardt C (2004) Biolistic transformation of plants with large DNA fragments: an efficient tool for functional complementation analysis in potato. Mol Breed 13:15–22

    Article  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 

  • Feinberg A, Vogelstein B (1984) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity (addendum). Anal Biochem 137:266–267

    Article  PubMed  CAS  Google Scholar 

  • Fritjers A, Zhang Z, van Damme M, Wang G, Ronald P, Michelmore R (1997) Construction of a bacterial artificial chromosome library containing large EcoRI and HindIII genomic fragments of lettuce. Theor Appl Genet 94:390–399

    Article  Google Scholar 

  • Fritzemeier K, Cretin C, Kombrink E, Rohwer F, Taylor J, Scheel D, Hahlbrock K (1987) Transient induction of phenylalanine ammonia-lyase and 4-coumarate:CoA ligase mRNAs in potato leaves infected with virulent races of Phytophthora infestans. Plant Physiol 85:34–41

    Article  PubMed  CAS  Google Scholar 

  • Gebhardt C, Valkonen JPT (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102

    Article  PubMed  CAS  Google Scholar 

  • Gebhardt C, Ritter E, Debener T, Schachtschabel U, Walkemeier B, Uhrig H, Salamini F (1989) RFLP analysis and linkage mapping in Solanum tuberosum. Theor Appl Genet 78:65–75

    Article  Google Scholar 

  • Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schachtschabel U, Kaufmann H, Thompson RD, Bonierbale MW, Ganal MW, Tanksley SD (1991) RFLP maps of potato and their alignment with the homologous tomato genome. Theor Appl Genet 83:49–57

    Article  Google Scholar 

  • Gebhardt C, Ritter E, Salamini F (2001) RFLP map of the potato. In: Phillips RL, Vasil IK (eds) DNA-based markers in plants (2nd edn) (Advances in cellular and molecular biology of plants, vol 6). Kluwer, Dordrecht, pp 319–336

    Google Scholar 

  • Gebhardt C, Walkemeier B, Henselewski H, Barakat A, Delseny M, Stüber K (2003) Comparative mapping between potato (Solanum tuberosum) and Arabidopsis thaliana reveals structurally conserved domains and ancient duplications in the potato genome. Plant J 34:529–541

    Article  PubMed  CAS  Google Scholar 

  • Gebhardt C, Ballvora A, Walkemeier B, Oberhagemann P, Schüler K (2004) Assessing genetic potential in germ plasm collections of crop plants by marker-trait association: a case study for potatoes with quantitative variation of resistance to late blight and maturity type. Mol Breed 13:93–102

    Article  CAS  Google Scholar 

  • Geffroy V, Sevignac M, De Oliveira JCF, Fouilloux G, Skrotch P, Thoquet P, Gepts P, Langin T, Dron M (2000) Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of quantitative trait loci with genes involved in specific resistance. Mol Plant Microbe Interact 13:287–296

    Article  PubMed  CAS  Google Scholar 

  • Ghislain M, Trognitz B, Herrera M, Solis J, Casallo G, Vasquez C, Hurtado O, Castillo R Portal L, Orillo M (2001) Genetic loci associated with field resistance to late blight in offspring of Solanum phureja and Solanum tuberosum grown under short-day conditions. Theor Appl Genet 103:433–442

    Article  CAS  Google Scholar 

  • Hamilton CM, Frary A, Xu Y, Tanksley SD, Zhang H-B (1999) Construction of tomato genomic DNA libraries in a binary-BAC (BIBAC) vector. Plant J 18:223–229

    Article  CAS  Google Scholar 

  • Jones J, Schlumukov L, Carland F, English J, Scofield S, Bishop G, Harrison K (1992) Effective vectors for transformation, expression of heterologous genes, and assaying transposon excision in transgenic plants. Transgenic Res 1:285–297

    Article  PubMed  CAS  Google Scholar 

  • Joos HJ, Hahlbrock K (1992) Phenylalanine ammonia-lyase in potato (Solanum tuberosum L.). Genomic complexity, structural comparison of two selected genes and modes of expression. Eur J Biochem 204:621–629

    Article  PubMed  CAS  Google Scholar 

  • Kanyuka K, Bendahmane A, Rouppe van der Voort JNAM, van der Vossen EAG, Baulcombe DC (1999) Mapping of intra-locus duplications and introgressed DNA: aids to map-based cloning of genes from complex genomes illustrated by analysis of the Rx locus in tetraploid potato. Theor Appl Genet 98:679–689

    Article  CAS  Google Scholar 

  • Kombrink E, Somssich IE (1995) Defence responses of plants to pathogens. Adv Bot Res 21:1–34

    Article  CAS  Google Scholar 

  • Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429

    Article  PubMed  CAS  Google Scholar 

  • Leonards-Schippers C, Gieffers W, Schafer-Pregl R, Ritter E, Salamini F, Gebhardt C (1994) Qualitative resistance to Phytophthora infestans in potato: a case study for QTL mapping in an allogamous plant species. Genetics 137:67–77

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Liu D, Raghothama K, Hasegawa P, Bressan R (1994) Osmotin overexpression in potato delays development of disease symptoms. Proc Natl Acad Sci USA 91:1888–1892

    Article  PubMed  CAS  Google Scholar 

  • Martin GB, Ganal MW, Tanksley SD (1992) Construction of a yeast artificial chromosome library of tomato and identification of cloned segments linked to two disease resistance loci. Mol Gen Genet 233:25–32

    Article  PubMed  CAS  Google Scholar 

  • McDowell JM, Woffenden BJ (2003) Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol 21:178–183

    Article  PubMed  CAS  Google Scholar 

  • Milbourne D, Meyer RC, Collins AJ, Ramsay LD, Gebhardt C, Waugh R (1998) Isolation, characterization and mapping of simple sequence repeat loci in potato. Mol Gen Genet 259:233–245

    Article  PubMed  CAS  Google Scholar 

  • Ming R, Moore P, Zee F, Abbey C, Ma H, Paterson A (2001) Construction and characterization of a papaya BAC library as a foundation for molecular dissection of a tree-fruit genome. Theor Appl Genet 102:892–899

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Paal J, Henselewski H, Muth J, Meksem K, Menéndez CM, Salamini F, Ballvora A, Gebhardt C (2004) Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J 38:285–297

    Article  PubMed  CAS  Google Scholar 

  • Payne G, Middlesteadt W, Williams S, Desai N, Parks D, Dincher S, Carnes M, Ryals J (1988) Isolation and nucleotide sequence of a novel cDNA clone encoding the major form of pathogenesis-related protein R. Plant Mol Biol 11:223–224

    Article  CAS  Google Scholar 

  • Pflieger S, Palloix A, Caranta C, Blattes A, Lefebvre V (2001) Defence response genes co-localize with quantitative disease resistance loci in pepper. Theor Appl Genet 103:920–929

    Article  CAS  Google Scholar 

  • Pierpoint W, Jackson P, Evans R (1990) The presence of a thaumatin-like protein, a chitinase and a glucanase among the pathogenesis-related proteins of potato (Solanum tuberosum). Physiol Mol Plant Pathol 36:325–338

    Article  CAS  Google Scholar 

  • Ritter E, Gebhardt C, Salamini F (1990) Estimation of recombination frequencies and construction of RFLP linkage maps in plants from crosses between heterozygous parents. Genetics 125:645–654

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Simko I (2002) Comparative analysis of quantitative trait loci for foliage resistance to Phytophthora infestans in tuber-bearing Solanum species. Am J Potato Res 79:125–132

    Article  CAS  Google Scholar 

  • Simko I, Costanzo S, Haynes KG, Christ BJ, Jones RW (2004) Linkage disequilibrium mapping of a Verticillium dahliae resistance quantitative trait locus in tetraploid potato (Solanum tuberosum) trough a candidate gene approach. Theor Appl Genet 108:217–224

    Article  PubMed  CAS  Google Scholar 

  • Song J, Dong F, Jiang J (2000) Construction of a bacterial artificial chromosome library for potato molecular cytogenetics research. Genome 43:199–204

    Article  PubMed  CAS  Google Scholar 

  • Trognitz F, Manosalva P, Niño-Liu D, Herrera M, Ghislain M, Trognitz B, Nelson R (2002) Plant defence genes associated with quantitative resistance to potato late blight in Solanum phureja x Solanum tuberosum hybrids. Mol Plant Microbe Interact 15:587–597

    Article  PubMed  CAS  Google Scholar 

  • Van Kan J, Van de Rhee M, Zuidema D, Cornelissen B, Bol J (1989) Structure of tobacco genes encoding thaumatin-like proteins. Plant Mol Biol 12:153–155

    Article  CAS  Google Scholar 

  • Van der Vossen E, Sikkema A, Hekkert B te L, Gros J, Stevens P, Muskens M, Wouters D, Pereira A, Stiekema W, Allefs S (2003) An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J 36:867–882

    Article  PubMed  CAS  Google Scholar 

  • Velzhahan R, Datta S, Muthukrishnan S (1999) The PR-5 family: thaumatin-like proteins. In: Datta S, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, pp 107–129

    Google Scholar 

  • Vinatzer B, Zhang H, Sansavini S (1998) Construction and characterization of a bacterial artificial chromosome library of apple. Theor Appl Genet 97:1183–1190

    Article  CAS  Google Scholar 

  • Wang Z, Taramino G, Yang D, Liu G, Tingey S, Miao G, Wang G (2001) Rice ESTs with disease-resistance gene- or defence-response gene-like sequences mapped to regions containing major resistance genes or QTLs. Mol Gen Genomics 265:302–310

    Article  CAS  Google Scholar 

  • Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Metraux JP, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 31085–1094

    Google Scholar 

  • Woo S, Jiang J, Gill B, Paterson A, Wing R (1994) Construction and characterization of a bacterial artificial chromosome library of Sorghum bicolor. Nucleic Acids Res 22:4922–4931

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Zhao X, Ding D, Paterson A, Wing R (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7:175–184

    Article  CAS  Google Scholar 

  • Zhu B, Chen T, Li P (1995a) Expression of three osmotin-like protein genes in response to osmotic stress and fungal infection in potato. Plant Mol Biol 28:17–26

    Article  PubMed  CAS  Google Scholar 

  • Zhu B, Chen T, Li P (1995b) Activation of two osmotin-like proteins genes by abiotic stimuli and fungal pathogen in transgenic potato plants. Plant Physiol 108:929–937

    Article  PubMed  CAS  Google Scholar 

  • Zhu B, Chen T, Li P (1996) Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta 198:70–77

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant (Project No. 96.7860.8-001.00) from the German Federal Ministry for Economic Cooperation and Development (BMZ). The authors are grateful to Ma. Del R. Herrera for providing the in vitro plant PD59 and DNA of the PD mapping population

Author information

Authors and Affiliations

  1. Max-Planck Institute for Plant Breeding Research, Carl von Linne Weg 10, 50829, Cologne, Germany

    Rosa A. Castillo Ruiz & Christiane Gebhardt

  2. Centro International de la Papa CIP, Apartado 1558, 12, Lima, Peru

    Carmen Herrera & Marc Ghislain

Authors
  1. Rosa A. Castillo Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carmen Herrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marc Ghislain
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christiane Gebhardt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christiane Gebhardt.

Additional information

Communicated by M.-A. Grandbastien

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruiz, R.A.C., Herrera, C., Ghislain, M. et al. Organization of phenylalanine ammonia lyase (PAL), acidic PR-5 and osmotin-like (OSM) defence-response gene families in the potato genome. Mol Genet Genomics 274, 168–179 (2005). https://doi.org/10.1007/s00438-005-0006-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-005-0006-7

Keywords

Search

Navigation