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PR-1 gene family of grapevine: a uniquely duplicated PR-1 gene from a Vitis interspecific hybrid confers high level resistance to bacterial disease in transgenic tobacco

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Abstract

A functional contribution of pathogenesis-related 1 (PR-1) proteins to host defense has been established. However, systematic investigation of the PR-1 gene family in grapevine (Vitis spp.) has not been conducted previously. Through mining genomic databases, we identified 21 PR-1 genes from the Vitis vinifera genome. Polypeptides encoded by putative PR-1 genes had a signal sequence of about 25 residues and a mature protein of 10.9–29 kDa in size. PR-1 mature proteins contained a highly conserved six-cysteine motif and pI values ranging from 4.6 to 9. A major cluster with 14 PR-1 genes was mapped to a 280-kb region on chromosome 3. One particular PR-1 gene within the cluster encoding a basic-type isoform (pI 7.77), herein named VvPR1b1, was isolated from various genotypes of grapevine (Vitis spp.) for functional studies. Sequence analysis of PCR-amplified DNA revealed that all genotypes contained a single VvPR1b1 gene except for a broad-spectrum bacterial and fungal disease resistant Florida bunch grape hybrid, ‘BN5-4’, from which seven different homologues were identified. Duplication of VvPR1b1-related genes encoding acidic-type PR-1 isoforms was also observed among several genotypes. However, transgenic expression analysis of grapevine PR-1 genes under strong constitutive promoters in transgenic tobacco revealed that only the basic-type VvPR1b1 gene duplicated in ‘BN5-4’ was capable of conferring high level resistance to bacterial disease caused by Pseudomonas syringae pv. tabaci.

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References

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

    Article  CAS  PubMed  Google Scholar 

  • Amoutzias G, Van de Peer Y (2008) Together we stand: Genes cluster to coordinate regulation. Dev Cell 14:640–642

    Article  CAS  PubMed  Google Scholar 

  • Antoniw JF, Ritter CE, Pierpoint WS, Van Loon LC (1980) Comparison of three pathogenesis-related proteins from plants of two cultivars of tobacco infected with TMV. J Gen Virol 47:79–87

    Article  CAS  Google Scholar 

  • Bonasera JM, Kim JF, Beer SV (2006) PR genes of apple: identification and expression in response to elicitors and inoculation with Erwinia amylovora. BMC Plant Biol 6:23

    Article  PubMed  Google Scholar 

  • Burrow MD, Chlan CA, Sen P, Murai N (1990) High frequency generation of transgenic tobacco plants after modified leaf disk cocultivation with Agrobacterium tumefaciens. Plant Mol Biol Rep 8:124–139

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chow LP, Chiu LL, Khoo KH, Peng HJ, Yang SY, Huang SW, Su SN (2005) Purification and structural analysis of the novel glycoprotein allergen Cyn d 24, a pathogenesis-related protein PR-1, from Bermuda grass pollen. FEBS J 272:6218–6227

    Article  CAS  PubMed  Google Scholar 

  • Chuang JH, Li H (2004) Functional bias and spatial organization of genes in mutational hot and cold regions in the human genome. PLoS Biol 2:0253–0263

    Article  CAS  Google Scholar 

  • Dutt M, Li ZT, Dhekney SA, Gray DJ (2008) A co-transformation system to produce transgenic grapevines free of marker genes. Plant Sci 175:423–430

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  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 266:576–593

    Article  CAS  PubMed  Google Scholar 

  • Hedges SB (1992) The number of replications needed for accurate estimation of the bootstrap P value in phylogenetic studies. Mol Biol Evol 9:366–369

    CAS  PubMed  Google Scholar 

  • Hong JK, Hwang BK (2005) Induction of enhanced disease resistance and oxidative stress tolerance by overexpression of pepper basic PR-1 gene in Arabidopsis. Physiol Plant 124:267–277

    Article  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Kim Y, Hwang BK (2000) Pepper gene encoding a basic pathogenesis-related 1 protein is pathogen and ethylene inducible. Physiol Plant 108:51–60

    CAS  Google Scholar 

  • Lawton K, Uknes S, Friedrich L et al (1993) The molecular biology of systemic acquired resistance. In: Fritig B, Legrand M (eds) Mechanisms of plant defense responses. Kluwer, Dordrecht, pp 422–432

    Google Scholar 

  • Li ZT, Gray DJ (2005) Isolation by improved asymmetric interlaced PCR and characterization of a seed-specific 2S albumin gene and its promoter from grape (Vitis vinifera L.). Genome 48:312–320

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Jayasankar S, Gray DJ (2004) Bi-directional duplex promoters with duplicated enhancers significantly increase transgene expression in grape and tobacco. Transgenic Res 13:143–154

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lodhi MA, Ye GN, Weeden NF, Reisch BJ (1994) A simple and efficient method for DNA extraction from grapevine cultivars and Vitis species. Plant Mol Biol Rep 12:6–13

    Article  CAS  Google Scholar 

  • Lodhi N, Ranjan A, Singh M, Srivastava R, Singh SP, Chaturvedi CP, Ansari SA, Sawant SV, Tuli R (2008) Interactions between upstream and core promoter sequences determine gene expression and nucleosome positioning in tobacco PR-1a promoter. Biochem Biophys Acta 1779:634–644

    CAS  PubMed  Google Scholar 

  • Maleck K, Levine A, Eulgern T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410

    Article  CAS  PubMed  Google Scholar 

  • Martin F, McInerney JO (2009) Recurring cluster and operon assembly for phenylacetate degradation genes. BMC Evol Biol. http://www.biomedcentral.com/1471-2148/9/36

  • Mitsuhara I, Iwal T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve rice PR-1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (120/180). Mol Genet Genomics 279:415–427

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Niderman T, Genetet I, Bruyere T, Gees R, Stinizi A, Legrand M, Fritig B, Mo′singer 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 108:17–27

    Article  CAS  PubMed  Google Scholar 

  • Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco plants. Plant Cell Physiol 39:500–507

    CAS  Google Scholar 

  • Ohshima M, Matsuoka M, Yamamoto N, Tanaka Y, Kano-Murakami Y, Ozeki Y, Kato A, Harada N, Ohashi Y (1987) Nucleotide sequence of the PR-1 gene of Nicotiana tabacum. FEBS Lett 225:243–246

    Article  CAS  PubMed  Google Scholar 

  • Sarowar S, Kim YJ, Kim EN, Kim KD, Hwang BK, Islam R, Shin JS (2005) Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep 24:216–224

    Article  CAS  PubMed  Google Scholar 

  • Smith H (1989) The mounting interest in bacterial and viral pathogenicity. Annu Rev Microbiol 43:1–22

    Article  CAS  PubMed  Google Scholar 

  • Suo Y, Leung DWM (2002) Accumulation of extracellular pathogenesis-related proteins in rose leaves following inoculation of in vitro shoots with Diplocarpon rosa. Sci Hort 93:167–178

    Article  CAS  Google Scholar 

  • Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2010) The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection. J Bacteriol 192:117–126

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. PNAS 95:15107–15111

    Article  CAS  PubMed  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. MPMI 10:624–634

    Article  CAS  PubMed  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The family 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, Pierpoint WS, Boller T, Conejero V (1994) Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12:245–264

    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 

Download references

Acknowledgments

This research was supported by the Florida Agricultural Experiment Station and the Florida Department of Agriculture and Consumer Services’ Viticulture Trust Fund.

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Correspondence to Dennis J. Gray.

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Communicated by K. Kamo.

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Li, Z.T., Dhekney, S.A. & Gray, D.J. PR-1 gene family of grapevine: a uniquely duplicated PR-1 gene from a Vitis interspecific hybrid confers high level resistance to bacterial disease in transgenic tobacco. Plant Cell Rep 30, 1–11 (2011). https://doi.org/10.1007/s00299-010-0934-5

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  • DOI: https://doi.org/10.1007/s00299-010-0934-5

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