Skip to main content

Advertisement

Log in

Pinus monticola pathogenesis-related gene PmPR10-2 alleles as defense candidates for stem quantitative disease resistance against white pine blister rust (Cronartium ribicola)

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

White pine blister rust, caused by the invasive fungus Cronartium ribicola, has been responsible for extremely high mortality of native western white pine (Pinus monticola) and other five-needle pines in natural stands throughout western North America. The presence of this non-native fungus has also led to greatly restricted use of western white pine for reforestation. A few families of defense proteins have been found as functional candidates involved in tree resistance to rust infection. Here we report genetic variation of a gene encoding a family 10 pathogenesis-related (PR) protein (PmPR10-2) in open-pollinated seed families with different levels of stem quantitative disease resistance (QDR). Six novel alleles and five common genotypes were identified inside the PmPR10-2 locus: these genetic variations included 33 single nucleotide polymorphisms (SNPs) throughout the gene regions and copy variation of a rare octanucleotide simple sequence repeat (SSR), 5′-AATTATTT-3′, in the gene intron. PmPR10-2 exhibited a moderate level (average r 2 = 0.42) of linkage disequilibrium. Two-thirds of the identified SNPs and the SSR marker were significantly associated with stem QDR levels. The PmPR10-2 genotype (H3:H3) exhibited the highest level of stem QDR (P < 0.01). Cost-effective and co-dominant SSR markers were developed and used for genotyping the PmPR10-2 locus using simple PCR, providing a potential molecular tool for accelerating screening efforts of white pine resistance against C. ribicola.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Beaulieu J, Doerksen T, Boyle B, Clément S, Deslauriers M, Beauseigle S, Blais S, Poulin PL, Lenz P, Caron S, Rigault P, Bicho P, Bousquet J, Mackay J (2011) Association genetics of wood physical traits in the conifer white spruce and relationships with gene expression. Genetics 188:197–214

    Article  PubMed  CAS  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  PubMed  CAS  Google Scholar 

  • Chadha P, Das RH (2006) A pathogenesis related protein, AhPR10 from peanut: an insight of its mode of antifungal activity. Planta 225:213–222

    Article  PubMed  CAS  Google Scholar 

  • Chen ZY, Brown RL, Damann KE, Cleveland TE (2010) PR10 expression in maize and its effect on host resistance against Aspergillus flavus infection and aflatoxin production. Mol Plant Pathol 11:69–81

    Article  PubMed  CAS  Google Scholar 

  • Dracatos PM, Cogan NOI, Dobrowolski MP, Sawbridge TI, Spangenberg GC, Smith KF, Forster JW (2008) Discovery and genetic mapping of single nucleotide polymorphisms in candidate genes for pathogen defence response in perennial ryegrass (Lolium perenne L.). Theor Appl Genet 117:203–219

    Article  PubMed  CAS  Google Scholar 

  • Echt CS, May-Marquardt P, Hseih M, Zahorchak R (1996) Characterization of microsatellite markers in eastern white pine. Genome 39:1102–1108

    Article  PubMed  CAS  Google Scholar 

  • Ekramoddoullah A (2004) Physiology and molecular biology of a family of pathogenesis-related PR-10 proteins of conifers. J Crop Improv 10:261–280

    Article  CAS  Google Scholar 

  • Ersoz ES, Wright MH, González-Martínez SC, Langley CH, Neale DB (2010) Evolution of disease response genes in loblolly pine: insights from candidate genes. PLoS One 5:e14234. doi:10.1371/journal.pone.0014234

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    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 

  • Farnir F, Coppieters W, Arranz JJ, Berzi P, Cambisano N, Grisart B, Karim L, Marcq F, Moreau L, Mni M, Nezer C, Simon P, Vanmanshoven P, Wagenaar D, Georges M (2000) Extensive genome-wide linkage disequilibrium in cattle. Genome Res 10:220–227

    Article  PubMed  CAS  Google Scholar 

  • Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • Gómez-Gómez L, Rubio-Moraga A, Ahrazem O (2011) Molecular cloning and characterisation of a pathogenesis-related protein CsPR10 from Crocus sativus. Plant Biol 13:297–303

    Article  PubMed  Google Scholar 

  • González-Martínez SC, Ersoz E, Brown GR, Wheeler NC, Neale DB (2006) DNA sequence variation and selection of tag single nucleotide polymorphisms at candidate genes for drought-stress response in Pinus taeda L. Genetics 172:1915–1926

    Article  PubMed  Google Scholar 

  • González-Martínez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175:399–409

    Article  PubMed  Google Scholar 

  • Hunt RS (1997) Relative value of slow-canker growth and bark reaction as resistance responses to white pine blister rust. Can J Plant Pathol 19:352–357

    Article  Google Scholar 

  • Kim SG, Kim ST, Wang Y, Yu S, Choi IS, Kim YC, Kim WT, Agrawal GK, Rakwal R, Kang KY (2011) The RNase activity of rice probenazole-induced protein1 (PBZ1) plays a key role in cell death in plants. Mol Cells 31:25–31

    Article  PubMed  CAS  Google Scholar 

  • Kinloch BB Jr (2003) White pine blister rust in North America: past and prognosis. Phytopathol 93:1044–1047

    Article  Google Scholar 

  • Kinloch BB Jr, Davis DA, Burton D (2008) Resistance and virulence interactions between two white pine species and blister rust in a 30-year field trial. Tree Genet Genomes 4:65–74

    Article  Google Scholar 

  • Krishnaswamy S, Srivastava S, Mohammadi M, Rahman MH, Deyholos MK, Kav NV (2008) Transcriptional profiling of pea ABR17 mediated changes in gene expression in Arabidopsis thaliana. BMC Plant Biol 8:91

    Article  PubMed  Google Scholar 

  • Krishnaswamy S, Baral PK, James MNG, Kav NV (2011) Site-directed mutagenesis of histidine 69 and glutamic acid 148 alters the ribonuclease activity of pea ABR17 (PR10.4). Plant Physiol Biochem 49:958–962

    Article  PubMed  CAS  Google Scholar 

  • Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness- and wood quality-related candidate genes in Douglas fir. Genetics 171:2029–2041

    Article  PubMed  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. doi:10.1093/ bioinformatics/btp187

    Article  PubMed  CAS  Google Scholar 

  • Liu J-J, Ekramoddoullah AK (2003) Root-specific expression of a western white pine PR10 gene is mediated by different promoter regions in transgenic tobacco. Plant Mol Biol 52:103–120

    Article  PubMed  CAS  Google Scholar 

  • Liu J-J, Ekramoddoullah AK (2004) Characterization, expression and evolution of two novel subfamilies of Pinus monticola cDNAs encoding pathogenesis-related (PR)-10 proteins. Tree Physiol 24:1377–1385

    Article  PubMed  CAS  Google Scholar 

  • Liu J-J, Ekramoddoullah AK (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68:3–13

    Article  CAS  Google Scholar 

  • Liu J-J, Ekramoddoullah AK (2008) Development of leucine-rich repeat polymorphism, amplified fragment length polymorphism, and sequence characterized amplified region markers to the Cronartium ribicola resistance gene Cr2 in western white pine (Pinus monticola). Tree Genet Genom 4:601–610

    Article  Google Scholar 

  • Liu J-J, Ekramoddoullah AK, Yu X (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant 119:544–553

    Article  CAS  Google Scholar 

  • Liu J-J, Hunt R, Ekramoddoullah AK (2004a) Recent insights into genetic resistance of western white pine to white pine blister rust. Recent Res Dev Biotech Bioeng 6:65–76

    CAS  Google Scholar 

  • Liu B, Zhang S, Zhu X, Yang Q, Wu S, Mei M, Mauleon R, Leach J, Mew T, Leung H (2004b) Candidate defense genes as predictors of quantitative blast resistance in rice. Mol Plant-Microbe Interact 17:1146–1152

    Article  PubMed  CAS  Google Scholar 

  • Liu J-J, Ekramoddoullah AKM, Piggott N, Zamani A (2005) Cloning of a pathogen/wound-inducible PR10 promoter from Pinus monticola and characterization in transgenic Arabidopsis plants. Planta 221:159–169

    Article  PubMed  CAS  Google Scholar 

  • Liu J-J, Sniezko R, Ekramoddoullah AK (2011) Association of a novel Pinus monticola chitinase gene (PmCh4B) with quantitative resistance to Cronartium ribicola. Phytopathology 101:904–911

    Article  PubMed  CAS  Google Scholar 

  • Neale DB, Ingvarsson P (2008) Population, quantitative and comparative genomics of adaptation in forest trees. Curr Opin Plant Biol 11:149–155

    Article  PubMed  CAS  Google Scholar 

  • Park CJ, Kim KJ, Park JM, Shin YC, Paek KH (2004) Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J 37:186–198

    Article  PubMed  CAS  Google Scholar 

  • Pavy N, Namroud M-C, Gagnon F, Isabel N, Bousquet J (2012) The heterogeneous levels of linkage disequilibrium in white spruce genes and comparative analysis with other conifers. Heredity 108:273–284

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Quesada T, Gopal V, Cumbie WP, Eckert AJ, Wegrzyn JL, Neale DB, Goldfarb B, Huber DA, Casella G, Davis JM (2010) Association mapping of quantitative disease resistance in a natural population of loblolly pine (Pinus taeda L.). Genetics 186:677–686

    Article  PubMed  CAS  Google Scholar 

  • Sniezko RA (2006) Resistance breeding against nonnative pathogens in forest trees—current successes in North America. Can J Plant Pathol 28(Sup 1):S270–S279

    Article  Google Scholar 

  • Sniezko RA, Kegley A (2003) Blister rust resistance experiences in Oregon and Washington: evolving perspectives. In: Stone J, Maffei H (eds) Proceedings of the 50th Western International Forest Disease Work Conference. 2002 October 7–11. Powell River, BC, Canada, pp 111–117

    Google Scholar 

  • Sniezko RA, Kegley AJ, Danchok R (2008) White pine blister rust resistance in North America, Asian and European species- results from artificial inoculation trials in Oregon. Ann For Res 51:53–66

    Google Scholar 

  • Soh HC, Park AR, Park S, Back K, Yoon JB, Park HG, Kim YS (2012) Comparative analysis of pathogenesis-related protein 10 (PR10) genes between fungal resistant and susceptible peppers. Eur J Plant Pathol 132:37–48

    Article  CAS  Google Scholar 

  • Somssich IE, Bollmann J, Hahlbrock K, Kombrink E, Schulz W (1989) Differential early activation of defense-related genes in elicitor-treated parsley cells. Plant Mol Biol 12:227–234

    Article  CAS  Google Scholar 

  • Suharyanto, Shiraishi S (2011) Nucleotide diversities and genetic relationship in the three Japanese pine species; Pinus thunbergii, Pinus densiflora, and Pinus luchuensis. Diversity 3:121–135

    Article  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Van der Hoorn RA, De Wit PJ, Joosten MH (2002) Balancing selection favors guarding resistance proteins. Trends Plant Sci 7:67–71

    Article  PubMed  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 

  • Wachowiak W, Balk PA, Savolainen O (2009) Search for nucleotide diversity patterns of local adaptation in dehydrins and other cold-related candidate genes in Scots pine (Pinus sylvestris L.). Tree Genet Genom 5:117–132

    Article  Google Scholar 

  • Weir BS (1996) Genetic data analysis II. Sinauer Associates, Sunderland

    Google Scholar 

  • Xie Y-R, Chen Z-Y, Brown RL, Bhatnagar D (2010) Expression and functional characterization of two pathogenesis-related protein 10 genes from Zea mays. J Plant Physiol 167:121–130

    Article  PubMed  CAS  Google Scholar 

  • Zubini P, Zambelli B, Musiani F, Ciurli S, Bertolini P, Baraldi E (2009) The RNA hydrolysis and the cytokinin binding activities of PR-10 proteins are differently performed by two isoforms of the Pru p 1 peach major allergen and are possibly functionally related. Plant Physiol 150:1235–1247

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported, in part, by the Canadian Forest Service and the CFS–GRDI fund awarded to JJL. We thank A. Zamany, J. Hutchinson, and L. Baerg at CFS for support on genotyping; J. Hill, A. Kegley, and the technicians at DGRC for support on phenotyping; and B. Crawford for critical review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jun-Jun Liu.

Additional information

Communicated by J. Dean

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. S1

Alignment analysis of PmPR10-2 nucleotide sequences. Multiple sequence alignment analysis was performed using an on-line ClustalW2 program provided by the European Bioinformatics Institute (http://www.ebi.ac.uk/Tools/msa/clustalw2/) (PDF 120 kb)

Supplementary Fig. S2

Phylogenetic analysis of the PmPR10-2 genomic sequences. Based on PmPR10-2 nucleotide sequence alignment result as shown in Fig. S1, a representative of phylogenetic trees was generated by MEGA 5.0 software using the neighbor-joining (NJ) method (PDF 174 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, JJ., Hammett, C. & Sniezko, R.A. Pinus monticola pathogenesis-related gene PmPR10-2 alleles as defense candidates for stem quantitative disease resistance against white pine blister rust (Cronartium ribicola). Tree Genetics & Genomes 9, 397–408 (2013). https://doi.org/10.1007/s11295-012-0561-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-012-0561-0

Keywords

Navigation