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Evidence for different QTL underlying the immune and hypersensitive responses of Eucalyptus globulus to the rust pathogen Puccinia psidii

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Abstract

The rust Puccinia psidii infects many species in the family Myrtaceae. Native to South America, the pathogen has recently entered Australia which has a rich Myrtaceous flora, including trees of the ecologically and economically important genus Eucalyptus. We studied the genetic basis of variation in rust resistance in Eucalyptus globulus, the main plantation eucalypt in Australia. Quantitative trait loci (QTL) analysis was undertaken using 218 genotypes of an outcross F2 mapping family, phenotyped by controlled inoculation of their open pollinated progeny with the strain of P. psidii found in Australia. QTL analyses were conducted using a binary classification of individuals with no symptoms (immune) versus those with disease symptoms, and in a separate analysis dividing plants with disease symptoms into those exhibiting the hypersensitive response versus those with more severe symptoms. Four QTL were identified, two influencing whether a plant exhibited symptoms (Ppr2 and Ppr3), and two influencing the presence or absence of a hypersensitive reaction (Ppr4 and Ppr5). These QTL mapped to four different linkage groups, none of which overlap with Ppr1, the major QTL previously identified for rust resistance in Eucalyptus grandis. Candidate genes within the QTL regions are presented and possible mechanisms discussed. Together with past findings, our results suggest that P. psidii resistance in eucalypts is quantitative in nature and influenced by the complex interaction of multiple loci of variable effect.

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References

  • Alves AA, Rosado CCG, Faria DA, da Silva Guimaraes LM, Lau D, Brommonschenkel SH, Grattapaglia D, Alfenas AC (2012) Genetic mapping provides evidence for the role of additive and non-additive QTLs in the response of inter-specific hybrids of Eucalyptus to Puccinia psidii rust infection. Euphytica 183:27–38

    Article  CAS  Google Scholar 

  • Alves MS, Dadalto SP, Gonçalves AB, De Souza GB, Barros VA, Fietto LG (2013) Plant bZIP transcription factors responsive to pathogens: a review. Int J Mol Sci 14:7815–7828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544

    Article  PubMed  Google Scholar 

  • Baldrich P, Campo S, Wu M-T, Liu T-T, Hsing Y-IC, Segundo BS (2015) MicroRNA-mediated regulation of gene expression in the response of rice plants to fungal elicitors. RNA Biol 12:847–863

    Article  PubMed  Google Scholar 

  • Balmelli G, Simeto S, Altier N, Marroni V, Diez JJ (2013) Long term losses caused by foliar diseases on growth and survival of Eucalyptus globulus in Uruguay. New For 44:249–263

    Article  Google Scholar 

  • Balmelli G, Simeto S, Marroni V, Altier N, Diez JJ (2014) Genetic variation for resistance to Mycosphaerella leaf disease and Eucalyptus rust on Eucalyptus globulus in Uruguay. Australas Plant Pathol 43:97–107

    Article  Google Scholar 

  • Batish DR, Singh HP, Kohli RK, Kaur S (2008) Eucalyptus essential oil as a natural pesticide. For Ecol Manag 256:2166–2174

    Article  Google Scholar 

  • Booth TH, Pryor LD (1991) Climatic requirements of some commercially important eucalypt species. For Ecol Manag 43:47–60

    Article  Google Scholar 

  • Bradshaw HD, Stettler RF (1995) Molecular genetics of growth and development in Populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. Genetics 139:963–973

    CAS  PubMed  Google Scholar 

  • Brondani RP, Williams ER, Brondani C, Grattapaglia D (2006) A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus. BMC Plant Biol 6:20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Canhoto C, Graça M (1999) Leaf barriers to fungal colonization and shredders (Tipula lateralis) consumption of decomposing Eucalyptus globulus. Microb Ecol 37:163–172

    Article  PubMed  Google Scholar 

  • Caplan J, Padmanabhan M, Dinesh-Kumar SP (2008) Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3:126–135

    Article  CAS  PubMed  Google Scholar 

  • Carnegie A (2015) First report of Puccinia psidii (myrtle rust) in Eucalyptus plantations in Australia. Plant Dis 99:161

    Article  Google Scholar 

  • Carnegie AJ, Lidbetter JR (2012) Rapidly expanding host range for Puccinia psidii sensu lato in Australia. Australas Plant Pathol 41:13–29

    Article  Google Scholar 

  • Carnegie A, Lidbetter J, Walker J, Horwood M, Tesoriero L, Glen M, Priest M (2010) Uredo rangelii, a taxon in the guava rust complex, newly recorded on Myrtaceae in Australia. Australas Plant Pathol 39:463–466

    Article  Google Scholar 

  • Carnegie A, Kathuria A, Pegg G, Entwistle P, Nagel M, Giblin F (2015) Impact of the invasive rust Puccinia psidii (myrtle rust) on native Myrtaceae in natural ecosystems in Australia. Biological Invasions 18(1):127–144

    Article  Google Scholar 

  • Chu Z, Ouyang Y, Zhang J, Yang H, Wang S (2004) Genome-wide analysis of defense-responsive genes in bacterial blight resistance of rice mediated by the recessive R gene xa13. Mol Gen Genomics 271:111–120

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Core Team R (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Coutinho T, Wingfield M, Alfenas A, Crous P (1998) Eucalyptus rust: a disease with the potential for serious international implications. Plant Dis 82:819–825

    Article  Google Scholar 

  • Crabill E, Joe A, Block A, van Rooyen JM, Alfano JR (2010) Plant immunity directly or indirectly restricts the injection of type III effectors by the Pseudomonas syringae type III secretion system. Plant Physiol 154:233–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui L-G, Shan J-X, Shi M, Gao J-P, Lin H-X (2014) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 80:1108–1117

    Article  CAS  PubMed  Google Scholar 

  • Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511

    Article  CAS  PubMed  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • DeYoung BJ, Qi D, Kim S-H, Burke TP, Innes RW (2012) Activation of a plant nucleotide binding-leucine rich repeat disease resistance protein by a modified self protein. Cell Microbiol 14:1071–1084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang C-IA, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci 103:8888–8893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doughty RW (2000) The Eucalyptus: a natural and commercial history of the gum tree. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Dutkowski G, Potts B (1999) Geographic patterns of genetic variation in Eucalyptus globulus ssp. globulus and a revised racial classification. Aust J Bot 47:237–263

    Article  Google Scholar 

  • Ellis J, Jones D (1998) Structure and function of proteins controlling strain-specific pathogen resistance in plants. Curr Opin Plant Biol 1:288–293

    Article  CAS  PubMed  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  CAS  PubMed  Google Scholar 

  • Ferreira F (1983) Eucalyptus rust. Rev Arvore 7:91–109

    Google Scholar 

  • Flor H (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:e69

    Google Scholar 

  • Freeman J, O’Reilly-Wapstra J, Vaillancourt R, Wiggins N, Potts B (2008a) Quantitative trait loci for key defensive compounds affecting herbivory of eucalypts in Australia. New Phytol 178:846–851

    Article  CAS  PubMed  Google Scholar 

  • Freeman JS, Potts BM, Vaillancourt RE (2008b) Few Mendelian genes underlie the quantitative response of a forest tree, Eucalyptus globulus, to a natural fungal epidemic. Genetics 178:563–571

    Article  PubMed  PubMed Central  Google Scholar 

  • Freeman JS, Whittock SP, Potts BM, Vaillancourt RE (2009) QTL influencing growth and wood properties in Eucalyptus globulus. Tree Genet Genomes 5:713–722

    Article  Google Scholar 

  • Freeman JS, Potts BM, Downes GM, Pilbeam D, Thavamanikumar S, Vaillancourt RE (2013) Stability of quantitative trait loci for growth and wood properties across multiple pedigrees and environments in Eucalyptus globulus. New Phytol 198:1121–1134

    Article  CAS  PubMed  Google Scholar 

  • Gavran M (2014) Australian plantation statistics 2014 update. Australian Bureau of Agricultural and Resource Economics and Sciences, Canberra

    Google Scholar 

  • Georges M, Nielsen D, Mackinnon M, Mishra A, Okimoto R, Pasquino AT, Sargeant LS, Sorensen A, Steele MR, Zhao X (1995) Mapping quantitative trait loci controlling milk production in dairy cattle by exploiting progeny testing. Genetics 139:907–920

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giblin FR, Carnegie AJ (2014) Puccinia psidii (Myrtle rust) - Australian host list. Retrieved from http://www.anpc.asn.au/myrtle-rust. Accessed 23 Oct 2014

  • Glen M, Alfenas A, Zauza E, Wingfield M, Mohammed C (2007) Puccinia psidii: a threat to the Australian environment and economy—a review. Australas Plant Pathol 36:1–16

    Article  Google Scholar 

  • Graça RN, Aun CP, Guimarães LM, Rodrigues BV, Zauza EA, Alfenas AC (2011) A new race of Puccinia psidii defeats rust resistance in eucalypt. Australas Plant Pathol 40:442–447

    Article  Google Scholar 

  • Graça RN, Ross-Davis AL, Klopfenstein NB, Kim M-S, Peever TL, Cannon PG, Aun CP, Mizubuti ESG, Alfenas AC (2013) Rust disease of eucalypts, caused by Puccinia psidii, did not originate via host jump from guava in Brazil. Mol Ecol 22:6033–6047

    Article  PubMed  Google Scholar 

  • Grattapaglia D, Vaillancourt R, Shepherd M, Thumma B, Foley W, Kulheim C, Potts B, Myburg A (2012) Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus. Tree Genet Genomes 8:463–508

  • Graves S, Piepho H, Selzer L, Dorai-Raj S (2012) multcompView: visualizations of paired comparisons. R package version 01–5, URL https://cran.r-project.org/web/packages/multcompView/index.html

  • Hadley W (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  • Hamilton M, Williams D, Tilyard P, Pinkard E, Wardlaw T, Glen M, Vaillancourt R, Potts B (2013) A latitudinal cline in disease resistance of a host tree. Heredity 110:372–379

    Article  CAS  PubMed  Google Scholar 

  • Heath M (2000) Hypersensitive response-related death. In: Lam E, Fukuda H, Greenberg J (eds) Programmed cell death in higher plants. Springer, Netherlands, pp 77–90

    Chapter  Google Scholar 

  • Hobert O (2008) Gene regulation by transcription factors and microRNAs. Science 319:1785–1786

    Article  CAS  PubMed  Google Scholar 

  • Hüberli D, Tommerup IC, Dobrowolski MP, Calver MC, St J, Hardy GE (2001) Phenotypic variation in a clonal lineage of two Phytophthora cinnamomi populations from Western Australia. Mycol Res 105:1053–1064

    Article  Google Scholar 

  • Hudson CJ, Freeman JS, Kullan AR, Petroli CD, Sansaloni CP, Kilian A, Detering F, Grattapaglia D, Potts BM, Myburg AA (2012) A reference linkage map for Eucalyptus. BMC Genomics 13:240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hudson CJ, Freeman JS, Jones RC, Potts BM, Wong MM, Weller JL, Hecht VF, Poethig RS, Vaillancourt RE (2014) Genetic control of heterochrony in Eucalyptus globulus. G3 4:1235–1245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iglesias-Trabado G, Carbaeira-Tenreiro R, Folgueiia-Lozano J (2009) Eucalyptus universalis: global cultivated eucalypt forest map (Version 1.2). In: Eucalyptologics: information resources on Eucalyptus cultivation worldwide. Retrieved from http://www.git-forestry.com (September 16th, 2015)

  • Jenkins CC, Suberkropp K (1995) The influence of water chemistry on the enzymatic degradation of leaves in streams. Freshw Biol 33:245–253

    Article  CAS  Google Scholar 

  • Johnson G, Burdon R (1990) Family-site interaction in Pinus radiata: implications for progeny testing strategy and regionalised breeding in New Zealand. Silvae Genet 39:55–62

    Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Junghans D, Alfenas A, Brommonschenkel S, Oda S, Mello E, Grattapaglia D (2003a) Resistance to rust (Puccinia psidii Winter) in Eucalyptus: mode of inheritance and mapping of a major gene with RAPD markers. Theor Appl Genet 108:175–180

    Article  CAS  PubMed  Google Scholar 

  • Junghans DT, Alfenas AC, Maffia LA (2003b) Escala de notas para quantificação da ferrugem em Eucalyptus. Fitopatol Bras 28:184–188

    Article  Google Scholar 

  • Kashi Y, Hallerman E, Soller M (1990) Marker-assisted selection of candidate bulls for progeny testing programmes. Anim Prod 51:63–74

    Article  Google Scholar 

  • Kawanishi T, Uematsu S, Kakishima M, Kagiwada S, Hamamoto H, Horie H, Namba S (2009) First report of rust disease on ohia and the causal fungus, Puccinia psidii, in Japan. J Gen Plant Pathol 75:428–431

    Article  Google Scholar 

  • Keith R, Mitchell-Olds T (2013) Genetic variation for resistance to herbivores and plant pathogens: hypotheses, mechanisms and evolutionary implications. Plant Pathol 62:122–132

    Article  Google Scholar 

  • Klement Z, Bozsó Z, Kecskés ML, Besenyei E, Arnold C, Ott PG (2003) Local early induced resistance of plants as the first line of defence against bacteria. Pest Manag Sci 59:465–474

    Article  CAS  PubMed  Google Scholar 

  • Kriticos DJ, Morin L, Leriche A, Anderson RC, Caley P (2013) Combining a climatic niche model of an invasive fungus with its host species distributions to identify risks to natural assets: Puccinia psidii sensu lato in Australia. PLoS ONE 8:e64479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labate CA, Assis TF, Oda S, Mello EJ, González ER, Zauza EAV, Mori ES, Moraes MLT, Cid LPB, Alfenas AC (2009) Eucalyptus. Compendium Transgen Crop Plants 9:35–108

    Google Scholar 

  • Lee H-A, Yeom S-I (2015) Plant NB-LRR proteins: tightly regulated sensors in a complex manner. Brief Funct Genomic. doi:10.1093/bfgp/elv012

    Google Scholar 

  • Li H, Ribaut J-M, Li Z, Wang J (2008) Inclusive composite interval mapping (ICIM) for digenic epistasis of quantitative traits in biparental populations. Theor Appl Genet 116:243–260

    Article  PubMed  Google Scholar 

  • Liu X, Chen Q, Wang Z, Xie L, Xu Z (2008) Allelopathic effects of essential oil from Eucalyptus grandis × E. urophylla on pathogenic fungi and pest insects. Front Forest China 3:232–236

    Article  Google Scholar 

  • Lu Y, Hatsugai N, Katagiri F, Ishimaru CA, Glazebrook J (2015) Putative serine protease effectors of Clavibacter michiganensis induce a hypersensitive response in the apoplast of Nicotiana species. Molecular plant-microbe interactions: MPMI-02-15-0036-R

  • Machado P, Alfenas A, Alfenas R, Mohammed C, Glen M (2015) Microsatellite analysis indicates that Puccinia psidii in Australia is mutating but not recombining. Australas Plant Pathol 44:455–462

    Article  CAS  Google Scholar 

  • Mamani EM, Bueno NW, Faria DA, Guimarães LM, Lau D, Alfenas AC, Grattapaglia D (2010) Positioning of the major locus for Puccinia psidii rust resistance (Ppr1) on the Eucalyptus reference map and its validation across unrelated pedigrees. Tree Genet Genomes 6:953–962

    Article  Google Scholar 

  • Martin JT, Juniper BE (1970) The cuticles of plants. Edward Arnold, London

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Minchinton E, Smith D, Hamley K, Donald C (2014) Myrtle rust in Australia. Acta Hortic 1055:89–90

    Article  Google Scholar 

  • Moon DH, Salvatierra GR, Caldas DG, de Carvalho MCG, Carneiro RT, Franceschini LM, Oda S, Labate CA (2007) Comparison of the expression profiles of susceptible and resistant Eucalyptus grandis exposed to Puccinia psidii Winter using SAGE. Funct Plant Biol 34:1010–1018

    Article  Google Scholar 

  • Morin L, Aveyard R, Lidbetter JR, Wilson PG (2012) Investigating the host-range of the rust fungus Puccinia psidii sensu lato across tribes of the family Myrtaceae present in Australia. PLoS ONE 7:e35434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D (2014) The genome of Eucalyptus grandis. Nature 510:356–362

    CAS  PubMed  Google Scholar 

  • Newman M-A, Von Roepenack E, Daniels M, Dow M (2000) Lipopolysaccharides and plant responses to phytopathogenic bacteria. Mol Plant Pathol 1:25–31

    Article  CAS  PubMed  Google Scholar 

  • Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP (2013) Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathog 9:e1003235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pegg G, Perry S, Carnegie A, Ireland K, Giblin F (2012) Understanding myrtle rust epidemiology and host specificity to determine disease impact in Australia. Cooperative Research Centre for National Plant Biosecurity, Bruce

    Google Scholar 

  • Pegg G, Brawner J, Lee D (2014a) Screening Corymbia populations for resistance to Puccinia psidii. Plant Pathol 63:425–436

    Article  Google Scholar 

  • Pegg GS, Giblin F, McTaggart A, Guymer G, Taylor H, Ireland K, Shivas R, Perry S (2014b) Puccinia psidii in Queensland, Australia: disease symptoms, distribution and impact. Plant Pathol 63:1005–1021

    Article  Google Scholar 

  • Pinkard E, Kriticos D, Wardlaw T, Carnegie A, Leriche A (2010) Estimating the spatio-temporal risk of disease epidemics using a bioclimatic niche model. Ecol Model 221:2828–2838

    Article  Google Scholar 

  • Piza ST, Ribeiro I (1988) Influência da luz e da temperatura na germinação de uredosporos de Puccinia psidii. Bragantia 47:75–78

    Article  Google Scholar 

  • Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genes Dev 19:374–378

    Article  CAS  Google Scholar 

  • Potts BM, Vaillancourt RE, Jordan G, Dutkowski G, Costa e Silva J, McKinnon G, Steane D, Volker P, Lopez G, Apiolaza L, Li Y, Marques C, Borralho N (2004) Exploration of the Eucalyptus globulus gene pool. In: Borralho N, Pereira J, Marques C, Coutinho J, Madeira M, Tomé M (eds) Eucalyptus in a changing world. Proceedings of an IUFRO conference, Aveiro, Portugal. RAIZ, Instituto Investigação de Floresta e Papel, pp 46–61

  • Rosado TB, Tomaz RS, Ribeiro Junior MF, Rosado AM, Guimarães LMS, Araújo EF, Alfenas AC, Cruz CD (2010) Detection of QTL associated with rust resistance using IBD-based methodologies in exogamic Eucalyptus spp. populations. Crop Breed Appl Biotechnol 10:321–328

    Article  Google Scholar 

  • Roux J, Greyling I, Coutinho TA, Verleur M, Wingfield MJ (2013) The Myrtle rust pathogen, Puccinia psidii, discovered in Africa. IMA Fungus 4:155

    Article  PubMed  PubMed Central  Google Scholar 

  • Santos MR, da Silva Guimarães LM, de Resende MDV, Rosse LN, Zamprogno KC, Alfenas AC (2014) Eucalypts rust (Puccinia psidii) resistance in Eucalyptus pellita. Crop Breed Appl Biotechnol 14:244–250

    Article  Google Scholar 

  • Thomma BP, Nürnberger T, Joosten MH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thumma BR, Southerton SG, Bell JC, Owen JV, Henery ML, Moran GF (2010) Quantitative trait locus (QTL) analysis of wood quality traits in Eucalyptus nitens. Tree Genet Genomes 6:305–317

    Article  Google Scholar 

  • Thumma B, Pegg GS, Warburton P, Brawner J, Macdonell P, Yang X, Southerton S (2013) Molecular tagging of rust resistance genes in eucalypts. CSIRO Plant Industry, Canberra

    Google Scholar 

  • Tobias PA, Park RF, Külheim C, Guest DI (2015) Wild-sourced Chamelaucium uncinatum have no resistance to Puccinia psidii (myrtle rust). Aust Plant Dis Notes 10:1–3

    Article  Google Scholar 

  • Tsuda K, Somssich IE (2015) Transcriptional networks in plant immunity. New Phytol 206:932–947

    Article  CAS  PubMed  Google Scholar 

  • Uchida J, Zhong S, Killgore E (2006) First report of a rust disease on ohia caused by Puccinia psidii in Hawaii. Plant Dis 90:524

    Article  Google Scholar 

  • Van Ooijen J (2009) MapQTL 6, Software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV, Wageningen

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wenzel G, Foroughi-Wehr B (1990) Progeny tests of barley, wheat, and potato regenerated from cell cultures after in vitro selection for disease resistance. Theor Appl Genet 80:359–365

    Article  CAS  PubMed  Google Scholar 

  • Williams DJ, Dancik BP, Pharis RP (1987) Early progeny testing and evaluation of controlled crosses of black spruce. Can J For Res 17:1442–1450

    Article  Google Scholar 

  • Wu R (1998) Genetic mapping of QTLs affecting tree growth and architecture in Populus: implication for ideotype breeding. Theor Appl Genet 96:447–457

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang J-W, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao S, Wang W, Yang X (2008) Evolution of resistance genes in plants. In: Heine H (ed) Innate immunity of plants, animals, and humans, nucleic acids and molecular biology, vol 21. Springer, Berlin, pp 1–25

    Chapter  Google Scholar 

  • Yuskianti V, Glen M, Puspitasari D, Francis A, Rimbawanto A, Gafur A, Indrayadi H, Mohammed C (2014) Species‐specific PCR for rapid identification of Ganoderma philippii and Ganoderma mastoporum from Acacia mangium and Eucalyptus pellita plantations in Indonesia. For Pathol 44:477–485

    Google Scholar 

  • Zauza EV, Alfenas A, Old K, Couto MF, Graça R, Maffia L (2010) Myrtaceae species resistance to rust caused by Puccinia psidii. Australas Plant Pathol 39:406–411. doi:10.1071/AP10077

    Article  Google Scholar 

  • Zhai J, Jeong D-H, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16

    Article  CAS  PubMed  Google Scholar 

  • Zhao J-P, Jiang X-L, Zhang B-Y, Su X-H (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS ONE 7:e44968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong S, Yang B, Puri K (2011) Characterization of Puccinia psidii isolates in Hawaii using microsatellite DNA markers. J Gen Plant Pathol 77:178–181

    Article  Google Scholar 

  • Zhuang J-Y, Wei S-X (2011) Additional materials for the rust flora of Hainan Province, China. Mycosystema 30:853–860

    Google Scholar 

  • Zobel B (1993) Clonal forestry in the eucalypts. In: Clonal forestry II. Springer, pp 139–148

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Acknowledgments

This research was supported by the Australian Government’s Collaborative Research Network involving the Sunshine Coast University, Griffith University and the University of Tasmania; the Biosecurity CRC; the National Centre for Future Forest Industries located at the University of Tasmania; and the Australian Research Council (DP140102552 and DP110101621). We thank Peter Ades, Josquin Tibbits, Simon Southerton, Bala Thumma and Karanjeet Sandhu for discussion, Corey Hudson for his now published linkage maps, Paul Tilyard for assistance with seed collection and data management and Lynne Forster, Hugh Fitzgerald and Helen Stephens for assessment of the other pathogens in leaf samples of the F2 progeny.

Data Archiving Statement

All individual genotype data relating to this study are available at: http://eprints.utas.edu.au/22705.

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Correspondence to J. S. Freeman.

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Communicated by D. Grattapaglia

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Butler, J.B., Freeman, J.S., Vaillancourt, R.E. et al. Evidence for different QTL underlying the immune and hypersensitive responses of Eucalyptus globulus to the rust pathogen Puccinia psidii . Tree Genetics & Genomes 12, 39 (2016). https://doi.org/10.1007/s11295-016-0987-x

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